Prevalence and risk factors of helminths and intestinal protozoa infections among children from primary schools in western Tajikistan

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Intestinal parasitic infections represent a public health problem in Tajikistan, but epidemiological evidence is scarce. The present study aimed at assessing the extent of helminths and intestinal protozoa infections among children of 10 schools in four districts of Tajikistan, and to make recommendations for control.


A cross-sectional survey was carried out in early 2009. All children attending grades 2 and 3 (age: 7-11 years) from 10 randomly selected schools were invited to provide a stool sample and interviewed about sanitary situation and hygiene behaviour. A questionnaire pertaining to demographic and socioeconomic characteristics was addressed to the heads of households. On the spot, stool samples were subjected to duplicate Kato-Katz thick smear examination for helminth diagnosis. Additionally, 1-2 g of stool was fixed in sodium acetate-acetic acid-formalin, transferred to a specialised laboratory in Europe and examined for helminths and intestinal protozoa. The composite results from both methods served as diagnostic ‘gold’ standard.


Out of 623 registered children, 602 participated in our survey. The overall prevalence of infection with helminths and pathogenic intestinal protozoa was 32.0% and 47.1%, respectively. There was pronounced spatial heterogeneity. The most common helminth species was Hymenolepis nana (25.8%), whereas the prevalences of Ascaris lumbricoides, hookworm and Enterobius vermicularis were below 5%. The prevalence of pathogenic intestinal protozoa, namely Giardia intestinalis and Entamoeba histolytica/E. dispar was 26.4% and 25.9%, respectively. Almost half of the households draw drinking water from unimproved sources, such as irrigation canals, rivers and unprotected wells. Sanitary facilities were pit latrines, mostly private, and a few shared with neighbours. The use of public tap/standpipe as a source of drinking water emerged as a protective factor for G. intestinalis infection. Protected spring water reduced the risk of infection with E. histolytica/E. dispar and H. nana.


Our data obtained from the ecological ‘lowland’ areas in Tajikistan call for school-based deworming (recommended drugs: albendazole and metronidazole), combined with hygiene promotion and improved sanitation. Further investigations are needed to determine whether H. nana represents a public health problem.


Infections with helminths (e.g. Ascaris lumbricoides, hookworm, Hymenolepis nana and Trichuris trichiura) and intestinal protozoa (e.g. the pathogenic Entamoeba histolytica and Giardia intestinalis) are closely linked with conditions of poverty, unsafe water, sanitation and hygiene [1]. More than 2 billion people might be infected with helminths, mainly in the developing world [2]. At highest risk of morbidity are pre-school and school-aged children and pregnant women [3]. Negative effects of helminth infections include diminished physical fitness and growth retardation, and delayed intellectual development and cognition [2,3]. Vitamin A deficiency, malabsorption of vitamin B12 and fat and nutritional deficiencies in children might be associated with G. intestinalis, which may lead to serious organ damage [4]. Morbidity due to E. histolytica includes diarrhoea and dysentery in children and liver abscess in severe cases [5].

It is widely acknowledged that helminthiasis and intestinal protozoa infections are of considerable public health importance in Tajikistan and elsewhere in Central Asia [6,7], but the geographical distribution and regional burden remain to be determined. Previous research has mainly focussed on parasitic diseases of livestock and most of the available literature is in Russian. Recently, the World Health Organization (WHO) presented a simple methodology to assess the prevalence of helminths, stratified by ecozones, for settings where information is scarce [8]. Once high-risk areas are identified (e.g. > 20% of school-aged children infected with soil-transmitted helminths), WHO recommends deworming of all school-aged children at least once every year [9]. Whenever resources allow, deworming should be complemented with improved access to safe drinking water and sanitation, health education and hygiene behaviour change, coupled with regular monitoring and surveillance. Several countries have launched their helminthiasis control programmes and made progress towards achieving deworming coverage rates of 75% of school-aged children [10].

The Swiss Health Reform and Family Medicine Support Project (Project Sino in short) in Tajikistan contributes to the national health sector reform programme. The project aims to improve the population’s health status and access to health services, particularly for poor groups. Among other issues, the project developed an accessible and sustainable family medicine model that is affordable by local communities as shown in pilot districts. The project initiates further evidence-based activities and encourages operational research at the interface of family medicine services and communities with an emphasis on reducing the burden of diseases that are of public health importance [11-16]. The aim of the present study was to assess the prevalence of helminths and intestinal protozoa infections among school-aged children in four districts of Project Sino, and to make recommendations for control.

Materials and methods

Study area and context

Tajikistan is a mountainous land-locked country in Central Asia with approximately 7 million inhabitants, most of whom live in rural areas (73.7% in 2009) [17,18]. In 2010, the per capita gross development product (GDP) was US$ 2, 000, and hence Tajikistan ranked at position 190 out of 228 countries included in the list of the CIA world factbook [19]. Even though the national economy has grown considerably in the past several years, two-thirds of the population still live on less than US$ 2.15 per day. Agriculture remains the primary sector of the national economy, contributing 24% of the national GDP and 66% of employment. Remittances are a vital source of income for many Tajik households, facilitated through working in the construction sector in Russia. Labour migrants are primarily young men from rural areas [20].

The regional climate is continental, close to Mediterranean with dominant spring-winter precipitation, hot and dry summers and cold winters [21]. Water is becoming increasingly scarce due to rapid shrinkage of glaciers, conflicts with neighbouring downstream countries on water provision used for irrigation purposes (for cotton and to a lesser extent rice cultivation), and deterioration of irrigation and drainage systems [20].

Our study was carried out in four districts of Project Sino located in the western part of Tajikistan in early 2009 (Figure ​(Figure1).1). Prior to our survey, relevant literature considering the local context of Tajikistan (e.g. peer-reviewed articles obtained from searching electronic databases such as PubMed and ISI Web of Knowledge) and reports and national statistics from WHOLIS and the WHO regional office in Europe were reviewed.

Figure 1

Prevalence of multiple species infection with helminths and pathogenic intestinal protozoa, stratified by school, in western Tajikistan in early 2009.

Selection of study population

Schoolchildren attending grades 2 and 3 (age: 7-11 years) were chosen according to WHO recommendations [22]. Schools are a convenient platform to conduct surveys and schoolchildren are at high risk of infections with helminths and other intestinal parasites. Selection of a relatively narrow age range results in smaller confidence intervals around point prevalence estimates. School enrolment rates are high in Tajikistan, i.e. 97% primary net school enrolment in 2005-2009 [23]. We adhered to a rapid appraisal methodology proposed by WHO, suggesting a minimum of 50 schoolchildren to be examined per school [8,9].

Study design and selection of schools

In a first step, the heads of educational departments from all four districts were asked by a Project Sino representative for community outreach activities in January 2009 to prepare a list of all primary schools in their respective district, including the number of children attending grades 2 and 3. A total number of 300 primary schools were listed in these districts. In 143 of these schools, less than 50 children attended grades 2 and 3, and hence these were excluded. Another 10 schools from one district were excluded because of recent deworming activities implemented by a non-governmental organization (NGO). From the remaining 147 schools, 10 were selected by means of a simple random sampling procedure. In each school, 60-70 children were selected (allowing for drop-outs to gather data from at least 50 children per school), and hence obtaining a minimal sample size of 500 fully complying children.

Field procedures

School directors from the selected schools and teachers of grades 2 and 3 were visited by the survey team 1 week prior to our cross-sectional parasitological and questionnaire surveys. A written informed consent form for the parents/guardians of participating children, a questionnaire for the household heads, and a small plastic container for collection of stool samples were left with the teachers and distributed to eligible children. The questionnaires were pre-tested in a village near Dushanbe, the capital of Tajikistan, and adapted prior to administration.

During the school-based survey, the signed informed consent sheets, household questionnaires and stool samples were collected. Unique identification numbers were assigned to each participating child. A short interview was held with each child, using a questionnaire pertaining to hygiene behaviour, drinking water and sanitation adapted from a standard tool provided by the joint monitoring programme (JPM) of WHO and UNICEF [24]. Each child was weighed to the nearest kg and measured to the nearest cm. At the end of the survey, each child was given a piece of soap and a small pack of iodine-fortified salt as a small token for their participation.

Laboratory procedures

From each stool sample, duplicate Kato-Katz thick smears were prepared on microscope slides shortly after stool collection by two experienced laboratory technicians from the Republican Tropical Disease Centre (RTDC) [25]. Thick smears were allowed to clear for 45-60 min prior to examination under a light microscope for helminth eggs. The number of helminth eggs was counted and recorded for each species separately. The slides were read on the spot and the teachers and directors were informed about the overall prevalence of helminth infections in their school.

In addition, approximately 1-2 g of stool was placed in a Falcon tube filled with 15 ml of sodium acetate-acetic acid-formalin (SAF) [26,27]. These SAF-fixed stool samples were transferred to a specialised laboratory in Italy and examined there by an experienced laboratory technician for the presence of helminths and intestinal protozoa using an ether-concentration technique, adhering to a standard protocol [28].

For quality control purposes, 10% of the Kato-Katz thick smears were randomly selected and read retrospectively by an experienced laboratory technician in Côte d’Ivoire. A senior laboratory technician from Switzerland checked approximately 5% of the SAF-fixed stool samples that were examined by the ether-concentration method. In case of discordant results, the slides were re-read and results discussed until agreement between the technicians was reached.

Ethical considerations

The study was approved by the Ministry of Health (MoH) of Tajikistan (reference no. 16/75-92). The study protocol was presented to the Deputy MoH and methodological issues related to the survey were discussed with the heads of collaborating partner institutes (RTDC and State Sanitary Hygiene Surveillance Department). The primary health care network managers of each district health centre and the administrative authorities at community level were informed about the study and their consent was obtained. Parents/guardians of participating children signed a written informed consent prior to study enrolment. Participation was voluntary and children were free to withdraw at any time. At the end of the study, each child was offered an anthelminthic treatment (single oral dose of 400 mg albendazole) free of charge [29]. A feedback session for key stakeholders (e.g. representatives from the MoH and collaboration institutions) was held at the end of the survey to present and discuss the findings and to jointly draft a plan of action.

Statistical analysis

Data were entered into EpiData version 3.1 (EpiData Association; Odense, Denmark) and internal consistency checks were done. Stata version 10 (Stata Corporation; College Station, TX, USA) was employed for statistical analysis. The children’s socioeconomic status was determined using a household-based asset approach that was adapted from previous studies in Tajikistan [11,14]. In brief, a wealth index was constructed by estimating household asset weights by means of a principal component analysis (PCA) methodology [30]. Nine variables were included in the PCA (i.e. frequency of meat consumption, refrigerator, radio, colour television, satellite, DVD recorder, car, mobile phone and fixed line phone). Missing values were replaced with the mean for the corresponding variable [31].

Sources of drinking water were grouped into ‘improved’ (i.e. piped water into dwelling/yard, public tap or standpipe, protected dug well/spring, bottle water and rainwater) and ‘unimproved’ sources (i.e. unprotected spring, cart with small tank, tanker truck and surface water) according to a classification used by the JPM of WHO and UNICEF [24].

With regard to the parasitological data, only children who had duplicate Kato-Katz thick smear readings plus results from the ether-concentration test were included in the final analysis. A helminth infection was defined as the presence of at least one helminth egg in one of the two Kato-Katz thick smears and/or the SAF-fixed stool sample. The presence of an intestinal protozoon cyst in the SAF-fixed stool sample subjected to an ether-concentration method was used as our diagnostic approach for these parasites. For helminths, infection intensity at the unit of an individual was determined as the arithmetic mean egg count from two Kato-Katz thick smears, multiplied by a factor 24 to obtain eggs per gram of stool (EPG). Helminth infection intensities were grouped into light (A. lumbricoides, 1-4, 999 EPG; H. nana, 1-1, 999 EPG; T. trichiura, 1-999 EPG); moderate (A. lumbricoides, 5, 000-49, 999; H. nana, 2, 000-9, 999 EPG; T. trichiura, 1, 000-9, 999 EPG); and heavy (A. lumbricoides, ≥50, 000 EPG; H. nana and T. trichiura, ≥10, 000 EPG) [29,32]. No hookworm eggs were found in the Kato-Katz thick smears. For Enterobius vermicularis, no attempt was made to estimate infection intensity, because the Kato-Katz technique lacks diagnostic accuracy for this helminth species [33]. Children were grouped into three age classes: (i) 7-8 years; (ii) 9 years; and (iii) 10-11 years.

Proportions were compared using Pearson’s χ2 and Fisher’s exact test as appropriate. Medians between groups were compared using the Student’s t-test and Bartlett’s test for equal variances, as appropriate. Risk factors for infection with H. nana, G. intestinalis and E. histolytica/E. dispar were analysed by fitting bi- and multivariate logistic regression models. Explanatory variables associated with infection and a P-value ≤0.15 were included into a multivariate logistic regression model. A stepwise backward elimination approach removing covariates above a level of 0.15 one after another was employed. Variations of conditions between schools were considered by introducing a school-level random effect. For all tests, 95% confidence intervals (CIs) were calculated.


Study compliance

From a total of 623 children registered in grades 2 and 3 in the 10 selected schools, 602 children participated in the cross-sectional survey, owing to an overall compliance of 96.6%. Reasons for non-compliance were absence due to recent travels (n = 9), absence of written informed consent (n = 3), feeling unwell (n = 2) or no specific reason (n = 7). Children’s age ranged between 7 and 11 years with a mean of 9.1 years. There was a borderline significant age difference between schools (Bartlett’s test for equal variances: χ2 = 16.54, degree of freedom (d.f.) = 9, P = 0.056). There were slightly more boys than girls (311 versus 291, P = 0.416) with no sex difference between schools (χ2 = 10.47, d.f. = 9, P = 0.314).

Household profiles

One quarter (24.5%) of the variability of the household’s socioeconomic status was explained by the first principal component. Greatest weight was given to households possessing a car (0.44), refrigerator (0.42) and DVD recorder (0.36). After standardising the asset weighed variables, households having a satellite (0.79), refrigerator (0.72) and car (0.64) were scored highest, whereas lowest scores were given to households with no colour television (-0.63), no mobile phone (-0.47) and no DVD recorder (-0.44). A wealth index was created for each child by building a total of all household asset scores and assigning accordingly each child into five wealth quintiles. Finally, each child was grouped into three wealth classes (bottom, 40%; middle, 40%; top, 20%) (Table ​(Table11).

Table 1

Wealth quintiles based on nine household assets for 602 children aged 7-11 years from 10 schools in western Tajikistan, early 2009

Most households comprised between 6 and 10 individuals. Every fifth household was smaller, counting 3-5 individuals. Large households with 11 persons and more accounted for 10% in our study sample. Two-thirds of the household heads were farmers or craftspeople. Regarding educational attainment, every other household head obtained a secondary school-leaving certificate (11 years of school or more), whereas almost every third had a university degree. Only 3% of the household heads reported not having received any education. With few exceptions, all households kept livestock, such as bullocks, cows, donkeys, goats, horses and sheep. In addition, half of the households kept chickens. Meat was consumed, on average, twice a week.

Slightly more than half of the households (53%) had improved drinking water sources, such as protected springs (20%) and public tap/standpipe (18%). The remaining 47% of the households depended on unimproved sources, i.e. surface water from irrigation canals, rivers and streams (38%), unprotected wells and springs and rain water. There was large heterogeneity of unimproved water sources at the unit of school, varying between 2% and 100%. With regard to sanitation, almost all households used pit latrines that are not connected to a sewage system. Three out of four households had their own latrines, whereas the remaining households shared sanitation facilities with their neighbours in the yard. Two households used a public sanitation facility.

Helminths and intestinal protozoa infections

Overall, 599 of the interviewed children had a single stool sample subjected to duplicate Kato-Katz thick smear reading and 594 of the children had a small portion of stool fixed in SAF that was examined by an ether-concentration technique for helminths and intestinal protozoa. Complete parasitological data were therefore available for a subsample of 594 participants. Table ​Table22 shows that the prevalence of infection with any helminths or pathogenic intestinal protozoa was 32.0% and 47.1%, respectively. The overall prevalence of soil-transmitted helminths was 8.6%. There was no statistically significant sex difference in the prevalence of any of the helminths identified (P > 0.05). H. nana was the predominant helminth species (25.8%), whereas all other helminths identified showed prevalences below 5%, e.g. A. lumbricoides (4.4%), hookworm (3.5%) and T. trichiura (1.4%). With regard to age, A. lumbricoides showed a statistically significantly higher prevalence in the youngest children (age 7-8 years, prevalence 9.0% versus 3.8% and 2.2% in 9-year-old and 10- to 11-year-old children; Fisher’s exact test, P = 0.021).

Table 2

Number (%) of schoolchildren infected with helminths and intestinal protozoa in western Tajikistan, early 2009

With regard to intestinal protozoa, the most common species was the non-pathogenic Entamoeba coli (65.7%). The pathogenic protozoa G. intestinalis and E. histolytica/E. dispar were detected in 26.4% and 25.9% of the children, respectively. The prevalence of the suspected pathogenic protozoon Blastocystis hominis was 19.9%. No sex-related differences were found for any of the intestinal protozoa identified.

The prevalence of single and multiple helminths and pathogenic intestinal protozoa species infections are displayed in Figure ​Figure1.1. Overall, 40.9% of all children had a single species infection, whereas 17.3% had a dual species infection and 4.9% harboured at least three intestinal pathogenic parasite species concurrently. There was considerable heterogeneity of overall infection prevalence between schools, ranging from 53.1% to 76.0%. Prevalence of multiple species infection across schools was between 9.7% and 42.0%. The youngest age group (7-8 years) exhibited a slightly higher infection prevalence of multiple species infection than their older counterparts, but the difference was not statistically significant (Fisher’s exact, P = 0.061).

Spatial distribution of intestinal parasite infections

The overall prevalence of any intestinal parasites (pathogenic and non-pathogenic) was 88.2%, ranging from 76.7% to 93.2% across schools. Twenty-seven children (4.6%) were infected with helminths only, with prevalences ranging from 1.7% to 7.8% at the unit of the school. More than half of the children were infected with intestinal protozoa only (56.2%, n = 334), with a range from 38.0% to 64.1% in individual schools. A total of 163 children (27.4%) harboured helminths and intestinal protozoa concurrently, between 18.3% and 54.0% at the unit of the school.

Most widespread co-infections were combinations with H. nana and G. intestinalis (5.2%), followed by H. nana and E. histolytica/E. dispar (3.9%). The most common triple infection was H. nana, E. histolytica/E. dispar and G. intestinalis (1.5%).

The prevalence of species-specific helminths and intestinal protozoa infections, stratified by school, is given in Table ​Table2.2. H. nana showed highest infection prevalence exceeding 30% in four schools. The highest infection prevalence of H. nana (38.0%) occurred in a school where the highest prevalence of A. lumbricoides (16.0%) and hookworm (10.0%) were also observed. T. trichiura infections were found only in two schools (8.5% and 6.0%). Regarding intestinal protozoa infections, prevalences exceeding 30% were observed in two schools for G. intestinalis (40.7% and 32.8%) and in two schools for E. histolytica/E. dispar (38.0% and 31.3%). The peak prevalence of E. histolytica/E. dispar was observed in the school where the highest helminth infection prevalence was noted.

Helminth infection intensities

Helminth infection intensities were estimated based on duplicate Kato-Katz thick smears. The overall geometric mean faecal egg count for H. nana was 383 EPG (95% CI: 311-471 EPG), for A. lumbricoides it was 223 EPG (95% CI: 154-321 EPG), and the respective estimate for T. trichiura was 125 EPG (95% CI: 71-222 EPG). All infections were of light intensity according to WHO cut-offs.

There was no statistically significant difference in infection intensity between boys and girls for H. nana (two-sample t-test, t = -0.014, d.f. = 71, P = 0.989) and A. lumbricoides (t = 0.020, d.f. = 19, P = 0.984). Infection intensity of H. nana decreased with age (ANOVA, Bartlett’s test for equal variances, d.f. = 71, 2; χ2 (2) = 11.50, P = 0.003). While the geometric mean faecal egg count of H. nana for children aged 7-8 years was 460 EPG (95% CI: 278-762 EPG), it was 401 EPG in 9-year-old children (95% CI: 297-541 EPG), and 308 EPG in the oldest age group investigated (95% CI: 210-450 EPG). Age-related differences were also found for A. lumbricoides (ANOVA, Bartlett’s test for equal variances, d.f. = 18, 2; χ2 (2) = 8.55, P = 0.014). The highest geometric mean faecal egg count was observed for 9-year-old children (290 EPG, 95% CI: 120-701 EPG), whereas lower faecal egg counts were observed for younger and older children (7-8 years, mean 215 EPG, 95% CI: 133-348 EPG; 10-11 years, mean 153 EPG, 95% CI: 38-610 EPG).

Risk factors for intestinal parasites

Table ​Table33 summarises demographic, socioeconomic, hygiene- and drinking water source-related risk factors for an infection with G. intestinalis, E. histolytica/E. dispar and H. nana according to bivariate and multivariate random effects models. Regarding drinking water sources, use of public tap/standpipe (odds ratio (OR) = 0.35, 95% CI: 0.12-1.00) emerged as a protective factor in the bivariate model for infection with G. intestinalis. Protected spring water was a protective factor for E. histolytica/E. dispar infections in the bi- and multivariate model (OR = 0.52, 95% CI: 0.31-0.88; OR = 0.41, 95% CI: 0.23-0.74, respectively). Moreover, protected spring water emerged as protecting factor for H. nana infections in the bi- and multivariate model (OR = 0.42, 95% CI: 0.20-0.88; OR = 0.44, 95% CI: 0.20-0.97).

Table 3

Results from bivariate non-random and random effects multivariate logistic regression models for risk factors of specific intestinal parasitic infections among schoolchildren in western Tajikistan, early 2009

Children belonging to households keeping sheep and poultry were at a slightly higher risk of an E. histolytica/E. dispar infection (OR = 1.61, 95% CI: 1.05-2.48; OR = 1.54, 95% CI: 1.05-2.25, respectively). Likewise, H. nana infection was associated with chicken farming both in the bi- and multivariate model (OR = 1.95. 95% CI: 1.31-2.90; OR = 2.04, 95% CI: 1.34-3.12). Socioeconomic status was significantly associated with H. nana infection, since children from households of the middle 40% were less likely to be infected compared to their poorer counterparts (OR = 0.58, 95% CI: 0.38-0.90).


The present cross-sectional survey determining the prevalence (and intensity) of infection with helminths and intestinal protozoa among 594 children aged 7-11 years in 10 randomly selected schools in western Tajikistan revealed that parasitic infections are a public health issue. Indeed, every third child was infected with helminths and almost every second child harboured at least one intestinal protozoon species. One out of five children had multiple species intestinal parasitic infections. Every fourth child was infected with H. nana, G. intestinalis and E. histolytica/E. dispar. The patterns of intestinal parasitic infections indicated spatial clustering: the school with the highest overall and multiple species infection prevalence showed the highest prevalences of H. nana, A. lumbricoides, hookworm and E. histolytica/E. dispar. Public well/standpipe as drinking water source was found to be a protective factor for G. intestinalis infections, whereas protected spring water reduced the risk of infections with H. nana and E. histolytica/E. dispar. Children from households keeping poultry were more likely to be infected with H. nana and E. histolytica/E. dispar than children from the remaining households.

The high overall prevalence of intestinal parasites, observed in our study, corroborates previous studies from Central Asia. A population-representative survey in children aged 6-15 years from Kyrgyzstan demonstrated an overall infection prevalence of 41% [7]. Unpublished parasitological data from surveys conducted by the Sanitary Epidemiological Service of Kyrgyzstan among 3, 427 school-aged children in 2006/2007 indicated an overall infection prevalence of 71.4%, with G. intestinalis being the most common intestinal protozoon species in that study (23.1%) [34]. Another school-based cross-sectional survey from Afghanistan showed that 47.6% of the subjects were infected with at least one soil-transmitted helminth, predominantly A. lumbricoides (40.9%) [35]. According to a recent WHO report, prevalence of soil-transmitted helminth infections in Tajikistan was estimated to range between 20% and 50% [10].

Significant spatial heterogeneity in the prevalence across schools was found, particularly for helminth infections. Lowest prevalences were found in the two schools in the mountainous area. Spatial disparities of infection prevalence were also described from school-based surveys in Haiti [36]. Geographical variation of different soil-transmitted helminths in a study from Zanzibar was interpreted with predominant soil types as a distinguishing factor [37]. Eight schools in our study are located in the ecological zone ‘lowland’, containing fine-grained alluvial or loessic soils [21] where intensive irrigated agriculture is practiced [38]. The observed clustering of intestinal parasites (i.e. H. nana, A. lumbricoides, hookworm and E. histolytica/E. dispar) in one of the investigated schools corroborates findings of small-scale clustering (e.g. household level). A. lumbricoides and T. trichiura were observed to aggregate at household level in a cross-sectional survey conducted in the People’s Republic of China [39]. Another study, conducted in rural Amazonian settlements, observed that almost half of the helminth infections were concentrated in only 5% of the surveyed households [40]. Some authors differentiated between domestic (household area) and public transmission sites (public places of work, streets, fields and schools) and recommended that control measures should target both domains [41].

Nearly half of all drinking water sources reported by the children in the current study were classified as unimproved sources, but a large variation was found (2-100% at the unit of the school). Teachers explained that electricity in their villages is often unstable and available only for a few hours per day, particularly during the winter season. When community water supply systems operated by electric pumps are interrupted, people draw water for domestic needs from open and unprotected sources such as irrigation canals and rivers. A large part of the latrines in the schools visited were inappropriately maintained (Figure ​(Figure22).

Figure 2

School latrines in two primary schools in western Tajikistan, early 2009.

Our findings underline UNICEF estimations from 2007; almost half of the rural households in Tajikistan depended on unimproved drinking water sources [42]. Unmet drinking water and sanitation standards in Tajikistan partially result from weak services of water supply and public sanitation. Only 23% of the population had access to a sewage system in 2003; 89% in urban areas but only 11% in rural areas [6]. Thus far, active participation mechanisms in water management involving public and private sectors and local communities are poorly developed [6,43].

Interestingly, the use of unimproved drinking water sources did not emerge as a risk factor for G. intestinalis and E. histolytica/E. dispar infection in our study. In other settings, however, water sources were identified as a risk factor for Giardia, as this intestinal protozoon species is commonly transmitted by ingesting cysts persisting in contaminated water or from person-to-person through the faecal-oral route [4]. Our study indicates that the use of drinking water from improved sources (public well/standpipe) is a protective factor for infections with E. histolytica/E. dispar, G. intestinalis and H. nana. Similar findings were observed for H. nana from Kyrgyzstan [7]. The use of tap water was reported to be associated with low infection prevalence of G. intestinalis compared to the use of surface water in a school-based survey in Côte d’Ivoire [44]. A study from Mexico City identified the storing of drinking water in unprotected containers (cisterns, tanks and bucks) as a risk factor for G. intestinalis [45].

Our study has some limitations. First, only one stool sample was collected from each participant. Previous research has shown that multiple stool sampling enhances the sensitivity of helminths and intestinal protozoa diagnosis [46,47]. Second, the Kato-Katz technique is inappropriate for accurate diagnosis of E. vermicularis and Strongyloides stercoralis. Indeed, the adhesive tape method is recommended for E. vermicularis diagnosis, but there are compliance issues with this method [33]. For S. steroralis diagnosis, the Baerman and/or the Koga agar plate method should be used [48]. To partially overcoming these shortcomings, we prepared duplicate Kato-Katz thick smears and preserved 1-2 g of stool that was subjected to an additional diagnostic approach, the ether-concentration method. Data from both methods combined were considered as diagnostic ‘gold’ standard. Third, no attempt was made to investigate seasonality. We speculate that the prevalence of parasitic infections might be higher in summer when children spend more time outside and might eat more frequently unwashed vegetables and fruits from the garden, as has been observed in neighbouring Kyrgyzstan [49].


The present study provides new insight into school-aged children’s infection status with helminths and intestinal protozoa in ecological ‘lowland’ areas of western Tajikistan. Considering the high infection prevalence of H. nana, E. histolytica/E. dispar and G. intestinalis observed here, a way forward may consist in locally adapted interventions, combining an initial school-based deworming and targeted health education programmes, promoting better hygiene and improved sanitation. Treatment with albendazole is proposed to control soil-transmitted helminthiasis, whereas metronidazole should be utilized against the two pathogenic intestinal protozoa. Previous research has shown that carefully designed school-based hygiene programmes effectively contributed to reduce infection intensity and re-infection rates [49-52]. A nationwide deworming programme in Tajikistan is currently conceived by the MoH and the RTDC. In 2010, a total of 32 laboratory technicians received refresher training on specific laboratory diagnostic techniques for identification of soil-transmitted helminths. In our view, further investigations are warranted to assess the true public health burden due to H. nana infection to guide future control efforts against this helminth, which represented the predominant species in our study area.

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

BM, JU and KW conceived and designed the study protocol, data collection forms and questionnaires for interviews. BM and GK planned, coordinated and supervised data collection in the field. GK, ZM and VJR conducted interviews and performed data collection. MB supervised the collection and analysis of parasitological data. MH, MK and LKL provided laboratory analyses of stool samples. Data analysis and writing up of the manuscript was done by BM. BM, JU and KW revised the manuscript. The final version of the manuscript was reviewed and approved by all authors prior to submission.


We thank all the schoolchildren, parents/guardians, heads of household, teachers, school principals and family doctors for their participation and assistance. We appreciated the support from the heads of jamoats and hukhmats, the Rayon Health Centres and Primary Health Care Network Managers of the health districts of Dangara, Shakhrinav, Tursunzoda and Varzob, and the regional and central management of the Department of State Sanitary Hygiene Surveillance Department. We acknowledge the management of RTDC (Dr. Saiffudin Karimov and Dr. Tohir Sherkanov), Medical Services Department (Dr. Bobokhojaev Oktam Ikramovich), UNICEF Tajikistan (Dr. Bakhruddinov Mutribjon) and the Institute for Zoology and Parasitology (Dr. Zamonidin Karimov) for technical and logistical support. We are grateful to Prof. Giuseppe Cringoli and Prof. Laura Rinaldi (University of Naples ‘Federico II’, Italy) for providing excellent laboratory facilities for copromicroscopic diagnosis and Dr. Peter Steinmann for scientific input. We thank Dr. Nick Bottone, head of Sino Project and Ms. Dilrabo Jabarova, Mr. Orif Zamirov and Ms. Malika Baimatova for organizational assistance. Our deepest thanks are addressed to the survey team for their commitment. This study was officially authorized by the MoH and our gratitude is addressed to Dr. Mirzoev Asamjon Safolovich, Deputy MoH. The research received funding by the Project Sino, which is funded through the Swiss Agency for Development and Cooperation (SDC).


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Malnutrition and Mortality Patterns among Internally Displaced and Non-Displaced Population Living in a Camp, a Village or a Town in Eastern Chad

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Daniel Tomé, Editor
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Certain population groups have been rendered vulnerable in Chad because of displacement of more than 200,000 people over the last three years as a result of mass violence against civilians in the east of the country. The objective of the study was to assess mortality and nutritional patterns among displaced and non-displaced population living in camps, villages and a town in the Ouddaï and Salamat regions of Chad.


Between May and October 2007, two stage, 30-cluster household surveys were conducted among 43,900 internally displaced persons (IDPs) living in camps in Ouaddai region (n = 898 households), among 19,400 non-displaced persons (NDPs) living in 42 villages in Ouaddai region (n = 900 households) and among 17,000 NDPs living in a small town in Salamat region (n = 901 households). Data collection included anthropometric measurements, measles vaccination rates and retrospective mortality. Crude mortality rate (CMR), mortality rate among children younger than 5 years (U5MR), causes of death and the prevalence of wasting (weight-for-height z score <−2) among children aged 6 to 59 months were the main outcome measures.


The CMR among the 4902 IDPs in Gozbeida camps, 4477 NDPs living in a village and 4073 NDPs living in a town surveyed was 1.8 (95% CI, 1.2–2.8), 0.3 (95% CI, 0.2–0.4), 0.3 (95% CI, 0.2–0.5) per 10,000 per day, respectively. The U5MR in a camp (n = 904), a village (n = 956) and a town (n = 901) was 4.1 (95% CI, 2.1–7.7), 0.5 (95% CI, 0.3–0.9) and 0.7 (95% CI, 0.4–1.4) per 10,000 per day, respectively. Diarrhoea was reported to be the main cause of death. Acute malnutrition rates (according to the WHO definition) among 904 IDP children, 956 NDPs children living in a village, 901 NDP children living in a town aged 6 to 59 months were 20.6% (95% CI, 17.9%–23.3%), 16.4% (95% CI, 14.0%–18.8%) and 10.1% (95% CI, 8.1%–12.2%) respectively. The study found a high mortality rate among IDPs and an elevated prevalence of wasting not only in IDP camps but also in villages located in the same region. The town-dweller population remains at risk of malnutrition. Appropriate contingency plans need to be made to ensure acceptable living standards for these populations.


Selecting a target population is a priority before implementing a food and relief aid program. Humanitarian aid agencies usually focus their effort on displaced population in emergency situations but pay little attention to the host population. Differences in outcome between residents and refugees have been reported in two studies but only after implementation of an intervention [1], [2]. There has been little research on the nutritional status and mortality among internally displaced and non displaced population prior to an intervention, particularly in Chad.

Over the last three years, more than 150 000 internally displaced persons fled to south-eastern Chad as a consequence of inter-ethnic conflict. A first wave of attacks carried out in April 2006 resulted in the internal displacement of 50 000 people, mainly in Ouaddai region. A second period of attacks, which started in October 2006 displaced another 100 000 people in Salamat region. Generally, those vulnerable populations had lost all their assets and farms, if not their relatives. Recurrent food shortages between two harvests were possibly worsened by the resettlement of these displaced people. Médecins Sans Frontières (MSF) began work in eastern Chad in 2006 and operations targeting internally displaced people, including feeding centres and primary care clinics, opened in 2007, were focused on 3 areas: Goz Beida, Am Dam and Am Timan (Figure 1). Despite the international relief effort providing food, water, shelter and health care for displaced persons, nutritional security may have been compromised for villagers and town-dwellers surrounded by camps. We conducted a survey to estimate mortality rates and the prevalence of malnutrition in these three specific populations prior to any intervention.

Figure 1

Location of Goz Beida, Am Dam and Am Timan in Eastern Chad.


We undertook 2-stage, 30 cluster household consecutive surveys in three sites in Eastern Chad: one in camps welcoming internally displaced people (IDPs) (Goz Beida region), one in villages (Am Dam district) and one in a small town (Am Timan), both in areas surrounded by camps hosting IDPs.

In each area, a sample size of 900 children aged 6 to 59 months was required to achieve a 5% precision around an estimated prevalence of wasting of 15% with 95% confidence assuming a design effect of 2. With an estimated mean household size of 5 persons and with children younger than 5 years comprising 20% of the population, a total sample of 900 households, or 4500 persons, was required in each area.

The crude mortality rate (CMR) for Chad was estimated to be 0.5 per 10 000 per day (based on CMR observed in these regions). Assuming a cumulative mortality of 2% of the total population for the period of interest (recall period contained between 51 days and 6 month) and a design effect of 4 [3], a sample size of 5000 in each area would result in a precision of 2% with 95% confidence.

The sampling among IDPs in Goz Beida included 4 clearly identifiable camps (Koloma, Koubigou, Gouroukoun and Gassiré). Population size was estimated using a combination of reports of community leaders, UNHCR data [4] and shelter counts. In Am Timan town, data were obtained from local authorities. For these two areas, clusters were randomly selected using global positioning system coordinates following cluster allocation proportional to the population size of the camps.

The sampling frame included all villages in Am Dam district that had more than 40 households. Population data were obtained from chiefs of villages, and adjusted using estimates made by the MSF exploratory mission and by local health workers. In the first stage of the survey, 30 clusters were assigned proportionally to village population size. In the second stage, households were selected using standard immunization program methods [5]. At the centre of the village, a team member spun a pen to randomly choose a direction in which to conduct the survey. All houses in that direction were listed, counting from the centre to the periphery of the cluster and the first house to be surveyed was chosen by randomly choosing a number on the list and selecting the corresponding house.

A household was defined as a group of people who usually live under the same roof and share meals. If more than one household was present in the same dwelling, one was randomly selected. If an adult member was not at home at the time of the survey, the survey team returned to the household later in the day. If there was still no adult present, the next household was chosen. Subsequent households were selected by proximity (the next nearest household).

We used a standardized, pre-tested questionnaire for data collection. This survey instrument was tested in a non surveyed area, including training performed over three days at each site. Each survey team included a community health worker, a local person who spoke Arabic and French, and a member of the expatriate MSF staff who acted as a supervisor. The questionnaire was in French and the questions were asked in Arabic. Surveys included anthropometric measurements, measles vaccination history and retrospective mortality data collection. Each cluster was completed in one working day.

At each site, crude mortality rate, mortality rate among children younger than 5 years, prevalence of wasting (weight-for-height z score <−2) and vaccination status among children aged 6 to 59 months were assessed using within the same survey design. Because ages of children were not recalled reliably, the target age range of 6 to 59 months was substituted as a height of at least 65 cm and less than 110 cm. A standard United Nations Children’s Fund (UNICEF) height board was used and children with a height of less than 85 cm were measured lying down. Weight was determined using a 25-kg Salter scale (UNICEF kit) that was calibrated daily. Acute malnutrition was defined according to standard weight-for-height z-score criteria or if there was pedal oedema.

A local event calendar was used to determine age and date of death. The total number of persons and children younger than 5 years present in each household was determined at the beginning of the survey in each site. Still births were counted neither as a live person nor a death. Neonates who had taken at least one breath after delivery were counted as dead.

The date most easily memorised among the surveyed populations was used to mark the beginning of the recall period. For Goz Beida and Am Dam, the celebration of the birth of the prophet Mohammed (Aïd el Mouloud) on March 30, 2007 was used, corresponding to a recall period of 51 days and 180 days, respectively. For Am Timan, the most applicable memorable date appeared to be the celebration of the beginning of the harvests on March 20, 2007, which gave a recall period of 207 days. Deaths in the household occurring among NDPs during the recall period were recorded. The calculation of the mortality rates was made using the current household census method. Inward migration to the sample households was assumed to be roughly equal to departures from those households. A series of structured questions were used to assign cause of death into categories based on World Health Organization case definitions [6]. Where corresponding local terms existed, such as diarrhoea, fever or malaria and respiratory tract infections, these were used to produce a less ambiguous classification. The questionnaire allowed other causes to be captured. Violence was not specifically asked about on the grounds that the surveyed areas were safe. Causes of death were recorded among NDPs but not among IDPs since a prospective mortality surveillance was scheduled in the camps.

Ethical Considerations

All of the organizations involved in the survey subscribed to the ethical principles outlined in the Declaration of Helsinki [7]. Districts Leaders and local Chiefs gave permission to conduct the survey. The interviewee was the most senior adult household member, who gave oral informed consent to participate in the study. For children aged 6 to 59 months, consent to anthropometric measurement was obtained from a parent or a guardian. No incentives were offered to study participants. No names were obtained or recorded except when respondents agreed to the referral of malnourished children or sick individuals to the relevant clinics.

Data were analysed using EpiInfo software, version 6.04b (Center for Disease Control and Prevention, Atlanta, Ga) which includes C Sample for determining ninety-five percent confidence intervals for cluster surveys.


Surveys were performed from May 21–26, 2007, in Goz Beida, from October 10–17, 2007, in Am Timan, and from October 21–25, 2007, in Am Dam district. We surveyed 898, 901 and 900 households in IDP camps, NDPs in villages and NDPs in a town respectively. One household (0.1%) refused to take part in the survey in Am Dam district. Adults were not present in their households on the day of the survey in 10 cases (1.1%). The main characteristics of the surveyed population are described in Table 1. Overall, the number of reported deaths over the recall period in Goz Beida, Am Dam district and Am Timan were 45, 27 and 28 respectively. Of these, 23 (51%), 13 (48%), and 13 (46%) respectively were in children younger than 5 years. Among the 4902 IDPs, 4477 NDPs living in a village and 4073 NDPs living in a town surveyed during the period of interest, the CMRs were 1.8 (95% CI, 1.2–2.8), 0.3 (95% CI, 0.2–0.4), 0.3 (95% CI, 0.2–0.5) per 10 000 per day respectively and the respective mortality rates for children younger than 5 years were 4.1 (95% CI, 2.1–7.7), 0.5 (95% CI, 0.3–0.9) and 0.7 (95% CI, 0.4–1.4) per 10 000 per day. Diarrhoea was reported to be the leading cause of death among NDPs (Table 2).

Table 1

Survey profiles and mortality rates by age group and location in Ouaddai and Salamat regions.
Table 2

Causes of death among the surveyed population.

Acute malnutrition among 904 IDP children, 956 village NDP children, 901 town NDP children aged 6 to 59 months were 20.6% (95% CI, 17.9%–23.3%), 16.4% (95% CI, 14.0%–18.8%) and 10.1% (95% CI, 8.1%–12.2%) respectively (Table 3). Reported measles vaccination coverage ranged from 18% to 76% (Table 3).

Table 3

Childhood malnutrition and measles vaccination history among children aged 6 to 59 months alive at survey time by Eastern Chad.


The prevalence of malnutrition was surprisingly high among NDPs living in villages, with more than 16% of children younger than 5 years being affected. This figure surpasses the 15% suggesting a very serious situation [8]. Our observation is even more alarming since the study was not performed at the peak season of acute malnutrition which is usually during the lean season (June to September) in similar areas of the Sahel [9][10]. However, comparisons with similar surveys carried out in the Sahelian zone should carefully be interpreted, since the effect of seasonality on malnutrition prevalence may differ from year to year, from country to country, and even from area to area [11]. Salamat region is considered the granary of Chad. The counter-season culture of berbere (a variety of sorghum) provides two harvests per year, creating a surplus that traditionally is exported to other regions including Ouaddai. This could explain the difference in the prevalence of malnutrition found between the two NDP populations. The 2006/2007 harvest was considered above average allowing exchanges of harvested cereals between the areas with surplus and those with shortages. Moreover, according to the National Rural Development Agency, productive rains were recorded in July and August, 2007, in the Sahelian zone of Chad. Producers were thus able to undertake agricultural activities. Despite this potential access to available food, several factors could explain our worrying results. Prices for food were higher than normal in the Ouaddai’s regional capital, Abeche [12] partly due to disruptions in trade because of insecurity and heavy rainfalls rendering roads impassable. In addition, certain crops were threatened by pests such as grain-eating birds, which reduced harvests in the affected areas.

This extremely precarious situation may have been worsened by the surrounding IDPs seeking for assistance from NDPs. Moreover, the stationing of military troops nearby at the time of the survey probably contributed to a reduction in the food supply in the markets.

While the town-dweller population remained at risk of malnutrition, malnutrition was well above the threshold of 15% among under 5 year-old children in the IDP camps. This finding is consistent with a previous survey from another Sahelian region conducted among displaced populations [13]. Similar surveys conducted in Eastern Chad over the last trimester of 2008 showed an acute malnutrition level above 10% among children under five [14]. Such repeated high rates at different times suggest that the malnutrition among displaced populations in this region is chronic in nature. The impact of seasonality is therefore probably milder than described for non displaced populations. Even if IDPs are sometimes allocated a small piece of land to grow crops, their food security mainly relies on external relief action. This observation underlines the humanitarian problem which needs to be addressed.

The CMR in the IDP camps was higher than the 1.0 per 10 000 per day that is recognized internationally as defining an emergency situation [8], [15] while the CMR among NDPs population remains low, and is even below the expected rate in sub-Saharan populations. The main diseases found among the surveyed population did not differ substantially from the typical causes of mortality in the Sahelian zone such as respiratory diseases, malaria and diarrhoea. The under 5-year mortality rate exceeded the 2 per 10 000 per day used as the emergency benchmark in the IDP population. Unfortunately, the causes of death were not recorded in this area but diarrhoea was recorded to be a major cause of consultation among children in the primary care clinics [16], reflecting the lack of hygiene and difficult access to drinking water. This precarious situation worsened when waterborne diseases such as hepatitis E arose in the camps [16]. This finding underlines the necessity of considering improvement of living conditions and sanitation as a priority when intervening in these populations.

Despite recent vaccination campaigns, the coverage of measles vaccination remained insufficient in IDP camps (76.2%) and among NDPs living in the town (40.0%). The alarmingly low coverage (18.1%) among NDPs of villages outlines the logistical difficulties of vaccinating in remote districts with hard-to-reach populations. In view of this inadequate coverage, humanitarian and governmental agencies should be aware of the risk of measles outbreaks not only in IDP camps but also in the surrounding NDP populations.

This survey has a number of limitations including recall bias, a well known limitation in such retrospective mortality surveys [17], [18]. Moreover, since the recall period was different among the studied populations, there could be differential recall bias, particularly in the cases of Am Timan and Am Dam where longer recall period were used. Under-reporting of deaths, or erroneous reporting of their date were more likely to occurred due to forgetfulness, and may have subsequently led to an underestimate of mortality rates among NDPs. Establishing causes of death using a verbal autopsy is always challenging (with the exception of violence) and makes the validity of such data uncertain. Nevertheless, the use of trained field teams, of a rather short recall period (<1 year), of unambiguous cause of death categories and of a well recognised calendar date should have limited them. Under-reporting of particular situations related to local customs (e.g. the death of a child before 7 days of life) may have led to an underestimate of the mortality rate. We can not exclude the possibility that some residents may have been mixed with NDP population in the camps (when they were relatives or where the residents may have be intentionally increased the stated size of the camps in order to increase the quantity of food distributed). The snapshot view given by a nutritional prevalence survey which provides a picture at one point in time only is another limitation. Such results are extremely useful for planning immediate activities, but may be more difficult to interpret for relief agencies trying to develop more long term and sustainable projects, particularly in such complex situations.

This observational study found a high mortality rate among the displaced population but also a high prevalence of wasting not confined to IDP camps but also evident in villages located in the same region. Although there is no evidence that the displaced people contributed to a deterioration in the situation of the residents, our findings underline the potential impact that a displaced population might have on food security and health status in an already fragile host population. We recommend that aid programmes conduct assessment of the local populations welcoming refugees or displaced people before intervention in order to address this issue. Nutritional status, mortality rates as well as health care facility and drinking water access should be evaluated in these assessments.


We greatly acknowledge the Médecins Sans Frontières staff and all the dedicated Chadian field workers and translators who assisted with this project. We thank Robin Bailey, MD, PhD, from the London School of Hygiene and Tropical Medicine for critically reviewing the manuscript.


Competing Interests: The authors have declared that no competing interests exist.

Funding: This research was funded entirely by Médecins sans Frontières-France and Médecins sans Frontières-Spain. The funders had no role in study design, data analysis, decision to publish, or preparation of the manuscript.


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Articles from PLoS ONE are provided here courtesy of Public Library of Science

Primary Pelvic Hydatid Cyst: A Case Report

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This is a case report of a young man who presented to us as a case of hypogastric pain and frequency of micturation. General physical examination and radiological evaluation confirmed a multiloculated pelvic swelling. Patient was subjected to laparotomy which confirmed the diagnosis of a primary pelvic hydatid disease. Patient was put on chemotherapy after surgery and is doing well on follow up.

1. Introduction

Hydatid disease is a zoonotic parasitic disease most frequently caused by echinococcus granulosus or echinococcus multilocularis. Echinococcus granulosus can reach any organ or tissue of the body where it develops into a small hydatid cyst [1]. The characteristic imaging findings have been described as calcification of the cyst wall, the presence of daughter cysts, or membrane detachment [2]. However the radiologic signs are often nonspecific. Serological tests may be helpful in the diagnosis, but even their reliability is not 100% [3]. Unusual sites of this disease can frequently cause diagnostic problems and lead to diagnostic delays and many potentially serious complications.

Peritoneal hydatidosis could be either primary or more frequently secondary to hydatid cysts in liver or rarely in spleen. Primary peritoneal hydatidosis is rare and has been reported to occur in only 2 percent of all abdominal hydatid disease cases [4]. We report a case of primary hydatid disease of the intraperitoneal pelvic space.

2. Case Report

A 23-year-old man presented with complaints of dull pain in hypogastric region and frequent micturition for the last 4 months. General physical examination of the patient was unremarkable. Abdominal examination was normal. Digital rectal examination revealed a large, smooth, symmetrical mass lying anterior to the rectum. Ultrasonography of abdomen revealed a large hypoechoic mass with echogenic septations in the pelvis posterior to the urinary bladder. Contrast-enhanced computerized tomogram (CECT) of abdomen and pelvis revealed a huge pelvic cyst 8 × 7 cm in diameter (Figure 1) lying between the urinary bladder and the rectum in the rectovesical pouch. Provisional diagnosis of primary pelvic hydatid disease was made, but hydatid serology was not suggestive of the disease. Radiological examination of chest (chest X-ray PA view) was normal. CECT of the chest is done in our setup only if chest X-ray shows a doubtful lesion in order to decrease the financial burden of the treatment. Exploratory laparotomy revealed a large hydatid cyst in the rectovesical pouch (Figure 2). There were no similar cystic masses in any other abdominal viscera (Figure 3). Cyst was completely excised without any spillage after packing the surrounding area with 1% cetrimide-soaked sponges. Final diagnosis was confirmed by pathological examination. Postoperative period was uneventful. Patient was put on 3 cycles of albendazole therapy; dose of the albendazole was adjusted according to the body weight of the patient. Each cycle of albendazole therapy was of one month duration. After each cycle patient was advised a holiday period of 2 weeks, and in that holiday period liver function and complete blood counts were assessed which in both holiday periods were normal, and subsequently 2nd and 3rd cycles were completed. This is a routine protocol in our department on all patients operated for hydatid cysts. I personally do not advocate laparoscopy in suspected lesions of hydatid disease because of the concern of spillage and it still is not a gold standard for such cysts. The histopathology confirmed it as a hydatid cyst caused by echinococcus granulosus. In spite of the fact that hydatid disease is quite common in our setup, we never encounter a hydatid disease secondary to echinococcus multilocularis.

Figure 1

CT showing a pelvic multiloculated hydatid cyst.
Figure 2

Intraoperative picture of a pelvic hydatid after complete mobilization.
Figure 3

CT showing no involvement of the liver.

3. Discussion

Hydatid disease or echinococcosis is a parasitic disease caused by infection with larva (metacestode) of the cestode echinococcus. Four species of the genus echinococcus are known to cause infection in humans: echinococcus granulosus (cystic hydatid disease), echinococcus multilocularis (alveolar hydatid disease), echinococcus vogeli, and echinococcus oligarthus (both causing polycystic hydatid disease) [5]. Echinococcus granulosus requires two hosts. Humans become accidental intermediate hosts. The most common site involved is the liver (59–75%), followed in frequency by lung (27%), kidney (3%), bone (1–4%), and brain (1-2%). Other sites such as the heart, spleen, pancreas, omentum, ovaries, parametrium, pelvis, thyroid, orbit, or retroperitoneum, and muscles are very rarely affected [6].

Peritoneal hydatid cyst, either primary or secondary, represents an uncommon but significant manifestation of the disease (approximately 13%). Intraperitoneal hydatid cysts are usually secondary to the rupture (spontaneous or accidental at surgery) of a primary hepatic, splenic, or mesenteric cyst [6]. A solitary cyst in the pelvic cavity can be considered primary only when no other cysts are present. In such a case, the hydatid embryo gains access to the pelvis by hematogenous or lymphatic route. Pelvic hydatid cysts usually present as a nonspecific mass with pressure effects on adjacent organs such as the rectum and urinary bladder. Rarely, they can cause obstructed labour, obstructive uropathy, and renal failure. Sometimes, they can rupture spontaneously [7]. Serology and imaging are the main tools for establishing diagnosis. Ultrasound is the preferred first-line imaging, but CECT gives more precise information regarding the morphology (size, location, neighbourhood, and number) of the cyst. Drug treatment with albendazole has been found to be successful in a proportion of cases, but drug therapy is generally not used as the primary treatment except in cases where the patient is not fit for surgery or the cyst size is smaller or deeply located. Surgery is the most effective treatment. Combination of preoperative albendazole therapy, surgery, and postoperative albendazole therapy is a useful regime. Albendazole suppresses the development of hydatid cysts following intraperitoneal inoculation of protoscolices [7]. En bloc resection without inducing rupture and spreading the daughter cyst is recommended treatment strategy and accepted to be curative for intramuscular hydatid disease [8, 9]. Partial cystectomy, however, is another commonly practiced modality of surgery where the surrounding adhesions or the removal of ectocyst is considered to do more harm than good.

Authors’ Contribution

F. Q. Parray, first and the corresponding author, worked up and operated upon the patient. S. N. Wani assisted and took all the clinical and radiological photographs. S.-ur-Rehman Khan diagnosed the patient radiologically. N. S. Malik looked for the literature and compiled the study.

Conflict of Interests

The authers declare that there is no conflict of interests.


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2. Pedrosa I, Saíz A, Arrazola J, Ferreirós J, Pedrosa CS. Hydatid disease: radiologic and pathologic features and complications. Radiographics. 2000;20(3):795–817. [PubMed]
3. Beggs I. The radiology of hydatid disease. The American Journal of Roentgenology. 1985;145(3):639–648. [PubMed]
4. Parray FQ, Gagloo MA, Bhat AH, Chowdri NA, Noor MM. Peritoneal hydatidosis. The Internet Journal of Surgery. 2007;9(2)
5. Khuroo MS. Hydatid disease: current status and recent advances. Annals of Saudi Medicine. 2002;22(1-2):56–64. [PubMed]
6. Yuksel M, Demirpolat G, Sever A, Bakaris S, Bulbuloglu E, Elmas N. Hydatid disease involving some rare locations in the body: a pictorial essay. The Korean Journal of Radiology. 2007;8(6):531–540. [PMC free article] [PubMed]
7. Seenu V, Misra MC, Tiwari SC, Jain R, Chandrashekhar C. Primary pelvic hydatid cyst presenting with obstructive uropathy and renal failure. Postgraduate Medical Journal. 1994;70(830):930–932. [PMC free article] [PubMed]
8. Parray FQ, Ahmad SZ, Sherwani AY, Chowdri NA, Wani KA. Primary paraspinal hydatid cyst: a rare presentation of echinococcosis. The International Journal of Surgery. 2010;8(5):404–406. [PubMed]
9. Arazi M, Erikoglu M, Odev K, Memik R, Ozdemir M. Primary echinococcus infestation of the bone and muscles. Clinical Orthopaedics and Related Research. 2005;(432):234–241. [PubMed]

Articles from Case Reports in Surgery are provided here courtesy of Hindawi Publishing Corporation

Business Models for Family Physicians – by, David Filhart

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Business Models for Family Physicians

By, David Filhart

Capstone Project

Davenport University

October 2014

Published in the Student Journal of Medicine: November, 2014

*Special thanks to Professor Dr. Timothy Delicath

for mentoring, editing, and suggestions.


Table of Contents



Table of Contents. 2

Abstract 3

Introduction.. 4

Secondary Research (Review of Literature). 9

Research methodology and design………………………………………………………………..……………….44

Data collection process…………………………………………………………………………………………………48

Data Analysis……………….……………………………………………………………..………………………………..52




Appendix ………………………………………………………………………………………..……………………………68



This project will closely analyze the different business models that are in play in the specialization of family medicine in the United States.  In this work, one will find that clear definitions and differentiations of the business models used in family medicine today are given.  With that, a careful look as to the various advantages and disadvantages are given herein.  Furthermore, an in-depth look into why there was a need to evolve and innovate from the traditional family medicine business model is looked into.  When examining this point there is analysis on the economic factors and other variables that came into play and which business models take care of each problem.  Also we examined which business models were the most viable and beneficial to the physician and the patient.  Specifically we looked at the happiness of the physician, the patient satisfaction, the annual income of the physician, and also their stress level.


Business Models for Family Physicians – by, David Filhart

As we examine the various business models for family physicians, the reader will come to recognize that they may come in many different varieties.  This paper examines why there are so many different business models in family medicine.  The reason that we are looking into this is because it seems that all physicians are playing with the same rules, yet they have so many different ways that they are playing within those rules.  Could there be a set of practices or an ultimate business model that would be more than satisfactory for all physicians?

We will also examine the different types of business models in detail so that we can try to understand this relatively new phenomenon as even today most of us are familiar and have the idea in our head of what and how a solo family physician would run their practice.  As we do this, we will look at the pros and cons of the different business models.  As we look into the various advantages and disadvantages of each business model, it is the hope of the author that this will also help to identify, define, and differentiate between the various business models for the reader.

We will also analyze the data that we received from first and second hand research.  The firsthand research was conducted through a variety of ways.  For instance, there were interviews conducted to the physicians via email, and also over the telephone, and finally face to face with the author.  The secondary research was gleaned from various scholarly articles that had been published and that the author of this paper thought was appropriate for this topic.  Finally we will synthesize the data that was gathered through the various methods to determine which business model would make the best business model for a family physician depending on a variety of factors such as their ultimate values and goals in practicing medicine and delivering excellent patient care.

Going through all of these stages of research and writing, our hope is that in this paper we will help students, physicians, and anyone else that is interested in the business models of family medicine to understand the different business models that are being used today.   As we do so, it is also the authors hope that this may possibly help to open the discussion as to what would be an even better business model in the future, that may not even be in existence today.


As there are many different ways to run a family physician to run a practice, it would be surprising to some to see the different and innovative ways that have evolved over the years.  This is due to the many different variables that the family physician is forced to deal with.  Having been exposed to many different ways that family physicians have as a business model, the author thought that it would be an interesting task to further research the various business models and to try to gather data that may help one to conclude the best set of practices that a family physician can use to be successful studies.

 Conducting the research by both first and secondhand sources has been really eye opening to the author as to the different business models those family physicians and other doctors are practicing.  It is the hope of the author is that an attempt to have synthesized the best parts here and that this will be beneficial and interesting to the reader, in such a way that there will be a better understanding not only to the difficulties that the family physician faces today, but also to some possible solutions to help these physicians.


The main objectives of this study are first to define and differentiate the different business models that family physicians are practicing in the United States today.  Another objective will be to understand why family physicians are looking at new and innovative ways to practice medicine as it relates to the business aspect.  Identifying the pros and cons of the various types of business models will also be an objective. The final objective is to help the reader to come to a conclusion of the viability of each business model.

Problem statement

The problem this study will address in particular are various and complex.  Because of different economic factors, various government laws and changing mandates Family physicians have been struggling to survive in the free market.  Other factors such as quality of patient care and time management have also been affected due to these factors. The family physicians have had to struggle to adapt their business model.  In order to stay in business, deliver quality healthcare, and to have a lifestyle by implementing new business practices that are more cutting edge than traditional the family physician in many cases is still struggling to survive in the healthcare industry today in the United States.  Finding the best business model for the family physician has been an ongoing process and is still up for debate (Goldberg, 2008).


Purpose of the Study

The purpose of this study is help the struggling family physician, and aspiring family physicians.  We will do this as we explore different business models.  This will better help us in order to identify a set of best practices.  A concomitant benefit will that this will also to help the reader to become better acquainted and familiar with the different business models that family physicians are using in the United States today.

 As this is done, hopefully the pros and cons of each respective model will be made clear, and the reader will be able to decide for themselves which business model, or combination thereof would be viable to them best suit their individual needs, wants, and style for their own preference.  Also, the reader will be able to see the why as to there being different business models for the family physician, any why they are continuing to evolve from traditional business models conventionally used in family practice.

            Finally, it is the author’s with that hopefully this paper may in some way help the reader to become inspired and to think of an even better business model for the family physician than what is presented herein, or what is currently being used today.

Research Questions

 When conducting the research, it was important to ask what the business model was exactly.  Also important was the why this business model would be necessary, and its viability in the real world.  What are the pros and cons of the various business models?  To go along with what was just said, what was it that the physicians in family medicine wanted to make them want to change the way that they practiced medicine?  Also, which practice was more beneficial, or what benefits did the patient see from the various business models?  Finally, what impact will each business model have on the lifestyle of the physicians?  When we attempt to answer these questions we will be able to solve the problem that family physicians are having today in their business practice as answering these questions will help us to identify the best and ideal set of practices that physicians can use, or are using today in their innovative business models.

Significance of the Study

For various reasons, family physicians have evolved and morphed the traditional and conventional business model into various forms (Goldberg, 2008).  This study will be significant insofar as it will help the reader to understand the different business models that the family physicians in the United States are practicing, and to further understand the pros and cons of each business model.


Literature review

In this section we will examine the various types of business models used by family physicians in the United States today.  We will also look at the advantages and disadvantages that each business model may present.  The way the research was organized was to give a brief overview of the business model.  After this we will examine why, and how this business model came about.  Next we will analyze the pros and the cons of the business model, as well as any other pertinent information that is useful to the reader.

Within each topic will be cited firsthand and secondhand research from personal surveys and researched literature respectively.  The different business models that will be examined are concierge medicine, the micro practice, the solo practice, the solo-solo practice, HMO’s, PPO’s, group practices, a traditional practice, health care homes,  and cash only practices, amongst any other variations.

Debra Goldberg put it well in her dissertation when she said that basically the external environment that many family medical practices face is so extremely complex.  Some of the variables that the family physician or practice has to deal with on a regular basis are the pressures and constant changes that come from regulatory sources.  Also an added pressure is the fact that reimbursement levels are decreasing instead of rising.  Another factor that is cumbersome for the family physician is having to deal with the changing of technology which seems to happen at a very rapid rate.  Finally, there is also a huge increase in patient and community expectations from their physician (Goldberg, 2008).

Concierge Medicine

To begin with, concierge medicine is gaining popularity in the field of family practice. Concierge medicine isn’t an entirely new idea in medicine however.  Although, the actual business model today is a bit different than it was fifty years ago (Hover, 2008).  It was interesting when talking to different physicians that are not in a concierge practice, that they would like to be in one and have thought about making the transition into a concierge practice. Needless to say, today’s definition of concierge medicine is different than the definition from yesteryear (Signature, 2013).

It is important to note, that in concierge medicine that there is a focus on preventative care.  This means that there is less hospitalization of the patients.  What is also great is that instead of a patient panel of say 3,000, most concierge physicians cap their practice at around 600 patients.  This definitely helps for better patient care.  This also helps to ease the stress of the physician.  This will not however help with the shortage of family practice physicians in the United States (Signature, 2013).

Concierge medicine is kind of like paying a physician a retainer fee in the legal world.  The fee that you pay can be a yearly amount that is spread over twelve months or in a lump sum, or whatever time table of payment is decided upon (Marshall, 2011). Originally concierge medicine was geared towards those with stratospheric incomes, now however, retainer fees at some practices have gone down and this has led to others with lower incomes to take advantage of and experience concierge service in medicine.

Concierge medicine is great for the patient if they really like the doctor, and they do not want to be inconvenienced by waiting more than a day for an appointment to see their physician.  The patient also is usually guaranteed more time in this type of business model with the physician.  This is especially appealing to patient who would like thirty minutes to an hour with their physician (Markiewicz, 2014).

Some of the reasons why concierge medicine became a popular niche in medicine are because a lot of physicians felt like they were seeing a huge number of patients, and not spending a lot of time with them.  For example, a physician could be booked with over twenty patients a day.  Oftentimes seeing 24 patients in a work day is the goal.  Sometimes this can average out to seeing a patient for 7-9 minutes maximum.  As one can empathize, it would be very advantageous to have such a schedule where you can see about a quarter or a third of the patients, and also be able to spend thirty minutes to an hour with them.  Not only would this be great for the patient, but it would be great for the physician, and this would equate to a mutually beneficial relationship and ultimately equate to phenomenal patient health care.

On the patient’s perspective, they often felt like they were paying too much for their healthcare and not getting enough time with the physician, and or the physician seemed rushed.  Another reason is because some people elected to pay for concierge medicine instead of having to deal with the hassle and cost of insurance, and concierge medicine allowed the patient a way to save money.  The patient would be able to save money with concierge medicine if they were to be able to pay less to the physician for their subscriber fee than to their insurance company premium.

There are many different variations of the concierge business model.  One thing that they all have in common is the fact that the patient has to pay a subscriber fee to the physician.  Usually the fee will ensure that the patient has 24/7 access to a physician. It usually also means that when a patient and a physician are in a concierge agreement, that the physician will have allotted at least an hour per patient visit.  In many instances the physician may actually then charge more to the patient if the allotted one hour visit with the physician is over for the month and then the physician may charge a fee by the minute for every minute that goes over the hour.

As stated earlier, the way a concierge practice is set up allows for the physician to accept an annual fee from the patient, for example.  This fee will cover whatever the physician and patient decide.  It could just be a fee for the patient to be accepted into the practice.  The fee might also cover the actual visit.  Sometimes the fee may even cover medications.  This is entirely up to the physician, and the patient.  The great thing about the retainer fee, for the physician and the patient, is that this allows the physician the luxury of seeing the patient for a longer visit instead of the rushed ten minute visit.

Most patients that can afford to pay for concierge medicine, also do keep their insurance for other reasons such as surgeries, or if they have to see a specialist.  Depending on the insurance the patient has, the medications may also be covered by the insurance, and even reimburse the physician on top of the subscriber fee that the patient pays to be a part of the concierge practice.  The concierge fee or subscriber fee is never covered by the insurance company however.

This translates into the physician only needing to see so many patients a day to make ends meet, which would be a fraction of what they were seeing, because they have the retainer fee coming in regularly.  For example, usually a healthy practice has around 2500 patients.  In concierge medicine, often the practice caps off the patient load at only 600 patients.

On a daily basis, a physician practicing concierge medicine may see 6 to 10 patients a day.  They also spend as much as thirty minutes to a half of an hour with each patient.  Elderly patients especially appreciate this as they are often managing multiple issues or problems with their health.  Oftentimes the patient, especially the elderly patient, has a caretaker that comes along with them to appointments.

The bringing of an additional caretaker can extend the meeting time with the patient as the caretaker is another person with information and who often expresses what the patient needs to, or at least prods the patient into saying what they should say if the patient does not remember or perhaps does not necessarily want to discuss a particular problem due to embarrassment or preference personally.  Concierge medicine is great for these types of patients as the doctor is not worried about the time constraints that may come if he or she had to see thirty patients a day.  Furthermore the caretaker and the patient do not feel they are imposing on the physician when they go in for a doctor visit.

The pros of a concierge practice are that the physician can see fewer patients in a day, and also see the patient for a longer duration of appointment.  This means that the work load will be a lot less, which equals more personal time for the physician to do other activities such as recreation or family time if they choose it.  At the very least, this is an option that is very inviting for a lot of physicians (Growth, 2014).

As far as the patient is concerned, the patient gets to get in to see the physician quicker, usually the same day that they call, and for a longer period of time.  Also, for the physician, there is a steady stream of income no matter how many patients they see, or do not see.  This type of business model also translates to less workload for the office staff.   Because there are less patients to manage for the practice, the workload is also lessened for the staff.

Some of the cons to concierge medicine are that the practice needs to have subscribers, and it could take time to get subscribers to this system.  Another con is that it may be more difficult for a physician to take time off as the patient will most likely expect service from their physician that they are retaining as opposed to a mid-level health provider such as a physician’s assistant or a nurse practitioner.

Sometimes it can be very difficult for a physician to get subscribers to their plan.  This is especially true because most patients are not accustomed to paying a subscriber fee for their healthcare, and perhaps do not want to, especially if they are already paying for big premiums in health insurance (Growth, 2014).

Most patients that are paying for concierge service want to make sure that they see their physician that they are paying for, and no one else.  Another con is that the physician may not feel comfortable asking their patients for a subscriber fee.  However, it may be surprising to the physician how many patients are willing to pay to be a subscriber to a concierge practice if the quality of care is increased.

Another difficulty a physician may have when transitioning to concierge medicine is which consulting company they would like to work with.  There are a variety of concierge consulting companies that will help the physician to make the transition to concierge.  Depending on a variety of factors the physician may want to use one concierge consulting company over the other as some have policies that allow for the physician to be more autonomous and more personalization in designing their concierge practice (Growth, 2014).

Solo-solo Practice

 A solo-solo practice is one where the physician is the only actual person working at the practice.  In other words, there is no insurance specialist, and there is not receptionist.  That means that the physician is dealing with the insurance company and they are answering their own phone.  This also means that there is no medical assistant to take the blood pressure or to handle the urine sample of the patients.  The physician answers their own phone, runs the EKG’s, takes care of the billing, etc.  This can be a very difficult way to practice for these very reasons.  A physician working for a big corporation has an administrative team that takes care of the hiring and firing.  They also probably have a department for billing.  In corporate medicine the physician does not clean the toilets or take out the garbage, but in a solo-solo practice the person that is cleaning the toilets and taking out the trash is the physician.  It is easy to see how one could lower the overhead by a solo-solo practice, but then one has to consider the opportunity cost that comes from having to do things like cleaning the toilets and taking out the trash, while the could be seeing patients and actually making money.  In other words, the main way to make money as a physician in family practice is to see patients.  This is the physicians core competency.  However, if they are busy doing other things like taking out the trash, then they are in essence losing money.

Sometimes certain tasks are outsourced to other entities.  For example the billing for a medical practice could be outsourced to another company for a nominal fee.  The billing can be very difficult to handle as this can be very time consuming and a tedious task having to deal with insurance companies and the like.  In other words the physician is the only person running the practice and performing all of the duties, save it be running the labs which are also usually outsourced, although the physician is still having to draw the blood from the patients if need be.

A physician may choose to have a solo practice because they want control of their whole practice.  Another reason why a physician would choose a solo practice is because the overhead will be cut down by a lot if they do not have to pay for other employees, such as the receptionist, billing department, medical assistant, nurse, phlebotomist, etc.  The physician may not want to deal with any other staff.

A patient may decide to go to a physician who has a solo practice because they feel that this helps them to have more confidentiality in their health care between their physician and themselves.  Also they may choose to see a solo practice physician because it may seem to be more personable to them as a physician running a solo practice has less of a patient load as they can only see so many patients in a day.  A patient may also find that it is easier to set up an appointment to see a solo family physician because of the lower patient load.

Usually, the way a solo practice is set up is self-explanatory.  They are usually run from the physician’s home.  However, some are also run from a small office.  With the advent of various technologies it is quite possible for a physician to take on all of the tasks that it takes to run an office.  For example, the physician may not have to spend time answering phones and setting appointments as appointments can be set up online and confirmations can be automated by email or telephone.

Some physicians don’t mind answering their own phone, and even go so far as to make their cellular  phone number available to the patients  Also, tasks like taking blood pressure can also be automated as there are electronic blood pressure cuffs that are very accurate and can be done as the physician is taking the history of the patient.  These are just a few of the things that physicians in family medicine are doing today that may seem atypical to the traditional family medical practice.

The pros of a solo practice are that you do not have to deal with any office politics.  This is especially nice if you are more introverted and does not care to make small talk with the staff.  Another plus about not having staff is that you do not have to spend the time or the resources to have to train them.  The physician also does not have to solve problems that can arise from personality conflicts that may arise between co-workers.  The physician also does not have to supervise or be a task manager for any other person except for themselves.  Also, the overhead is a lot lower due to the lack of staff or employees.

Because you are responsible for doing everything, this may be nice as there will not be any monotony and you will always be busy doing something, from billing, cleaning, replying to emails, and marketing.   Another plus is that if the practice fails, there is no one to blame it on except for you.

Some of the cons are that there is no one to substitute for you, for example, if you need to take time off.  You are the only employee.  Also, you have to do all of the work.  This means everything.  A lot of the things some physicians would feel are beneath them after all of their hard work in school.  Also, all of these other tasks can take away from the big money maker which is seeing patients.  Having to do a bunch of other tasks may cut into the time available for actually seeing patients. Another con is that if the practice fails, you only have yourself to blame (also see pros).

Many solo practice models are what is used in small towns because there is less competition from corporations.  Also the small town doctor may choose this practice model in a rural setting because the physician is actually the right fit for this type of lifestyle and environment as it takes a certain type of physician personality to make it in a solo practice in a rural area as evidenced by the high turnover of family physicians in rural areas in the United States (Stucke, 2009).  In fact, in states like Florida, the family physician solo practice has fallen from sixty-nine percent to just over forty percent (Bryant, 1998).

An entity that is really putting a strain also on the solo practice is that of the managed care practice.  That is what health maintenance organizations are.  These organizations are forcing solo practice physicians out of business because insurance companies give them contracts with a lot of patients, and the patients are charged less as there is a volume discount to be in the HMO or the PPO. This is in turn making it very difficult for the solo family physician as they are losing patients to the HMO’s and the PPO’s and they do not have the negating power of a large group to deal with the negotiation of the contract that would come if physicians banded together into a group.  So this means that the intimate care of patients that has been practiced for centuries in the traditional solo physician family practice is becoming extinct in a lot of ways.  This then means that patient care is becoming less intimate and more managed by a team of physicians or a health care team.  Some argue that for this reason managed care is better than solo practice care as far as the quality of healthcare that the patient gets is concerned (Bryant, 1998).

On the other hand, one study suggests that the productivity of the physician is much more for a physician in solo practice as opposed to a physician that is working for a managed health care team.  This is kind of like saying that competition between the two models is give and take as one has strengths where the other has weaknesses (Bryant, 1998).

Micro Practice

A micro practice is very similar to a solo-solo  practice, with the main difference that of being a physician who is in a micro practice will often have at least one other staff member, usually a receptionist/medical assistant.  This is so the physician will not have to answer their own phones, draw labs, or take vital signs. These are just a few of the unique tasks and practices that you will see a physician in a micro practice perform (Guglielmo, 2006).

A physician in Portland named Dr. Ott said that she did a lot of research before she actually switched to the micro practice from a more traditional practice in the year 2008.  Before Dr. Ott did this however, she, ultimately realized that even though her overhead would be low, and the stress level would be low, that she would indeed have more responsibilities that she did not worry about before, like the cleaning of the building, collections, insurance negotiations, and other responsibilities that are usually delegated to other people in a larger practice or group setting (Hands, 2011).

The reason that a physician may want to have a micro-practice is because they want to cut the costs of having a lot of employees, while at the same time keeping someone on that can do a lot of other tasks, thus allowing the physician to focus more on the medical side of the office.  Virtually every other aspect of a micro practice is similar to that of a solo-solo practice.  Although there is a crisis in family medicine due to the shortage, it has been said that the micro practice will not help to alleviate this in any way because they usually see less patients per practice (Davis, 2008).

To go back to Dr. Ott, it is interesting to note that since the six years that she started her micro practice, and taking on doing everything, that she let herself have a little bit of help. Although she is still considered a micro practice, she allowed for help in the cleaning department, as well as some billing, and an answering service (Hands, 2011).

Physicians that practice medicine in the micro practice model seem to be very happy (Happy, 2011).  They really seem to enjoy the interaction with the patients and the flexibility to make their own hours.  This is probably due to the less stress they feel with the lower overhead costs.  Also contributing to their happiness is the sense of owning their very own practice (Happy, 2011).

Even though on average they get paid less, they are also under less stress, and usually feel that this trade-off is well worth it. In fact, in a recent article, it was found that because of the less overhead, and the stresses that come with a larger staff, and running a larger organization, that this actually equates to more fulfilling practice for the physician as they do not have to worry about the things that are not related to patient care (Jespersen, 2006).

In addition to this the patients also enjoy going to a micro practice.  This could very well be because they feel that they are getting quality care for their money.  This is because the patient gets to spend more time with the physician.  This could also be because the patient is in an environment that seems more warm and friendly, due to the atmosphere (Kerr, 2007).

In a recent article published by the Morning Sentinel, it follows a physician who worked in corporate medicine for a long time.  The physician stated that she was secure in her corporate life, but then saw that there was a different way to practice in an article that she had read.  This physician decided to start a micro practice.  One of the patients that was seeing this new physician stated how she was especially surprised to find that she could get into the practice without a long wait.  One of the previous family physicians that she called said that she would have to wait for three to four months for an appointment, whereas the physician that was practicing in the new micro practice accepted the patient that day.  This really made the patient satisfied.

What was even more satisfying for the patient however, was that the physician from the micro practice was able to direct the ill patient to the necessary specialists that were needed to get the patient back in good health.  The patient felt that, after she got healthy again, that she did not want to bother the micro practice doctor, but to her surprise, the doctor called her to follow up and see how she was doing.  This really made the patient happy, and the patient came to the realization that the doctor did want to hear from her (Jespersen, 2006).

Many physicians describe the frustration that they have to spend so much time doing paperwork that they feel is unnecessary.  So, this makes sense also because the less paperwork there is to do, the less stress there will be, and furthermore this could mean more time with patients, and it usually does (Lactis, 2008).  For all of these reasons it seems that the combination makes it much more of a pleasurable experience for the patient to go to a physician that practices in the micro practice business model in the United States (Painter, 2006).

Traditional Solo-Practice

  A more traditional solo practice is where a physician has a full staff, consisting of a medical assistant, who would take the vital signs and bring the patient back.  There may also be a receptionist that works the phones and greets the patients.  There may also be an insurance and or billing specialist. Also, there may be a person or a department for marketing.   Finally, there may be an office manager who helps to make sure all of the pieces are running smoothly and that can supervise all of the office workers.  There can be of course many variations of the way an office is set up, however this is the most conventional way (Practice, 2011).

The office manager in a traditional solo practice helps they physician to be able to take care the patient care and also to let the physician know of any problems or concerns that may arise in the day to day business of the practice.  An office manager can also serve as a liaison between the staff and the physician.   All of these tasks may also be combined, shared, or overlapped with other responsibilities and duties that are necessary to run a smooth office.

In addition to the office staff, a physician may elect to have a number of mid-level providers such as nurse practitioners and or physician’s assistants. The mid-level health providers can be an excellent source of revenue as they can see patients on behalf of the physician.  This can increase the amount of patients that a practice sees in a day.  This can also add quite a bit to the revenue stream of the practice as well as the profitability of the said practice (Journal, 2004).

A physician may elect to be in a solo practice because they like things done their way (Beaulieu-Volk, 2014).  They also enjoy having the appendages of an office staff and or mid-level health providers to keep the practice running smoothly.  The traditional solo physician has their independence, as well as a team to help the practice.

Some of the pros of having a traditional solo practice are that of enjoying the camaraderie of the office staff.  This can be like a team with the purpose of the team being to provide excellent patient care (Bryant, 1998).  This can in turn have a synergistic effect and increase the positive energy of the office.  Another pro is that the physician can delegate certain responsibilities and duties to the staff as they may deem necessary.

Additionally, depending on the state laws, the physician with mid-level health providers may be able to be out of the office while the nurse practitioner or the physician’s assistant is seeing patients.  This would allow for the physician to be more flexible in taking time off for whatever reason they may have.  However in some states the physician does need to be in close proximity to the practice, even in the building, when managing mid-level health providers.

Another important pro in being a traditional solo practice is that the physician is independent.  They are independent from the policies and rules that are outlined by administration.  They also do not have to deal with being treated with disrespect from the any administration and do not have to worry about getting written up or being evaluated every few months.  The physician also does not have to worry about getting their pay docked if they do not see a certain number of patients.  This type of practice can be a huge reduction of stress if the physician is not up to dealing with administration looking over their shoulder (W______, personal communication, October 5, 2014).

In a traditional solo practice the physician is the one who gets to call the shots on how they want the practice to be run.  They have no other supervisor.  They have no other partner or partners that they have to deal with, or to consult.  When there is a decision to be made, or a change needs to be made, the physician can decide what they feel is best and executes their vision.  The physician is ultimately the head boss, unless the physician has a wife, then she is the head boss.

Even though many of these advantages are great, the disadvantages of a solo practice can also be great.  For example, there is a family medicine doctor that is said to not even be able to give away his practice (Gardiner, 2011). This is a huge disadvantage, especially if the physician was banking on the sale of the practice for money to place towards retirement.

Due to the ever competitive medical field, with corporate medicine being the stiffest competition, it is very difficult for a solo practice to survive (Girion, 2008).  With that being said however, with the advent of new technology and the costs coming down from such, many physicians in solo practice are taking advantage of this.  The technology that is available today is actually giving a lot of family physicians a chance whereas if they did not have this they could be in even more trouble economically than they are now (Naik, 2007).

In a recent article that was referred to earlier, we learn of a family practice physician that could not even give his practice away (Gardliner, 2011).  We learn that this family physician is in a predicament that many solo practice family physicians are in.  The article argues that quite possibly this type of medical business model will soon become extinct due to the mandates that are forcing this way of practicing medicine very difficult and some may say obsolete.

The article follows Dr. Sroka, who himself employs the equivalent of five full time employees.  In order for Dr. Sroka to make a profit, he needs to see four patients an hour.  If Dr. Sroka only sees three patients an hour he will just barely break even.  The Doctor works long hours.  Many of his patients he has had for over thirty years.  One year he made over three hundred thousand dollars, and this year he will be lucky if he makes over one hundred thousand dollars.  The reason why he can’t give away his practice which boasts about four thousand patients is because he is working so hard for so little money (Gardiner, 2011).

Most new physicians that may be looking to buy a practice are burdened with a lot of debt and also want a lifestyle.  In the article it states that over half of the family physicians coming out of residency are women.  These female physicians as it is stated in the article that they preferred or wanted the weekends off, the ability to go to their kids soccer games, and want to go shopping and enjoy life while paying off their student debts.  This dream is virtually impossible if they were to buy Dr. Sroka’s practice (Gardiner, 2011).

Dr. Sroka’s son says that he feels that his dad is just going to lose it one of these days as there are new mandates that come out all of the time that he just can’t keep up with.  One example of this is the electronic medical record which Dr. Sroka may not even be able to afford, or let alone have the desire to learn how to use so late in his career (Gardiner, 2011).

Group Practice

 Although the official definition from Medicare and Medicaid for a group practice is 25 or more physicians together, for the purposes of this paper, and what is known and what actually makes sense and is used in the real business world, we will not be using that definition here (Lee, 2013).

A group practice is a medical practice where there is more than one physician in the practice.  This can range from two physicians to very large groups of over eighty physicians.  They are also fully staffed in the office and may utilize mid-level health care providers to help bring in more revenue and profitability to the practice.

A physician may choose to be in a group practice because of the various advantages. One major advantage is being able to rotate being on-call.  This is very hard if the physician is solo, and a solo physician may feel tied to the practice.  Physicians in a group practice can also cover for each other when they are going on vacation or emergencies.

The phrase power in numbers definitely rings true here in the group practice.  This is because the group of physicians will have increased bargaining power when working with and negotiating contracts with the insurance companies.  There is also usually more structure as far as vacations and people that are willing and able to cover for you when you are on vacation.

Being in a group practice can come in various forms.  Usually, there are a set of standards or guidelines that must be adhered to in order to be a part of the group.  For example, some of the mandated polices could reflect the hours of operation, or standard procedures.  Group practices come in all different shapes and sizes.  The autonomy of the physician can also vary by degrees depending on the group.  Some group practices will recruit physicians and they will staff the office and even the building to the physician.

This is because often times, resources are pooled to help the physicians in their practice.  For example, a certain percentage of the budget may go to advertising and marketing for the physicians in the group. This would obviously benefit all of the physicians that practice under the group’s banner.  Also, when physicians are part of a group, they often refer patients to other physicians in the group.  This is also mutually beneficial between the physicians in the group as this helps to keep patients coming through the doors.

Some disadvantages of being in a group are the loss of some control over the way that you would want the practice set up.  For example, the physician may not be in charge of hiring staff, and may be stuck with whoever is assigned to the office.  This may prove to be difficult as certain personalities can clash.  Also, the person that is hired for the job may not be performing as well as a physician would want, but not bad enough to get fired, and there really would not be much the physician could do about it.  This is only in some cases, like there are many different variations of the group practice.

Depending on the deal made with the group, there may be certain criteria and quotas that need to be met in order for the physician to be a part of the group.  For example the physician may have to see so many patients a day in order to receive a quarterly bonus.  This is because oftentimes resources are pooled to help the physicians in their practice, so everyone has to pull their weight.  This could add a lot of extra stress to the physician.  For example, a certain percentage of the budget may go to advertising and marketing for the physicians in the group. This would obviously benefit all of the physicians that practice under the group’s banner.  Also, when physicians are part of a group, they often refer patients to other physicians in the group.  This is also mutually beneficial between the physicians in the group as this helps to keep patients coming through the doors.

Another disadvantage would be is having to deal with any negative repercussions that could come if there was a physician or controversial scandal that occurred that would tarnish the brand equity of the group’s name.  This is because things that happen under the group name could negatively impact you as a physician as your name would be associated with it.  This may be a rare incidence, but it does happen unfortunately. This would be very frustrating if you were an ethical physician, to have your name associated with something that you may have had nothing to do with.

Another situation that may be difficult to deal with in a group would be the hassle of making changes.  For example, if there was a certain electronic medical record that the group was using, but that the physician did not like for some reason or the other, the physician may end up being stuck with that software and be irritated by it on a daily basis.  This could be frustrating in the form of the Electro cardiogram machine that is used, or to the company that is contracted to run the labs, the insurance companies that the group decides to accept or reject, and to any other policy and procedure that is agreed upon in the group.  This may be the case if the group thinks that they could save money by using one type or brand of equipment, and another physician may not be satisfied with its performance.  Furthermore, if the equipment were not as good as they thought, and they spent a lot of money on the equipment, then the group would have wasted a lot of money and the frustration and the morale of the physicians and employees would go down, but the physician would almost be stuck as they would be under contract.

Another big disadvantage would be that when a person or a physician signs a contract or becomes a part of a group, there is usually a non-compete clause in the agreement.  This means that if as a physician you become fed up with the group, and decide to leave, you may not be able to practice in the same location, within a certain radius of any of the physicians in the group, and you would not be able to have your patients follow you.  This could be very difficult for the physician that has roots in the area in which they live, or possibly have children that are integrated into the community, church, or school.  Another difficulty would be the consideration of the spouse and what they would want to do.

This would mean that you would have to wait out your no compete clause and or move to another location and start all over.  This would be indeed very difficult as it can take a lot of time and effort to build a practice.  Because of this the physician may decide to stay with the group even though it is frustrating and difficult, thus making life somewhat miserable when it comes to practicing medicine and working (Editors, 2009).  The larger the medical group, the more difficult it may be to get things done as far as change is concerned as this usually means more channels and red tape to deal with.


Medical Home Practice

This is a unique niche in the medical world that has actually been around since the 1960’s (Business, 2011).  In this business model, the physician basically runs the medical home, and the medical home is a place where people can go for all of their health care needs from cradle to grave.  So a patient could come in to see their family physician, and if they needed to see a specialist, the specialist would be available in the same location.  To be clear, there is a team of medical health care providers that are able to communicate with each other, and communicate with the patient.  This is a great business model for the patient especially if they want a one stop type of shop for their healthcare.  This is really great for the physician as communication between colleagues is much easier as they are in close proximity to one another.

The advantage of this type of practice is that the patient will, in theory, be better taken care of because of the effective channels of communication that are in close proximity.  This is good for the patients of a family physician as the health care team will be working close together for the benefit of the patient.

One major disadvantage of the medical home business model is that it has been found to be more expensive to run than most other medical practice models.  This would most likely equate to less money being taken home by the family physician.  This would also equate to less money for everyone working in the medical home.  For this reason it seems that the medical home has been stagnant as far as growth is concerned, especially when comparing it to new and trendier business models for the family physician such as the micro-practice.

Preferred Provider Organization

Otherwise known as a PPO, this type of health organization is good for the patient that does not necessarily want all of their care coordinated through the primary care physician.  In other words, if a patient wanted to see a specialist like a dermatologist, the patient could do that if the dermatologist that they went to see was in the preferred provider organization.  The patient would not a referral from another physician first in order to get a referral.

For the physician, being a part of this organization may be good as the subscribers would have you as an option should they choose to use your services.  For example, if a patient does want to go to a family physician, and you are a member of the PPO, or under contract by them, then the patient would see your name on the list and possibly choose you as a physician (Bayley, 1998).

Another advantage for the family physician that is a part of the Preferred Provider Organization would be that, similar to a group practice, the team infrastructure would be there and because there is usually a large group of physicians that are contracted with the Preferred provider organization, there is bargaining power in this.

Some of the disadvantages would be that what would come with being a part of any large organization, which would be for example, having to deal with administration, personalities, policies, and other nonsense that one may not find in a smaller situation.  For example, a physician may have to see so many patients a month to fulfill a quota.  Furthermore, the physician may be told how to practice medicine.

To amplify this, let’s take for example, if the physician feels that a certain test is necessary, the preferred provider organization may ultimately say no and request another procedure be in effect first.  This would either be to save the preferred provider organization money, or to make the organization money. This ultimately helps the bottom line of the PPO.

If a physician feels that a patient needs a particular treatment, this could be very frustrating for a physician that feels that for the best interest of the patient that something else needs to be accomplished for that patient’s benefit, and yet it is rejected by the PPO.   It is incredibly interesting that some articles have stated that PPO’s are actually really popular amongst patients (Hurley, 2004).  This could be because the patient enjoys the ability to be able to go to a specialist without having to get a referral from a family physician.  The way that PPO’s keep this type of health care costs down is by offering the physician a bonus for keeping the costs of healthcare low and by practicing conservative medicine (Hurley, 2004).

Health Maintenance Organization

Otherwise known as an HMO, it is similar to a preferred care provider in the sense that the family physician will be a part of a network of physicians in this organization (McBride, 1995).  One of the main differences between a health maintenance organization and a preferred provider organization is that in the health maintenance organization the patient cannot just see any physician in any specialty that they want without a referral, even if the specialist is in the organization (Bayley, 1998).

In a health maintenance organization, the patient must first go to their primary care provider, which could be the family physician that is listed as a provider in the health maintenance organization.  If the primary care physician sees that the patient needs to go to a specialist, the physician will then make a referral to the specialist that is in the health maintenance organization.  In other words, all referrals have to go through the primary care physician first, which in a lot of cases would be the family physician.

It is argued by health maintenance organizations that this type of business model actually saves a lot of money for healthcare.  Health maintenance organizations argue that a lot of unnecessary procedures and services are avoided by this as much can be handled by the family physician instead of the premiums that are paid for seeing a specialist (Bayley, 1998).  This can be especially frustrating to the patient however, especially if a patient really believes that they need to see a specialist and their primary care physician has a different opinion.

All of the rest of the advantages and disadvantages would probably be similar in a health maintenance organization then they are for the preferred provider organization for the physician as far as dealing with administration and policies and procedures.  Although there is a certain amount of security that comes with working in a big organization, such as the luxury of working with other physicians and health care providers on a health care team, it definitely comes with a price.  One of those prices is physician autonomy.

It seems that physicians that work for health maintenance organizations are the most dissatisfied with their work.  In fact, they often fee overworked, and underpaid.  It has been said that in one article that they feel powerless and undervalued.  This article stated that out of the 24 physicians that were working for the health maintenance organization that they had a huge concern and that was of coping with their frustrations.

An advocate for the physicians stated that it was imperative to make sure that the physicians felt valued and also that a sense of autonomy in practicing medicine was also restored to them in order to ensure their well-being (Healthcare, 2004).  This would be very important for the health maintenance organization to do if they wanted to keep their physicians happy and for them to have longevity in their career.  One could only empathize how frustrating this could be, especially after having struggled and gone through all of the work it takes to become a physician, to be not happy with your work.

Cash Only Practice

A cash only practice is a business model that is being increasingly popular although it accounts for a small percentage of medical practices today.  In a cash only practice, the patient pays the physician directly.  In other words, the physician does not receive any money from insurance companies or any other organization (Castens, 2009).  The patient either pays with cash, check, or credit card.

A lot of times, when a physician has what is referred to as the cash only practice, they will give the receipt to the patient.  This receipt that the patient is given will have the proper billing codes on it.  What the patient can do with these billing codes on the receipt is take that and present it to their insurance company if they have one and get reimbursed by them (Chen, 2010). This practice saves the physician and their practice the time and resources that it takes trying to fight with the insurance companies in order to get reimbursed by them.

The advantages of having a cash only practice is that for the physician, they get paid immediately. They also do not have to deal with insurance companies that are notorious for not paying physicians.   They may not do this if they feel that a procedure is not necessary.  Also, insurance companies have been known to change their policies, so that if a policy is proper one month, it may not be proper the next month, thus causing a headache for the physician and their billing department.

Needless to say, not having to deal with insurance companies in a cash-only business model is a great relief for family physicians.  In fact, it has been said that insurance companies are so hard to deal with, and physicians are so frustrated with dealing with insurance companies, that the cash-only business model was born out of that frustration.

It is interesting how out of adversity sometimes the need to overcome them gives us creative solutions, as was the case for cash-only practices.  Another positive is that physicians and patients alike are coming to the conclusion that there is actually a mutually beneficial relationship that can be had between a patient and the physician without health insurance companies meddling in their business (Wlazelek, 2008).

Some of the advantages to the patient is that sometimes paying the physician directly for services is cheaper than actually having to pay premiums to their insurance every month.  The case may be that paying the physician for services may actually be cheaper than even paying their copay that the patient has to pay on top of their monthly premium (J. Fortes, personal communication, September 15, 2014).  This would be a great choice for a patient and a physician as the hassle of dealing with the insurance company is out of the equation.  Furthermore, insurance companies often charge or bill way more than a cash-only practice does.

The disadvantages of a cash only practice are that some people do not have the cash to pay for services, such as Medicaid patients.  This could dramatically decrease the number of potential patients that a physician may have available to them. This can definitely be a reason why some cash-only practices fail (Frank, 2008).

One interesting aspect of the cash-only practice model is that this can actually help the uninsured.  Some practices make it very difficult to see patients with no insurance.  However, the practices that are not dependent on insurance, and can lower their prices, are actually places where those that are uninsured may afford to go.  For example, a group of Texas physicians designed a cash only practice to specifically go after the uninsured patient demographic (Shinkman, 2014).

This business model of the cash-only practice really helped the people as they could not afford health insurance, or because the people felt that the insurance company was ripping them off.  When the word got out that there were physicians that were seeing patients without insurance for a reasonable price the people without insurance were glad to go to the cash-only medical practice that were affordable with a great quality of care (Shinkman, 2014).

One interesting example of the cash-only model is by a practice called Medical Associates of Lehigh Valley.  This group of physicians served approximately 100,000 patients.  The group became increasingly frustrated with dealing with the different insurance agencies as they would each have a different set of guidelines for the physicians to follow.  To add to this frustration, the guidelines are constantly changing.  So, for example, if a medication is covered by the insurance company to treat a diabetic patient one month, well, three months later on a follow up visit the same medication may not be covered so the patient has to switch prescriptions.  The insurance companies will do this without notifying the physician (Wlazelek, 2008).

This practice by the insurance companies would be especially frustrating if the physician and the patient know that the medication that was approved actually worked well for the patient, and now do to insurance constraints has to switch.  Medical Associates of Lehigh Valley figures that they can reduce the hassle of dealing with the health insurance companies by charging the patient and letting the patient seek reimbursement from their insurance company for either all or part of the fee.  This will cut costs as the Medical Associates of Lehigh Valley will not have to worry about a billing department, and will also not have to spend hours on the phone with the insurance companies arguing for reimbursement for proper patient care (Wlazelek, 2008).


Research Methodology and Design

As the author contemplated and pondered what would be the best method for gathering primary research and information, it was concluded that a set of direct and open ended questions would be the best way to find out from the actual physicians themselves about their business model that they are using in their family medicine practice.  These questions were reviewed and validated by the author’s peers before they were used in the primary research.  As the information from the interviews were recorded, it was then analyzed mathematically to come to conclusions of the effectivity of the business model when compared to the variables of income, lifestyle, stress level, happiness, and patient satisfaction.


A huge bulk of the information that was gleaned for this project was found from the literature review.  Fortunately there has been a lot of information in the form of various publications that document the different business models that physicians, specifically those in the field of family medicine, are currently implementing in the United States today.  Some of the aspects that this literature review revealed as far as the various family medicine business models are concerned were the reasons why there were possibly so many different business models for the family physician, as well as the differentiation between the different business models.

There was also gleaned from this secondary research the advantages and disadvantages of the various business models as they apply both to the physician and the patient.  Also, there was insight as to the strengths and weaknesses of the various business models and which business models would be most viable in the future for the family physician.

Furthermore, there was also, when appropriate, an in depth look to various stories or anecdotes that the author felt better grasped the big picture and or illustrated various points as to the general feeling of the physician, practice, and the patients.  This would come in the form of stories that were related to the author of the various publications that the author felt was appropriate to share as they were related to the various business models that the family physicians are using and evolving today in the United States.

There was also primary research conducted by the author in the form of face to face interviews, as well as interviews that were conducted via email.  The interviews were conducted from physicians that are practicing various business models all over the United States in order to try to get a general flavor and generalizations or common threads that these various business models may have to make them better classified and defined when attempting to differentiate between them.  While conducting the email correspondence, the author made sure that a good number of the questions were open ended to allow for the respondents to open up and put their own expression into the interview.

Interview Format

            The author conducted a variety of interviews that were face to face.  These face to face interviews were with Dr. E___ , a group practice family physician.  Dr. W_______, a physician that is practicing in the corporate medical system, Dr. J_______, who runs a cash-only practice, and Dr. B______, who operates a micro practice.

As stated earlier, these questions were reviewed and validated by the author’s peers before they were used in the primary research.  As the information from the interviews was recorded, it was then analyzed mathematically to come to conclusions of the effectivity of the business model when compared to the variables of income, lifestyle, stress level, happiness, and patient satisfaction.

The author actually also interned with each of those physicians and was able to also see firsthand how the practices are operated on a daily basis.  During this time the author was also able to get a general feeling of the office staff, practice, and patients.  The author was also able to see firsthand the interaction that the physicians had with their patients.  When appropriate, the author was also able to see the physicians interact with staff and administration, insurance companies, and other aspects of running a medical practice.

There were also a couple of telephone interviews, as well as a number of interviews that were conducted via an email questionnaire.  The author found various physicians across the United States to send these interviews to by finding their practices on the internet and their email addresses in the contact section of their websites.

The interviewees were at the very minimum asked a variety of questions (see Appendix A) that were related to finding out more about their particular business model.

Limitations and Assumptions of the Interview Questions and also in the Recording of the Data

            Although the primary research yielded valuable data, it is important to realize that due to time constraints and the relatively small sample size that the data may be limited.  The author attempted around 60 interviews, with less than half responding, and about half of those that did respond, responded with an answer of not being interested in being interviewed.

It is important to note that another flaw in the data could be that the people being interviewed may have skewed their responses due to the Hawthorne Effect, meaning that because they were being interviewed for an academic project that they could have exaggerated some of their responses in order to make their business model or situations look better or worse than it really was.

However, regardless of the Hawthorne Effect or any other bias, it is assumed that the interviewees were honest and their data and answers that were provided are presented as such.  The Hawthorne Effect was a concern as some of the data and answers could have been exaggerated.  It would have been ideal to have some of the information come from other sources such as staff, or accountants, to get a more accurate and unbiased answer.

It is also assumed that the author would not skew the information due to an observer expectancy bias, as the author has hopes and dreams of one day running their own family medicine practice with a particular business model in mind.  The observer expectancy bias indicates that the person that is conducting the research can unknowingly or knowingly skew the data and results to the expected or desired conclusions that the person has desired in their head.

Data Collection Process – Findings from primary research

The primary data that was collected through face-to-face interviews, telephone interviews, and interviews via email, all provided different perspectives and points of view that were unique to the physician and to their practice business model.  The face-to-face interviews were with physicians that the author actually interned with and spent time working in their practice.  The phone interviews and the interviews via email were randomly conducted with any family physician that would respond to the request for interview submitted by the author.

It was interesting to find that although each physician considered themselves as a part of a certain business model, that the author found that within each business model there were variations and differences between each physician’s style of implementation of that business model.  In addition to the style of the practice, other factors that would contribute to a physician’s variations between certain business models of the same niche was the stage in which the physician is in their career.  This meaning that the physician could be at the end of their career, nearing retirement, or just beginning their practice, or anywhere in between those stages.  For example, a physician that considered himself in a micro-practice but was almost into retirement and considered himself at the end of his career.  The difference between this physician and a physician just transitioning into a micro practice would be that the physician nearing retirement was making more money and working more.  Also, it was interesting to see the older physician took on more duties such as maintenance.

Generally speaking, the happiest physicians the author interviewed were those that were working for themselves in some sort of solo capacity, and the physicians that worked for a group or corporate medicine were the least happy.  It also seemed that the physicians that worked for a group or for a corporation did however make more money annually on average.  What was also interesting is that the physicians that worked for a corporation or a group were very vocal when in saying that they often considered going into concierge medicine, or a cash-only practice, or a micro practice.

The happiest physician that I encountered was a physician that had a micro practice that was cash-only.  This physician also had multiple mid-level health care providers working for her.  She was happy because she did not have to deal with insurance companies.  She also was well paid and appreciated by her patients.  She had a huge inflow of patients, but a lot of them were seen by her mid-level health care providers.  She had a low overhead.  Before she started her cash-only micro practice she had twenty years of experience working for corporate medicine.  She said that as she was older that she wanted to work smarter, not harder.  She was able to take all of the time off that she wanted and still made a great living as her mid-level health providers saw a lot of the patients (J_____, personal communication, October 01, 2014).

On the other end of the spectrum, the most miserable appearing physician was working for a big corporation.  He was making a lot of money, and had some great incentives if he made certain goals.  However, he was always stressed out, and worked long hours in order to meet his goal.  He also had problems with staff that seemed to be out of his control as he was not the one to be able to hire or fire employees.  He also mentioned to me personally that he really did not appreciate having to be evaluated by the administration, and he did not like getting written up when a patient complained.  He usually put in around sixty hours a week at work, but then volunteered at a free clinic a couple of nights a week also.  The author has chosen to withhold this physician’s name (Name withheld, personal communication, October 01, 2014).


Comparing the Primary Data to the Literature Review

  When we compare the primary data collected to the literature review, we see that they do in fact closely correlate one with another.  For example, the physicians that were read about in the literature review, we can see that the happier ones are the ones that are doing their own practice, and the physicians that are the most stressed out seem to be the physicians that are working in corporate medicine.  This seems to be the truth in family practice.

Another correlation that was found was that the physicians that made the most money annually were not necessarily the most happiest.  This was found in the literature to be true as well as from primary research.  However, it is also important to note that some of the physicians that made a lot of money comparatively to their colleagues could also be very happy.

It also seemed that a downside to practicing medicine in the United States today, especially as it applied to the family medicine specialty, was that all of the different rules and regulations seemed to be “superfluous” to practicing medicine as the rules and regulations do not really progress the practice of medicine or the quality of patient care (John Mochata, personal communication, October 02, 2014).  This seems to be the downsides as all physicians seem to agree on this common belief, no matter what their business model of practicing medicine is.

One difference that the author did note in the literature review that the author did not come across in primary research was the failures in certain business models that could happen.  For example there was in the literature review a cash only practice that failed (Frank, 2008).  This would be understandable as it is difficult to interview physicians in a failed business practice as they are currently working somewhere else and do not necessarily care to advertise that they were in a practice that did in fact fail.


Data Analysis

            The way the data was analyzed was by taking the recorded answers from the physicians that responded, then mathematically figuring out the average of the individual responses were, within the business model that the physician claimed was implemented in their family medical practice. When we analyzed the data, we could see that out of the physicians that responded to being interviewed, and also partially in combination with the data found in the literature review, we could illustrate the following graphs from the results: As we can see the family physician on average makes between $150-220 thousand a year for full time hours.  We can also see the stress level for the physicians that are working in a corporate setting are amongst those with the highest stress level.  We can also see that physicians in corporate medicine are also amongst the highest paid.  Interestingly enough, as far as their personal happiness is concerned, the corporate family physician is the least happy.

We can also see that the happiest physicians seem to be those in solo-solo practices, micro practices, or cash only practices.  We can also see the stress levels are lower in these areas of particular business models.  It is interesting to note that these physicians on average do not necessarily make the most money compared to their colleagues. However there were some outliers that made an annual salary that could be comparable to the highest paid corporate physician.


According to the data and research, the author believes that this implies that physicians that do not work for corporate medicine, or that do not have to deal with insurance companies, are the happiest.  This is because the physician has a primary focus of delivering the best possible patient care that he or she has the ability to deliver.  This is a very difficult thing to do in and of itself, let alone having to deal with the distractors that a physician would have to deal with just in order to pay his staff, and any other overhead that a physicians practice may have, just to stay in business.  This seems to be correlated with the fact that they have on top of all of this, an increase in stress in their jobs is also due to administrative watch-dogs and the like.  It can be very frustrating for a physician that is working as hard as they can to deliver quality care to their patients, only to have administration say that they are not seeing enough patients per hour, or that they need to see more patients in a day in order to get a pay raise.  It is also very frustrating for a physician to get evaluated by administration, especially as the evaluation can influence their income.  It is also an added stress to a physician when they have to deal with getting written up by administration when a patient complains.  All of these things combined can dramatically raise a stress level of a physician.

It also seems that the more government makes mandates and rules that this adds to the stress of medicine.  Additionally these extra rules and mandates do not necessarily improve the quality of care.  The author recalls working with a physician that was well respected by patients, as well as colleagues.  This physician had been practicing medicine for over forty years, and was very successful and skilled as a physician.  Then the government mandate that physicians were supposed to start using electronic medical records in order to get an increase in reimbursements from Medicare and Medicaid.  This physician, even though he was very competent, and his hand taking notes on paper worked just fine over the last forty years, found that he was increasingly frustrated having to learn how to use the computerized electronic medical record.  This also was frustrating for the physician as this took a huge amount of time, more than ten times that of taking notes by hand.

We can also see that the amount of money that a physician makes does not seem to correlate necessarily with the level of happiness that they have in their lives.  Although, it is also important to note that physicians that made a lot of money compared to their colleagues were not necessarily depressed or saddened either.

The author also believes that this implies that the happier the physician, the happier the patient.  If the physician is happy then the patient can benefit from this.  The patient will benefit by the way the service that they get in their healthcare from their physician.  Therefore it is very important for the physician to work in an environment where they are happy in order to deliver the best possible patient care in the family medicine specialization.



            It is the recommendation of the author, that after much research and consideration, that the ultimate business model for the family physician now and in the future would be that of a cash-only micro practice.  The reason that the author recommends this is because these business models tend to be the ones with the least amount of stress, thereby increasing the happiness level of the physician and the patient. One of the reasons for a happier patient is because they are receiving better patient care, and one of the reasons that the patient feels this way is because in these particular business models the patient can see the physician for thirty minutes to an hour sometimes, and they do not feel rushed with the visit from the physician.

The combination of the cash-only micro practice business model is also very lucrative as a business model.  This is most likely because the overhead costs are cut dramatically in the business models of this type.  This in turn increases the percentage of net earnings.

The ultimate family medicine business model practice should also hire as many mid-level providers as the state law will allow.  This will allow the physician to increase their income as well as see as many patients as they desire, and not have to worry if the block their schedule out for other responsibilities.   In this business model however, it is important to note that in some cases the physician feels more like an office manager as they have to manage the mid-level health providers, such as the nurse practitioner and the physician’s assistant.

The author would also ultimately and strongly recommend that for the physician to try to keep costs down, and to keep the stress level as low as possible when practicing medicine.  Remember that patient care is the primary focus.  When this is done, the physician can appropriately align their business design and personal goals in the best way.  If the physician does this, their business model will most likely be a successful one.




            It seems that there are many different business models to choose from, and there are so many factors to consider.  Keeping it simple however is going to be the best way for a physician to maximize their happiness and well-being.  This will also translate to patients being satisfied with their physician as they receive excellent care.

There should not be unnecessary time restrictions when a patient visits their physician.  In corporate medicine a physician is lucky to spend seven actual minutes with the patient face to face.  This can be really frustrating for the patient as they may feel rushed.  This is also frustrating for the physician as they do not like to feel like they are rushed either.  The patient may feel like they are burdening the physician if they take any more of their time, and this can be very dangerous.  This can lead to the patient being unwilling to give a full and proper history to the patient, thereby possibly jeopardizing the patients’ health, and this is the last thing that should be done in healthcare, as patient care should always be the primary focus.

There should not be excess mandates and government to take away from the practice of medicine.  It is widely felt that these mandates do not enhance or improve the practice of medicine.  Therefore, they do not increase the quality of patient care.  This is just a problem that adds to the stress, time, and ultimately monetary resources of the family physician.

There should not be administration always looking over the doctor’s shoulder to make sure that profits are maximized.  This type of business model adds a lot of stress to the physician.  It can also be humiliating to them.  This in turn becomes a distraction to the primary goal of healthcare, which is patient care.

When a physician decides on what business model is for them, they need to take a close look at themselves, their values, why they are in medicine, and their goals.  When these factors are taken into consideration, the physician will better be able to excise the unnecessary variables that are taking away from the practice of good medicine.  Also they will be able to implement the best set of business practices, which will allow them to be able to maximize and deliver the best possible patient care, which should be the goal of health care.



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Interview Questions – Business Models for Family Medicine

  1. How many years have you been in family medicine?
  2. What type of business model is your practice, or that you work in (you can choose more than one answer here)?
  3. How many hours per week is your average work week?
  4. What is the average number of patients that you see in a day?
  5. What is the average amount of time that you spend per patient visit?
  6.  What is your daily stress level on a scale of “1-10″ (with “10″ being the most stressful)?
  7. What is your average annual gross income (the average of the last two years)?
  8. What are the pros of your business model?
  9. What are the cons of your business model?
  10. On a scale of “1 – 10″, what would you say is you level of happiness (with “10″ being the happiest)?
  11.  What recommendations and or advice do you have?



Polyphasic characterization and genetic relatedness of low-virulence and virulent Listeria monocytogenes isolates

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Currently, food regulatory authorities consider all Listeria monocytogenes isolates as equally virulent. However, an increasing number of studies demonstrate extensive variations in virulence and pathogenicity of L. monocytogenes strains. Up to now, there is no comprehensive overview of the population genetic structure of L. monocytogenes taking into account virulence level. We have previously demonstrated that different low-virulence strains exhibit the same mutations in virulence genes suggesting that they could have common evolutionary pathways. New low-virulence strains were identified and assigned to phenotypic and genotypic Groups using cluster analysis. Pulsed-field gel electrophoresis, virulence gene sequencing and multi-locus sequence typing analyses were performed to study the genetic relatedness and the population structure between the studied low-virulence isolates and virulent strains.


These methods showed that low-virulence strains are widely distributed in the two major lineages, but some are also clustered according to their genetic mutations. These analyses showed that low-virulence strains initially grouped according to their lineage, then to their serotypes and after which, they lost their virulence suggesting a relatively recent emergence.


Loss of virulence in lineage II strains was related to point mutation in a few virulence genes (prfA, inlA, inlB, plcA). These strains thus form a tightly clustered, monophyletic group with limited diversity. In contrast, low-virulence strains of lineage I were more dispersed among the virulence strains and the origin of their loss of virulence has not been identified yet, even if some strains exhibited different mutations in prfA or inlA.


Listeria monocytogenes, a facultative intracellular pathogen, is one of the major causes of food-borne infection in humans [1]. Although rare, invasive listeriosis is a public health concern due mainly to its high fatality rate evaluated at 20-30% [2]. The clinical outcome of listeriosis is influenced by the pathogenic potential of the infecting strain which is in part related to its serotype [3]. It is now known that isolates 1/2a, 1/2b and 4b are responsible for 96% of human infections and most outbreaks are caused by strains of serotype 4b whereas serotype 1/2a has been associated with sporadic cases [4]. Serotypes 4a and 4c are predominant in animal, food or environment [5].

Unfortunately, there is currently no standard definition of virulence levels and no comprehensive overview of the evolution of L. monocytogenes strains taking into account the presence of low-virulence strains [5]. Different studies have shown that L. monocytogenes isolates form a structured population, composed of divergent lineages [6]. The large majority of isolates clusters into two lineages, but two additional lineages have been identified. However, these lineages correspond more to different but overlapping niches than to virulence-related clusters. We previously described low-virulence L. monocytogenes strains using a method that combines a plaque-forming (PF) assay with the subcutaneous (s.c.) inoculation of mice [3]. Using the results of cell infection assays and phospholipase activities, the low-virulence strains were assigned to one of four groups by cluster analysis. Sequencing of virulence-related genes highlighted the molecular causes of low virulence. Group I included strains that exhibited two different types of mutation in the prfA gene: either a single amino acid substitution, PrfAK220T, or a truncated PrfA, PrfAΔ174-237 [7]. In Group III, strains exhibited the same mutations in the plcA, inlA and inlB genes that lead to a lack of InlA protein, an absence of PI-PLC activity and a mutated InlB [8]. The fact that numerous strains exhibit the same substitutions in virulence genes suggests that they could have common evolutionary pathways. In contrast, Ragon et al. reported that numerous L. monocytogenes strains exhibit different mutations in the inlA gene due to convergent evolution [9]. These data emphasize the interest of providing a framework for the population study based on the virulence of this bacterium.

The aim of this study was to assign the new low-virulence strains identified by different methods to phenotypic and genotypic Groups using cluster analysis, and to study their relatedness with virulent Listeria monocytogenes strains using pulsed-field gel electrophoresis and multi-locus sequence typing analyses


Phenotypic characterisation of the low-virulence strains

The combination of PF assays followed by s.c. injections of immunocompetent mice, allowed us through different studies, to collect 43 low-virulence strains mainly of serotypes 1/2a (51%) and 4b (28%), which are usually related to sporadic and epidemic human cases of listeriosis, respectively [4] (Table ​(Table1).1). In this study, a strain is considered a low-virulence strain when fewer than 4 mice out of 5 inoculated become infected with a mean number of bacteria in the spleen less than 3.45 ± 0.77 log [3].

Table 1

Characterization of the low-virulence L. monocytogenes strains

As previously performed, these low-virulence strains were classified using an ascendant clustering hierarchical technique [3]. Six groups according to the values of four factors (level of cell invasion, number of plaques formed, and enzymatic activities of the two phospholipases C) have been obtained (Table ​(Table1).1). Group-I included 15 strains that did not enter cells, formed no plaques and had no phospholipase activity. Group-II consisted of only one strain entering cells, forming no plaques and only expressing PI-PLC activity. Group-III comprised nine strains entering cells, forming no plaques and only expressing PC-PLC activity. In this new analysis, the previously described Group-IV [7] has now been divided into 3 sub-Groups. The new Group-IV included nine strains forming plaques but fewer than virulent strains (mean 3 log versus 5). Three out of 9 strains were also characterized by a very low level of PC- and PI-PLC. The new Group-V comprised six strains also forming plaques but fewer than virulent strains and characterized by their very high PI-PLC activity. Finally, Group-VI contained three strains forming plaques within 48 h. In contrast the other strains formed plaques within 24 h, classic time necessary to count the plaque number.

Genotypic characterisation of the low-virulence strains

Sequencing the prfA, plcA, plcB, inlA and inlB genes allowed us to observe that some phenotypes correlate with genotypic mutations which have been demonstrated to be the cause of the low virulence (Table ​(Table1)1) [7]. The sequences of the PrfA, InlA and ActA fragment were compared to those of the EGDe strain (serotype 1/2 – GenBank accession number AL591824) or F2365 strain (serotype 4 – GenBank accession number AE017262), according to the serotypes of the strains.

The phenotypic Group-I strains exhibited mutations in PrfA compared to the EGDe strain and were subdivised into 2 genotypic Groups: the PrfAK220T (genotypic Group-Ia) and the truncated PrfAΔ174-237 (genotypic Group-Ib) previously described [8,11]. One strain (NP26) exhibited a new putative causal mutation in prfA, K130Q, and is the only one of serotype 4b exhibiting a PrfA mutation (herein defined as genotypic Group-Ic).

Two genotypic Groups were also identified for the phenotypic Group-III strains. One harbored exactly the same mutations in the plcA, inlA and inlB genes, characteristic of the previously genotypic Group-IIIa [8]. Only one strain (AF105) belonged to Group-IIIb and harbored a mutation at least in the inlA gene.

No genotyping Group has been defined for the phenotypic Groups-II because this Group is formed by only one strain. The Group-IV, -V and –VI strains did not exhibit specific DNA sequence of the prfA, inlA and actA fragment genes, that allowed us to assign genotyping Groups. No causal mutations could have been displayed explaining the low virulence of these Groups.

PFGE profiles

To study the genetic relationships between the low-virulence strains, the 43 low-virulence strains were compared with 49 virulent strains (based on both the mouse s.c. inoculation and PF assays) selected on the basis of matching serotypes and origins (Additional file 1).

This analysis revealed three major branches (Figure ​(Figure1)1) probably corresponding to the lineages I, II and IV described by Ward et al. by a SNP analysis [12]. In their study lineages I and III isolates formed, indeed, a sister group to lineage II strains, while the lineage IV represented a divergent sister clade. However, the small number of lineage IV strains did not allow us to conclude in this distribution. Nonetheless, as observed by Ward et al., lineage I included strains of serotype 1/2b, 4b, 4d, 4e, 3b and 7, whereas lineage II included strains of serotype 1/2a, 1/2c and 3a. Lineage III and IV included strains of serotype 4a, 4b and 4c. PFGE typing of the 92 isolates resulted in 69 different patterns, most of them grouped into 16 clusters with a similarity percentage above 85%. All strains gave interpretable PFGE patterns after restriction by AscI enzyme, whereas three virulent strains of lineage III/IV (serotype 4a and 4c) gave no profiles after ApaI restriction, possibly due to the methylation of restriction sites [13,14].

Figure 1

Dendrogram constructed for PFGE analysis using the UPGMA method with BioNumerics v.4.6 software showing the genetic relationships between 92 L. monocytogenes strains. The low-virulence strains are in red. Green lines indicate the division into

No clear correlation could be made between the PFGE clusters and the virulence levels of the strains and even though seven clusters included only virulent strains, the low-virulence strains were distributed in 9 clusters out of 16 (indicated by green lines in Figure ​Figure1),1), often mixed with virulent strains. Within the same lineage, the low-virulence strains were clustered according to their serotype. This observation is supported by the fact that strain NP26 belongs to the phenotypic Group-I which was grouped in lineage I with serotype 4b strains, whereas all the other strains of the phenotypic Group-I were grouped in lineage II with serotype 1/2a strains.

In the lineage II, the low-virulence strains were grouped according to their genotyping Groups, but were sometimes clustered with virulent strains. Only strains of the genotypic Group-Ia formed one specific cluster. All strains of the genotypic Group-IIIa were grouped together, but on the same branch as strain A23 (similarity percentage >80%). This clustering can be explained by the demonstration that the A23 strain had the same genotypic mutations as the Group-IIIa strains, but exhibited some virulence in our in vivo and in vitro virulence tests [15]. In the same way, all strains of the genotypic Group-Ib belonged to the same cluster, but with two virulent strains.

In the lineage I, the phenotypic Groups-IV, -V and -VI did not form specific clusters but were mixed with virulent strains (Figure ​(Figure1).1). This is probably related to the absence of a genotypic Group and probably corresponds to multiple genomic backgrounds. No low-virulence strain was found in lineage III/IV, but the small number of strains in this lineage hampered us to conclude in the rate of low-virulence strains.

Sequencing of virulence and housekeeping genes

To investigate the population structure and diversity of the low-virulence strains compared to virulent strains, three virulence genes were sequenced (prfA, inlA and actA) as well as seven housekeeping genes (acbZ, bglA, cat, dapE, dat, ldh, and lhkA). The dendrograms of the concatenated nucleotide sequences of virulence and housekeeping genes performed with the NJ method were presented Figure ​Figure2A2A and ​and2B,2B, respectively. They showed different relationships among lineages and in part for some lineage I low-virulence strains. In the housekeeping-gene tree, lineage III/IV strains formed a sister group to lineage I isolates as previously described [16]. However, as also observed by Tsai et al.[16], this was not the case with the virulence-gene tree where the strains of serotype 4a and 4c formed different branches. In the same way, all strains of serotype 4b were on the same branch in the housekeeping-gene tree. That was not the case in the virulence-gene tree where few strains of serotype 4b were on the same branch as strains of serotype 1/2b and 3b. Similar variations were observed for strains of serotype 1/2a which were on the same branch in the housekeeping-gene tree, whereas with the virulence-gene tree, 7 strains were on different branches than the other 34 serotype 1/2a strains (bootstrap 100%). This observation comforted the hypothesis that numerous recombinations have occurred with the virulence genes.

Figure 2

A Dendrogram of the prfA, actA and inlA gene sequencing using the NJ method with BioNumerics v.4.6 software showing the genetic relationships between 92 L. monocytogenes strains. The tree was constructed on the basis of the mean matrix distances

Similar variations between the two trees were also observed for low-virulence strains of lineage I. For example, with the virulence-gene tree 2 low-virulence strains of serotype 4b and 2 of serotype 4d were on the same branch as virulent strains of serotype 1/2b, 3b, and 7. This is not the case for the housekeeping-gene tree. As observed with PFGE, for the lineage II, both trees suggested that i) all the low-virulence strains of the same genotyping Group are on the same branch, and ii) the genotypic Group-Ia was closer to the genotypic Group-IIIa than to the genotypic Group-Ib. In lineage I, the low-virulence strains of phenotypic Groups-IV, -V and -VI were, in contrast, mixed with virulent strains showing that evolution of their virulence genes had occurred independently. This is also related to the fact that no genotyping group has been detected for these lineage I strains.

Twenty-six out of the 43 low-virulence strains (60%) and 11 out of the 49 virulent strains (22%) had a truncated InlA protein (Table ​(Table2),2), grouped in only 7 ST. Remarkably, all low-virulence strains of lineage II had a truncated InlA protein, compared to only three out of 18 low-virulence strains of lineage I. In addition, a correlation exists between the genotyping Groups and inlA mutations. All strains of the genotypic Group-Ia harboring the PrfAK220T mutation exhibited the inlA mutation at codon 77. Similarly, all strains of the genotypic Group-Ib harboring the PrfAΔ174-237 mutation exhibited a stop-codon at codon 189, and all strains of genotypic Group-IIIa had an insertion after the codon 13, leading to a truncated InlA.

Table 2

Mutational events in the inlA gene

MSTree analysis

To analyze in greater detail the population structure of the low-virulence strains, the 92 strains were analyzed and compared with the 656 L. monocytogenes isolates included in a previous study [18]. As no low-virulence strain was found in lineage III/IV, we presented only the lineages I and II.

This analysis showed that low-virulence strains of genotypic Group-Ia, -Ib, and -IIIa were distributed among three specific closely related STs (13, 31, 193) (Figure ​(Figure3).3). The ST 13 was formed with 10 Group-Ia low-virulence strains and one strain (Lm74905) belonging to the comparative set (in white). The analysis of this strain revealed that it exhibited the PrfAK220T mutation and the same truncated InlA characterizing the genotypic Group-Ia. Likewise, the Lm85820 strain which grouped in the ST31 (in white) exhibited the same mutation in InlA than the low-virulence strains of this ST, but no mutation in PfrA. Remarkably, although all strains of the ST31 had InlA mutations, only half of these strains also had the PrfAΔ174-237 mutation. In this analysis, the A23 strain corresponds to a singleton (ST196) with only one mismatch with Group-IIIa and two with Group-Ia. It is related to Group-Ib through ST11.

Figure 3

Minimum spanning tree based on allelic profiles by using BioNumerics version 4.6. (Applied-Maths, Sint-Martens-Latem, Belgium). The comparative set included 656 L. monocytogenes strains from the French Reference Centre for Listeria and the WHO

Overall, half of the low-virulence strains (22 out of 43), belonging to the genotyping Groups-Ia, -Ib and -IIIa, are likely to have descended from a single virulent 1/2a ancestral bacterium. In contrast, the other strains were distributed into five clonal complexes and 10 STs and may be regarded as virulence variants of L. monocytogenes strains.

Contribution of the optical mapping

To investigate the genomic relationship between the A23 strain and the closely related low-virulence strains belonging to Group-IIIa strains, two strains (BO43 and 416) were compared with the A23 strain using optical mapping and the in silico reference EGDe map (Figure ​(Figure4).4). The EGDe optical map was approximately 20% different from the maps of the Group-IIIa and A23 strains, whereas the A23 strain showed 99% similarities with Group-IIIa. Two fragments (3 and 4) (63 and 47 kb, respectively) had been inserted in the chromosome of the A23 strain but not in the EGDe strain. Fragments 5, 6 and 7 (52, 50 and 41 kb, respectively) represent the fragments inserted in the chromosomes of the BO43 and 416 strains. A supplementary fragment 8 (125 kb) was inserted in the chromosome of the BO43 strain.

Figure 4

Aligned optical maps for Group-III (BO34, 416) and A23 strains and in silico reference EGDe map. In the pair-wise alignments, lines connecting two chromosomal maps indicate a discontinuity in the alignment of fragments. Chromosomal inversions are indicated

This analysis confirms that all the Group-IIIa strains are very similar to each other and to the A23 strain. Indeed the insertion of the fragment 4 is located at the same place as the fragment 7 and could be inserted in the region of the lmo2589 gene annotated as similar to a transcription regulator T and R / AcrR family. The fragment 3 present in the A23 strain is different from the fragment 5, present in the Group III strains and could explain the increase of virulence of the A23 strain. The fragment 3 could be inserted in the region of the lmo2073 gene annotated as similar to ABC transporter and the region of the lmo2074 gene (similar to unknown proteins). The fragment 5 could be inserted in the region of the lmo2105 gene, annotated as similar to ferrous iron transport protein B. The fragment 6 present in the Group III strains could explain the decrease of virulence of these strains compared to the A23 strain. Indeed the annotation of the EGDe strain indicates that this insertion was found in the lmo2467 gene, located upstream of the clpP gene and its promoter, involved in the rapid and adaptive response of intracellular pathogens during the infectious process [19].


For a long time, all L. monocytogenes isolates were regarded as strictly pathogenic at the species level, and were always related to disease. However, from the experimental data collected over recent years, it has become clear that L. monocytogenes demonstrates serotype/strain variations in virulence and pathogenicity rate [5]. The population structure of 43 low-virulence strains was investigated with that of 49 virulent strains to estimate their diversity from virulent strains. We also investigated whether low-virulence strains formed a homogeneous subpopulation of L. monocytogenes or whether they originated from a random loss of virulence genes and thus diversified in multiple distinct directions.

We based our analysis on PFGE and different DNA-sequence-based approaches. The PFGE gave the greatest discriminatory power. Indeed PFGE gave profiles for different strains that by another way were grouped together in MSTrees. For example, ST2 (Figure ​(Figure3)3) comprised low-virulence strains of the phenotypic Groups-I, -V, and -VI, which had different PFGE profiles. Similarly, the low-virulence strains AF105 and LSEA-99-23 exhibited the same MLST profile but had distinct profiles in PFGE. Interestingly, MSTree identified specific ST for half of the low-virulence strains belonging to lineage II.

Overall, we identified low-virulence L. monocytogenes strains in both lineages I and II. No hypothesis could be advanced for the lineage III/IV, as they were few strains studied here represented these lineages. Our population structure showed that low-virulence strains are linked firstly according to their lineage, then to their serotypes and after which, they lost their virulence suggesting a relatively recent emergence. MSTree analyses showed that low-virulence strains belonging to lineage II formed a tightly clustered, monophyletic group with limited diversity, in contrast to the low-virulence strains of lineage I. All our observations further supported the fact that some correlations existed between virulence level and point mutations, base substitutions inducing a stop-codon, or inactivation of different virulence proteins, rather than on horizontal transfer or gene loss [7,8,20]. A characteristic of lineage II low-virulence strains was that all strains had a point mutation in the virulence inlA gene. Interestingly, there was a strong correlation between the inlA mutation and the genotypic group which were based on the mutations responsible for the virulence lost. Moreover, all strains of ST31 had only two different inlA mutations, but only the strains with the mutation type 5, according to Van Stelten also have the PrfAK220T mutation [17]. This observation suggested that the inlA mutation appeared before the prfA mutation. Regardless of the nature of mutations in inlA in the different low-virulence strains, there was clearly a link between their prevalence in food environments and the inlA mutations. Indeed, the inlA mutations were identified mainly in serotypes 1/2a and 1/2c from lineage II isolated from food and food-processing environments [17,21]. As such, it is reasonable to hypothesize that variations within these groups have been shaped to a greater extent by selective constraints operating in food manufacturing-plants.

It is intriguing that InlA, and to a lesser extent PrfA, which are important bacterial factors for host colonization, were lost. This pattern could be explained either by relaxation of the selective constraint to maintain InlA and PrfA function or by a selective advantage provided by the loss of functional virulence proteins in the ecological niche occupied by these strains. Clonal families might be adapted to different niches, and their occurrence as mammalian pathogens may be of limited significance for their evolutionary success in the long term. Considering all altered factors, the low-virulence strains could represent over 50% of the L. monocytogenes strains [5]. The fact that the growth of some low-virulence L. monocytogenes strains was impaired on selective medium suggests that the prevalence of these strains may be higher than that currently reported [22]. Moreover, only a few L. monocytogenes strains isolated from the environment and/or food have been analyzed, in contrast to strains of human origin. Developing reliable and easy-to-perform virulence tests could be useful, particularly for risk analysis, where it is important to evaluate the risk associated with the consumption of food products contaminated with L. monocytogenes not only on the basis of levels of bacterial contamination but also on the virulence level of the strains.

In this complex diversity scheme, the case of the A23 strain is very intriguing. Indeed, it is still virulent in mice, despite non-functional major virulence genes, due to point mutations in inlA, inlB and plcA that characterize the genotypic Group-IIIa [15]. This strain was found to be in the same cluster as the Group-IIIa strains using PFGE and MLST analyses, but to be in a specific ST using MSTree (ST 196 and 193, respectively). The fact that this strain has an additional mutation in mpl compared to Group-IIIa strains [15] suggests that it evolved from this group and thus reacquired virulence genes after initial virulence-gene loss. However, optical mapping does not support this hypothesis, since compared to the EGDe genome, specific fragments have been inserted in the genome of the Group-IIIa strains but not in strain A23, suggesting that the Group-IIIa strains have evolved from the latter. The complete sequencing of the genome of these strains should clarify this question.

This analysis corroborated the classification obtained for the phenotypic Groups-I and –III. Moreover the new detected low-virulence strains exhibiting the same phenotypes and harbouring the same mutations in the virulence genes, as previously observed, reinforced our observations. The new results allowed us to subdivide the former Group-IV into 3 new Group-IV, -V and –VI and to suggest different hypothesis concerning the population structure and diversity of the low-virulence strains compared to virulent strains.


The data presented in the present study show indeed that the diversity and population structure according to the virulence level of L. monocytogenes strains is complex and based on different mechanisms which seem to differ according to the lineage of the strains and thus to their ecological niches. However, from a practical perspective, this strain population does not correspond to a new species within Listeria. The relatively clear differences between virulent and non-virulent strains or species make these bacteria an attractive model for examining the lost of pathogenicity in this genus and for applying these principles to logical predictions of how certain pathogens will behave in a population over evolutionary time.


Strains and culture conditions

The 92 L. monocytogenes strains used in this study are described in the Additional file 1. The non-virulent L. innocua BUG499 strain was used as negative reference. All isolates were collected from independent sources at different dates. L. monocytogenes strains were defined as virulent or low-virulence using a virulence test combining a PF assay performed with the human colon adenocarcinoma cell line HT-29 and subcutaneous inoculation of mice into the hind footpads of immunocompetent Swiss mice as previously described [3]. Animal experiments were carried out in strict accordance with French recommendations. The protocol was approved by the Val de Loire Ethics Committee for Animal Experiments (n° 2011-07-02). For analysis, strains were cultured for 8 h in brain-heart infusion broth (Becton Dickinson, Fisher, Illkirch, France) at 37°C.

The collection of 656 L. monocytogenes strains from the French Reference Centre for Listeria and the WHO Collaborative Centre for Foodborne Listeriosis were used for the minimum spanning tree (MSTree) (comparative set; Figure ​Figure3)3) as previously described [9,18].

Phenotypic characterization of the low-virulence strains

The PF assay performed on HT-29 cells and invasion assays performed on Caco-2 and Vero cells were previously described [8]. The detection of the PI-PLC activity assays were analyzed in the culture supernatant with tritium-labelled L-α- phosphatidyl-inositol [8] and the PC-PLC activity was assessed after incubating with lecithin suspension, at 510 nm [7]. Experiments were carried out in duplicate and repeated twice for each strain. The values obtained allowed us to perform an agglomerative hierarchical clustering, based on Ward’s method and the Euclidean distance, to identify groups (clusters).

Pulsed-Field Gel electrophoresis (PFGE)

The PFGE protocol used in this study was the PulseNet standardized molecular subtyping protocol in accordance with Graves and Swaminathan [23].

The gels were photographed under UV transillumination, and the images were digitized and analyzed using BioNumerics v4.6 software (Applied-Maths, Sint-Martens-Latem, Belgium). The matching of band patterns was based on the DICE coefficient. Dendrograms were created using the Unweighted Pair Group Method with arithmetic mean. Strains were considered to be indistinguishable and were assigned to the same PFGE profile when the dendrogram indicated an index of relatedness of 100% verified by visual examination of band patterns.

Gene sequencing and multi-locus sequence typing (MLST)

The nucleotide sequencing of prfA, inlA, inlB and plcA genes and sequence analyses were described previously [7,8]. The clpP gene and its flanking regions (lmo2467 and lmo2469) were amplified from total isolated DNA using PCR. Primers and temperature annealing are listed in the Additional file 2.

The prfA and inlA virulence genes were fully sequenced, whereas the actA gene was partially sequenced. Seven housekeeping genes (acbZ, bglA, cat, dapE, dat, ldh, and lhkA) were selected for the MLST analyses (Additional file 2: Table S2) [9]. Alleles and sequence types (ST) are freely available at For analyses, sequences were concatenated either for the virulence or the housekeeping genes in an MLST scheme. For each MLST locus, including the 748 L. monocytogenes strains, an allele number was given to each distinct sequence variant. MLST analysis links profiles so that the sum of the distances (number of distinct alleles between two profiles) is minimized [24]. Each circle represented in Figure ​Figure33 corresponds to a ST number, attributed to each distinct combination of alleles on the seven genes. The size of the circle corresponds to the number of strains with that particular profile.

The dendrograms of the concatenated nucleotide sequences of virulence and housekeeping genes with the Neighbor-Joining (NJ) method and MLST analysis were performed using BioNumerics v4.6.

Optical mapping

Optical maps were prepared on the Argus™ Optical Mapping System by OpGen (Gaithersburg, MD USA), as described previously [25]. This method scans and assesses the architecture of complete bacterial genomes. Briefly, following cell lysis, genomic DNA molecules were spread and immobilized onto derivatized glass slides and digested by NcoI. After restriction digestion, a small gap in the DNA at the precise location of the restriction endonuclease cleavage site is left. The DNA digests were stained with YOYO-1 fluorescent dye, and photographed with a fluorescence microscope interfaced with a digital camera. Automated image-analysis software located and sized fragments, based on YOYO-1 binding and assembled multiple scans, into whole-chromosome optical maps. The average size of each restriction fragment (measured in 30–100 different molecules in the assembly) was determined and used to create a linear “consensus map” on which each restriction site is represented by a vertical line.

Nucleotide sequences

The DNA sequences of the MLST loci have been deposited in GenBank under accession numbers EU294615-EU294706 (abcZ), EU294707-EU294797 (bglA), EU294798-EU294889 (cat), EU294890-EU294981 (dapE), EU294982-EU295073 (dat), (EU295074-EU295165 (ldh), EU295166-EU295257 (lhkA), EU294523-EU294614 (prfA), EU295258-EU295336 (actA), and EU295337-EU295423 (inlA).

Competing interests

The authors declare that they have no competing interests.

Authors’ contributions

OG and ST carried out the molecular genetic studies, participated in the sequence alignment. AK carried out the PFGE analysis. MR and AL carried out the MLST analysis. SMR carried out the phenotypic studies. BS performed the statistical analysis. GK carried out the optical mapping. LM and ALM participated in the design of the study. PhV and SMR conceived of the study, and participated in its design and coordination, helped to draft the manuscript. All authors read and approved the final manuscript.

Supplementary Material

Additional file 1:

Describes theListeria strains used in this article[[7],[8],[10],[15],[26-30]].

Additional file 2:

Describes the primers used for the amplification and sequencing of the housekeeping genesabcZ,bglA,dapE, dta, kat,ldh and lhkAand the virulence genes prfA, actAandinlA. The primers used for the verification of an inserted fragment in the “clpP” region have been also given.


This study was supported by grants from the Conseil Régional du Centre and the Ministère de l’Agriculture et de la Forêt, by Institut Pasteur (Paris, France), and the Institut de Veille Sanitaire (Saint-Maurice, France). It was also funded by an INRA food research programme. S. Témoin holds a Doctoral fellowship from the Région Centre and the Institut National de Recherche Agronomique.


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