COMUNICACIONES REPORTS

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1 COMUNICACIONES REPORTS COMUNICAÇÕES EPIDEMIOLOGICAL STUDY OF INTESTINAL PARASITIC INFECTIONS IN A RURAL AREA FROM ZULIA STATE, VENEZUELA L. CHACIN-BONILLA, N. GUANIPA, G. CANO, A.M. PARRA, J. ESTEVEZ and X. RALEIGH SUMMARY A point prevalence survey for intestinal parasites was conducted in 890 subjects 7 months to 75 years of age in a rural community of Zulia State, Venezuela. Single stool specimens were collected and examined using iron-hematoxylin stained fecal smears and formalin-ether concentration. The overall parasitic infection rate was 64.5% and 50.7% of the population had multiple infections. Pathogens were observed in 52.3% of the subjects. Ascaris lumbricoides (23.9%) and Trichuris trichiura (15.2%) were the most common helminths and, among the protozoa, Giardia lamblia was the most prevalent (21.8%). These parasites predominated in children. Entamoeba histolytica infections were identified in 9.4% of the subjects, with a high percentage of asymptomatic cyst carriers (85.7%). Entamoeba polecki was observed in one case. The overall amebic prevalence rate was (32.6%). The high rates of parasitic and multiple infections reflect the low living conditions of the study population and the public health importance of these agents in the area. Intestinal parasitic infections constitute one of the main medical and public health problems in Latin America (Raccurt et al. 1977; Penot et al. 1978; Lawrance et al. 1980; Aguilar 1981; Botero 1981; Kilpatrick et al. 1986). In Venezuela, background levels of parasitic infections in the population are generally unknown since most of the surveys have been either wholly or in large part based on clinical population and routine hospital techniques have been used for the examination of stool specimens. Extensive studies of helminth infections all over the country in showed high infection rates with Trichuris trichiura (77%), Ascaris lumbricoides (59%) and hookworm (52%). The latter had a lower prevalence (27%) in coastal areas, including Zulia State. Preva- KEY WORDS / Intestinal parasites / Epidemiology / Venezuela / Leonor Chacín de Bonilla. Doctor in Medical Sciences from the Universidad del Zulia, Maracaibo; Postgraduate course in Parasitology at Tulane University, New Orleans, LA, U.S.A. Titular Research Professor at the Universidad del Zulia and chief of the Parasitology Section of the Instituto de Investigaciones Clínicas, Facultad de Medicina, LUZ. Member of the System for the Promotion of Researcher, Level II. Address: Instituto de Investigaciones Clínicas, Apartado 1151, Maracaibo, Venezuela. Neuro Guanipa. In Memoriam. Georgina Cano. Licenciate in Biological Sciences, Universidad del Zulia, Maracaibo. Research Scientist, FUNDA- CITE-ZULIA, Maracaibo. Address: Fundacite-Zulia. Apartado 376, Maracaibo, Venezuela. Ana María Parra. Licenciate in Nutrition and Dietetics and M.Sc. in Health Administration, Universidad del Zulia, Maracaibo. Asisstant Research Professor at the Universidad del Zulia. Address: Instituto de Investigaciones Clínicas, Apartado 1151, Maracaibo, Venezuela. Jesus Estevez. Physician from the Universidad del Zulia, Maracaibo. Aggregate Research Professor at the Universidad del Zulia. Address: Instituto de Investigaciones Clínicas, Apartado 1151, Maracaibo, Venezuela. Xiomara Raleigh. Chemical Technician. Address: Instituto de Investigaciones Clínicas, Apartado 1151, Maracaibo, Venezuela. Corresponding Author: Leonor Chacín-Bonilla. Instituto de Investigaciones Clínicas. Apartado Maracaibo, Venezuela. Phone and fax numbers: /98/04/ $ 3.00/0 241

2 RESUMEN Se realizó un estudio de prevalencia puntual de parasitos intestinales en 890 individuos de 7 meses a 75 años de edad en una comunidad rural del Estado Zulia, Venezuela. Se examinó un espécimen fecal por persona mediante frotis teñidos con hematoxilina férrica y concentrados con formol-éter. La tasa de infección parasitaria con una o más especies fue de 64.5% y el 50.7% de la población tenía parasitosis multiples. Se observaron parásitos patógenos en el 52.3% de los individuos. Ascaris lumbricoides (23.9%) y Trichuris trichiura (15.2%) fueron los helmintos más comunes y entre los protozoarios, Giardia lamblia fue el más prevalente (21.8%). Estos parásitos predominaron en niños. Se identificaron infecciones por Entamoeba histolytica en 9.4% de los sujetos, con un alto porcentaje de portadores asintomáticos (85.7%). Se observó Entamoeba polecki en un caso. La prevalencia amibiana total fue de 32.6%. Las tasas altas de infección parasitaria y parasitosis multiples reflejan las bajas condiciones de vida de la población estudiada y que estos agentes infecciosos constituyen un problema de salud pública en el area. lences of infection with Strongyloides stercoralis and Taenia spp. were 0.9% and 1.3%, respectively (Benarroch 1961). This study appears to be the first and unique detailed investigation of human helminthiasis in the country. Entamoeba histolytica infection rates have been estimated to be as high as 42.9% (Sociedad Venezolana de Gastroenterología 1962). However, this infection is misdiagnosed in this region, as in other areas of the world (Walsh 1986), since the diagnosis is usually based on direct fecal examination and Entamoeba hartmanni is not recognized as a separate species. Epidemiological data of intestinal parasites are sparse. In the last two decades, few studies in communities have been recorded (Yarzabal et al. 1983; Morales et al. 1984; Chourio-Lozano et al. 1988; Diaz et al. 1989, 1992). The lack of detailed work on the epidemiology of intestinal parasites in Venezuela for over 35 years, stimulated us to undertake studies of this nature. In order to obtain a more accurate picture of the status of these agents in the region, surveys have been performed in representative samples of several communities of low socio-economic status in Zulia State, northwestern Venezuela (Chacín- Bonilla and Dikdan 1981; Chacín-Bonilla et al. 1984, 1987, 1990 a, 1992 a, 1993) thus avoiding the bias inherent in the study of selected populations. These surveys have been based in the examination of single stool specimens, using accredited techniques for the diagnosis of intestinal parasites, such as, iron - hematoxylin staining (Tompkins and Miller 1947) and formalin-ether concentration (Ritchie 1948). The data have contributed to the knowledge of the epidemiology of intestinal parasites in the country, indicating high infection rates, at least with one species (54-92%) and multiple infections (49-89%). Trichuris trichiura (27-83%) and A. lumbricoides (20-75%) have been the most common parasites. Low infection rates with hookworm and S. stercoralis (1-8%, each one), Hymenolepis nana (1-10%), and Taenia spp. (0-0.3%), have been noted. Among protozoa, Giardia lamblia, has been the predominant pathogen (11-18%) and Entamoeba coli the most prevalent ameba (18-28%). Entamoeba histolytica and E. hartmanni have revealed prevalences of 3-9% and 1-6.5%, respectively. The present study provides additional objective data on the current parasitological situation in Venezuela. A point prevalence survey for intestinal parasites was conducted in a rural population Figure 1. Sketch map of Zulia State showing location of the study community ( ) and other previously surveyed areas ( ) from which no records of parasitic infections exist. Materials and Methods Study community The survey was undertaken in Machango a rural town, situated below sea level on the eastern coast of Maracaibo lake in the Baralt Municipium, Zulia State (Fig. 1). Topographically the area is flat and most of the streets are unasphalted, with soils of the clay type. The climate is tropical with a mean daily temperature of 28 o C. However, during the sunny periods which are prevalent most of the year, shades temperatures exceed 35 o C and exposed ground temperatures exceed 40 o C. The annual rainfall ranges from 900 to 1200 mm. It is irregular and usually predominant in the months april, may and from october to december. Baralt Municipium is 2816 Km 2 in size with a population, based in the 1992 census, of inhabitants (39.3% are in rural areas) and a population density of 21.6 persons per Km 2. At the time of the survey the population of Machango consisted of 1000 inhabitants belonging to 171 families sparsely distributed. The village features a low socio-economic status and poor environmental sanitation. The inhabitants are mainly agricultural workers (67.3%) and nine percent are unemployed, 43.6% are illiterate and health education is generally poor. Rubbish is burned in 66.7% of the households and in the remainder it is thrown away on the adjacent bushes. Homes lack indoor plumbing and other modern facilities. 242

3 Water is provided by trucks and storaged in pipes. Most of the families (61.2%) are fairly clean, a few (6.7%) are clean and the rest (32.1%) has poor hygiene. Forty six percent of the housing units have latrines, in the others defecation occurs in certain areas of the backyards of the houses or near the village in surrounding underbrush. Overcrowding (more than two persons per dormitory) is present in 38.2% of the households. In most of these (90.3%) there are domestic animals, such as, cats, dogs, poultry and pigs. Survey methods The parasitological survey was carried out during the dry season, between may and september Preliminary visits, with the assistance of the local medical staff, were made to each household to ensure understanding of the aim of the survey and to verify acceptability and cooperation. The majority of the families (165) collaborated in the study. Data pertaining to family identification, socio-economic conditions and gastrointestinal complaints were recorded. Single fecal specimens were obtained from each of 890 individuals and taken to the health center of the community. A portion of each specimen was preserved in formalin and fecal smears were made for immediate fixation in Schaudinn s fixative (Melvin and Brooke 1969). The material was then transported to the laboratory to be processed and examined by iron-hematoxylin-stained smears (Tompkins and Miller 1947) and formalin-ether concentration (Ritchie 1948) techniques. Facilities were not available for examination for Cryptosporidium parvum. Statistical analysis For data analysis, chisquared and Fisher s exact tests were used. Results were considered significant if the P value was less than Since the number of individual ameba infections was small for critical analysis, the amebic prevalence rate (APR), suggested as an index to protozoan infection (Brooke et al. 1955) was calculated; an individual infected with one or more of the most common amebae (E. coli, E. histolytica, E. hartmanni and Endolimax nana) was counted as a single positive. Results The estimated prevalences of intestinal parasites in the 890 individuals examined are shown in Table I. Sixteen different parasitic species were identified. Infection rates with one or more parasites and with any pathogen were high (64.5 and 52.3%, respectively). The most common helminths were A. lumbricoides (23.9%) and T. trichiura (15.2%). Among protozoa, G. lamblia was the predominant with a high overall infection rate (21.8%); other flagellates showed low prevalences. Entamoeba coli and E. nana presented similar infection rates of 14.8% and 13.7%, respectively. Entamoeba histolytica was observed in 9.4% of the subjects with a high rate of asymptomatic cyst carriers (85.7%); trophozoites with ingested red boold cells were found in only five of the infected cases (5.9%). Entamoeba hartmanni was detected with a lower frequency (6.1%). Entamoeba polecki and Balantidium coli, were seen in one and two cases, respectively. The overall amebic prevalence rate (32.6%) was high. A high percentage (50.7%) of multiply infected persons was observed. Most of them carried two or three different organisms (Table II).There was a steady decrease in the percentage of subjects harbouring progressively higher numbers. The number of species infecting an individual did not vary according to age. Breakdown by age groups is given in Table III. The highest rate of infection with TABLE I INTESTINAL PARASITE PREVALENCES IN 890 SUB- JECTS FROM MACHANGO A. lumbricoides and T. trichiura occurred in the 7-12 year group. These infections were significantly more frequent in this age and the youngest group than in those aged (P< 0.05), (P<0.0001) or >45 (P<0.02) years. G. lamblia was frequent in all the age groups. However, this protozoan exhibited a high plateau in the children and adolescents, with a slight peak in the youngest group, and then declined in adults. The prevalence rates in the two children groups were highly significant with respect to the adult groups (P Positive specimens Parasite No. % Ascaris lumbricoides Trichuris trichiura Hookworm Strongyloides stercoralis Hymenolepis nana Giardia lamblia Chilomastix mesnili Trichomonas hominis Balantidium coli Entamoeba histolytica Entamoeba hartmanni Entamoeba coli Entamoeba polecki Endolimax nana Iodamoeba butschlii Dientamoeba fragilis Amebic prevalence rate Any pathogen Parasitic infection rate TABLE II FREQUENCY (%) OF SINGLE AND MULTIPLE INFEC- TIONS BY AGE OF 574 PARASITIZED INDIVIDUALS Age group (years) >45 All ages No. of species n=141 n=130 n=95 n=141 n=67 n=574 One Two Three Four Five Six Seven <0.0001), while the rate in the 13 to 18 year old group varied to a less extent in regard to the and >45 age groups (P <0.005) and P<0.001, respectively). No other statistical significances were noted according to age. The APR in each age group was high. A somewhat lower rate was noted in the youngest age group, then it reached a plateau around 34% in the 7 to 12 age group and remained levelled through the >45 age group. No significant differences were noted in regard to sex. However, there was a tendency for the APR 243

4 to increase with age in females, while in males it peaked in school children (Table IV). No clear-cut correlation between parasite prevalences and environmental factors could be found. Discussion Although underestimation of prevalence of intestinal parasites may result from the present data since single stool specimens were examined, a great variety of species (16), high infection rates with at least one of them (64.5%) and multiple parasitoses (50.7%) were observed, suggesting the frequent exposure to human fecal contamination of this population. These results are consistent with other recent studies (Yarzabal et at. 1983; Chourio-Lozano et al. 1988; Díaz et al. 1989, 1992). The prevalences of helminths, specially those of A. lumbricoides and T. trichiura were not as high as it can be expected from a rural population of a developing country. Indeed, seventy five percent of the rural people of Venezuela harboured helminths in the 1970s and in the neighboring country, Colombia, they are parasitized twice as frequently as those from urban areas (Botero 1981). The sparse host population of the village and the dry season, during which the survey was performed, together with the open space, and the unshaded immediate environment of households might interfere to some extent with transmission of parasites. These factors might explain the fact that A. lumbricoides was the predominant helminth, since the ova of this parasite is extremely resistant as compared to the more delicate whipworm ova. Besides, the presence of clay soils in the area is not favourable for the development of the latter (Beaver et al. 1986). Hookworm infection was very rare despite it is conventionally described as a disease of rural areas, but it is particularly a TABLE III PERCENTAGE OF INTESTINAL PARASITIC INFECTIONS BY AGE IN MACHANGO problem in agricultural areas with excess water resources, which play an essential role in the maintenance of the infection in a community, but this is not the case in this study. The type of soil in Machango, besides its environmental conditions, may have diminished the risk of Age groups (years) Parasite > 45 n = 218 n = 166 n = 147 n = 248 n = 111 Ascaris lumbricoides Trichuris trichiura Hookworm Stongyloides stercoralis Hymenolepis nana Giardia lamblia Chilomastix meslini Trichomonas hominis Balantidium coli Entamoeba histolytica Entamoeba hartmanni Entamoeba coli Entamoeba polecki Endolimax nana Iodamoeba butschlii Dientamoeba fragilis Amebic prevalence rate TABLE IV PERCENTAGE OF INTESTINAL PARASITIC INFECTIONS BY SEX IN MACHANGO Age groups (years) Males Females > >45 Parasite n=107 n=86 n=84 n=109 n=51 n=111 n=80 n=63 n=139 n=60 Ascaris lumbricoides Trichuris trichiura Hookworm Strongyloides stercoralis Hymenolepis nana Giardia lamblia Chilomastix mesnili Trichomonas hominis Balantidium coli Entamoeba histolytica Entamoeba hartmanni Entamoeba coli Entamoeba polecki Endolimax nana Iodamoeba butschlii Dientamoeba fragilis Amebic prevalence rate infection since loose, friable soil is more effective than heavier soils for hookworm larvae to develop (Augustine 1926; Hominick et al. 1987). The no detection of Taenia spp. might be due to the methodology used because it is not always a reliable mean of diagnosis of these parasites, however they appear to be very uncommon in the region (Chacín-Bonilla and Dikdan 1981; Chacín-Bonilla et al. 1984, 1987, 1990 a, 1992 a, 1993). The infection rates with E. histolytica in this and previous studies ( %) are lower than those recorded be- 244

5 TABLE V COMPARISON OF PREVALENCE (%) OF INTESTINAL PARASITES IN MACHANGO AND OTHER AREAS FROM ZULIA STATE, VENEZUELA Urban areas * Rural areas Parasite Santa Rosa, San Luis, La Loma, Potreritos, Pueblo Nuevo Machango, Maracaibo San San Rafel La Cañada Miranda Baralt ** PD= Francisco del Mojan PD=23.2 PD=29.7 PD=21.6 PD= PD=75.3 Ascaris lumbricoides Trichuris trichiura Hookworm Strongyloides stercoralis Hymenolepis nana Taenia spp Giardia lamblia Chilomastix mesnili Trichomonas hominis Balantidium coli Entamoeba histolytica Entamoeba hartmanni Entamoeba coli Entamoeba polecki Endolimax nana Iodamoeba butschlii Dientamoeba fragilis Amebic prevalence rate Taenia spp Parasitic infection rate Multiple infections n=260 n=342 n=327 n=258 n=767 n=890 * Urban areas: >2500 persons ** PD: Population density (inhabitants per Km 2 ) at the time the survays were conducted fore in the area. The differences might be explained by the fact that our findings are based on the examination of stained fecal smears and E. hartmanni is considered as a separate species. In this study, most of the infected subjects were asymptomatic cyst passers and only a few had hematophagous amebae, unique microscopical evidence of invasion. Although this result probably underestimates the presence of hematophagy, our studies suggest that most of the cases of amebiasis in this region are symptomless. In fact, serological surveys of this infection with the hemagglutination test (Chacín-Bonilla et al. 1982; 1990b) showed seropositivity rates as high as 46%, but most of the reactors had low titers and most of the infected subjects had no demonstrable antibodies, suggesting a high level of transmission but a low prevalence of amebic disease. Entamoeba polecki and B. coli, common parasites of pigs, were observed in one and two cases, respectively. The former, which is still considered to be a rare parasite of humans, has been recorded eigth times in Venezuela (García Laverde 1977; Chacín-Bonilla 1992 b). The latter has been rarely recorded in this area. However, a relatively high concentration was noted in a community with close contact with pigs (García Laverde and Chacín - Bonilla 1975). It is noteworthy that, with the exception of A. lumbricoides, the most common parasite in this population was G. lamblia. Its prevalence was high, similar to that of A. lumbricoides and higher than those of other helminths and protozoa. The flaqellate was frequent in all the age groups. These findings and the fact that this parasite is currently the most frequently identified agent of waterborne disease in the United States accounting for over one hundred waterborne outbreaks worldwide (Craun 1990) suggest that drinking water may be an important route of transmission for contracting grandiasis in this community. The higher frequency of G. lamblia, A. lumbricoides, and T. trichiura in children may be related to the hygienic habits inherent to this age. No significant differences were noted among the age groups with regard to other parasitic infections. However, statistical significances might have been obtained if a larger number of infected subjects with each species had been observed. The high APR for all age groups suggests that these people acquire protozoan infections at an early age and continue at a high level throughout life. Continous transmission may be responsible for the no variation in the prevalence of infection among different age groups. These findings suggest that drinking water, a common factor for all the population, might be the main source of protozoan infections. However, direct spread of cysts from person-to-person, might be a contributory factor since, although no statiscally significant, there was a tendency for the APR to increase with age in females, who remain behind in the village and are in higher and closer contact with children. Therefore, they are likely of getting protozoan infections through this mechanism of transmission and the possibilities of contagions would augment with increassing age. Similar results were noted in other study (Chacín- Bonilla et al a). Undoubtedly there is an interrelation of environmental factors and several routes of tranmission may be implicated for intestinal parasites. In this rural settling, deficient environment and personal hygiene, unadequate disposal of feces, and lack of safe water could constitute a risk of direct or indirect exposure to contaminated material. The presence of pathogens in source waters may have a significant health risk to the exposed population, depending on the level of the contamination and the degree of treatment to achieve potable water. The present results show the need that health authorities look for the presence of pathogenic parasites, bacteria and viruses and the significance of drinking water in transmitting these etiologic agents at Machango, so that the public health risks can be defined and the appropriate control strategies can be developed In all of our epidemiological studies on intestinal parasites, stool samples have been collected, preserved, processed and examined using the same methodology. This help to provide a sound basis for comparing the prevalence 245

6 of parasites in each area of Zulia State. In contrast to previously surveyed villages, in this study A. lumbricoides was more frequent than T. trichiura, which is the most prevalent helminth in the Caribbean region (Raccurt et al. 1977; Grell et al. 1981) and it has been and still appears to be the dominant parasite in Venezuela (Benarroch 1961; Chacín-Bonilla and Dikdan 1981; Chacín-Bonilla et al. 1984, 1987, 1990 a, 1992 a) (Table V). The former communities, but one, are located just on the shores of the humid coast land of Maracaibo lake (Fig. 1) and moisture, which is a determinating factor in the distribution of helminths (Beaver 1986), appear to favour the development of their infective stages. Machango is far from the coast and its climatic and physical features appear to affect to a more extent the less resistant whipworm ova. The present findings agree remarkably with those observed before in demonstrating that high rates of parasitic infection with at least one species, multiple parasitoses and APR is the rule in communities of low socio-economic status of this region. In all places where there is a high prevalence of intestinal parasites, living conditions are inversely low. In fact, the village with the highest rate of parasitism, La Loma, San Rafael del Mojan, has the highest poverty rate (75-80%) and the worst environmental sanitation. Among these marginal populations there are many environmental and personal factors which may influence the presence and prevalence of these agents, but it is notewhorthy that the amount of intestinal parasitism is higher and seem to be overwhelming in those with the higher population densities. Zulia is a bordering state and during the last decades there has been an increasing immigration from Colombia, in addition to the usual emigration of the rural population of the country to urban centers, looking for better living conditions. Thus, most of the population of the state and that of the Maracaibo Municipium, where the capital city is located, is urban (86 and 99%, respectively). The uncontrolled urbanization of the urban areas, has brought about an increase of households without indoor plumbing and other modern facilities. This situation has probably augmented the amount of contamination occurring in these areas increasing the likelihood that a resident will come in contact with fecal deposits and therefore with infective forms of intestinal parasites. The prevalence of A. lumbricoides has been associated with high population densities (Diesfeld 1969) and it has been higher in urban areas of Vietnam (Colwell et al. 1971). On the other hand, although the unsafe drinking water of the state may be an important route of transmission of protozoa, the higher APR in the urban communities with the highest population densities, suggests that the direct route of transmission from personto-person, plays an important role in these areas. It is not known wheather the prevalence of intestinal parasites changes significantly with time in one region. However, the current and former surveys are strong evidences that intestinal parasites, specially helminths, tend to perpetuate and remain highly endemic in several areas of Zulia State, and perhaps among much of the country, since 55% of its population is poor. The data suggest that these agents constitute an important public health problem in this area and reflect no improvement in the standard of living of most of the population over the past four decades. ACKNOWLEDGEMENTS We are very grateful to Mrs. Socorro de Padrón for her valuable assistance. 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