A 6 year Geohelminth infection profile of children at high altitude in Western Nepal
© Mukhopadhyay et al; licensee BioMed Central Ltd. 2008
Received: 31 August 2007
Accepted: 27 March 2008
Published: 27 March 2008
Geohelminth infections are a major problem of children from the developing countries. Children with these infections suffer from developmental impairments and other serious illnesses. This study aimed to measure the prevalence of geohelminth infection, infection intensity as well as the change in the intensity in children from Western Nepal over years.
This 6-year hospital based prospective study at the Manipal Teaching Hospital, Pokhara included children (< 15 years) visiting the hospital from Kaski and 7 surrounding districts. Samples were also collected from children in the community from different medical camps. Three stool samples from every child were processed using direct and concentration methods. The Kato-Katz technique was used for measuring the intensity of infection.
The overall prevalence in hospital - attending children was 9.2% with 7.6% in preschool (0 – 5 y) and 11.0% in school-age (6 – 15 y) children, and in community 17.7% with 14.8% in pre-school and 20.5% in school-age children. Ascaris lumbricoides, Trichuris trichiura, Ancylostoma deodenale and Strongyloides stercoralis were the common geohelminths with a gradual decrease in worm load over the years. School-age children were found to be significantly more prone to geohelminth infection as compared to preschool children, but no statistical difference was detected by gender, district as well as season.
This heavy infection of geohelminths in children should be corrected by appropriate medication and maintaining strict personal hygiene. Health education, clean water, good sewage management and a congenial environment should be ensured to minimise infection.
Geohelminth infections are a major problem in developing countries of the South-east Asian region [1, 2], yet there is little information for most of the countries that describes the intensity of the problem. There are relatively simple but effective control strategies for these widespread diseases which, unfortunately, are often overlooked. The public health burden of these helminth infections has been consistently underestimated, although school-age children are at highest risk and may suffer from nutritional deficits, cognitive impairments, serious illnesses, and in occasional cases, death [2–8]. The risk of the individuals suffering geohelminth infection-related morbidity appears to be a joint function of the number of species harboured and/or the infection intensity of any species [9, 10].
Geohelminth infection prevalence rate of nearly 100% has been reported from local population in Nepal [11–13], whereas the annual prevalence rate among rural population during years 1985–92 was documented within the range of 18.0–36.6% with a marginal decrease in successive years . The incidence, however, showed an increase after the year 1992. A baseline parasitological survey (supported by the World Food Programme) in 1996 from Parsa and Dailekh districts in Nepal among 711 school children (mean age 9.266), showed an overall prevalence of 90% with Ascaris lumbricoides 21.9%, Trichuris trichiura 19.2% and hookworm 64.7%. Moderate to heavy infection was seen in 20% of the children. Boys were more infected than girls .
The inhabitants of Kaski and the surrounding districts like Lamjung, Manang, Myagdi, Baglung, Parbat, Shangha and Tanahu use tap water as well as river/lake water for drinking and household purposes. Some houses are pucca (made of brick and cement) with attached bathroom. Health control measures like tap water supply, deworming programmes of school-age children, decontamination of well water sources have been started but have failed to protect against exposure to environmental health risks due to frequent supply of unsafe drinking water, inadequate sanitation and excreta disposal, poor drainage, inadequate solid waste removal, lack of animal control, and improper protection of catchment area which have all been identified as important risk factors in the transmission of geohelminth infection [16, 17]. Some home-based water treatment systems with filtration, flocculation and safe sealed storage containers are used by the local people. Lack of hygienic behaviour by children and adults clearly increase the risk of geohelminth infection [18, 19]. Home gardens are a source of income generation as well as a regular source of fruits and vegetables in this part, where night soil is used as manure and most of the people work bare-foot . This makes them more susceptible to geohelminthiasis.
The aim of this study is to report the prevalence and intensity of geohelminths in children, and its association with seasonal variation in Western Nepal.
Pokhara the capital city of Kaski district (one of the seventy-five districts of Nepal), Gandaki zone, is located in the western part of Nepal at an altitude of 2,713 feet/827 m above sea level. The annual rainfall is approximately 3,200 mm, highest being in the months of July to September with an average monthly temperature of 16–26°C. The prospective hospital based study was conducted at the Manipal Teaching Hospital, Pokhara for a period of 6 years (October 1999 – May 2005). This institute hospital is the only tertiary care centre at Pokhara which caters services to the people of the Kaski and its surrounding districts.
Three stool samples were collected in waterproof screw capped plastic containers from each of the 2062 (1204 males and 858 females) children below 15 years, who provided informed written consent/child assent. The consent was obtained either from the parents of the children or the adult guardians (e.g. school teacher) accompanying the children. The children were either admitted to the hospital or visited the out patient department. Three stool samples were also collected from 220 children (126 males and 96 females) who came for medical care at different medical camps as a part of community survey in all the 8 districts, including Kaski. These children had not visited hospital for at least 2 months, and had not received any antihelminthic treatment. The sample size was not uniform from every camp. The samples were processed immediately using direct method. Formol – Ether concentration method was used to increase the yield of helminth eggs . The Kato-Katz technique was used to measure the intensity of infection since it provides an accurate measure of the number of eggs present [21, 22]. Intensity of infection was described as range of infection, arithmetic mean and geometric mean. Infection intensity was further classified as light, moderate and heavy according to WHO criteria .
Every year was divided into 4 seasonal patterns: January – March (Spring), April – June (Summer), July – September (Monsoon) and October – December (Winter) according to the local meteorological office.
Statistical analysis was done using SPSS 15 for Windows. Comparison of categorical variables was carried out with Chi-square continuity correction or Fischer's exact tests. Normally distributed data were analyzed using Student's t – test and analysis of variance (ANOVA). Association among soil-transmitted helminth species was investigated by 2 × 2 contingency table, for which the Chi-square statistics was calculated. Values of p < 0.05 were taken as significant. The study received approval from the institutional ethical board. Quality check on our methodology for egg counting was maintained by examining each specimen by three different staff members and if the variation in the results of microscopy was < 10%, it was taken into consideration .
The children were divided into two age groups: 0–5 years (pre-school) and 6–15 years (school-age). Study group comprises 1099 preschool and 963 school-age children and control group comprises 108 preschool and 112 school-age children.
The overall prevalence of the geohelminth infection was 9.2% (189/2062) in children attending hospital whereas 17.7% (39/220) in children in community. In the study group, 83 (43.9%) preschool and 106 (56.1%) school-age children had infection. The prevalence of geohelminth infection in the preschool children was 7.6% (83/1099) in hospital and 14.8% (16/108) in community whereas in school-age children, 11.0% (106/963) in hospital and 20.5% (23/112) in community.
Distribution of geohelminths by age
0 – 5 years
6 – 15 years
AL + TT
A + H
H + TT
The study population surveyed in the Western Nepal and the intensities of geohelminths
Total no. of stool examined (n = 2062)
No. (%) of positive stool (n = 189)
Distribution of geohelminths by year
No. of samples studied n = 2062
No. of positive samples number (%) Total 189
Mixed infection Total 29
356 – 88596
112 – 1212
4656 – 8564
578 – 99624
102 – 924
4438 – 5172
412 – 110124
88 – 1278
2516 – 5554
456 – 112342
48 – 720
1302 – 4122
162 – 6778
24 – 578
226 – 4664
24 – 4762
28 – 234
232 – 5236
138 – 4654
78 – 172
412 – 912
Prevalence and intensities of geohelminths, by gender, age and season in the children attending hospital in Western Nepal
Total no. of cases studied
Total no. of Positive cases (n = 189)
146 – 112342
28 – 1278
886 – 8564
24 – 110124
24 – 924
232 – 5666
0 – 5 y (1099)
146 – 66428
28 – 924
226 – 5486
6 – 15 y (963)
24 – 112342
24 – 1278
232 – 8564
258 – 99624
78 – 1278
226 – 7822
24 – 112342
98 – 1034
1022 – 8564
138 – 88596
48 – 156
684 – 5172
Geohelminth infections are prevalent in many countries, especially in tropics and subtropics and continue to be of importance due to their high prevalence and effects on morbidity in the population . To our knowledge, this is one of the most descriptive hospital based geohelminth studies from the South East Asian region, which has been carried out to determine the prevalence and intensity in children at a high altitude. Three aspects enhance the importance of this study: (1) This is one of the few and most exhaustive studies over a period of 6 years on geohelminths carried out at high altitude, (2) our study mainly concerns children of Western Nepal who usually have low nutritional uptake and high energy expenditure, and (3) this study measures the prevalence, infection intensity and changes in the intensity over years.
The infection rate among children in hospital (9.2%) and in the community (17.7%) from our study was not high as reported in other studies [24–27], although none of these studies were carried out at high altitude. However, a study from the plain lands of Sri Lanka showed low prevalence, ranging from 2.0–5.4% in 1997–99 . Despite inadequate sanitation, poor hygiene (indiscriminate defecation), inaccessible health care and poverty of this region, the results obtained in our study are markedly lower than the other developing as well as developed countries [24–27]. This may be due to execution of proper heath control measures in Kaski district like municipality tap water, deworming programmes for school-age children and health education regarding treatment of well water. A study from the high altitude of Bolivia showed the prevalence rates of 18.0% and 23.8% in school and community surveys , which are comparable to our findings.
Few authors have suggested that the altitude along with its unique environmental characteristics have a prominent effect over the infection pattern in human beings [30–32]. Western Nepal is located at a high altitude where the average monthly temperature is 16–26°C with high evapotranspiration and intense solar radiation. These characteristics are in additional to the typical lower partial oxygen pressure in ambient air at high altitude. Geohelminths like A. lumbricoides and T. trichiura have similar life cycles and are transmitted by eggs which require optimum environmental conditions and time to embryonate into the infective stage, once voided in the host faeces. The moisture in the soil during monsoon and late summer help in the molding within the eggs. The presence of autochthonous hookworm and S. stercoralis is worth mentioning, since similar high altitude study from Bolivia highlighted the absence of these two nematodes in their study . A 12-month-study in slum areas found significant reductions of the prevalence and the intensity of A. lumbricoides and T. trichiura infections , where seasonal variation was considered as one of the probable explanations . However, the lack of significant association with seasonal changes in our case strengthens the findings in the Bolivian study, that the transmission is not always seasonal. However, results from a hospital based survey do not warrant significance and additional community surveys in this geographical area would help understand this pattern.
The comparative high infection load of both A. lumbricoides and hookworm in children does not correspond to the intensity pattern of T. trichiura, which is always light. This finding may perhaps be related with the difference in egg viability of this species [31, 32]. The prevalence of A. lumbricoides and T. trichiura is also associated with age. A. lumbricoides infection is highest among children and decreases with age whereas infection of T. trichiura rises during childhood and adolescence and an increase is seen till old age . A study from rural Honduran communities observed that tap water, as a source of drinking water might be responsible for the high prevalence of A. lumbricoides, but not infection with T. trichiura, whereas heaviest infection with both the species was encountered in those communities, where people had to walk long distance to get water . However, the reason for this association was not certain. In Pokhara, almost all the houses are supplied with municipal tap water, which might have a coincidental association with the high load of A. lumbricoides as compared to T. trichiura. Results obtained from three samples for an individual were more significant than compared to single specimen analysis. Of the three samples collected, occasionally in one sample no geohelminth was detected but results were positive for the remaining samples. This may be due to intermittent shedding of geohelminth eggs/larva in stool .
Many observers have indicated a definite relation between gender and the transmission of infection . In our study, both males and females have a more or less similar infection rate. The infection rate could depend on the role giving one or other sex greater exposure to the contaminated soil. The significantly increased intensity of geohelminth infection in school-age children can be explained by the fact that they are more exposed to unhygienic practices, contaminated foods and water. Children below 5 years are usually under direct supervision of the parents and consume home prepared foods. Although the prevalence of infection is more in the community level, the intensity is higher in those children who visited hospital. Light infections in community children are mostly asymptomatic, whereas moderate to heavy infection might give rise to clinical symptoms. Since the survey is hospital based, it does have many drawbacks. The findings suggest that there might be an overall increase in prevalence of geohelminth in this geographical area. However, few children attended hospital with heavy infection than in the previous years, which might be an effect of regular prescription of antihelminthic drugs to the children from the hospital. The true picture might be different, which can only be assessed with mass community survey in this area. It would also be interesting to study the association of spatial patterns and environmental risk factors including the elevation, temperature and annual rainfall from each district with that of helminth infections. The treatment follow up of the children was not done due to poor turn up, which could have provided the evidence of the effectiveness of the deworming programme.
The Kaski district (Pokhara) in Western Nepal can be classified as Grade III according to WHO grading system . However, a hospital-based study may not be appropriate to draw a conclusion regarding community prevalence and label it an endemic area. The study would be a healthy base for future community epidemiological studies of geohelminthic infection in Nepal.
We acknowledge the active cooperation of all the patients and participants who are involved in this study and the helpful attitude of the clinician friends attending those patients.
- Montresor A, Crompton DWT, Hall A, Bundy DAP, Savioli L: Guidelines for the evaluation of soil-transmitted helminthiasis and schistosomiasis at community level. Geneva, Switzerland: World Health Organization. WHO/CTD/SIP/98.1.
- WHO: Prevention and Control of Intestinal Parasitic Infections. Report of a WHO Expert Committee. Geneva, Switzerland: World Health Organization, Technical Report Series. 1987, , no.749Google Scholar
- Callender JEM, Grantham-McGregor S, Walker S, Cooper ES: Trichuris infection and mental development in children. Lancet. 1992, 339: 181-10.1016/0140-6736(92)90246-Y.View ArticlePubMedGoogle Scholar
- Cooper ES, Whyte-Allenge CAM, Finzi-Smith JS, MacDonald TT: Intestinal nematode infections in children: the pathophysiological price paid. Parasitology. 1992, 104 (Supplement): S91-S103.View ArticlePubMedGoogle Scholar
- Crompton DWT, Montresor A, Nesheim MC, Savioli L: Controlling disease due to helminth infection. 2003, Geneva, Switzerland: World Health OrganizationGoogle Scholar
- Savioli L, Bundy D, Tomkins A: Intestinal parasitic infections: a soluble public health problem. Transactions of the Royal Society of Tropical Medicine and Hygiene. 1992, 86: 353-354. 10.1016/0035-9203(92)90215-X.View ArticlePubMedGoogle Scholar
- Nokes C, Bundy D: Does helminth infection affect mental processing and educational achievement?. Parasitology Today. 1994, 10: 14-18. 10.1016/0169-4758(94)90348-4.View ArticlePubMedGoogle Scholar
- Levav M, Mirsky AF, Schantz PM, Castro S, Cruz ME: Parasitic infection in malnourished school children: effects on behaviour and EEG. Parasitology. 1995, 110: 103-110.View ArticlePubMedGoogle Scholar
- Booth M, Bundy DAP, Albonico M, Chwaya HM, Alawi KS, Savioli L: Associations among multiple geohelminth species infections in schoolchildren from Pemba Island. Parasitology. 1998, 116: 85-93. 10.1017/S003118209700190X.View ArticlePubMedGoogle Scholar
- Ezeamama AE, Friedman JF, Olveda RM, Acosta LP, Kurtis JD, Mor V, McGarvey ST: Functional Significance of Low-IntensityPolyparasite Helminth Infections in Anemia. J Infect Dis. 192 (12): 2160-70. 10.1086/498219. 2005 Dec 15; Epub 2005 Nov 11.
- Rai SK: Helminthic infestation in local Nepalese people. Ankur, Institute of Medicine Central Campus (Nepal). 1980, 4: 69-74.Google Scholar
- Reily C: 1980, Dooly Foundation, Kathmandu, Nepal: Gorkha Report
- Estevez EG, Levine JA, Warren J: Intestinal parasites in a remote village in Nepal. J Clin Microbiol. 1983, 7: 160-161.Google Scholar
- Rai SK, Nakanishi M, Upadhyay MP, Rai CK, Hirai K, Ohno Y: Effect of intestinal helminth infection on some nutritional parameters among rural villagers in Nepal. Kobe J Med Sci. 1998, 44: 91-98.PubMedGoogle Scholar
- Bordignon GP, Shakya DR: A deworming programme in Nepal supported by the World Food Programme. Controlling disease due to helminth infections. Edited by: Crompton DWT, Montresor A, Nesheim MC, Savioli L. 2003, World Health Organization, GenevaGoogle Scholar
- Crompton DWT: Ascaris and childhood malnutrition. Trans Royal Soc Trop Med Hyg. 1992, 86: 577-579. 10.1016/0035-9203(92)90133-W.View ArticleGoogle Scholar
- Kang G, Mathew MS, Rajan DP, Daniel JD, Mathan MM, Mathan VI, Muliyli JP: Prevalence of intestinal parasites in rural Southern Indians. Trop Med Int Health. 1998, 3: 70-75. 10.1046/j.1365-3156.1998.00175.x.View ArticlePubMedGoogle Scholar
- Naish S, McCarthy J, Williams GM: Prevalence, intensity and risk factors for soil-transmitted helminth infection in a South Indian fishing village. Acta Tropica. 2004, 91: 171-187. 10.1016/j.actatropica.2004.04.004.View ArticleGoogle Scholar
- Holland CV, Taren DL, Crompton DWT, Nesheim MC, Sanjur D, Barbaeu I, Tucker K, Tiffany J, Rivera G: Intestinal helminthiases in relation to the socioeconomic environment of Panamanian children. Soc Sci Med. 1988, 26: 209-213. 10.1016/0277-9536(88)90241-9.View ArticlePubMedGoogle Scholar
- CARE Nepal: A study of the evaluation of home gardening programme in Bajura and Mahottari districts. 1995, Project Report, Nepal, Kathmandu: CARE NepalGoogle Scholar
- Gillespie SH: Intestinal Nematodes. Principles and Practice of Clinical Parasitology. Edited by: Gillespie SH, Pearson RD. 2001, John Willy & Sons, Ltd, New York, 21: 562-583.View ArticleGoogle Scholar
- Ash LR, Orihel TC, Savioli L: Bench aids for the diagnosis of intestinal parasites. 1994, Geneva, Switzerland: World Health OrganizationGoogle Scholar
- WHO: Intestinal protozoan and helminthic infections: report of a WHO Scientific Group. WHO Tech Rep Ser. 1981, 666-Google Scholar
- Hillyer GV, Soler De Galanes M, Lawrence S: Prevalence of intestinal parasites in a rural community in north-central Puerto Rico. Bol Assoc Med PR. 1990, 82: 111-114.Google Scholar
- Ferrari JO, Ferreira MU, Camargo LM, Ferreira CS: Intestinal parasites among Karitiana Indians from Rondonia State, Brazil. Rev Inst Med Trop Sao Paulo. 1992, 34: 223-225.View ArticlePubMedGoogle Scholar
- Oberg C, Biolley MA, Duran V, Matamala R, Oxs E: Intestinal parasites in the riverside population of Villarrica Lake Chile. Bol Chil Parasitol. 1993, 48: 8-11.PubMedGoogle Scholar
- Ferreira CS, Ferreira MU, Nogueira MR: The prevalence of infection by intestinal parasites in an urban slum, Sao Paulo, Brazil. J Trop Med Hyg. 1994, 97: 121-127.PubMedGoogle Scholar
- Behnke JM, Clercq DD, Sacko m, Gilbert FS, Ouattara DB, Vercruysse J: The epidemiology of human hookworm infections in the southern region of Mali. Trop Med Int Health. 2000, 5: 343-354. 10.1046/j.1365-3156.2000.00553.x.View ArticlePubMedGoogle Scholar
- Flores A, Esteban JG, Angles R, Mas-Coma S: Soil-transmitted helminth infections at very high altitude in Bolivia. Trans Royal Soc Trop Med Hyg. 2001, 95: 272-277. 10.1016/S0035-9203(01)90232-9.View ArticleGoogle Scholar
- Meakins RH, Harland PSEG, Carswell F: A preliminary survey of malnutrition and helminthiasis among school children in one mountain and one lowland Ujamaa village in northern Tanzania. Trans Royal Soc Trop Med Hyg. 1981, 75: 731-735. 10.1016/0035-9203(81)90164-4.View ArticleGoogle Scholar
- Crompton DWT, Nesheim MC, Pawlowski ZS: Ascaris and its public health significance. 1989, London, New York and Philadelphia: Taylor & FrancisGoogle Scholar
- Appleton CC, Gouws E: The distribution of common intestinal nematodes along an altitudinal transect in KwaZulu – Natal, South Africa. Ann Trop Med Parasitol. 1996, 90: 181-188.PubMedGoogle Scholar
- Hadju V, Stephenson LS, Mohammed HO, Bowman DD, Parker RS: Improvements of growth, appetite, and physical activity in helminth-infected school boys 6 months after single dose of albendazole. Asia Pacific J Clin Nutr. 1998, 7: 170-176.Google Scholar
- Cabrera BD: Reinfection and infection rates of ascariasis and trichuriasis among school children in relation to seasonal variation in the Philippines. South Asian J Trop Med Pub Hlth. 1984, 15: 395-401.Google Scholar
- Verle P, Kongs A, De NV, Thieu NQ, Depraetere K, Kim HT, Dorny P: Prevalence of intestinal parasitic infections in northern Vietnam. Trop Med Int Health. 2003, 8: 961-964. 10.1046/j.1365-3156.2003.01123.x.View ArticlePubMedGoogle Scholar
- Smith HM, DeKaminsky RG, Niwas S, Soto RJ, Jolly : Prevalence and intensity of infections of Ascaris lumbricoides and Trichuris trichiura and associated socio-demographic variables in four rural Hounduran communities. Mem Inst Oswaldo Cruz. 2001, 96: 303-314. 10.1590/S0074-02762001000300004.View ArticlePubMedGoogle Scholar
- The pre-publication history for this paper can be accessed here:http://www.biomedcentral.com/1471-2458/8/98/prepub
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.