BPKIHS, Dharan, Nepal 2 M.Sc. student, Dept. of Microbiology,

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1 International Journal of Advances in Health Sciences (IJHS) ISSN Vol 3, Issue 2, 2016, pp Research Article A Study of Prevalence of Intestinal Helminthic Infections and Associated Risk Factors among the Tea Estates workers of Ilam District, Eastern Region of Nepal Sah RB 1, Shah U 2 and Jha N 3 1 Associate Professor, School of Public Health and Community Medicine, BPKIHS, Dharan, Nepal 2 M.Sc. student, Dept. of Microbiology, Sunsari Technical College Pvt. Ltd., Dharan, Nepal 3 Professor & Chief, School of Public Health and Community Medicine, BPKIHS, Dharan, Nepal [Received-25/05/2016, Accepted-05/06/2016, Published- 25/06/2016] Corresponding Author Dr Ram Bilakshan Sah Associate Professor School of Public Health and Community Medicine B.P. Koirala Institute of Health Sciences Dharan, Nepal Phone: bilaksah@yahoo.com ABSTRACT Introduction: Intestinal parasites are widely prevalent in developing countries, probably due to poor sanitation and inadequate personal hygiene. It is estimated that as much as 60% of the world s population is infected with intestinal parasites, which may play a significant role in morbidity due to intestinal infections. Objectives: To measure the prevalence of intestinal Helminthic Infections and to identify risk factors associated with Helminthic Infections among the tea garden workers in Ilam district of Nepal. Materials and Methods: A Community based cross-sectional study was conducted among tea garden workers in Ilam district of Nepal. Out of 4 tea estates in Ilam District, 2 tea estates (Ilam Municipality and Kanyam) were selected randomly. Out of total 150 tea workers (30 in Ilam Municipality and 120 in Kanyam), 98 workers participated in the study. Semi-structured questionnaire was administered to the study subjects and Microscopic Examination of Stool was done. The Chi square test was used to measure the association of risk factors and helminthic Infections.

2 Results: Overall prevalence of intestinal helminthic infections among the tea garden workers was 18.4 percent. Hookworm species was found higher (10.2%) in comparison to other worms i.e. Ascaris lumbricoides (5.1%), Trichuris trichuria (2%) and Hymenolepsis nana (1%). Risk factors like Dalit in ethnicity, not treat water before drinking, not using soap before meal and after defecation, not having latrine, not wearing sandals, unhygienic clothes cleanliness, habit of nail biting and thumb sucking were found to be significant relationship in the causation of intestinal helminthic Infections. Conclusions: The findings of this study showed that intestinal helminthic infections remain highly endemic in the Tea Estates workers due to the poor personal hygiene and sanitary conditions. This strongly indicates a need for a comprehensive program to combat intestinal helminthes associated morbidity and mortality. Key words: Prevalence, Intestinal helminthic infections, Risk factors, Tea Estates workers, Ilam INTRODUCTION Intestinal parasitic infection is one of the major health problems in develop countries. It has been estimated to affect some 3.5 billion people globally and 450 million are thought to be ill as a result of such infections. 1 Intestinal helminthic infection i.e., Ascaris lumbricoides, hookworms, and Trichuris trichuira infection represents the most common neglected tropical disease (NTD) in South Asia 2 and has been increasingly recognized as an important public health problem, particularly in developing countries, including Nepal 3. The reported prevalence of intestinal parasitosis in Nepal varies considerably with over 90 percent prevalence in some areas. Overall helminthic infections alone rank fourth in the top ten lists of diseases in Nepal. The intestinal parasitosis remains to be one of the major problems in bigger cities like Kathmandu as well because of the contamination of the drinking water and soil by feces. 4 Previous studies have indicated that the prevalence of helminthic infection in a community is largely determined by individual characteristics or hygiene behavior. 5 For example, not using soap for hand-washing (Olsen et al.) 6 or not wearing sandals or shoes when walking outside (Phiri et al.) 7 were two important behavioral risk factors for helminthic infection in low and flat land areas in Nepal. Hence the present study was carried out to measure the prevalence of helminthic infections and to identify risk factors associated with helminthic infections among the tea garden workers in Ilam district of Nepal. Methodology A Community based cross-sectional study was conducted from 13 th December 2015 to 27 th December 2015 in tea garden workers in Ilam district of Nepal. This was a two weeks study to fulfill epidemiological management carried out by students of MBBS 3 rd year Batch 2013 of B. P. Koirala Institute of Health Sciences, Dharan, Nepal. This research was based on random selection of the study area Ilam District. Four tea estates under Nepal Tea Development Cooperation (NTDC) at Ilam District are Ilam Municipality, Kanyam, Soktim and Chilimkot. Out of 4 tea estates of Ilam District, 2 tea estates (Ilam Municipality and Kanyam) were selected randomly. Out of total 150 tea workers (30 in Ilam Municipality and 120 in Kanyam), 98 workers participated in the study. Ethical clearance was taken by Institutional Review Committee of B P Koirala Institute of Health Sciences, Dharan, Nepal. Written permission was taken from each incharge of Nepal Tea Development Cooperation (NTDC) at Ilam Municipality, Kanyam, and participants. Tea garden workers of both sexes, aged 18 years and above, having working experience of Sah RB, et al. 110

3 minimum 6 months and those who gave written consent were included in the study. Semi-structured questionnaire was administered to the study subjects and Microscopic Examination of Stool was done. In each visit more than 15 workers was enrolled & same number of plastic bottles was given for stool collection and collected next day morning. Microscopic examination of stool was done by preparing slide using Normal Saline and Lugol's Iodine to observe the ova of different intestinal helminthic parasites. First we used low power lens and afterwards the high power lens. Then we observed ova of different intestinal helminthic parasites. 8 The confidentiality and privacy of the study was maintained; name of the individuals or participating group was not disclose after the study. All interviewed questionnaires were indexed and kept on file. Data was entered in Microsoft Excel and converted into SPSS (Statistical Package for Social Science) 11.5 version for statistical analysis. The prevalence was calculated, Chisquare test was used to measure the association between risk factors and intestinal helminthic infections. The confidence level was set at 5% in which probability of occurrence by chance is significant if P< 0.05 with 95% Confidence Interval. RESULTS Table 1: Distribution of Helminthic Infections among study population Helminthic Infections Frequency Percent Helminths Positive Negative Total Name of Helminths Hookworm Ascaris lumbricoides Trichuris Trichuria Hymenolepsis nana Total Table 1 shows the status of helminthic infections among the Tea Estates workers of Ilam District. A total intestinal helminthic infection was found to be 18.4 percent. Hookworm was seen highest in comparison to other helminthes. Table 2: Association between sociodemographic characteristics with Helminthic Infections Helminthes Helminthes Characteristics Positive Negative Age years years >60 years Gender Male Female Religion Hindu Others (Muslim, Buddhist, Christian) Ethnicity Brahmin/Chhetri Janajati 12 (26.1) 6 (13.3) 0 (0.0) 2 (8.7) 16 (21.3) 14 (19.2) 4 (16.0) 2 (5.6) 4 (12.5) 34 (73.9) 39 (86.7) 7 (100.0) 21 (91.3) 59 (78.7) 59 (80.8) 21 (84.0) 34 (94.4) 28 (87.5) Total P-Value Sah RB, et al. 111

4 Dalit 12 (40.0) 18 (60.0) 30 Education Illiterate Below SLC SLC & above SLC 14 (23.7) 4 (12.5) 0 (0.0) 45 (76.3) 28 (87.5) 7 (100.0) Total 18 (18.4) 80 (81.6) 98 SLC: School leaving certificate The prevalence of helminthic infections was seen higher in female than male but the difference was not significant. The respondents from Dalit were found significantly higher helminthic infections than other ethnic groups (P<0.05). The helminthic infection was higher among study population who was illiterate than below School leaving certificate (SLC) and none of the participants were found to be helminthes positive who was SLC pass and above but the difference was not significant (Table 2). Table 3: Association between personal hygiene and food habit with Helminthic Infections Helminthes Helminthes Characteristics Positive Negative Source of drinking water at home Stream well Tap Water treat before drinking Yes No Hand wash before meal No wash Water only Soap Bath Regular Irregular Have latrine Yes No Hand wash after defecation Soap Water only Nothing Sandal wear Yes No Skin Clean Not clean Nail Cut clean Uncut & Unclean Clothes Clean Not clean Nail Biting Yes No 7 (33.3) 4 (25.0) 7 (11.5) 9 (11.5) 9 (45.0) 7 (58.3) 7 (30.4) 4 (6.3) 2 (10.5) 16 (20.3) 7 (9.3) 11 (47.8) 2 (3.1) 40 (40.0) 12 (50.0) 10 (12.3) 8 (47.1) 15 (23.1) 3 (9.1) 5 (11.9) 13 (23.2) 6 (9.2) 12 (36.4) 10 (52.6) 8 (10.1) 14 (66.7) 12 (75.0) 54 (88.5) 69 (88.5) 11 (55.0) 5 (41.7) 16 (69.6) 59 (93.7) 17 (89.5) 63 (79.7) 68 (90.7) 12 (52.2) 62 (96.9) 6 (60.0) 12 (50.0) 71 (87.7) 9 (52.9) 50 (76.9) 30 (90.9) 37 (88.1) 43 (76.8) 59 (90.8) 21 (63.6) 9 (47.4) 71 (89.9) Total P-Value < <0.001 < <0.001 Thumb Sucking Yes 13 (50.0) 13 (50.0) 26 <0.001 Sah RB, et al. 112

5 No 5 (6.9) 67 (93.1) 72 Food Habit Vegetarian Non-Vegetarian Cooking duration < 30 min 30 min Antihelminthic drugs taken Yes No 0 (0.0) 18 (18.9) 4 (28.6) 14 (16.7) 3 (100.0) 77 (81.1) 10 (71.4) 70 (83.3) 6 (14.0) 37 (86.0) (21.8) 43 (78.2) 55 Total 18 (18.4) 80 (81.6) Table 3 shows the study population using soap and water after defecation had significantly lower prevalence of helminthic infections than those using only water (P<0.001). The study population who did not wear sandal and shoes showed significantly higher prevalence of helminthic infections than those wear sandal (P<0.05). The association was also seen among the unhygienic clothes cleanliness and helminthic infections (P<0.05). The helminthic infections was seen higher among study population having the habit of nail biting and thumbs sucking (P<0.001). DISCUSSION Intestinal parasitic infection is most prevalent throughout the world, particularly in developing nations. Nepal is a landlocked, impoverished and least developed country located in South Asia where 70% of public health problems are due to infectious disease. 9 Intestinal parasitosis is one of the major causes of morbidity and mortality in Nepal. 4 Prevalence of worm infestation in this study was found to be 18.4 percent which is high as compared to the study conducted by Patel et al in Oman (9.4%) 10. Another study conducted by Parajuli RP et al in different parts of Nepal which showed 3.3% in Birendranagar in Chitwan, Nepal, 3.5% in Kuleshor in Kathmandu, Nepal, 11.7% in Kanyam in Ilam, Nepal, 17% in Birendranagar in Chitwan, Nepal which is also lower than our study. 11 This high rate of prevalence among tea tribe workers may be associated with unsanitary living style, poor socio-economic conditions, usual contact with soil and consumption of vegetables, fruits and water contaminated with infected faeces which was not considered in this study. The prevalence rate of Hookworm was found to be 10.2% followed by Ascaris lumbricoides (5.1%), Trichuris trichiura (2%) and Hymenolepsis nana (1%). A study conducted by Shrestha R et al in Bhaktapur district, Nepal showed seven different types of helminth parasites which were: Ascaris lumbricoides (22.6%), Trichuris trichiura (6.1%), Strongyloides stercoralis (1.8%), Hookworm (1.6%), Taenia sp. (1%), Hymenolepis nana (0.8%) and Enterobius vermicularis (0.4%). 12 These parasites had also been reported from rural area of Kirtipur, Nepal (Chaudhari 2004) 13, from rural areas of Southern Nepal (Sherchand et al. 1997) 14 and from Chepang children of Taklung, Gorkha, Nepal (Pokhrel 2005) 15. Several previous studies have shown that Hookworm was the most prevalent helminth parasite in Nepal (Estevez et al , Sherchand et al , Yong et al , Kunwar et al ). Similarly, some other studies have shown Trichuris trichiura as the most common helminth (Shrestha 1983 in Panchkhal 19, Uga et al , Pokhrel 2005 in Gorkha 15, Rai et al ). Reported previously (Gupta and Gupta , Manandhar , Sukupayo ) which also showed A. lumbricoides as most prevalent Sah RB, et al. 113

6 helminth in Nepal followed by T. trichiura. Williams-Blangero et al. (1993) 25 concluded that Roundworm, Whipworm and Hookworm were endemic in Nepal and were the major health problem for the population which seems to be still true. The high prevalence of soil transmitted helminthes (A. lumbricoides, T. trichiura, S. stercoralis and Hookworm) among helminthes has been increasingly recognized by WHO as an important public health problem, particularly in developing countries. A fecal-oral route is the established route of transmission of roundworm 26, 27 infection, but not hookworms infection. Similarly, a transdermal route of transmission is the established route of hookworm transmission, 27 but not roundworm infection. The reason for the difference might be the geography of the place or the socioeconomic condition of the study area and the habit of the study participants in relation to hygienic circumstances. The prevalence of hhelminthic infections was seen higher in female (21.3%) than male (8.7%) but the difference was not significant. But a study conducted by Emana D et al in South- Western Ethiopia in 2015 showed the prevalence of intestinal parasitic infection was slightly higher in male (43.1%) compared to female (40.5%) although the differences were not significant statistically. 28 This finding contradicts our earlier reports in which there were no gender differences in STH burden. 5 However, generally in Nepal, women work in agriculture and household activities to a significantly higher degree than men. 29 In the current study, females were involved more than men in agricultural activities (personal observation and communication with social workers). This might explain the elevated risk of helminthic infections burden among female participants as indicated by Brooker et al. 30 The prevalence of hhelminthic infections was seen significantly higher in Dalit (40%) than Janajati (12.5%) and Brahmin/Chhetri (5.6%). Ethnically, the prevalence of helminthic infections was higher among the Dalits and Tibeto-Burmans in comparison to Indo-Aryans. Similar results have been reported by Rai et al 21 and Rai et al 9 in Nepal. So, this value shows poor sanitation and water contamination and low socio-economic status affects in parasitic infestation and correlate with previous study. Dalits in Nepal have a relatively low literacy rate, unhygenic habits and low socio-economic status. 31 The prevalence of worm infestation was significantly higher among the workers drinking untreated water (45%) as compared to those drinking treated water (11.5%). The rate of infection was higher (29.4%) who using untreated water for drinking purpose whereas lower rate (9%) was found those using treated water for drinking. 32 This pattern of infection has also been reported by Wani et al. from India. 33 The reason is that treated water (boiling of water) for drinking purposes kills the microorganisms and prevents transmission of infection. Thus poor hygiene practices associated with type of water may be probable risk factor for increased parasitic infection. The infection rate of worm infestation among hand washing with soap and water after defecation was significantly lower (3.1%) than only use water (40%). This behavior might have stemmed from occupational life style as well as the people s perception of hygiene. Most people have lunch in their agricultural fields where they have neither enough water nor soap to wash. After working in the field, the people usually wash their hands with little water, because they believe that this cleans their hands sufficiently. On the basis of several interviews, it was found that such hand washing practices were thought Sah RB, et al. 114

7 to be good enough protection from helminthic infection. 5 Olsen et al. have also reported similar hand washing practices in Kenya. 6 Such risky behavioral habits, together with heavy population density in expanding suburbs, may have contributed to the survival of helminthic 34, 35 infection in these communities. Regular wearing of sandal or shoes had a significantly lower prevalence of helminthic infections (12.3%) than those did not wear sandal or shoes (47.1%). Behavioral habits of the people were associated with occupational lifestyle. For example, according to several interactions with community people, it was found that participants prefer to be bare foot while working in the agricultural fields, stating that wearing sandals or shoes is not comfortable. In addition, during personal communications, participants from the Khokana community claimed that it is useless to wear sandals or shoes to commute from their homes to the agricultural fields because of the proximity of homes to fields. Human feces, possibly contaminated with worm eggs, were observed on the stream banks, in the farmlands, or on small roads used by the people walking barefoot to and from their agricultural fields in all of the communities studied. 5 Based on previous research, it is presumed that some of the factors responsible for this prevalence may include; not wearing of shoes or footwear when walking around at home since this expose the skin to penetration by soil transmitted helminths infective larvae, e.g., Ancylostoma duodenale and S. stercoralis, biting of nails and failure to wash hands with soap and water, may also result in helminths entering the body via the oral-fecal route, e.g., Ascaris lumbricoides (Sah et al., 2013). 36 Poor environmental sanitation may also have resulted in this prevalence of helminthes (Ayalew et al., 2011), since, these organisms strive well in unhealthy environs and are very opportunistic in invading the human body e.g., Ascaris lumbricoides. 37 Among associated risk factors, hand washing habit before meal and toilet, and latrine usage habit were the major factor among tea tribe workers in the study area. Our results were in agreement with other studies from other parts of 38, 39 Ethiopia. This highlighted the need for integrated control of helminthic infections, i.e. deworming should be backed-up with health education to prevent re-infection. Because, the only way of re-infection with helminthes is exposure to the infective stages from contaminated environment as these parasites do not multiply within the human host. A first limitation is the small sample size available in the sub-group analysis which may affect the risk of type II error. Secondly, possible effects of sampling bias caused by non-random selection of participants might limit the generalizability of the findings. That is, since participants were selected on a first-come firstserve basis, there could be a chance that people with health concerns would be more likely to be included. CONCLUSION Intestinal helminthic infections are the major public health problem among the tea garden workers in Ilam district of Nepal, where the prevalence and intensity of infections is at alarming rate. Hookworm was seen highest in comparison to other helminthes. Risk factors like Dalit in ethnicity, not treat water before drinking, not using soap before meal and after defecation, not having latrine, not wearing sandals, unhygienic clothes cleanliness, habit of nail biting and thumb sucking were found to be significant relationship in the causation of intestinal helminthic Infections. Prevalence of helminthic infections in the study area was quite high and calls for at least annual mass drug Sah RB, et al. 115

8 administration in addition to prompting preventive actions like health education, personal hygiene and provision of clean water and improve the environmental sanitation and personal hygiene. ACKNOWLEDGMENT We would like to thank to School of Public Health and Community Medicine for approval of our research work. We would like to acknowledge the 5 th semester students of MBBS Batch of 2013 who helped us during the study period and participants of the tea garden workers in Ilam district of Nepal for their kind co operation. Conflict of Interest: No conflict of interest Funding: None REFERENCES 1. WHO. World Health Report- Conquering Suffering Enriching Humanity. Geneva: WHO, Lobo DA, Velayudhan R, Chatterjee P et al. The neglected tropical diseases of India and South Asia: review of their prevalence, distribution, and control or elimination. PLoS Negl Trop Dis 2011; 5 (10): e Shakya B, Rai SK, Singh A et al. Intestinal parasitosis among the elderly people in Kathmandu Valley. Nepal Med Coll J 2006; 8: Rai SK. Parasitic Diseases in Nepal. Federation of Asian Parasitologists, Japan 2005: Parajuli RP, Umezaki M, Watanabe C. Behavioral and nutritional factors and geohelminth infection among two ethnic groups in the Terai region, Nepal. Am J Hum Biol 2009; 21: Olsen A, Samuelsen H, Onyango-Ouma W. A study of risk factors for intestinal helminth infections using epidemiological and anthropological approaches. J Biosoc Sci 2001; 33: Phiri K, Whitty CJ, Graham SM et al. Urban/rural differences in prevalence and risk factors for intestinal helminth infection in southern Malawi. Ann Trop Med Parasitol 2000; 94: Godkar PB, Godkar DP. Microscopic examination of stool specimen. Text Book of Medical Laboratory Technology. 2 nd ed. Mumbai: Bhalani Publishing House; P Rai SK, Hirai K, Abe A, Ishiyama S, Rai G, Ono K. Intestinal parasitoses among school children in a rural hilly area of the Dhading district, Nepal. Nepal Med College J 2002; 4: Patel PK, Khandekar R. Intestinal parasitic infections among schoolchildren of the Dhahira Region of Oman. Saudi Med J 2006; 27: Parajuli RP, Fujiwara T, Umezaki M, Konishi S, Takane E, Maharjan M et al. Prevalence and risk factors of soiltransmitted helminth infection in Nepal. Trans R Soc Trop Med Hyg 2014; 109 (4): 1-9. doi: /trstmh/tru Shrestha R, Maharjan M. Prevalence of intestinal helminth parasites among schoolchildren of Bhaktapur district, Nepal. Nepalese Journal of Zoology 2013; 1 (1): Chaudhari B, Mishra PN, Sherchand JB. Prevalence of Human Intestinal Parasites in rural village development committee, Machchhegaun, Kathmandu. Royal Nepal Academy of Science and Technology, Khumaltar, Lalitpur 2004,SSZ-Ps8: Sherchand JB, Ohara H, Sherchand S, Cross JH, Shrestha MP. Intestinal Parasitic Infection in Rural Areas of Southern Nepal. Journal of Institute of Medicine 1997; 19 (3): Sah RB, et al. 116

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