Efficacy of a single dose albendazole chemotherapy on human intestinal helminthiasis among school children in selected rural tropical communities

Ekaett e Godwin Edelduok, Felicia Nkechi Eke1, Ngozi Evelyn Ezenwaji1, Chinedu Ifeanyi Atama1, Joseph Effi ong Eyo1 Department of Biological Sciences, Akwa Ibom State University, Ikot Akpaden, Mkpat Enin, Akwa Ibom State, 1Department of Zoology and Environmental Biology, University of , , State, Nigeria

ABSTRACT ORIGINAL ARTICLE Introduction: The impact of chemotherapy on human intestinal helminthiasis among school children in semi- urban tropical communities of Igbo-Eze South Local Government Area of , South-Eastern Nigeria, was investigated. Materials and Methods: Stool samples were obtained from 1296 school children (ages 4-15 years) from six schools randomly selected from the study area. Helminth eggs were recovered from stool samples. Those infected were treated with single oral dose of 400 mg albendazole tablets and re-examined for helminth eggs 4 weeks post- treatment. Results: Out of 1296 school children examined, 106 (8.1%) of the children were signiicantly (P < 0.05) infected with human intestinal helminths thus: 64 (4.9%) with Ascaris lumbricoides, 33 (2.5%) with hookworm and 9 (0.7%) with Trichuris trichiura. Out of the 64 children infected with A. lumbricoides, there was a reduction in the prevalence of infection by 18.8%. Furthermore, out of the 33 children infected with hookworm, there was a reduction in the prevalence of infection by 15.1%. Out of the nine children infected with T. trichiura, there was a reduction in the prevalence of infection by 22.2%. Conclusion: These indings suggest intestinal helminth speciicity to the eficacy of albendazole. Thus, further research into the development of more effective antihelminthic drugs is necessary.

Key words: Albendazole, Ascaris lumbricoides, chemotherapy, hookworm, human intestinal helminthiasis, rural tropical communities, school children, Trichuris trichiura

Introduction be affected.[5] Thus, human intestinal helminthiasis constitutes an important public health problem. Human Human intestinal helminthiasis is among the most intestinal helminthiasis can be prevented and controlled common infections afflicting humans in developing through various measures. According to Crompton,[4] countries. They are one of the world’s most important measures to control these infections should be aimed causes of retardation of physical and intellectual growth in at reducing morbidity. Chemotherapy has been an children.[1,2] Between 500 million and 1 billion people are important measure used in controlling human intestinal estimated to be infected annually world-wide.[3] According helminthiasis.[6,7] The approach used in chemotherapy to Crompton[4] an estimated 1472 million persons is often the mass treatment of human populations harbor Ascaris lumbricoides, 1298 millions are infected with antihelminthic drugs, a process known as mass with hookworm and about 1049 million with Trichuris drug administration.[7] World Health Organization trichiura. The global estimated prevalence of anemia (WHO) is actively promoting the approach of using in hookworm infection and of cognitive impairment in antihelminthic drugs in the community to lower the hookworm, Ascaris and Trichuris infections indicated intensity of human intestinal helminthiasis.[7] School- that for each parasite, 10-50 million persons may age children can benefit at any time from appropriate antihelminthic treatment given to reduce the intensity Access this article online of infections.[8,9] Human intestinal helminthiasis can be Quick Response Code: Website: treated with different drugs depending on the parasite www.atmph.org involved. The efficacy of mebendazole against soil- transmitted nematode infections has been reported to [9] DOI: be high. Other antihelminthic drugs recommended 10.4103/1755-6783.127776 by WHO for the control of soil-transmitted nematodes include albendazole, levamisole and prattle.[7] However, there have been concerns about the sustainability of

Correspondence: Prof. J. E. Eyo, Department of Zoology and Environmental Biology, University of Nigeria, Nsukka, Enugu State, Nigeria. E-mail: [email protected]

Annals of Tropical Medicine and Public Health | Jul-Aug 2013 | Vol 6 | Issue 4 413 Edelduok, et al.: Efficacy of albendazole on human intestinal helminthiasis deworming with antihelminthic drugs and the emergence Ethical issues of resistance. Thus, many of studies have been carried Informed oral consent was obtained from the pupil and out to assess the impact of chemotherapy on human headmasters/headmistresses of the schools. In addition, intestinal helminthiasis.[9-15] This notwithstanding, a meeting was held with the parents/guardians of the much still remains to be known about the impact pupils, informing them of the importance of the study of a single dose chemotherapy on human intestinal and seeking for their consent. Any pupil not willing to helminthiasis especially among infected children of Igbo- take part in the study was excluded. Pupils who were Eze South Local Government Area (LGA). Therefore, positive for human intestinal helminths were treated this study was carried out to investigate the impact of with appropriate antihelminthic drugs using trained alblendazole chemotherapy on school children infected nurses. The study was approved by the University of with human intestinal helminths in Igbo-Eze South Nigeria Teaching Hospital Research Ethics Committee. LGA, Nigeria. Collection and examination of stool samples Materials and Methods Stool samples were collected monthly for a period of 6 months. Each of the selected pupils was given a small Study area bottle in which they collected their stool samples. The The study was carried out in rural tropical bottles were labeled with the pupil’s name, age and sex. communities in Igbo-Eze South LGA, Enugu State, On collection of the stool samples, they were taken to the Nigeria. The sampled communities were Ibagwa-Aka, Parasitology and Public Health Laboratory, Department of Iheakpu-Awka, Iheaka, Ovoko, Itchi and . The Zoology and Environmental Biology, University of Nigeria, headquarters of Igbo-Eze South LGA is at Ibagwa-Aka. Nsukka, Enugu State, Nigeria for examination. At the Igbo-Eze South LGA is located between latitudes 7°19′ laboratory, for the diarrheic stool samples, a drop of fresh East and 7°28′ East and longitudes 7°00′ North and physiological saline was placed on a slide. Using a tooth 6°53′ North.[16] The area is in the guinea savannah peak, a small amount of a stool sample was mixed with forest mosaic zone of Nigeria. The study area has two saline and examined under the microscope using first, the main seasons; the rainy and dry seasons. The rainy ×10 objective followed by ×40 objectives to identify the season usually starts in April and ends in September eggs.[19] For the non-diarrheic stool samples, the formol- while the dry season usually starts in October and ends ether concentration technique was employed.[19] Using a in March. The soil is moist and porous, which favors stick, 1 g of the stool sample mixed with physiological the survival of soil-transmitted helminths ova. The saline was put in a screw-cap bottle containing 4 ml of inhabitants of this area are mainly subsistent farmers 10% formol water. The bottle was capped and mixed and traders. There are 17 health centers in the area, by shaking for about 20 s. Thereafter, the stool sample with a General Hospital at Itchi. The total population was sieved and the suspension collected in a beaker. of people in the study area is 75,368.[17] There are 44 The suspension was transferred to a tube and 3 ml of primary schools with 14,994 pupils in the study area; ether was added. The tube was stoppered and mixed by 8860 males and 6134 females.[18] Each of the schools shaking for 1 min. Thereafter, the stopper was removed have six classes; primary 1-6. and centrifuged immediately at 3000 rpm for 1 min. After centrifuging, four layers were evident; the top layer of ether, Selection of schools and pupils thin layer of debris, formalin and sediment in the bottom Six schools were used for this study. Primary schools with parasites. An applicator stick was used to loosen the in the study area were listed out and six schools layer of stool debris from the side of the tube. The ether, were randomly selected (Township School 1, Ibagwa, debris and formalin were then carefully poured off. The Community Primary School 3, Itchi, Central School, sediment was mixed, transferred to a slide and covered Ovoko, Central School, Iheaka, Community Primary with a cover glass. The slide was examined under the School 1, Unadu and Community Primary School, microscope using first, the ×10 objective followed by ×40 Iheakpu-Awka) using table of random numbers. objective to identify the eggs.[19,20] Infection was defined From each of the six schools selected, 36 pupils were by the presence of eggs of human intestinal helminths randomly sampled for the presence of helminth egg in in the stool samples. The number of pupils infected with fecal matter. Six pupils were selected from each class human intestinal helminthiasis and the type of human (classes 1-6) to make up a total of 36. This was done intestinal helminths’ eggs observed were recorded.[19] using the register of each class. When any selected pupil was absent, a pupil after the indicated one was Post-treatment monitoring sampled for replacement. A total of 1296 pupils were Pupils found to be infected with intestinal helminths sampled at the end of 6 months (July-December 2005). were administered with single oral doses of 400 mg

414 Annals of Tropical Medicine and Public Health | Jul-Aug 2013 | Vol 6 | Issue 4 Edelduok, et al.: Efficacy of albendazole on human intestinal helminthiasis albendazole tablets. Their stool samples were collected Table 1: Prevalence of human intestinal helminths among again after 4 weeks post-treatment and examined school children in the study area for the presence or absence of intestinal helminths. Human Number Number Overall Prevalence Treatment was said to be effective when the parasites intestinal examined infected prevalence (%) within the were not observed and ineffective when parasites were helminths (%) infected group observed during the examination.[19,20] found (106) A. lumbricoides 1296 64 4.9 60.4 Hookworm 1296 33 2.5 31.1 Data analysis T. trichiura 1296 9 0.7 8.5 Differences in the prevalence of infection were Total 106 8.1 100.0 2 determined using the χ test from the contingency A. lumbricoides = ascaris lumbricoides, T. trichiura = trichuris trichiura tables. χ2 test was also performed to compare the effectiveness of treatment on the different human intestinal helminths recorded during the study. The Table 2: Effectiveness of treatment of infected children with drugs (single oral dose of 400 mg albendazole analysis was performed using Statistical Package for tablets) in the study area Social Sciences (SPSS) version 22.0 (IBM SPSS, IBM Infection Number infected Effi cacy of treatment Corporation, Armonk, New York 10504-1722, USA). and treated Effective (%) Not effective (%) Results and Discussion A. lumbricoides 64 12 (18.8) 52 (81.2) Hookworm 33 5 (15.1) 28 (84.9) Human intestinal helminthiasis is important health T. trichiura 9 2 (22.2) 7 (77.8) problems in the school-age population. This study Total 106 19 (15) 87 (67.0) has shown that human intestinal helminthiasis is A. lumbricoides = ascaris lumbricoides, T. trichiura = trichuris trichiura prevalent among school children in the study area. Of the 1296 school children examined for human intestinal reported of low efficacy of a single dose of albendazole helminthiasis, 106 (8.1%) were infected thus; 64 (4.9%) against trichuriasis.[14] Treatment failures recorded after were infected with A. lumbricoides, 33 (2.5%) were 4 weeks of treatment may be attributed to re-infection, infected with hookworm, while 9 (0.7%) were infected resistance of the parasites to drugs and decline in the with T. trichiura. However, within the infected group, efficacy of the drug. This signals the need for close the prevalence was 60.4%, 31.1% and 8.5% for A. monitoring of the performance of the drug against human lumbricoides, hookworm and T. trichiura infections, intestinal helminth parasites in the area. Re-infection respectively [Table 1]. There was a significant difference is usually an important factor in treatment. Elkins and in the prevalence of infections among the school children others reported A. lumbricoides re-infection reaching (P < 0.05). The higher prevalence of A. lumbricoides 55% of pretreatment rates.[29] Quinnell and others infection than hookworm and T. trichiura infections was reported of rates of hookworm re-infection reaching 80% consistent with some previous reports.[21,22] This finding of pretreatment rates,[30] while T. trichiura re-infection has important health implications for morbidity and had been reported to reach 44% of pretreatment rates.[31] transmission rates. The treatment of school children Similarly, Albonico et al. reported high rates of post- who had intestinal helminths infections with single treatment re-infection for human intestinal helminths in oral dose of 400 mg albendazole tablets led to reduction areas of high endemicity.[32] It is possible that re-infection in the prevalence of intestinal helminth (18.8% for A. may have occurred due to poor sanitary conditions and lumbricoides, 15.1% for hookworm and 22.2% for T. lack of proper health education.[3,33] Despite re-infection trichiura), but were largely not effective as exemplified however, regular treatment to reduce the worm burden by the high prevalence of post-treatment helminths consistently could prevent some of the morbidity (81.2% for A. lumbricoides, 84.9% for hookworm and associated with chronic infection. 77.8% for T. trichiura) [Table 2]. In contrast with our study, reports of high efficacies of albendazole against Furthermore, it is possible that the parasites may human intestinal helminthiasis may be attributed to have developed resistance to the drug. This possibility differences in geographical locations, climatic conditions needs to be explored; using methods such as the egg and hygiene; which scored low among the sampled hatch assay[34] to assess the susceptibility of intestinal pupils.[23-27] Nevertheless, Hall and Nahar[28] had shown helminths to albendazole. Also, the possibility that single oral dose of 400 mg albendazole gave cure rate of combining this drug with another effective of less than 40.0% for A. lumbricoides and T. trichiura antihelminthic drug to prolong its useful therapeutic in children in Bangladesh. Moreover, the low cure rate of life should be explored. Albonico et al. noted that albendazole against trichuriasis (22.2%) observed in this combination therapy with drugs with differing modes study was consistent with that of Adams and others who of action is an alternative strategy to improve efficacy

Annals of Tropical Medicine and Public Health | Jul-Aug 2013 | Vol 6 | Issue 4 415 Edelduok, et al.: Efficacy of albendazole on human intestinal helminthiasis and lower the risk of resistance.[13] Indeed, Mani thankful to the Department of Zoology and Environmental et al. had reported high efficacy of co-administration Biology, University of Nigeria for the provision of laboratory of albendazole and diethylcarbamazine against space, equipments and analytical packages for the study geohelminthiasis,[35] while Belizario and others also and Miss Nkechinyere Onah, Department of Zoology and reported high efficacy of a combination of albendazole Environmental Biology, for typing the manuscripts. There is no conflict of interest among the authors and with any and ivermectin and a combination of albendazole and organizations. diethylcarbamazine, against trichuriasis compared [36] with a single dose of albendazole. References

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