|Year : 2014 | Volume
| Issue : 1 | Page : 56-61
Prevalence and pattern of soil-transmitted helminthiasis among pregnant women in a tertiary health facility, southeast Nigeria
Ikechukwu B O Dimejesi1, Odidika U J Umeora1, Vincent Emeka Egwuatu2
1 Department of Obstetrics & Gynaecology, Ebonyi State University, Abakaliki, Ebonyi State; Department of Obstetrics & Gynaecology, Federal Teaching Hospital, Abakaliki, Nigeria
2 Enugu State University, Enugu, Enugu State, Nigeria
|Date of Web Publication||25-Aug-2014|
Dr. Ikechukwu B O Dimejesi
PO Box 980. Abakaliki, Ebonyi State
Source of Support: None, Conflict of Interest: None
Context: Pregnant women in resource-scarce countries are vulnerable to helminthic infestation. Aims and Objectives: to document the prevalence and pattern of soil-transmitted helminthic infestation among booked expectant mothers in this region. Materials and Methods: This was a descriptive cross sectional study. Pregnant women who were counseled and consented to the study were randomly recruited at the booking clinic. They were interviewed and had their blood and stool specimens collected for laboratory analysis. Data was analysed using epi info statistical package version 3.4.1. Result: One hundred and thirty one (32.4%) stool samples out of the four hundred and four samples yielded positive results. The helminth species isolated included Ascaris lumbricoides, Hookworm, Trichuris trichuria, Strongyloides stercoralis and Enterobius vermicularis. Ascaris lumbricoides (65.6%) was the most prevalent. Two women (1.5%) had mixed infections. Though the intensity of infection was generally low. Conclusion: Antenartal clinic attendees in Abakaliki have some degree of helminthic infestation, routine deworming during the prenatal period is advocated.
Keywords: Farming, infestation, public health, pregnancy, poverty
|How to cite this article:|
Dimejesi IB, Umeora OU, Egwuatu VE. Prevalence and pattern of soil-transmitted helminthiasis among pregnant women in a tertiary health facility, southeast Nigeria. Afr J Med Health Sci 2014;13:56-61
|How to cite this URL:|
Dimejesi IB, Umeora OU, Egwuatu VE. Prevalence and pattern of soil-transmitted helminthiasis among pregnant women in a tertiary health facility, southeast Nigeria. Afr J Med Health Sci [serial online] 2014 [cited 2019 May 20];13:56-61. Available from: http://www.ajmhs.org/text.asp?2014/13/1/56/139445
| Introduction|| |
Helminthic infections are an important public health problem especially in developing countries of Africa and Asia, , where it engenders a health burden on the poor populations.  Soil-transmitted helminth infection caused by nematode worms is the most prevalent of neglected tropical diseases with an estimated 3.8 billion persons infected, 720 million clinical cases and an estimated 135,000 deaths attributable to the clinical complications annually.  The greatest numbers of soil-transmitted helminth infections occur in Sub-Saharan Africa, the Americas, China, and East Asia. 
The important soil-borne helminthes include Ascaris lumbricoides, hookworm, and Trichuris trichiura. About 1.5 billion individuals are infected with Ascaris, primarily in Africa and Asia.  Ascariasis is also endemic in the United States including the Gulf Coast, in Nigeria, and in Southeast Asia.  It is estimated that 70% of the worm population is harbored by 15% of the human host population.  These heavily infected individuals are at risk of developing severe diseases, with the major source of transmission being environmental contamination.  Pregnant women are a vulnerable group who can be affected by soil-transmitted helminthiasis.  In pregnancy, soil-transmitted helminthiasis during pregnancy is a major cause of anemia in Africa. 
An estimated one-third of all pregnant women in developing countries are infected with hookworm infection,  this amounts to about 44 million of the developing world's 124 million pregnant women. , Susceptibility to heavy infestation has genetic, immunological, socio-cultural, and behavioral components.  However, the greatest single predictor of heavy worm burden is age. 
Worm infection during pregnancy does not only adversely affect the mother but also the unborn child.  The burden of helminthic infection in girls and women especially during pregnancy has been reported to constitute the most important component of their global disease burden.  Associated maternal morbidity may be considerable and this includes iron deficiency anemia and impaired nutritional status, and for the fetus, decreased birth weight, intrauterine growth restriction, and adverse birth outcomes. These effects may, however, differ by area and degree of helminth burden. ,
In Nigerian villages and towns, helminthic infection is so important because of the attributable high rates of morbidity and sometimes mortality.  Abakaliki Ebonyi State is an urban area with majority of the prenatal clients of rural habitation. The burden, prevalence, and species distribution of soil-transmitted helminths in pregnant women in our environment have not been previously documented. The research questions therefore are: what is the prevalence of soil-transmitted helminthic infestation among this population and what are the worm species commonly encountered. Answers to these may inform policy formulation as to the desirability or otherwise of routine antihelminthics in pregnancy.
| Materials and Methods|| |
Abakaliki is the capital of Ebonyi State. Ebonyi State is one of the five states in the southeast geopolitical zone of Nigeria. Ebonyi state was created in 1996. It is situated within the Guinea Savannah vegetation belt of Nigeria. The climate is characterized by a high uniform temperature, moderate-to-heavy seasonal rainfall, and high relative humidity. Dry season extends from November to March, and rainy season from April to October. The environment is conducive for transmission of soil-transmitted helminths as the sanitary conditions are inadequate and the climatic conditions support the survival of the parasite eggs or larvae in the warm and moist soil. Most of the populace are impoverished and peasant farmers.
The population of Ebonyi State is about 2.2 million and that of Abakaliki, the capital territory, is 278,560, with females comprising 52.6% and males 47.8%.  The inhabitants are a mixture of people from different ethnic groups, but majority are Ibo-speaking. Houses in the capital city and suburbs are predominantly built of concrete floors and walls, and roofed with corrugated galvanized iron sheets. There is no properly organized sewage and refuse disposal system. The city and its environs have inadequate water supply. The main source of water is from tap-borne water, bore-holes, and deep wells for urban dweller, and streams, dams/ponds, shallow/deep wells, and shared community boreholes for the majority of rural dwellers. Within the Abakaliki capital territory, most of the drainage system consists of open gutters, majority of which are usually blocked with sand, refuse, and human excreta. Waste is left in open spaces or containers, littering the surrounding or burnt freely into the open air with consequent environmental pollution.
Native Ebonyians are mainly peasant farmers, but the creation of the state in 1996, witnessed increase in white collar jobs and politicians. Others are traders, businessmen, students, artisans, semi-skilled and unskilled workers in the rice milling and stone quarry industries scattered all over the capital territory. Majority of them are Christians and few are traditional religionists and animists. Poverty and ignorance are prevalent. The health problems of the populace are catered by a heterogeneous mixture of orthodox and nonorthodox medical practitioners as well as spiritualists and herbalists. Two tertiary health institutions, Ebonyi State University Teaching Hospital and Federal Medical Centre, are located within the state capital. They cater for the tertiary health needs of the inhabitants and parts of the surrounding states: Abia, Cross River, Benue, and Enugu. The Obstetrics and Gynecology department of EBSUTH has 50 obstetric and 20 gynecological beds. An average of 2500 pregnant women book for antenatal care annually, with an average annual delivery rate of 1600.
The hospital operates a free antenatal care policy supported by the State government. Patients, who had their antenatal care with the facility, are regarded as 'booked' patients. While patients who had their antenatal care elsewhere or did not have at all and were referred because of complications in pregnancy, labor, or puerperium are regarded as 'unbooked'. The booking clinic is held every Wednesday, whereas the antenatal clinic is held at Abakaliki from Monday to Friday except on Wednesday, and is run by consultants and resident doctors. Antenatal women are seen based on appointment. Obstetric problems detected during the clinic are addressed accordingly, and those requiring admission are admitted into the ward. Thereafter further management is according to departmental protocols.
This was a laboratory-based cross-sectional descriptive study conducted in the Obstetrics and Gynecology Department of the Ebonyi State University Teaching Hospital, Abakaliki. It included all pregnant women who presented for their first prenatal care visit at the booking clinic irrespective of the gestational age, did not have any of the exclusion criteria, and consented to the study. They were consecutively enrolled into the study till the desired sample size was achieved.
The exclusion criteria included: Clients who have taken anthelminthics in index pregnancy or within 3 months before conception and those who did not consent.
The social class of the participants was calculated based on the formula of Olusanya et al., which takes into consideration the educational status of the woman and her spouses' income. 
Women with proven cases of worm infestation were treated with a single dose of levamisole.
An interviewer-administered questionnaire was used to obtain socio-demographic information, educational status, and environmental characteristics. Stool and blood samples were also collected from each participant for laboratory analysis.
These specimens were examined by any of the two laboratory scientists dedicated to this research work within 24 h. A third laboratory scientist also dedicated to this research, at intervals randomly selected specimen samples for cross checking for quality control.
Ethical issues and approval
The objectives of the research and its implications were explained to the pregnant women with the consent form. The approval of the study was obtained from the Ethics and Research Committee, Ebonyi State University Teaching Hospital, Abakaliki. Participation was after signing the consent form and a participant could withdraw from the study at any time without consequences for her antenatal services. Cases of helminthiasis were adequately treated.
Data management and analysis
The data obtained were fed into EPI info version 3.4.1 of the Centre for Disease Control, Atlanta USA 2007 and analyzed. Descriptive statistical analysis included frequencies and means frequencies of socio-demographic variables. Women with helminthiasis were taken as cases while those without the infestation were used as controls. The chi-square test was used to test for associations between categorical variables while the t-test was used to compare means. A P-value of less than 0.05 was taken to be significant. Results are presented in simple frequency distribution tables.
| Results|| |
Four hundred and fifty (450) booked pregnant women participated in this study. Forty-six (46) of the stool samples were collected overnight, and as such were not analyzed. Four hundred and four (404) stool samples were found suitable for analysis, giving a percentage of 90% and these were analyzed. One hundred and thirty-one (32.4%) stool samples, out of the 404 samples analyzed for helminths, yielded positive results. The helminth species isolated included A. lumbricoides, hookworm, T. trichiura, Strongyloides stercolaris, and Enterobius vermicularis. This gave a prevalence of helminthic infection in pregnancy of 32.4%. Of the positive samples, the species prevalence of A. lumbricoides −65.6%, hookworm −20.6%, S. stercoralis −8.4%, E. vermicularis −3.8%, and T. trichiura −1.5%[Figure 1]. Among the 131women whose stool samples were positive for helminthes, 2 (1.5%) had mixed infections. The intensity of infection was heavy in 4%, moderate in 29%, and light in 67% of the infected pregnant women. The mean egg count was 731 epg of feces [Figure 2].
|Figure 1: The prevalence of the helminth species among antenatal women at EBSUTH, Abakaliki|
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The socio-demographic data showed that majority of the participants (155; 38.4%) were aged 25-29 years. While those aged less than or equal to 19 years were 10 (2.5%) women, and only 4 (1%) women were aged 40 or over. Majority of the pregnant women were married 396 (98%). Majority of them also were in the parity of 1-4, which formed 63.6% of the study population. The nulliparas constituted 19.3% and grandmultiparas formed 17.1% [Table 1].
There were 214 (53%) urban dwellers and 190 (47%) rural dwellers in this study. Majority of the participants were Christians 395 (97.5%) and Ibos 392 (97%). Most of the participants were petty traders 107 (26.2%). Others were civil servants 77 (19.1), house wife 68 (16.8%), farmer 53 (13.1%), hair dresser 48 (11.9%), teacher 31 (7.7%), health workers, 13 (3.1%), professionals, 6 (1.5%), and clergy, 1 (0.2%).
The educational status and social classes of the pregnant women with helminths are shown in [Table 2]. The greatest number of infected women had primary education (51; 39%). This was closely followed by 50 (38%) women with secondary education and 30 (23%) who had postsecondary education. [Table 2] indicates that 44 (33.6%) women were in social class 5; others were (31; 23.7%) in social class 4, 25 (19%) in social class 3, 20 (15.3%) in social class 2, and 11 (8.4%) in social class 1. When analyzed, education and social classes had P values of 0.007 and 0.000001, respectively, which were statistically significant at a P-value of 0.05.
|Table 2: Education and social classes of the booked pregnant women with helminths|
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Majority (53; 40.5%) of the antenatal women who were positive for helminths used bush for toilet, 47 (35.8%) used pit toilet, and 31 (23.7%) used water closet. This was statistically significant, P-value of 0.005.
The mean packed cell volume (PCV) value of women without infection was 31.23%. This was higher compared with the mean PCV of those with infection of 30.51%. The difference between mean PCV for the noninfected and infected women was not statistically significant (P value 0.176). The lowest mean PCV value, of 29.59% was among women with hookworm infestation [Table 3].
|Table 3: Pattern of soil-transmitted helminths and booking mean packed cell Volume (PCV - %)|
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There were 44 (10.9%) urban dwellers and 87 (21.5%) rural dwellers whose stool samples were positive for helminths. This gave an urban and rural prevalence of helminthiasis of 10.9% and 21.5%, respectively. This had a P-value of 0.0000001, which was statistically significant. The study also showed that 157 (38.9%) of the study population had access to tap running water. Of this number, 130 (32.2%) were urban dwellers and 27 (6.7%) were rural dwellers. It also indicated that 38 women participants with worms had access to tap running water, whereas 93 participants of those without access to tap running water also had worms. This had a P-value of 0.007, which was statistically significant at a P-value of 0.05.
| Discussion|| |
The prevalence of helminthic infection was 32.4% in this study. A. lumbricoides was the most prevalent species (65.6%), followed by hookworm (20.6%), S. stercoralis (8.4%), E. vermicularis (3.8%), and T. trichiura (1.5%). The prevalence of helminthic infection in our study was higher than the prevalence of 11.8% reported in Enugu in 2005 by Ozumba et al. and 17.9% reported among pregnant women in Thailand by Liabsuetrakul et al. in 2009.  The fact that Enugu has remained a capital city from the colonial era to date may account for availability of basic social infrastructures, clean portable water, good sanitary conditions, planned and hygienic environment with a better socioeconomic life of the inhabitants. However, in both studies, this study and the Ozumba et al. study, A. lumbricoides was the most prevalent species. This has public health implications as the route of infection is oro-fecal. This prevalence of 32.4% was lower when compared with the prevalence of 73.9%, documented in Venezuela in 2006 by Alfonso et al. The Venezuela study was a multicenter one (15 centers and involved nine states) and was more representative. Also A. lumbricoides was the most prevalent species. Egwunyenga et al., in a hospital-based study in Nigeria, on plasmodium/intestinal helminth coinfections among pregnant women reported a prevalence of helminthiasis in pregnancy of 48.3% and A. lumbricoides as the most prevalent species. This is higher than the documented prevalence in this study.
The education of the women with helminths in this study was mainly primary (39%), secondary (38%), and postsecondary (23%). The infestation is less with higher the level of education attained. This may have to do with knowledge of personal hygiene, better quality of life, and proper food preparation. The greatest number of women with helminths was seen in the social class 5. This quickly points to the fact that the burden of helminthic infection is borne by the poor. Bethony et al., in 2006, reported that the poor people in developing countries endure the burden of worm infestations.  In Ebonyi state, most women are impoverished with no source of income. They have no jobs and depend mostly on menial jobs for sustenance of their families. This study indicated that low level of education and social status are associated risk factors for worm infestation in pregnancy.
Pregnant women who live in urban areas had less worm infestation than those in rural areas. This could be attributed to better living conditions, better environmental sanitation, and more access to clean portable water. The use of bush method of latrine, which was more common in the rural area, was another factor for increased prevalence of helminths among the pregnant women in the area. Agriculture is the main occupation of the native Ebonyian. Thus farming with associated bare foot is common among the rural populace may seriously encourage increased worm infestation among the rural pregnant women.
The general mean PCV values for all the helminth species in pregnancy were noted to be lower than that of noninfected pregnant women. Particularly, those women with hookworm had the lowest mean PCV. This may not be unconnected with the proven fact that hookworm causes anemia in pregnancy by hookworm-induced blood loss and associated iron deficiency anemia. The noninfected mean PCV of 31.23% was higher than the mean PCV of 30.51% in women with helminthes. The difference in the mean PCV of women without infection and women with infection was 0.72%. This gave a t-test of −1.363 and a P-value of 0.176, which was not statistically significant. Statistically there was no difference in the mean PCV value between the infected and noninfected in the Enugu study reported by Ozumba et al. in 2005. 
The limitations of this research study include: it does not cover the effect of worms on the woman, pregnancy, and her new-born, as patients were not followed up to delivery and postpartum periods. The study is an institutional based and may not be a reflection of helminthiasis in the community.
| Conclusion|| |
Soil-transmitted helminth infections in pregnancy will remain a public health threat in our environment for a long time and in those areas of the world where poverty is endemic, as in the poor resource countries of the world. The high antenatal prevalence of helminths noted in this study calls for routine antenatal care de-worming to reduce the chronic morbidity of the infection. However, it must be noted that without improved water supplies and proper environmental sanitation, the expected benefits of antenatal antihelminthic cannot be relied upon for sustainable decimations in parasite intensity.
| References|| |
|1.||de Silva NR, Brooker S, Hotez PJ, Montresor A, Engels D, Savioli L. Soil-transmitted helminth infections: Updating the global picture. Trends Parasitol 2003;19:547-51. |
|2.||World health organization. Soil-transmitted helminthiasis [online] 2006. Available from: http://www.who.int//neglected-diseases_disease/en [Last accessed on 2009 Dec 09]. |
|3.||Gbakima AA, Sherpard M, White PT. Intestinal helminth infections in rural school children in Njala Sierra leone. East Afr Med J 1994;71:792-6. |
|4.||World Health Organization. Prevention and control of schistosomiasis and soil-transmitted helminthiasis. Report of a WHO expert committee, WHO Tech Rep; Ser No 912.1 Geneva, Switzerland: World Health Organization; 2002. |
|5.||Crompton DW. How much helminthiasis is there in the world? J Parasitol 1999;85:397-403. |
|6.||Embil J, Pereira L, White F, Gamer J, Manuel F. Prevalence of Ascaris lumbricoides infection in a small Nova Scotian community. Am J Trop Med Hyg 1984;33:595-8. |
|7.||Bundy DA, Chan MS, Savioli L. Hookworm infection in pregnancy. Trans R Soc Trop Med Hyg 1995;89:521-2. |
|8.||Liabsuetrakul T, Chaikongkeit P, Korviwattanagarn S, Petrueng C, Chaiya S, Hanvattanakul C, et al. Epidemiology and effect of treatment of soil-transmitted helminthiasis in pregnant women in southern Thailand. Southeast Asian J Trop Med Public Health 2009;40:211-22. |
|9.||Fuseini G, Edoh D, Kalifa BG Knight D. Plasmodium and intestinal helminthes distribution among pregnant women in the Kassena-Nankana District of Northern Ghana. Entomol Nematol 2009;1:19-20. |
|10.||World Health Organization. Bench AIDS for the diagnosis of intestinal parasites. Geneva, Switzerland: WHO; 1994. |
|11.||Ozumba UC, Ozumba NA, Anya S. Helminthiasis in pregnancy in Enugu, Nigeria. J Health Sci 2005;51:291-3. |
|12.||Hercberg S, Galan P. Nutritional anaemia. Baillieres Clin Haematol 1992;5:143-8. |
|13.||McGregor IA, Wilson ME, billewicz WZ. Malaria infection of the placenta in the Gambia, West Africa, its incidence and relationship to stillbirth, birth weights and placenta weight. Trans R Soc Trop Med 1983;77:232-344. |
|14.||Stephenson LS, Lathan MC, Ottesen EA. Malnutrition and parasitic helminth infections. Parasitology 2000;121:23-38. |
|15.||Egwunyenga AO, Ajayi JA, Nmorsi OP, Duhlinska-Popova DD. Plasmodium/intestinal helminth co-infections among pregnant Nigerian women. Mem Inst Oswaldo Cruz 2001;96:1055-9. |
|16.||Villar J, Klebanoff M, Kestler E. The effect on fetal growth of protozoan pregnancy. Obstet Gynecol 1989;74:915-20. |
|17.||Bello CS, Ianyigna KB, Olutu CO. Intestinal parasites in Jos: A four year review. Niger Med Pract 1997;34:11-3. |
|18.||Federal Republic of Nigeria official gazette, No 24, Lagos 15 th May 2007 Vol. 94, Government notice No 221: p. 31184. |
|19.||Olusanya O, Okpere E, Ezimokhai M. The importance of social class in voluntary fertility control in a developing country. West Afr J Med 1985;4:205-12. |
|20.||Rodríguez-Morales AJ, Barbella RA, Case C, Arria M, Ravelo M, Perez H, et al. Intestinal Parasitic Infections among pregnant women in Venezuela. Infect Dis Obstet Gynecol 2006;2006::23125. |
|21.||Bethony JS, Brooker M, Albonico SM, Geiger A, Loukas D, Diemert D, et al. Soil-transmitted helminth infections: Ascariasis, trichuriasis and hookworm. Lancet 2006;367:1521-32. |
[Figure 1], [Figure 2]
[Table 1], [Table 2], [Table 3]