|Year : 2015 | Volume
| Issue : 2 | Page : 65-70
Intestinal nematodes infection among pregnant women in Benin City
Frederick Olusegun Akinbo1, Emily Okonye1, Adedapo Babatunde Anibaba Ande2
1 Department of Medical Laboratory Science, University of Benin, Benin City, Edo State, Nigeria
2 Department of Obstetrics and Gynaecology, University of Benin Teaching Hospital, Benin City, Edo State, Nigeria
|Date of Web Publication||14-Jun-2018|
Dr. Frederick Olusegun Akinbo
Department of Medical Laboratory Science, University of Benin, Benin City, Edo State
Source of Support: None, Conflict of Interest: None
Introduction: Enteric parasitic diseases are common in the developing counties and are of major health problem due to their high prevalence rate, and effect on both nutritional and immune status of the population. This study was conducted to determine enteric parasitic infections among pregnant women in Benin City, Edo State, Nigeria. Materials and Methods: A total of 332 participants which consisted of 232 pregnant women and 100 nonpregnant adult females were recruited in this study. Blood and fecal specimens were obtained from each participant. The blood sample was analyzed for hemoglobin concentration and the fecal sample used for investigating intestinal parasites. Results: An overall prevalence of 2.2% of enteric parasitic infections among pregnant women was observed while no parasite was reported among the nonpregnant women. Age, not always washing hand, occupation, source of food and anemia were significantly associated with enteric parasitic infections among pregnant women. The enteric parasites recovered among pregnant women were Ascaris lumbricoides and hookworm. A. lumbricoides had a prevalence of 80% of enteric parasitic infection while hookworm had 20%. Conclusion: Measures to reduce the effect of enteric parasitic infections among pregnant women are advocated.
Keywords: Benin City, intestinal nematode infections, pregnant women
|How to cite this article:|
Akinbo FO, Okonye E, Anibaba Ande AB. Intestinal nematodes infection among pregnant women in Benin City. Niger J Exp Clin Biosci 2015;3:65-70
| Introduction|| |
Parasitic diseases are common in the developing counties and are of major health problem due to their high prevalence rate, and effect on both nutritional and immune status of the population. Gastro-intestinal parasites of human are common in the tropics because of the favorable climate, environmental and sociocultural factors that enhance their transmission. These parasitic infections are distributed throughout the world and generally associated with the condition of improper hygiene, lack of access to safe water, and poor sanitary habits.,, Enteric parasitic infections caused by pathogenic helminthic and protozoan species are endemic globally. These enteric parasites include: The protozoan Entamoeba histolytica, Giardia intestinalis, Cryptosporidium species, Isospora belli and the soil-transmitted helminthes Ascaris lumbricoides, hookworm infections, Strongyloides stercoralis, Trichuris trichiura, Enterobius vermiscularis., Of these, the soil-transmitted helminthiases are ancient diseases that have continued to cause misery and disability in poor populations. About 2 billion people harbor these infections worldwide, of which 300 million suffer associated severe morbidity annually.
Most women in developing countries, such as Nigeria go through their lives without ever enjoying a state of good health free of intestinal parasites. An estimated 24 million women become pregnant each year in sub-Saharan Africa and due to behavioral and immune changes; a majority of these women are susceptible to parasitic infections with poor pregnancy outcomes. Geohelminthiases are transmitted through the practice of soil eating common amongst children in many developing countries. The high prevalence of infection in pregnant women is indicative of fecal pollution of soil and domestic water supply around homes due to poor sanitation and improper sewage disposal. Due to the close relationship with children, pregnant women are at high risk of enteric parasitic infections. Intestinal parasitic infections seldom affect reproductive capacity in man but in countries with low socioeconomic standards as well as increased maternal malnutrition, a high incidence of these infections can contribute to unfavorable prognosis for the mother and child. In areas endemic of soil-transmitted helminthiasis, intestinal parasitic infections may lead to increasing anemia and risk to health in pregnancy, reduced birth weight and survival of the babies.,,, Certain deficiencies macro- and micro-nutrients such as total energy, protein, and possible folate and zinc deficiencies may also be induced by specific helminths., The socioeconomic impact of chronic intestinal parasitic infections resulting from malabsorption, malnutrition, stunting growth, and chronic anemia can destabilize endemic communities and reinforce local poverty which may hinder national economic development., Infections with A. lumbricoides, hookworms and T. trichiura have been associated with anemia.A. lumbricoides infection has been reported as the cause of impaired fat digestion, reduced vitamin absorption, and temporary lactose intolerance. Amoebiasis has also been implicated as the cause of poor maternal iron status and reduced fetal growth.
There is a paucity of information on the enteric parasitic infections among pregnant women in Benin City, Edo State, Nigeria. Thus, this study was conducted to determine enteric parasitic infections among pregnant women in Benin City, Edo State, Nigeria.
| Materials and Methods|| |
The study was carried out at the University of Benin Teaching Hospital, Benin City, Nigeria. The University of Benin Teaching Hospital is a tertiary hospital in Benin City, Edo State, Nigeria.
A cross-sectional study was conducted among asymptomatic pregnant women attending antenatal clinics at the University of Benin Teaching Hospital, Benin City from April to November 2014. A total of 332 participants which consisted of 232 pregnant women attending antenatal clinics at the University of Benin Teaching Hospital, and 100 nonpregnant adult females within the University community that served as controls were recruited in this study. Pregnant women that accepted to participate were included while those on anti-parasitic agents were excluded from this study. Random sampling technique was employed in this study. Informed consent was sought from participants prior to specimen collection. The University of Benin Teaching Hospital Ethical Committee approved the protocol for this study. Sample size was determined by the formula:
N = 4pq/12
Where N is sample size, p is the prevalence of enteric parasitic infections among pregnant women in the previous study, q is 100-p, and l is a permissible error (5% of p).
Assuming a prevalence of 82.8%, therefore, q = 17.2 and L = 4.14
N = 4 × 82.8 × 17.2/4.142
N = 332.4 ≈ 332
Therefore, 332 sample were collected.
Specimen collection and processing
Blood and fecal specimens were obtained from each participant. Five milliliters of venous blood collected from each participant and dispensed into an ethylene diamine tetra-acetic acid container and mixed. Hemoglobin concentration was determined using a Sysmex KX-21 hematology analyzer (Sysmex Corporation, Kobe, Japan).
Freshly voided fecal specimen was collected into a clean, transparent wide-mouthed universal container. The fecal specimens were processed using the formol ether concentration technique and smears were examined microscopically for intestinal parasites. Briefly, 1 g of feces was emulsified in 4 ml of formol saline and mixed. This was sieved and to the filtrate, 4 ml of diethyl ether was added. The filtrate was centrifuged at 3000 rpm for 1 min and the supernatant discarded. From the deposit, saline and iodine preparations were made and examined for the presence of intestinal parasites.
The frequency data obtained were analyzed using Chi-square while the odds ratio (OR) was calculated for potential risk factors. The software INSTAT (GraphPad Software Inc., La Jolla, CA, USA) was used for all statistical analyses. A significant association was determined using P < 0.05.
| Results|| |
The prevalence of enteric parasitic infections among pregnant women was 2.2% while no parasite was recovered from the nonpregnant women. Being pregnant was however not a significant risk factor for acquiring enteric parasitic infections (OR = 4.859; 95% confidence interval [CI] = 0.2660, 88.782; P = 0.3231) [Table 1].
Pregnant women within the age group of 41-50 years (P = 0.0330), that are traders (P = 0.0186), who do not always wash their hands (P = 0.0239) and eat from food vendors (P = 0.0096) significantly affected the prevalence of intestinal parasitic infection. However, pregnant women's educational status (P = 0.1170), trimester (P = 0.1004) and whether they walk barefooted (P = 0.0882) did not significantly affect the prevalence of intestinal parasitic infection [Table 2]. Among pregnant women with anemia, 5.4% had intestinal parasitic infections while their counterparts without anemia had no intestinal parasitic infections. Indeed, anemia was a significant risk factor for acquiring intestinal parasitic infections among the pregnant women (OR = 17.914; 95% CI = 0.9779; 328.19; P = 0.0190) [Table 3].
|Table 2: Relationship between demographic characteristics and enteric parasitic infections|
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|Table 3: Effect of anemia on enteric parasitic infections among pregnant women|
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The enteric parasites recovered from pregnant women in this study were A. lumbricoides and hookworm. A. lumbricoides and hookworm had a prevalence of 80% and 20% respectively (data not shown).
| Discussion|| |
Parasitic diseases are predominant in the developing countries and are of a major health hazard because of their high prevalence rate, and effect on both nutritional and immune status of the population. The burden of disease that is imposed on women of child bearing age, especially pregnant women, may define the single most important contribution of enteric parasitic infections to the calculation of their global burden., There is a paucity of information on enteric parasitic infections among pregnant women in Benin City, Edo State, Nigeria. Thus, this study was conducted to determine enteric parasitic infections among pregnant women in Benin City, Edo State, Nigeria.
An overall prevalence of 2.2% of enteric parasitic infections was observed among pregnant women in this study. This is lower than that previously reported studies in Warri (23.47%), Ibadan (43.4%) both in Nigeria, and 73.9% in Venezuala. The difference may be due to geographical location and hygiene. In terms of location, our study was conducted among urban dwellers in Benin City, Nigeria while the study of Rodríguez-Morales et al. was conducted among semi-urban and rural pregnant women in Venezuela. In terms of hygiene, rural women may acquire helminth infections in the process of growing the family's food. Indeed, Vietnamese women have been reported to be infected as a result of the use of improperly composted human feces as manure. Similarly, lack of efficient environmental sanitation was suggested as a possible reason for the high prevalence in Ibadan, Nigeria. None of the nonpregnant women recruited for this study had any parasitic infection. Pregnancy was associated with asymptomatic intestinal parasitic infection (OR = 4.859 95% CI = 0.2660, 88.782). Pregnancy has been reported to lower immunity as a result of general immunosuppression, sustained by elevated levels of cortisol, which allows fetal allograft retention but renders the woman susceptible to various infectious diseases. This may explain the findings in this study. However, the association observed in this study failed to reach statistical significance (P = 0.3231).
The age of the pregnant women significantly affected the prevalence of asymptomatic intestinal parasitic infection (P = 0.0330) with the age group 41-50 years having the highest prevalence. This finding is not in agreement with the report of Akinbo et al. where pregnant women below 29 years were at increased risk of intestinal helminth infections. The difference could be due to the fact that Wekesa et al. subjects live in slum settlements and were mostly rural dwellers as opposed to our subjects, the majority of which live in the city.
The level of education of pregnant women in this study did not significantly affect the prevalence of intestinal parasitic infection (P = 0.1170). This is not in agreement with the findings of Wekesa et al. which reported that pregnant women with a primary level of education were at a higher risk of intestinal parasitic infection. The difference could be due to geographical location.
The occupation of pregnant women significantly affected enteric parasitic infections, with traders having the highest prevalence 10.3% (P = 0.0186). Alli et al. reported significantly higher prevalence among farmers followed by traders. It is important to note that none of our pregnant subjects were farmers. Traders are more likely to eat and drink from questionable sources as they carry out their activities. Traders are likely to have a low educational status which may contribute to a large extent, poor personal hygiene standards. This may explain the reason for this finding.
Not washing hands regularly by pregnant women was significantly associated with asymptomatic intestinal parasitic infection (OR = 9.484; 95% CI = 1.522, 59.081 P = 0.0239). This agrees with a previous report. This finding underscores the importance of hand washing after each activity as an effective way of preventing and controlling parasitic diseases.
Asymptomatic intestinal parasitic infections were significantly more among pregnant women who patronize food vendors (P = 0.0096). Man acquires enteric parasitic infections by ingesting the infectious stage in contaminated food, drink or soil. Food vendors are likely to have a low educational background and to an extent, poor hygiene standards. This may explain the findings in this study.
Pregnant women that always walk barefooted had the highest prevalence of asymptomatic intestinal parasitic infections among pregnant women in this study (6.3%), albeit, this prevalence was not statistical different (0.0882) from those that do not always (3.9%) and those that never walk barefooted (0.7%). Soil pollution is a major factor in the transmission of enteric parasitic infections in a community which are transmitted through poor sanitary habits of indiscriminate defecation. The filariform larvae of hookworm and ova of other soil-transmitted helminths flourish in damp soil and grass, which may be found around homes as occasioned by rain floods. Many people walk and play in open field barefooted, and these habits increase the chances of contacting infections like hookworm and S. stercoralis infections.
Gestational age did not significantly (P = 0.1004) affect the prevalence of asymptomatic intestinal parasitic infections, though, those in the second trimester had the highest prevalence. The finding that pregnant women in the second trimester had the highest prevalence of intestinal parasitic infections had previously been reported. Many authors have suggested deworming of pregnant women after the first trimester to reduce the risk of anemia and its associated sequelae on the pregnant woman and the fetus.,,
Parasitic infections are known to cause anemia among subjects. The most important cause of pathological chronic loss of blood and iron in tropics is Ancylostoma duodenale, Necator americanus and other soil-transmitted helminths, especially among children. Anemia was significantly associated with enteric parasitic infections among pregnant women in this study (OR = 17.914; 95% CI = 0.9779, 328.19; P = 0.0190). Rodríguez-Morales et al. reported that anemia in pregnancy was associated with intestinal parasitic infections. This was observed in this study.
In this study, the parasites recovered from pregnant women were A. lumbricoides and hookworm. A. lumbricoides had a prevalence of 80% of enteric parasitic infection while hookworm had 20%. Similar parasites were observed by Omorodion et al., Wekesa et al. and Ayeh-Kumi et al. There were no intestinal parasites recovered from the control population.
| Conclusion|| |
An overall prevalence of 2.2% enteric parasitic infections was observed among pregnant women. Pregnant women between the ages of 41 and 50 years that were farmers, those that did not always wash their hands and those patronizing food vendors were more likely to have an asymptomatic intestinal parasitic infection and be anemic. Measures to reduce the effect of enteric parasitic infections among pregnant women are advocated.
We thank the management of University of Benin Teaching Hospital, Benin City, Edo State for providing us with the patients used in this study.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Alli JA, Okonko IO, Kolade AF, Nwanze JC, Dada VK, Ogundele M. Prevalence of intestinal nematode infection among pregnant women attending antenatal clinic at the University College Hospital, Ibadan, Nigeria. Adv Appl Sci Res 2011;2:1-13.
Obiamiwe BA, Nmorsi P. Human gastro-intestinal parasites in Bendel state, Nigeria. Angew Parasitol 1991;32:177-83.
WHO. Prevention and Control of Intestinal Parasitic Infections, Tech. Rep. 749. Geneva, Switzerland: World Health Organization; 1987.
WHO. The Control of Schistosomiasis and Intestinal Nematodes: World Health Report Database No. WHOCDSCSIP991; 1999.
Steketee RW. Pregnancy, nutrition and parasitic diseases. J Nutr 2003;133 5 Suppl 2:1661S-7.
Akinbo FO, Okaka CE, Omoregie R. Seasonal variation of intestinal parasitic infections among HIV-positive patients in Benin City, Nigeria. Ethiop J Health Sci 2011;21:191-4.
Omorodion OA, Isaac C, Nmorsi OP, Ogoya EM, Agholor KN. Prevalence of intestinal parasitic infection among tertiary institution students and pregnant women in south-south, Nigeria. J Microbiol Biotechnol Res 2012;2:815-9.
WHO. Schistosomiasis and soil-transmitted helminthiasis — An unprecedented opportunity for control. In: WHO. Communicable Diseases 2002 - Global Defence Against the Infectious Diseases Threat. Geneva, Switzerland: World Health Organization; 2003.
Amuta E, Houmsou R, Mker S. A comparative study of intestinal parasitic infections among women at different reproductive stages in Makurdi, Benue State-Nigeria. Internet J Biol Anthropol 2008;3:1-3.
van Eijk AM, Lindblade KA, Odhiambo F, Peterson E, Rosen DH, Karanja D, et al.
Geohelminth Infections among pregnant women in rural western Kenya; a cross-sectional study. PLoS Negl Trop Dis 2009;3:e370.
Brooker S, Hotez PJ, Bundy DA. Hookworm-related anaemia among pregnant women: A systematic review. PLoS Negl Trop Dis 2008;2:e291.
Villar J, Klebanoff M, Kestler E. The effect on fetal growth of protozoan and helminthic infection during pregnancy. Obstet Gynecol 1989;74:915-20.
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.
Nurdia DS, Sumarni S, Suyoko, Hakim M, Winkvist A. Impact of intestinal helminth infection on anemia and iron status during pregnancy: A community based study in Indonesia. Southeast Asian J Trop Med Public Health 2001;32:14-22.
Savioli L, Crompton DW, Neira M. Use of anthelminthic drugs during pregnancy. Am J Obstet Gynecol 2003;188:5-6.
Stephenson LS, Latham MC, Ottesen EA. Malnutrition and parasitic helminth infections. Parasitology 2000;121 Suppl:S23-38.
Hotez P. Hookworm and poverty. Ann N
Y Acad Sci 2008;1136:38-44.
Hotez PJ, Fenwick A, Savioli L, Molyneux DH. Rescuing the bottom billion through control of neglected tropical diseases. Lancet 2009;373:1570-5.
Ndyomugyenyi R, Kabatereine N, Olsen A, Magnussen P. Malaria and hookworm infections in relation to haemoglobin and serum ferritin levels in pregnancy in Masindi district, western Uganda. Trans R Soc Trop Med Hyg 2008;102:130-6.
Akinbo FO, Ikedje A, Okaka CE. Intestinal parasitic infections among artisans in Benin City, Nigeria. Niger J Clin Basic Sci 2013; 10:66-9.
Pena-Rosas JP, Nesheim MC, Garcia-Casal MN, Crompton DW, Sanjur D, Viteri FE, et al.
Intermittent iron supplementation regimens are able to maintain safe maternal hemoglobin concentrations during pregnancy in Venezuela. J Nutr 2004;134:1099-104.
Steer PJ. Maternal hemoglobin concentration and birth weight. Am J Clin Nutr 2000;71:1285S-7S.
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;23:1-5.
Humphries DL, Stephenson LS, Pearce EJ, The PH, Dan HT, Khanh LT. The use of human faeces for fertilizer is associated with increased intensity of hookworm infection in Vietnamese women. Trans R Soc Trop Med Hyg 1997;91:518-20.
Meeusen EN, Bischof RJ, Lee CS. Comparative T-cell responses during pregnancy in large animals and humans. Am J Reprod Immunol 2001;46:169-79.
Akinbo FO, Okaka CE, Omoregie R. Prevalence of intestinal parasitic infections among HIV patients in Benin City, Nigeria. Libyan J Med 2010;5:1-6.
Wekesa AW, Mulambalah CS, Muleke CI, Odhiambo R. Intestinal helminth infections in pregnant women attending antenatal clinic at Kitale district hospital, Kenya. J Parasitol Res 2014;2014:823923.
Mordi RM, Ngwodo PO. A study of blood and gastro-intestinal parasites in Edo state. Afr J Biotechnol 2007;6:2201-7.
Schmidtmann ET, Bobian RJ, Belden RP. Soil chemistries define aquatic habitats with immature populations of the Culicoides variipennis
). J Med Entomol 2000;37:58-64.
Agbolade OM, Abimbola WA, Bolarinwa OI, Akinboye DO, Ogunkolo OF. Parasitic infestations, anaemia and blood glucose level in out-patients of a secondary health centre in south-western Nigeria. World J Med Sci 2009;4:147-50.
Ayeh-Kumi PF, Nti SA, Duedu KO, Addo-osafo K, Obeng RA, Mortu S, et al
. Intestinal parasitosis among pregnant women in Accra, Ghana. Ghana J Allied Health Sci 2008;2:9-14.
[Table 1], [Table 2], [Table 3]
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