|Year : 2020 | Volume
| Issue : 1 | Page : 26-31
Prevalence of intestinal helminth infection among human immunodeficiency virus/acquired immune deficiency syndrome patients attending Aminu Kano teaching hospital
Abdulhadi Sale Kumurya1, Fatima Salahu Ibrahim1, Nura Muhammad Bunza2
1 Department of Medical Laboratory Science, Faculty of Allied Health Sciences, Bayero University, Kano, Nigeria
2 Department of Medical Microbiology, School of Medical Laboratory Sciences, Usmanu Danfodiyo University, Sokoto, Nigeria
|Date of Submission||25-Sep-2019|
|Date of Acceptance||10-May-2020|
|Date of Web Publication||31-Jul-2020|
Mr. Nura Muhammad Bunza
Department of Medical Microbiology, School of Medical Laboratory Sciences, Usmanu Danfodiyo University, Sokoto
Source of Support: None, Conflict of Interest: None
Background: Helminth and human immunodeficiency virus (HIV) infections have a major effect on the host immune system, and coinfection is widespread. About 17%–66% of the world populations are infected with helminth and approximately 24% of the world's population is infected with intestinal helminth. The majority of this infection occurs in resource-limited settings like sub-Saharan Africa which includes Nigeria. Materials and Methods: Stool samples were collected from 297 participants comprising 150 HIV/acquired immune deficiency syndrome (AIDS)-infected individuals as test group and 147 HIV/AIDS-uninfected individuals as control group attending Aminu Kano Teaching Hospital. The samples were examined using direct wet mount and formol-ether concentration techniques. Results: The overall prevalence of intestinal helminth infection was 18.0% for the test group and 2.7% for the control group. Hookworm was found to be the most prevalent intestinal helminth parasite detected with 7.07%, followed by Ascaris lumbricoides (2.69%) and Fasciola species (0.67%), respectively. Some protozoan parasites were also detected, namely Entamoeba coli (3.4%) and Entamoeba histolytica (2.7%). Six of the participants had multiple infections with hookworm and E. histolytica (3 [1.0%]), A. lumbricoides and E. coli (2 [0.7%]), and A. lumbricoides and E. histolytica (1 [0.3%]). A statistically significant association was observed between the type of toilet used, animal rearing, handwashing, and intestinal helminth infection (P 0.02, 0.003, and 0.000). No statistical association exists between sources of water, walking barefooted, and intestinal helminth infection (P 0.211 and 0.942). Conclusion: This study revealed an increased prevalence of intestinal helminth infection among the test group than the control group, as such stool examination should be part of the routine laboratory investigations for HIV/AIDS patients to have effective and proper management of the patients.
Keywords: Formol-ether concentration, human immunodeficiency virus/acquired immune deficiency syndrome, intestinal helminth
|How to cite this article:|
Kumurya AS, Ibrahim FS, Bunza NM. Prevalence of intestinal helminth infection among human immunodeficiency virus/acquired immune deficiency syndrome patients attending Aminu Kano teaching hospital. Niger J Exp Clin Biosci 2020;8:26-31
|How to cite this URL:|
Kumurya AS, Ibrahim FS, Bunza NM. Prevalence of intestinal helminth infection among human immunodeficiency virus/acquired immune deficiency syndrome patients attending Aminu Kano teaching hospital. Niger J Exp Clin Biosci [serial online] 2020 [cited 2020 Oct 27];8:26-31. Available from: https://www.njecbonline.org/text.asp?2020/8/1/26/291194
| Introduction|| |
Helminth infection is one of the most common and neglected diseases affecting >30% of the world's population. They are the most common parasitic agent of human disease in Africa and other developing countries producing a burden of disease that exceed better known conditions, including malaria and tuberculosis. Helminth infection is prevalent in these regions because of a combination of economic underdevelopment and conducive climate which are favorable for the development and survival of the larvae of the helminthic parasite. The rate of infection is high in sub-Saharan Africa where the majority of the human immunodeficiency virus (HIV) and acquired immune deficiency syndrome (AIDS) are concentrated. It is estimated that approximately 2 billion (24%) of the world's population are infected with intestinal helminthes., In Nigeria, intestinal helminthic infections have continued to prevail because of low level of standard of living, poor environmental sanitation, and ignorance of simple health-promoting procedure. The most important intestinal helminthes are the soil-transmitted helminthes, such as Ascaris lumbricoides, Trichuris trichiura, and Strongyloides stercoralis, and hookworms.
Intestinal helminthic infection has been shown to be common among people with HIV/AIDS in Africa, with a prevalence ranging from 17% to 66% depending on the methods used to identify the helminth. Helminth and HIV infections have a major effect on the host immune response, and coinfection is widespread., The main problem of patients with HIV/AIDS is diarrhea and severe weight loss, which would be the cause of death too., The rate of diarrhea in HIV-infected people in developed countries has been reported about 30%–60% and in developing countries like Africa, 90%. Unfortunately, in >50% of the cases, the causes of diarrhea in HIV/AIDS patients are undiagnosed.
| Materials and Methods|| |
It is a comparative cross-sectional study.
The study was conducted at Aminu Kano Teaching Hospital (AKTH), which serves as a referral center and is located along Zaria road within Kano metropolis. The state has a total land area of 20,760 km2. It laid on latitude 11°N and longitude 8E. Kano state borders with Katsina state to the Northwest, Jigawa state to the Northeast, Bauchi state to the Southeast, and Kaduna state to the south-west.
Stool samples were collected from patients who had consented to participate in the study in clean, dry, leak-proof, and wide-mouthed plastic specimen containers.
Saline wet mount
The saline wet mounts were made by mixing about 2 mg fecal sample in a drop of normal saline placed on a clean glass slide. Any gross fiber or particle was removed and then gently covered with a cover slip avoiding air bubbles and over flooding. The smears were examined under a microscope using × 10 and × 40 objectives.
Iodine wet mount
Iodine wet mount was made by emulsifying small amount of the stool sample in a drop of five times diluted solution of Lugol's iodine on a clean glass slide and then covered with a coverslip. The smears were examined under the microscope using × 10 and × 40 objectives for the presence of parasites ova or larva.
Sedimentation technique using formal ether
About 0.5 g of stool sample was transferred to 10 ml of 10% formalin in a 15 ml centrifuge tube, mixed, and allowed to stand for 30 min for adequate fixation. The fecal suspensions were then strained through two layers of gauze in a funnel into a centrifuge tube. About 4 ml of diethyl ether was added to the tubes, closed with a stopper, and vigorously shaken for 30 s. The mixture was centrifuged for 2 min at 500 g and the supernatant decanted. A small amount of the well-mixed sediment was placed on a clean glass slide and then covered with a coverslip. It was then examined under the microscope for the presence of parasites.
Data derived were analyzed using the Statistical Package for the Social Science version 20.0 (IBM, Chicago, IL, USA). Categorical data were analyzed using the Chi-square test. P ≤ 0.05 was considered statistically significant at a 95% confidence interval.
Ethical approval to conduct this study was obtained from the Ethics and Research Committee of AKTH, Kano State, in accordance with the clinical and university standard. The objectives and procedures of the research were explained to the subjects. Informed consent was obtained from all the participants prior to sample collection.
| Results|| |
Of the 150 HIV/AIDS Participants enrolled in the study, the overall intestinal helminth prevalence was found to be 27 (18.0%) and 4 (2.7%) for the HIV noninfected control group, as shown in [Table 1]. Individual intestinal helminth infection rate revealed that hookworm had the highest prevalence of 13.33% for test group and 0.68% for the control group, followed by Ascaris lumbricoides (test group = 3.33% and control group = 2.04%) and Fasciola (test group = 1.33% and control group = 0%), respectively [Table 2].
|Table 1: Prevalence of intestinal helminthic infection in human immunodeficiency virus/AID patients and control group|
Click here to view
|Table 2: Frequency of intestinal helminthes parasites in human immunodeficiency virus/AIDS patients and control group|
Click here to view
In addition to the intestinal helminth identified during the study, some protozoan parasites were equally detected, namely Entamoeba histolytica (8 [2.7%]) and Entamoeba coli (10 [3.4%]). Six of the participants had mixed infection with hookworm and E. histolytica (3 [1.0%]), A. lumbricoides and E. coli (2 [0.7%]), and A. lumbricoides and E. histolytica (1 [0.3%]) [Table 3].
|Table 3: Prevalence of intestinal protozoan parasites and multiple infections among human immunodeficiency virus/AIDS patients|
Click here to view
Gender-specific infection rate shows that males had the highest prevalence of 59.3% than the females (40.7%) counterpart for the test group, whereas females had the highest infection rate of 75% than males (25%) for the control group. Participants within the age group of 31–40 years recorded the highest prevalence of intestinal helminth infection in both test (44.4%) and control (50%) groups. Based on the level of education, the study revealed that for the test group, patients with secondary school education had the highest infection (33.3%), while those with primary education recorded the highest infection (50%) for the control group. The study according to marital status indicated that single (unmarried) participants were more infected with intestinal helminth parasites for both test (40.7%) and control (75%) groups [Table 4].
|Table 4: Sociodemographic distribution of intestinal helminthic infection among human immunodeficiency virus/AIDS patients and healthy control group|
Click here to view
Based on risk factors associated with intestinal helminth infection, the study revealed that participants with well as the source of water, pit latrine for toilet, rear animals, and washed their hands before eating had the highest prevalence for both control (75%, 75%, 50%, and 75%) and test (51.9%, 51.9%, 74.1%, 88.9%) groups, while those who always walked via footed recorded more infection (55.6%) for the test group, as shown in [Table 5].
|Table 5: Distribution of risk factors associated with intestinal helminthes infection among human immunodeficiency virus/AIDS patients and control group|
Click here to view
| Discussion|| |
Owing to the deterioration of the immune system because of HIV infection, there are numerous types of opportunistic infections, of which intestinal parasitic infection, which includes helminth, is a universally recognized problem.
The overall prevalence of intestinal helminth parasite in HIV/AIDS-infected individuals in the study group was 18.0%. This is lower than the figure obtained by Abdulhadi and Adamu that reported a prevalence rate of 32.0% in Kano State. This finding is also lower when compared with the previous reports (67.1%) by Timothy et al. in Gwagwada, Kaduna, 43.0% prevalence by Gundri et al. in Adamawa, and Modjarrad et al. in Zambia. Other report from Ebonyi State has a prevalence of 24.4%. A much lower prevalence of 9.1% by Oriakpono et al. in Northeast Nigeria and 2.5% by Longdoh et al. in Cameroon were recorded. This observed difference could be due to the study population and the laboratory methods of identification employed.
A total of 3 types of intestinal parasite were detected in HIV/AIDS patients and two types in the control group, with hookworm being the most prevalent (7.07%), followed by A. lumbricoides (2.6%) and Fasciola (0.67%). A study carried out in Kano reported a similar prevalence of 5.8% hookworm. A higher prevalence of 23% was reported in Kano state, 14.0% in Southwest Nigeria, 20.6% in Benin City, and in Uganda 24%. A lower prevalence rate of hookworm 4.2% was reported in Abuja. The differences could be as a result of environmental and behavioral patterns of the people in the study.
The prevalence of some protozoan parasites detected during the study indicated E. coli as the most frequent with a prevalence rate of 3.4%, followed by E. histolytica (2.7%). A report of 4.3% prevalence of E. coli was obtained in another study in Kano and 6.7% E. histolytica in Abuja, Nigeria. This is contrary to the finding of this study. Multiple infections among the study participants also exist, hookworm and E. histolytica, A. lumbricoides and E. coli, and A. lumbricoides and E. histolytica. The presence of multiple infections could be because of low immunity possessed by the study participants that made them prone to opportunistic infections.
The pattern of intestinal helminth infection among the study participants showed that males have the highest prevalence rate of the infection in subject group (59.3%). However, this conforms to the findings of Abelau et al. in Plateau, who reported a higher prevalence in males than females, and contrary to the findings of Ekpenyong and Eyo. No statistical association was found between gender and helminthic infection (P 0.655).
Of the various age groups studied, this study found that helminth parasites were most common among 31–40 years range. This is in agreement with Abelau et al. in Plateau but contrary to Modjarrad et al. in Zambia (24.9%). In Ethiopia, Fontenent et al. reported >70.0% of adults with intestinal helminth infection, in contrast to this findings Alo et al. report <1% of adults being infected with intestinal helminth infection among HIV individuals in North India. Behavioral and ecological patterns may contribute to the differences in parasite distribution.
In accordance with the occupation, the study found out that students had the highest rate of intestinal helminth parasitic infection in both HIV-infected and HIV-uninfected individuals (48.1% and 50.0%). No statistical relationship exists between occupation and helminth infection (P 0.929). This is contrary to the finding of Abelau et al. in Plateau. The reason for the high prevalence among this group could be attributed to the environmental factors and differences in sample size.
The study reveals that water source as the risk factor to intestinal helminth infection in the study participants is statistically not significant (P 0.211). Those who have well as water source had a higher prevalence (51.9%) in the test group and 75.0% in the control group when compared to other sources of water. This conforms to the findings of Isyaku et al. in Sokoto and another report in South Africa.
Toilet type, rearing of animals, handwashing, and intestinal helminth show a statically significant association (P 0.022, 0.003, and 0.00), respectively, in both HIV-infected and uninfected individuals. This is contrary to the finding of Isyaku et al. in Sokoto and in South Africa. More so, no statistically significant association was found between walking barefooted and intestinal helminthic infection (P 0.942). This conforms to the finding of Nwokeocha et al. in River State, Nigeria. This difference could be a result of the difference in topology, environmental sanitation, and sample size.
| Conclusion|| |
The study revealed that the intestinal helminth infection was relatively common among the study population with an overall prevalence of 18.0% prevalence, which is low. This low prevalence can be attributed to the different demographic distribution of helminth and HIV infection where HIV is more common among youths and helminths among children of school age.
In this study, a statistically significant association was found between intestinal helminth infection and HIV.
Various risk factors predisposing individuals to helminth infection have also been investigated although few show no statistical significance which may be as a result of the study environment factors and sample size.
Financial support and sponsorship
Conflicts of interest
There are no conflicts of interest.
| References|| |
Enobong I, Anochie CI, Azubuike JC, Nkanginimie KE. Intestinal Heiminthic Infection in Pediatric and Child Health in a Tropical Region. 2nd
ed. Oweri, Nigeria: African Educational Services; 2007. p. 438-44.
Hotez PJ, Brindley PJ, Bethony JM, King CH, Pearce EJ, Jacobson J. Helminth infections: The great neglected tropical diseases. J Clin Invest 2008;118:1311-21.
Okodua M, Adeyeba OA, Talfeng YM, Okpala HO. Age andsex distribution of intestinal parasitic infections among HIV infected subjects in Abeokuta, Nigeria. Online J Health Allied Sci 2003;4:3-5.
Bangert M, David H, Steve W, Chistopher F, Dirk E. Cross-cutting contribution of the end of neglected tropical disease to the sustainable development goal. Infect Dis Poverty 2017;6:73-75.
Udonsi JK. Necator americanus
: A cross sectional study of rura community in relation to some clinical sign. Ann Trop Med Parasitol 1984;78:443-445.
Hosseinipour MC, Napravnik S, Joaki G, Gama S, Mbeye N, Banda B, et al
. HIV and parasitic infection and the effect of treatment among adult outpatients in Malawi. J Infect Dis 2007;195:1278-82.
Bundy D, Sher A, Michael E. Good worms or bad worms: Do worm infections affect the epidemiological patterns of other diseases? Parasitol Today 2000;16:273-4.
Michael E, Bundy DA, Grenfell BT. Re-assessing the global prevalence and distribution of lymphatic filariasis. Parasitology 1996;112(Pt 4):409-28.
Ramakrishnan K, Shenbagarathai R, Uma A, Karitha K, Rajendran R. Prevalence of intestinal parasitic infections in HIV/AIDS patients with diarrhea in Madurai city, South India. Jundishaphur J Infect Dis 2007;60:209-10.
Fallahi S, Badparva E, Nahrvanian H, Mohammmadi M. Comparison of the prevalence of intestinal parasites in HIV-Positive and AIDS Patients in Khorramabad city in 2006-2007. J Kerman Univ Med Sci 2009;16:166-72.
Mohandas K, Sehgal R, Sud A, Malla N. Prevalence of intestinal parasitic pathogens in HIV-Seropositive individual in Northen India. J Infect Dis 2002;55:83-4.
Sara A, Masoumeh A, Mohamad GD, Mahdi T, Fatemeh H. Prevalence of intestinal parasites in HIV-positive patients attending Ahvas health center in 2012; cross sectional study in South of Iran. J Chronic Dis Manage 2015;5:24-85.
Ado K. Geographical and History of Kano in Three Year of Good Governance Shekarau Stewardship in Kano State. Research and Documentation Directorate, Government House Kano; 2009.
Arora DR, Arora BB. Medical Parasitology. 4th
ed. New Delhi: CBS Publisher & Distributors, Dary Ganj; 2014. p. 244.
Ochei J, Kolhatkar A. Medical Laboratory Science Theory and Practice. West Patel Nagar, New Delhi: Tata McGraw Hill; 2007. p. 949.
Kaushal KD, Ganga P, Sanjir S, Surbhi M, Shiv L, Usha KB. Enteric opportunistic parasites among HIV infected individuals: Risk factors associated and immune status. Jpn J Infect Dis 2007;60:76-81.
Abdulhadi SK, Adamu H. Prevalence of intestinal helminth infection among HIV Infected people in infectious Disease Hospital, (IDH), Kano Nigeria. Int J Biomed Health Sci 2006;2:10-15.
Timothy A, Ezekiel K, Oricha KA. Studies on the intestinal helminths infestation among primary school children in Gwagwada, Kaduna, Northwestern Nigeria. J Biol Agric Healthc 2013;3:48-53.
Gundri MA, Kwalaghe BT, Hamidu A. Sanitary quality of domestic water supply in Dakawogji, Taraba state, Nigeria. Niger J Parasitol 2001;21:131-6.
Modjarrad K, Zulu I, Redden DT, Njobvu L, Freedman DO, Vermud SH. Prevalence and predictors of intestinal helminth infection among human immunodeficiency virus type-1 infected adult in an urban setting. Am J Trop Med Hyg 2005;73:777-82.
Maria LO, Nnamdi BO, Bede L, Roland L. Prevalence and intencity of helminth infection in human immunodeficiency virus infected children in Abakiliki, Ebonyi State, Southeast Nigeria. J Dent Med Sci 2017;16:81-6.
Oriakpono JE, Sani AF, Wama BE. Intestinal helminthic Infection in Numan Northeast Nigeria. Innov Space Sci Res J 2014;5:102-5.
Longdoh AN, Nguedia JC, Shey DN, Fon D, Fouamo HK, Tanue E, et al
. Low prevalence of intestinal helminth infection among HIV patients in Cameroon. J Microbiol Biotechnol 2012;1:1-7.
Abdullahi S, Samaila AA, Abubakar IS, Yusuf SM, Borodo MM, Babashani M,et al
. Prevalence of intestinal parasites among HIV/AIDS patients in Kano, Nigeria. Kano J Med Sci 2008;2:37-40.
Frederick OA, Christopher EO, Richard O. Prevalence of intestinal parasitic infection among HIV patients in Benin City, Nigeria. Libyan J Med 2010;5:5506-9.
Ndibazza J, Webb EL, Lule S, Mpairwe H, Akello M, Oduru G, et al
. Associations between maternal helminth and malaria infections in pregnancy and clinical malaria in the offspring: A birth cohort in Entebbe, Uganda. J Infect Dis 2013;208:2007-16.
Abaver DT, Nwaobegahay JM, Goon DT, Tweriebor BC, Anye DN. Prevalence of intestinal parasitic infections among HIV/ADS patients from two Health institution in Abuja. Afr Health Sci 2011;11:824-7.
Abelau M, Goselle ON, Udeh EO, Popova DD, Popov TV. A comparative study of the prevalence of helminth parasite in HIV seropositive and seronegetive individual in Plateu state, Nigeria. Niger Ann Nat Sci 2011;11:22-33.
Ekpenyong EA, Eyo JE. Prevalence of Intestinal helminthes Infections among Schooling children in Tropical Semi-urban Communities. Anim Res Int 2008;5:804-10.
Fontenent AP, Canaveras SJ, Gharavi L, Newman LS, Kotzin B. Target organ localization of memoeryCD4(+) T cells in pateints with chronic beryllium disease. J Clin Invest 2002;110:1473-82.
Alo EB, Anosike JC, Danburan JB. A survey of intestinal helminths among students of post-primary institutions in Adamawa state, Nigeria. Appl Parasitol 2002;34:1-7.
Isyaku NT, Nock IH, Ndamis IS, Luka SA. Status and risk factors assoiated with infantile geohelminth infection in Sokoto state, Nigeria. J Pharm Biol Sci 2015;10:34-40.
Adeleke OA, Yogeswaran P, Wright G. Intestinal helminth infections amongst HIV-infected adults in Mthatha General Hospital, South Africa. Afr J Prim Health Care Fam Med 2015;7:910.
Nwokeocha GC, Eze NC, Flourence ON. Geohelminth infection and associated risk factors among children living in selected shanty (Batcher) settlement in Port Harcourt metropolis, River State, Nigeria. Int J Trop Dis Health 2018;29:1-8.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]