|Year : 2017 | Volume
| Issue : 1 | Page : 15-20
Risk factors of intestinal parasitic infections among human immunodeficiency virus-infected patients on highly active antiretroviral therapy
FO Akinbo1, PJ Anate2, DB Akinbo2, R Omoregie3, S Okoosi4, A Abdulsalami5, B Isah6
1 Department of Medical Laboratory Science, School of Basic Medical Sciences, University of Benin, Benin City, Nigeria
2 Department of Medical Laboratory Science, Acheivers University, Owo, Ondo State, Nigeria
3 Department of Medical Microbiology, School of Medical Laboratory Sciences, University of Benin Teaching Hospital, Benin City, Nigeria
4 Department of Medicine, General Hospital, Obangede, Nigeria
5 Department of Clinical Services, Zonal Hospital, Okene, Nigeria
6 Department of Hospital Services, State Ministry of Health, Okene, Nigeria
|Date of Submission||20-Jun-2016|
|Date of Acceptance||24-Oct-2016|
|Date of Web Publication||19-Apr-2017|
F O Akinbo
Department of Medical Laboratory Science, School of Basic Sciences, University of Benin, Benin, Edo State
Source of Support: None, Conflict of Interest: None
Background: Highly active antiretroviral therapy (HAART) improves immunity and reduces the occurrence of enteroparasitic infections.
Aim: This study aimed to determine the prevalence and risk factors of intestinal parasitic infection among human immunodeficiency virus (HIV) patients on HAART in Kogi State, Nigeria.
Methods: Blood and stool specimens were collected from 511 subjects including 411 HIV patients on HAART and 100 apparently healthy non-HIV individuals. The blood specimens were used to determine CD4 count and haemoglobin concentration, whereas the stool specimens were processed to detect intestinal parasites using standard techniques. Socio-demographic data were obtained with the aid of a questionnaire.
Results: Entamoeba histolytica was the predominant parasites recovered generally and in both genders as well as being the only parasite that was associated with immunodeficiency as measured by CD4 count <200 cell/μL (P = 0.0059) HIV status was a significant risk factor for acquiring intestinal parasitic infection (odds ratio = 8.213 95% confidence interval = 1.971, 34.225; P = 0.0012). Among the other risk factors, CD4 count <200 cell/μL (P < 0.0001) and farming (P = 0.0202) were associated with intestinal parasitic infections among HIV patients on HAART.
Conclusion: An overall prevalence of 14.4% of intestinal parasitic infections was observed among HIV patients on HAART in this study. Routine diagnosis of intestinal parasites among HIV patients on HAART is advocated.
Keywords: Human immunodeficiency virus, intestinal parasitic infection, Kogi state, risk factors
|How to cite this article:|
Akinbo F O, Anate P J, Akinbo D B, Omoregie R, Okoosi S, Abdulsalami A, Isah B. Risk factors of intestinal parasitic infections among human immunodeficiency virus-infected patients on highly active antiretroviral therapy. Port Harcourt Med J 2017;11:15-20
|How to cite this URL:|
Akinbo F O, Anate P J, Akinbo D B, Omoregie R, Okoosi S, Abdulsalami A, Isah B. Risk factors of intestinal parasitic infections among human immunodeficiency virus-infected patients on highly active antiretroviral therapy. Port Harcourt Med J [serial online] 2017 [cited 2022 Aug 12];11:15-20. Available from: https://www.phmj.org/text.asp?2017/11/1/15/204718
| Introduction|| |
Acquired immunodeficiency syndrome (AIDS), referred to as 'Ugiagbe' in local parlance, is caused by human immunodeficiency virus (HIV). It is characterised by progressive damage to the immune system, resulting in the development of various opportunistic infections., The HIV has emerged as a global health problem, with serious medico-economic and social implications. Sub-Saharan Africa remains by far the most affected region accounting for almost 70% of the global total of new HIV infections, with 24.7 million people living with HIV in 2013., In Nigeria, 3.2 million people are living with HIV with 210,000 deaths annually.
Intestinal parasitic infections are among the most common infections worldwide and about 3.5 billion persons, mostly children, are estimated to be infected. In Nigeria, intestinal parasitic infection constitutes a major public health challenge. Poorly planned housing, improper waste disposal, gross environmental pollution and poor environmental situations among others are driving forces for this observation., Illiteracy, absence of clean drinking water and poverty has been shown to promote infection with intestinal parasites. These have been reported as driving forces for HIV infection.
One of the main features of HIV infection is immunosuppression that leads to exposing the subject to a variety of microbial and parasitic attacks. Moreover, in the tropics, there is a consistent association between HIV infection and other diseases including malaria, Mycobacterium tuberculosis and intestinal parasitosis. Intestinal parasitic infections have been observed in HIV-infected patients, although the prevalence varies based on location, the age of the study population, stage of the disease and laboratory methods used. People with HIV infection are vulnerable to opportunistic infections and malignancies that take advantage of the opportunity offered by a weakened immune system. Antiretroviral treatment increases the length and quality of life and productivity of patients by improving survival and decreasing the incidence of opportunistic infections in people with HIV through reduction of the viral load and increasing the level of CD4 cells. With the advent of highly active antiretroviral therapy (HAART) in 1996, to control HIV infection as well as improving the immune system of these patients, reduced occurrence of enteroparasitic infections has been observed. There is no report on the effect of HAART on the prevalence of intestinal parasitic infection among HIV patients on HAART in Kogi state, Nigeria. Against this background, this study was conducted to determine the prevalence and risk factors associated with intestinal parasitic infections among HIV patients on HAART in Kogi state, Nigeria
| Methods|| |
This study was conducted at the General Hospitals and Comprehensive Health Centres in Adavi, Okene, Ajaokuta and Ogori-Magongo local government areas of Kogi state. These health institutions are centres for HIV infection management in the State. The drugs used in the HAART regimen for HIV-infected patients include zidovudine, lamivudine and nevirapine. Random sampling method was employed to select participants. Patients who are not on HAART, those on anti-parasitic agents and those with AIDS-defining conditions were excluded from the study. Apparently healthy age-matched non-HIV-infected were recruited as controls. A pre-designed structured questionnaire was used to collect biodata and socio-demographic characteristics for this study during sample collection. Informed consent was obtained from participants before specimen collection. The protocol for this study was approved by the Ethics and Research Committee of the Kogi State Ministry of Health, Kogi state, Nigeria.
Sample collection and processing
Blood and stool samples were collected from each participant. A volume of 5 ml of venous blood sample was collected from each participant into ethylene diamine tetraacetic acid (EDTA) and mixed. The blood samples were analysed for CD4+ T lymphocytes cell count using flow cytometry (Partec GmBh, Münster, Germany). In brief, 20 μl of CD4 PE antibody was placed into a test tube, to this 20 μl of well mixed whole EDTA blood sample of the patient was added and mixed gently. The mixture was incubated in the dark and agitated at 5 min intervals for 15 min at room temperature. Eight hundred microliters of CD4 buffer was added and mixed gently. The Partec test tube containing the mixture was inserted to the flow cytometry for counting.
Haemoglobin concentration was determined using an auto-analyser-Sysmex KX-21N (Sysmex Corporation, Kobe, Japan). Anaemia was defined as haemoglobin concentration of <13 g/dl for males and 12 g/dl for females using the WHO criteria.
Freshly produced stool specimens were processed using the formol-ether concentration technique and viewed microscopically for the presence of intestinal parasites. In breif, about 1 g of feces was emulsified in 4 ml formol-saline and agitated. The mixture was sieved. To the filtrate, 4 ml diethyl ether was added and agitated. The mixture was spun at 3000 rpm for 1 min. The faecal debris on the side of the tube was detached with the aid of a plastic pipette and the supernatant discarded. From this sediment, saline and iodine mounts were prepared and examined for the presence of parasites.
The data obtained was analysed using Chi-squares test and odd ratio analysis. The statistical software INSTAT ® was used for the analysis (GraphPad Software Inc., La Jolla, CA, USA).
| Results|| |
Five hundred and eleven subjects including 411 HIV-infected patients on HAART and 100 apparently healthy non-HIV-infected individual that served as controls were recruited for this study. The age of the participants ranged from 19 to 62 years.
HIV status was a significant risk factor for acquiring intestinal parasitic infection (odds ratio [OR] =8.213 95% confidence interval [CI] =1.917, 34.225; P = 0.0012). HIV patients with CD4 count <200 cells/μL (P < 0.0001) and were farmers (P = 0.0202) had significantly higher prevalence of intestinal parasitic infection. Other risk factors did not significantly affect the prevalence of intestinal parasitic infections among HIV patients on HAART [Table 1] and [Table 2].
|Table 1: Effect of human immunodeficiency virus status on the prevalence of intestinal parasitic infection|
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|Table 2: Risk factors of intestinal parasitic infection among human immunodeficiency virus patients|
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A total of 59 intestinal parasites were recovered from HIV patients on HAART and Entamoeba histolytica was the most prevalent generally and in both genders. Giardia intestinalis, Taenia species and Hookworm were only recovered from females [Table 3].
None of the intestinal parasites were significantly (P > 0.05) associated with anaemia [Table 4], whereas only E. histolytica infection was significantly associated with CD4 count <200 cells/μL (OR = 3.985 95% CI = 1.563, 10.162; P = 0.0059) [Table 5].
|Table 5: Effect of CD4 count on the prevalence of intestinal parasitic infection|
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| Discussion|| |
HAART has also been reported to significantly reduce the morbidity and mortality of HIV infection  with reduction in enteroparasitic infection. Lack of data on the effect of HAART on the prevalence of intestinal parasitic infection among HIV patients on HAART in Kogi state, Nigeria, necessitated this study.
A prevalence of 14.4% of intestinal parasitic infection among HIV patients on HAART was observed in this study. This is higher than the 5.3% reported in Benin City, Nigeria. The difference could be due to geographical location and the setting of the research. Among children with diarrhoea, prevalence of the infection has been reported to vary with geographical locations, regions within the same country and even over time in the same location and population. This study was carried out in Kogi state, North Central, Nigeria while that of Akinbo and Omoregie  was carried out in Benin City, South-South, Nigeria. Akinbo and Omoregie  study was conducted among patients receiving care in a tertiary health institution located in an urban setting, whereas the HIV patients in this study received their care from primary and secondary health institutions located in rural settings. Although HAART has been reported to improve immune status, thereby preventing the occurrence of opportunistic parasitic infections, the prevalence observed in this study was high. A range of 3.9%–6.2% has been reported among non-HIV subjects in Nigeria., However, a prevalence of 2% was observed among non-HIV subjects in this study.
The finding that HIV status was significantly associated with intestinal parasitic infections agrees with a previous study among HAART-naïve HIV patients. The studies that observed parasitic infections among HIV patients on HAART did not look at association between HIV (on HAART) and intestinal parasitic infection.,, The main findings of these studies are lower prevalence of intestinal parasitic infections among HIV patients on HAART.
The finding that gender was not significantly associated with intestinal parasitic infections among HIV patients on HAART agrees with previous reports,, whereas similar finding among non-HIV subjects had been previously noted.
HAART promotes the reconstitution of the immune system of HIV-infected persons, thereby reducing the occurrence of opportunistic parasitic infections.,, Cellular immunity is the major defense against intestinal parasitic infections. Akinbo and Omoregie  reported that CD4 count <200 cells/μL was significantly associated with intestinal parasitic infections among HIV patients on HAART. This was also observed in this study. Akinbo and Omoregie  opined that, although HAART improves immunity, HIV patients on HAART with CD4 count <200 cells/mL are still prone to intestinal parasitic infections.
In this study, the prevalence of intestinal parasitic infections was highest among HIV patients with diarrhoea. This is inconsistent with previous reports., With the exception of occupation, other studied risk factors did not significantly affect the prevalence of intestinal parasitic infections. This is not in agreement with a previous study among HAART-naïve HIV patients where all the studied risk factors significantly affected the prevalence of intestinal parasitic infections. In this study, HIV patients on HAART that were farmers had significantly higher prevalence of intestinal parasitic infections compared with their counterparts in other occupation. The process of farming increases the risk of exposure to intestinal parasitic infections.
A total of 59 intestinal parasites were recovered in this study. Generally and in both genders, E. histolytica was the most prevalent agent of intestinal parasitic infection among HIV patients on HAART. A previous study among HIV patients on HAART in Benin City, Nigeria, reported A. lumbricoides as the most prevalent intestinal parasite while S. stercoralis was the most prevalent in a similar study from Brazil. The difference could be due to geographical location. Other intestinal parasites recovered in this study included A. lumbricoides, S. stercoralis, hookworm, G. intestinalis and Taenia species. A. lumbricoides, Hookworm and S. stercoralis were the only intestinal parasites recovered in Akinbo and Omoregie  study.
HIV patients on HAART without anaemia had approximately 1–4-fold risk (OR = 2.007 95% CI = 1.112, 3.622; P = 0.0294) of acquiring intestinal parasitic infection (data not shown). This implies that among HIV patients on HAART, anaemia was not associated with intestinal parasitic infection (OR = 0.498). This is not in agreement with a previous report. The reason for this difference is unclear. However, the cause of anaemia in HIV-positive patients is multifactorial and includes infections, neoplasm, dietary deficiencies, blood loss, medications and antibodies to antiretroviral agents., The finding that none of the intestinal parasitic agents were significantly associated with anaemia agrees with a previous report.
Only E. histolytica was significantly associated with CD4 count <200 cells/μL and this finding was not consistent with a previous report among HAART-naïve HIV patients where E. histolytica was not significantly associated with CD4 count <200 cells/μL. Among HIV patients on HAART, A. lumbricoides has been reported to be significantly associated with <200 cells/μL  – a finding that was not observed in this study.
It is important to note that opportunistic coccidian parasites were not searched for in this study and they have been reported among HIV patients on HAART. This may indicate that the prevalence of intestinal parasitic infection among HIV patients may be higher than reported.
| Conclusion|| |
An overall prevalence of 14.4% of intestinal parasitic infection among HIV patients on HAART was observed in this study. The prevalence of intestinal parasitic infection among HIV patients on HAART were higher among those with CD4 count <200 cells/μL and those who practice farming as occupation. Routine diagnosis of intestinal parasites among HIV patients on HAART is advocated.
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Conflicts of interest
There are no conflicts of interest.
| References|| |
Omoregie R, Ogefere HO, Okolie MN, Umahoin IR. Prevalence of pulmonary tuberculosis among subjects infected with human immunodeficiency virus (HIV) strains 1 and 2. J Med Lab Sci 2007;16:40-3.
Okolie MN, Eghafona NO, Omoregie R. Anti-human immunodeficiency virus agents. J Med Lab Sci 2003;12:1-14.
Ngwai YB, Nwankwo HN, Adoga MP. Multi-drug resistant Escherichia coli
from human immunodeficiency virus/acquired immunodeficiency syndrome (HIV/AIDS) patients in Keffi, Nigeria. Int Res J Microbiol 2011;2:122-5.
Oladeinde BH, Phil RO, Olley M, Anunibe JA. Prevalence of HIV and anemia among pregnant women. N Am J Med Sci 2011;3:548-51.
Houmisou RS, Amita EU, Olusi TA. Prevalence of intestinal parasites among primary school children in Makurdi, Benue State, Nigeria. Internet J Infect Dis 2010;8:1-5.
Uneke CJ, Nnachi MI, Arua U. Assessment of polyparasitism with intestinal parasitic infections and urinary schistosomiasis among school children in a semi-urban area of South Eastern Nigeria. Internet J Health 2009;9:1-7.
Ikeh EI, Obadofin MO, Brindeiro B, Baugherb G, Frost F, Vanderjagt D, et al.
Intestinal parasitism in rural and urban areas of North Central Nigeria: An update. Internet J Microbiol 2006;2:1.
Nkenfou CN, Nana CT, Payne VK. Intestinal parasitic infections in HIV infected and non-infected patients in a low HIV prevalence region, West-Cameroon. PLoS One 2013;8:e57914.
Mehraj V, Hatcher J, Akhtar S, Rafique G, Beg MA. Prevalence and factors associated with intestinal parasitic infection among children in an urban slum of Karachi. PLoS One 2008;3:e3680.
Tladi LS. Poverty and HIV/AIDS in South Africa: An empirical contribution. SAHARA J 2006;3:369-81.
Veas F, Rey JL. HIV infection and parasitosis in tropical area. Cah Health 1991;1:189-201.
Ghimire P, Sakpota D, Manandhar SP. Cryptosporidiosis: Opportunistic infections in HIV/AIDS patients in Nepal. J Trop Med Parasitol 2004;27:7-10.
Akinbo FO, Okaka CE, Machado RL, Omoregie R, Onunu AN. Cryptosporidiosis among HIV-infected patients with diarrhea in Edo State, Midwestern Nigeria. Malays J Microbiol 2010;6:99-101.
Hogg RS, Yip B, Kully C, Craib KJ, O'Shaughnessy MV, Schechter MT, et al.
Improved survival among HIV-infected patients after initiation of triple-drug antiretroviral regimens. CMAJ 1999;160:659-65.
Willemot P, Klein MB. Prevention of HIV-associated opportunistic infections and diseases in the age of highly active antiretroviral therapy. Expert Rev Anti Infect Ther 2004;2:521-32.
Beutler E, Waalen J. The definition of anemia: What is the lower limit of normal of the blood hemoglobin concentration? Blood 2006;107:1747-50.
Cheesbrough M. Parasitological Tests. Cambridge: University Press, 1999; 178-308.
Gea-Banacloche JC, Lane HC. Immune reconstitution in HIV-1 infection. AIDS 1991;13:525-38.
Akinbo FO, Omoregie R. Intestinal parasitic infections in HIV-infected persons on highly active antiretroviral therapy (HAART) in Benin City, Edo State, Nigeria. Genet Med Biomark Health Sci 2011;3:119-22.
Petri WA Jr., Miller M, Binder HJ, Levine MM, Dillingham R, Guerrant RL. Enteric infections, diarrhea, and their impact on function and development. J Clin Invest 2008;118:1277-90.
Odunukwe N, Idigbe O, Kanki P, Adewole T, Onwujekwe D, Audu R, et al.
Haematological and biochemical response to treatment of HIV-1 infection with a combination of nevirapine + stavudine + lamivudine in Lagos Nigeria. Turk J Haematol 2005;22:125-31.
Akinbo FO, Omoregie R, Eromwon R, Igbenimah IO, Airueghiomon UE. Prevalence of intestinal parasites among patients of a tertiary hospital in Benin city, Nigeria. N Am J Med Sci 2011;3:462-4.
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.
Bachur TP, Vale JM, Coêlho IC, Queiroz TR, Chaves Cde S. Enteric parasitic infections in HIV/AIDS patients before and after the highly active antiretroviral therapy. Braz J Infect Dis 2008;12:115-22.
Teklemariam Z, Abate D, Mitiku H, Dessie Y. Prevalence of intestinal parasitic infection among HIV positive persons who are naive and on antiretroviral treatment in Hiwot Fana Specialized University Hospital, Eastern Ethiopia. ISRN AIDS 2013;2013:324329.
Nobre V, Braga E, Rayes A, Serufo JC, Godoy P, Nunes N, et al.
Opportunistic infections in patients with AIDS admitted to an university hospital of the Southeast of Brazil. Rev Inst Med Trop Sao Paulo 2003;45:69-74.
Derouin F, Lagrange-Xelot M. Treatment of parasitic diarrhea in HIV-infected patients. Expert Rev Anti Infect Ther 2008;6:337-49.
Omalu IC, Yako AB, Duhlinska DD, Anyanwu GI, Pam VA, Inyama PU. First detection of intestinal microsporidia in Northern Nigeria. Online J Health Allied Sci 2005;3:4.
Moyle G. Anaemia in persons with HIV infection: Prognostic marker and contributor to morbidity. AIDS Rev 2002;4:13-20.
Omoregie R, Egbeobauwaye A, Ogefere H, Omokaro EU, Ekeh CC. Prevalence of antibodies to HAART agents among HIV patents in Benin City, Nigeria. Afr J Biomed Res 2008;11:
Akinbo FO, Okaka CE, Omoregie R, Adamu H, Xiao L. Unusual Enterocytozoon bieneusi
genotypes and Cryptosporidium hominis
subtypes in HIV-infected patients on highly active antiretroviral therapy. Am J Trop Med Hyg 2013;89:157-61.
[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]