Prevalence of enteric parasitic infections among people living with HIV in Abeokuta, Nigeria

Introduction Enteric parasitic infections have been increasingly recognized as etiology of life-threatening chronic diarrhea in PLWHA in sub-Saharan Africa. This study investigated the prevalence and burden of intestinal parasitic infection among PLWHA in Abeokuta, southwest Nigeria. Methods Freshly passed stool samples were collected from PLWHA. Detection of Cryptosporidium spp and Microsporidium spp was carried out with Kinyoun's stain and Weber's Chromotrope-based stain respectively. Investigation of other intestinal parasites was done using the direct saline preparation and formol-ether concentration methods. CD4+ T cell count was measured using Partec flow cytometry technique Results A total of 231 (males: females 96:135; mean age 31.81±11.40 years) PLWHA were recruited into the study, among whom 84 (36.4%) were infected with at least one intestinal parasites. Fifty two (22.5%) individuals were positive for Cryptosporidium spp and a significant association between Cryptosporidium sppand diarrhea was observed (p=0.006). Seven (3.0%) were positive for Microsporidium spp. Helminths recovered included Ascaris lumbricoides (20.8%), hookworm (6.5%), Strongyloides stercoralis (4.3%), Trichuris trichiura (5.6%) and Taenia spp. (5.6%). Cryptosporidium spp, Microsporidium spp and S. stercoralis were significantly associated with CD4+ count ≥ 200 cells/mm3 (p<0.05). Cryptosporidium sppand A. lumbricoides were significantly observed among patients that are anti-retroviral therapy (ART) naive. Conclusion High prevalence of opportunistic parasitic infection was significantly correlated with diarrhea, low CD4+ count and ART naïve individuals in the study. These findings re-emphasize the need for early diagnosis of opportunistic parasites and appropriate intervention among PLWHA.


Introduction
Enteric parasitic infections are important and common features of Human Immunodeficiency Virus infection (HIV), causing significant morbidity and responsible for about 80% of Acquired Immune Deficiency Syndrome (AIDS)-related deaths [1,2]. Co-infections of HIV and opportunistic parasites, including intestinal protozoa and helminths, are of concern in resource-poor settings where the health status of the population is generally poor and these opportunistic parasites very common [3]. The resultant effect of such parasitic infections include chronic diarrhea, weight loss, and malnutrition, which has been associated with death among AIDS patients [4]. HIV has the capacity to circumvent and weaken human immune system providing the impetus for increased infection with parasites such as Cryptosporidium spp., Microsporidium spp, Giardia intestinalis, and Strongyloides (S) stercoralis [4].
Cryptosporidium spp, Microsporidia and other coccidian parasites have emerged as significant causes of persistent diarrhea in People living with HIV/AIDS (PLWHA) [5]. These pathogens have been recognized as worldwide causes of diarrhea in all age groups, yet their most significant impact have been felt among individuals with weakened immune systems, especially PLWHA and organ transplant recipients [6]. In immunocompromised individuals, diarrheal infections goes beyond the inconvenience of frequent watery stool but may result in severe and potentially life-threatening dehydration, electrolyte loss and malnutrition, and eventually death [7]. Transmission of Cryptosporidium is mainly through the fecaloral route in contaminated water and food, as well as through person-to-person spread and contact with infected animals [8].
Microsporidiosis, caused by Microsporidia, another important opportunistic pathogen causing significant morbidity in PLWHA [9], is also associated with life-threatening chronic diarrhea and systemic disease [10] and are caused by members of Enterocytozoon and Encephalitozoon genera [11]. The route of transmission is usually by ingestion of the spores, including evidence of spore inhalation or rectal transmission [12].
Nigeria has the highest number of PLWHA (3.2 million) after South Africa (6.8 million) [13]. HIV causes progressive depletion of the CD4+ T cells, leading to life-threatening opportunistic infections during the natural course of the disease [14]. In immunocompromised patients, the intestinal parasites play a major role in causing chronic diarrhea accompanied by weight loss [15], with diarrhea reported in up to 50% of PLWHA in developed countries prior to the use of antiretroviral therapy (ART), and in up to 80% of those in resource-limited countries [14,16]. Antiretroviral therapy increases the length and quality of life and productivity of patients by improving survival and decreasing the incidence of opportunistic infections in PLWHA through the reduction of circulating viremia and increasing the level of CD4+ cells [16].
Previous studies in Nigeria have investigated intestinal parasitic infections in relation to ART and CD4+ count [17,18]. There is therefore the need for continuous surveillance of the prevalence and impact of these intestinal parasites among PLWHA, so as to provide guidance on prevention and control of co-infections, as well as reducing associated morbidity and mortality.  [19,20]. Blood samples were analyzed for CD4+ T cell estimates by flow cytometry. Patients with loose/ watery stool who also confirmed the passage of such stool for 2 to 3 times within the last 24 hours were considered to be having diarrhea.

Discussion
Parasitic infections are major public health concern among PLWHA in developing countries, particularly in sub-Saharan Africa, with its high burden of HIV infections [21]. Down-regulation of the immune system, a hallmark of HIV infection, renders an individual extremely susceptible to numerous opportunistic parasitic infections [22].
Among such infections, gastrointestinal parasites are some of the leading causes of morbidity and mortality in, and are a universally recognized problem in PLWHA [21][22][23]. In this study, the overall prevalence of intestinal parasitic infection among PLWHA was found to be 36.4%. The result is almost similar to the findings from Ethiopia [8], Cameroon [23], and Saudi Arabia [24], but lower than those previously reported in Nigeria [18], India [25], Cameroon [26] and Lao PDR [27]. Such differing prevalence rates might be due to differences in geographical location, sensitivity of diagnostic techniques, immune status of study participants, environmental hygiene and possible increased awareness, amongst others. Several species of intestinal opportunistic parasites have been reported among PLWHA [16], with Cryptosporidium spp, Microsporidium spp and S. stercoralis the most commonly encountered in this study. Cryptosporidium spp, which was found to be responsible for diarrhea in 10-20% of PLWHA worldwide [28], has been reported among PLWHA in Nigeria [29], and more importantly in those with CD4+ T-cell counts of less than 200 cells/mm 3 [18]. Limited evidence suggests that antiretroviral therapy (ART) reduces prevalence of helminth infections in PLWHA [30,38]. In this study, the prevalence of both helminth and protozoa intestinal infections was higher in ART naïve PLWHA compared to those already on ART.

Conclusion
In conclusion, this study reveals a high prevalence of opportunistic parasitic infections, significantly correlated with diarrhea and low  Overall prevalence of the enteric pathogen is still high compared to a previous report, which suggests that much effort is needed to control these pathogens among PLWHA.
Page number not for citation purposes 5

Competing interests
The authors declare no competing interests.

Authors' contributions
Specify

Acknowledgments
The authors are grateful to all the patients who participated in the study.