Intestinal parasitic infections in HIV-infected patients and domestic animals in Ekiti State, Nigeria

doi:10.21203/rs.3.rs-4363858/v1

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Intestinal parasitic infections in HIV-infected patients and domestic animals in Ekiti State, Nigeria

https://doi.org/10.21203/rs.3.rs-4363858/v1

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Individuals infected with human immunodeficiency virus (HIV) have a high chance of developing parasitic intestinal infections. The presence of zoonotic parasites in animal faeces is also believed to be evidence of readily available sources of infection for humans with these parasites. This study therefore evaluates the prevalence of intestinal parasitic infections among HIV-infected patients and domestic animals. A cross-sectional hospital-based study was carried out at three antiretroviral therapy clinics in Ekiti State, Southwest, Nigeria between February 2018 and December 2019. A total of 330 HIV-infected patients and 77 domestic animals (within their environment) were studied. Faeces were collected and processed using formol-ether concentration and modified Ziehl-Neelsen techniques for the detection of intestinal parasites and Cryptosporidium oocysts, respectively. Socio-demographic and clinical data were collected using structured questionnaires. Fisher’s Exact Test statistical analysis was used to test the level of significance at p < 0.05. The overall prevalence of intestinal parasitic infections among the study population of HIV patients and their pets were 15.5% and 12% respectively. The most predominant parasitic infections amongst the HIV patients was Cryptosporidium sp., (49.0%), while Taenia and Hymenolepis sp. were least with 5.9% each. The CD4 count < 200 (OR: 10.2, 95% CI: 4.3–23.7), and diarrhoea (OR: 7.0, 95% CI: 3.2–17.8) were detected to be the significant associated variables with Cryptosporidium infection. Cryptosporidium sp., (32.1%), Ancylostoma caninum (7.1%) and Toxocara canis (7.1%) were parasites of zoonotic potential detected in animals of participants. Improving public health measures that would emphasize personal hygiene and regular deworming of immunocompromised pets by certified veterinarians is recommended.

Intestinal parasites

HIV-infected patients

domestic animals

Nigeria

Sevem gastrointestinnal parasites were detected in the population of HIV-Infected patients studied, with Cryptosporidium having the highest detectable prevalence
Diarrhoea and CD4 count less than 200mm³ were found to be the two key risk factors for Cryptosporidium infection in the HIV patients
Pets within the same envirnment with the HIV-infected patients were found to be infected with diverse species of gastrointestinal parasites of puplic health significance

Intestinal parasites such as protozoa and helminthes are regarded as a major source of illness and mortality around the world. The burden is notably high in developing nations, where the majority of HIV/AIDS patients are found, and where factors such as poverty and hunger may accelerate the development of both diseases (UNAIDS/WHO, 2002; Bangert et al., 2017)

In HIV/AIDS patients, intestinal parasites such as Cryptosporidium, Trichuris Trichiura Ascaris lumbricoides, Strongyloides stercoralis, and hookworms have been detected; among these parasites, Cryptosporidium, an opportunistic producing Diarrhoea parasite, has been reported to be common (WHO, 2016; Bangert et al., 2017). Infection by intestinal parasites may reduce the well-being of HIV infected individuals (Abaver et al., 2011), and can be spread from person to person, via close interaction with infected animals or via the fecal-oral route through the ingestion of food and water contaminated with resistant oocyst/cyst, and ova (Samie et al., 2013).

Due to their impact on the immune system and increased vulnerability to HIV infection and the clinical development to AIDS, it is believed that intestinal parasitic infections represent a significant contributor to HIV infection in Africa (Kaniyarakkal et al., 2016; Assefa et al., 2017). The prevalence of Cryptosporidium in immunocompromised individuals, especially HIV-infected individuals with CD4 + T-cells count less than 200 cells/mm3, may increase due to lack of health care and inadequate absorption or resistance of antiretroviral drugs caused by poor treatment compliance (CDC, 2019). In addition, The lack of drinking and clean water, poor hygiene and unsafe environmental conditions have been generally responsible for the prevalence of Cryptosporidium and other intestinal parasites commonly found among HIV-infected people in most African countries (Mariam et al., 2008; Abaver et al., 2011)

Animals may play an important role in the epidemiology of some zoonotic parasites such as Cryptosporidium, Ancylostoma caninum and Toxocara canis, thereby constituting probable risk for human health due to the possibility of transmission of these parasites (Larrieu et al., 2001; Velho et al., 2003).

Several studies have reported prevalence of Cryptosporidium and other gastrointestinal parasites in HIV patients worldwide, India (Kaniyarakka et al., 2016), Ethiopia (Gebre et al., 2019), Burkina Faso (Zida et al., 2017), Brazil (Mohandas et al., 2002), Italy (Brandonosio et al., 1999) and in Nigeria (Akinbo et al., 2010; Obateru et al., 2017; Amoo et al., 2018) However, the role of animals in the epidemiology of parasite that may constitute potential risk to HIV patients are lacking, especially in developing countries including Nigeria. This study therefore evaluates the prevalence of Cryptosporidium and other intestinal parasitic infections among HIV-infected patients and domestic animals in Ekiti State

Study design and Sampling location

This study, a cross-sectional, hospital-based was carried out from February 2017 to December 2018 at three antiretroviral therapy clinics within Ekiti State, Nigeria. Ekiti State is one of the six States in the Southwest geopolitical region, located at 7° 40′ north latitude and 5° 5′ east longitude. It has a population of 2,398,957 (census estimates for 2006). The humidity of the zone is elevated and the temperature range from 21°C to 28°C.

Sample collection

Fresh faeces of 330 HIV-infected individuals were collected inside a clean, leak-proof universal bottle after patients had been given appropriate instruction. Fresh faeces of 77 of three species of animals were also collected using standard procedures. Samples were labelled and transported to the laboratory. Samples collected were then stored in the refrigerator at 4ºC until processed for trophozoite, cysts/oocysts and ova detection. In addition, socio-demographic and clinical data were collected using structured questionnaires

Laboratory analysis

The stool samples were processed using formol-ether concentration techniques to detect trophozoite/cyst, larvae and ova of intestinal parasites (Cheesbrough, 2005). The modified Ziehl-Neelsen staining technique was performed to identify Cryptosporidium oocysts as described by Cheesbrough, (2005)

Statistical Analysis

Data entry and analysis were performed using GraphPad Prism Software (Graph-Pad Software Inc., La Jolla, CA, USA). Descriptive summaries were presented in terms of charts and proportions as applicable. Fisher’s Exact Test was used to determine the association between different variables. Odds ratio was calculated to estimate the risk attributable to different factors with confidence intervals and a P-value ≤ 0.05 was considered significant

Ethical Consideration

Ethical approval

s were received under the following numbers, EKSUTH/A67/2017/02/023, HMB/AD.595/22, and UI-ACURECH/18/0085 were obtained. Informed consent of the patients were obtained, while each volunteer signed and/or thumb printed on the consent document.

Socio demographic characteristics of HIV-infected patients

The age of HIV-positive subjects ranged from 18 to 75 years with a mean age of 41. There were 85 (25.8%) males and 245 (74.2%) females with most of them formally educated (reading and writing ability). Individuals with CD4 T cell count less than 200 cells/µl accounted for 18.9%. Most (85.8%) of the participants were on ART, while 71.8% of them registered no animal interaction. Of the participants, only 15.5% had diarrhoea (Table 1).

Human study

Of the 330 faecal samples obtained and analysed from patients diagnosed with HIV, 51 (15.5%) were positive for eggs and oocysts of gastrointestinal parasites (Table 1). Single-infection-positive samples were 96.1% (49/51), while those with multiple infections were 3.9% (2/51). Seven genera of gastrointestinal parasites were detected in all, including Cryptosporidium, Strongyloides, Entamoeba, Ascaris, Ancylostoma sp., Hymenolepis and Taenia sp. Cryptosporidium sp. 49.0% (25/51) was the highest and the least was Hymenolepis nana 5.9% (3/51), and Taenia sp. 5.6% (3/51) (Table 2)

The overall occurrence of Cryptosporidium in HIV-infected participants in this study was 7.6% (25/330), while Cryptosporidium oocysts among HIV-infected patients were 8.2%, 9.3%, 25.5%, 27.6%, 12.8%, and 27.6% in males, age ≥ 30, patients with diarrhoea, CD4 < 200 cell / cmm³, ART-naïve and animal contact, respectively. Among these factors, subjects with CD4 count < 200 cells/microlitre and with diarrhoea had about 10 times (p = 0.0002, 95% CI: 4.3–23.7) and 7 times (p = 0.004, 95% CI: 3.2–17.8) the risk of getting infected with Cryptosporidium, respectively (Table 1).

Animal study

In this study, 77 faecal samples were collected from 3 species of animals including 17 goats (Capra aegagrus hircus), 47 chickens (Gallus gallus), and 13 (Canis lupus familiaris), out of which an overall prevalence rate of 12% (9/77) of Cryptosporidium infection was obtained. The distribution of Cryptosporidium oocyst were 15% (2/13), 10% (5/47), and 15% (2/17) in dogs, chicken and goats, respectively. Other groups of intestinal parasites detected among the animals were protozoan [39.3% (Cryptosporidium sp., Eimeria sp.)], Cestodes [10.2% (Choanotaenia sp., Raillietina sp.)], and Nematodes [17.9% (Ascaridia galli, Toxocara canis, and Ancylostoma caninum)] (Table 2).

Table 1

Risk factors of *Cryptosporidium* infection in HIV-infected patients in Ekiti State South Western Nigeria
Variable	No. % Studied	No. % Infected	OR	95% CI	P-value
Age (years) < 30 ≥ 30	75 (22.7) 255 (77.3)	7 (9.3) 18 (7.1)	1.4	(0.5–3.2)	0.468
Sex Male Female	85 (25.8) 245 (74.2)	7 (8.2) 18(7.3)	1.1	(0.4–2.5)	0.813
Education Formal Informal	302 (91.5) 28 (8.5)	23 (7.6) 2 (7.1)	1.1	(0.4–4.8)	0.642
CD4 count <200 ≥200	58 (18.9) 249 (81.1)	16(27.6) 9 (3.6)	10.2	(4.3–23.7)	0.0002
Stool Consistency Diarrhoeic Non- Diarrhoeic	51 (15.5) 279 (84.5)	13(25.5) 12(4.3)	7.6	(3.2–17.8)	0.0001
Animal contact Yes No	93 (28.2) 237 (71.8)	16(27.6) 9 (3.6)	1.2	(0.5–2.8)	0.649
HAART Yes No	283 (85.8) 47 (14.2)	19 (6.7) 6 (12.8)	2.0	(2.8–5.3)	0.145

Table 2

Percentage of single and mixed infection out of the total positive samples detected in HIV-infected patients and animals.
Parasites	Number positive/percentage (%)
Parasites	Humans Goat	Chicken	Dog
Entamoeba histolytical/dispar	5(9.8) -	-	-
Taenia sp.	3 (5.9) -	-	-
Hymenolepis sp.	3(5.9) -	-	-
Strongyloides stercoralis	6(11.8) -	-	-
Ascaris lumbricoides	5(9.8) -	-	-
Ancylostoma sp.	4(7.8) -	-	-
Cryptosporidium sp.	25(49.0) 2(7.1)	5(17.9)	2(7.1)
Eimeria sp.	2(7.1)	-	-
Monieza sp.	- 1(3.6)	-	-
Choanotaenia sp.	- -	1(3.6)	-
Raillietina sp.	- -	1(3.6)	-
Ascaridia galli	- -	5(17.9)	-
Toxocara canis	- -	-	2 (7.1)
Ancylostoma caninum	- -	-	2 (7.1)
Cryptosporidium sp. + S. stercoralis	2(3.9) -	-	-
Toxocara canis + A. caninum	- -	-	2 (8.7)
Choanotaenia sp. + A. galli	- -	1(3.7)	-

Intestinal parasites, in particular opportunistic ones, are a frequent cause of morbidity and death in individuals infected with HIV. This study reports the occurrence of intestinal parasites in HIV-positive individuals. Studies undertaken in Nigeria as well as other parts of the world also reported intestinal parasitic infections in HIV patients but with variation in results. Akinbo et al, (2010) recorded similar occurrences in HIV patients in Nigeria, Gebre et al, (2019) in Ethiopia, Pavie et al, (2012) in France and Sarfati et al, (2006) in Cameroon. However, Da silva et al, (2005) in Brazil, Mohandas et al, (2002) in India and Tiwari et al, (2013) in Nepal reported higher prevalence than what we have in the present study. The reason for the discrepancies may be due to sampling techniques and size, variation sanitation and hygiene practices, food, water, and other sources of parasitic infection.

Among HIV-positive subjects in this study, Cryptosporidium was found to be the most prevalent intestinal parasite compared to other intestinal parasites. Similar occurrence have been documented in various states in Nigeria by Obateru et al, (2017) in Ilorin, Adesiji et al, (2007) and Oyedeji et al, (2015) in Ile Ife and Amoo et al, (2018) in Abeokuta, Ogun State

Cryptosporidium infection in this study was found to be associated with CD4 < 200 cell /µl and HIV patients with diarrhoea. Low CD4 count (Ayinmode et al., 2014) and diarrhoea (Erhabor et al., 2011) are known risk factors for infection by this protozoan parasite.

The high occurrence and correlation of Cryptosporidium infection with low CD4 count observed in this study is an indication that the parasite is an opportunistic infection freely causing disease in those whose immunity is weak or impaired. (Ghimire et al., 2004). The diarrhoea observed could be a result of disruption of normal intestinal physiology by parasitic infection which usually causes loss of villous enterocytes, villous atrophy and mal-absorptive and secretory pathologies (Abdel-Messih et al., 2005)

The present study identified Entamoeba histolytica as another protozoan parasite infecting HIV individuals in the area under investigation. Previous studies have also reported the occurrence of this parasite in immunocompromised patients such as those infected with HIV (Fontanet et al., 2000; Baldursson & Karanis, 2011).

This study detected S. stercoralis, another bowel nematode in sampled HIV-infected patients. This is similar to the survey by Paboriboune et al, (2014) from Democratic Republic of Congo. The presence of S. stercoralis in HIV infected individuals as an opportunistic infection could be directly linked to the parasite's ability to propagate and persist in infected host through auto-infection and in the environments as free-living forms for a long period of time. These characteristics help the parasite to cause hyper-infection in individuals with weak immunity (Gotuzzo et al., 1999; Marcos et al., 2011; Paula and Costa-Cruz, 2011).

Other nematodes identified in the present study include Ascaris sp. and Ancylostoma sp. Several studies have confirmed ascariasis in HIV-infected people in sub-Saharan Africa (Akinbo et al., 2010; Gedle et al., 2015; Hailemariam et al., 2004). The common occurrence of Ascaris lumbricoides has been associated with its ubiquitous nature and the ability to persist under severe environmental conditions by producing large amounts of resistance ova in the tropics (WHO, 1981). Poverty and inadequate hygiene practices have been known to worsen infection prevalence in both immunocompetent and patients with weak immunity (‘larcain and Holland 2000; Dibua et al., 2013).

The detection of Ancylostoma sp. in HIV-infected individuals in this study is consistent with the results of other investigators in Ethiopia (Gedle et al., 2015) and Nigeria (Pennap et al., 2015). Food habits and people's hygiene, as well as warm temperatures, were established as risk factors for Hookworm infection (Olsen et al., 2001; Traub et al., 2004; Asaolu and Ofoezie, 2003).

This study also found Taenia and Hymenolepis sp. in some examined samples. These tapeworms were also found in Indian (Mohandas et al. 2002) and Ethiopia (Fisseha et al. 1999) in gastrointestinal parasitism among HIV-infected people. Infection with cestodes has been associated with bad hygiene practices and ingestion of meat products that are not properly processed. (Mwanjali et al., 2013). The detection of Taenia and Hymenolepis sp. in these individuals may have some zoonotic implications, as Hymenolepis sp. and some Taenia sp. (e.g Taenia solium) are transmitted from animals to humans (Reeder and Palmer, 2001; Syadaf et al., 2013). More studies are required to further access the risk of zoonosis to HIV- infected individuals

The findings of this study showed that some pets in contact with examined HIV patients were infected with diverse species of gastrointestinal parasites. Cryptosporidium sp., Toxocara canis and Ancylostoma caninum are considered to be of public health significance. Cryptosporidium sp. in infecting animals is known to be responsible for debilitating diarrhoeic condition in HIV infected patients (CDC, 2015), while T. canis and A. caninum in infecting dogs are known aetiology of cutaneous larva migrans (creeping eruption) and visceral (ocular) larva migrans in humans, respectively (Velho et al., 2003; Larrieu et al., 2001). The presence of ova and oocysts of zoonotic parasites in animal faeces of HIV-infected patients are evidences of readily available infection sources of these parasites to humans in studied area. It is therefore recommended that pets of immunocompromised should be regularly dewormed by certified veterinarians

Although, other parasites detected in in-contact animals such as Ascaridia galli, Choanotaenia sp., and Raillietina echinobothrida, Monieza sp., and Eimeria sp. are yet to have documented evidence of their involvement in zoonosis. It is important to ensure that animals in contact with HIV-infected individuals are “parasites free” to avoid aberrant parasites in the humans.

In conclusion, Cryptosporidium infection was found to be the most common intestinal parasite among HIV-infected patients and their pets. Routine screening service for Cryptosporidium and other intestinal parasites is important in the clinical management of HIV-infected patients in the studied area.

Competing interests:

None declared.

UNAIDS/WHO (2002) HIV Epidemic Update. UNAIDS, Geneva
Bangert M, Molyneux DH, Lindsay SW, Fitzpatrick C, Engels D (2017) The cross-cutting contribution of the end of neglected tropical diseases to the sustainable development goals. Infectious Disease of Poverty. 4;6(1):73. 10.1186/s40249-017-0288-0
Organization WH (2016) World Health Organization. Soil Transmitted Helminth Infections: fact sheet
Abaver D, Nwobegahay J, Goon D, Iweriebor B, Anye D (2011) Prevalence of intestinal parasitic infections among HIV/AIDS patients from two health institutions in Abuja, Nigeria. Afr Health Sci 11(3):24–27
Samie A, Tsipa MA, Bessong P (2013) The epidemiology of Cryptosporidium in cats and dogs in the Thohoyandou region, South Africa. Afr J Microbiol Res 7:2510–2518
Kaniyarakkal V, Mundangalam N, Moorkoth AP, Mathew S (2016) Intestinal Parasite Profile in the Stool of HIV Positive Patients in relation to Immune Status and Comparison of Various Diagnostic Techniques with Special Reference to Cryptosporidium at a Tertiary Care Hospital in South India. Adv Med. 6;2016:3564359. 10.1155/2016/3564359
Assefa Y, Gilks CF, Lynen L, Williams O, Hill PS, Tolera T, Malvia A, Van Damme W (2017) Performance of the Antiretroviral Treatment Program in Ethiopia, 2005–2015: strengths and weaknesses toward ending AIDS. International Journal of Infectious Diseases. 2017;60:70–76. 10.1016/j.ijid.2017.05.012
Centers for Disease Control and Prevention. Division of HIV/AIDS Prevention, National Center for HIV/AIDS, Viral Hepatitis, STD, and, Prevention TB August 6,2019
Mariam ZT, Abebe G, Mulu A (2008) Opportunistic and other intestinal parasitic infections in AIDS patients, HIV seropositive healthy carriers and HIV seronegative individuals in southwest Ethiopia. East Afr J Public Health 5(3):169–173
Larrieu E, Costa MT, Cantoni G, Alvarez R, Cavagion L, Labanchi JL, Bigatti R, Araya D, Herrero E, Alvarez E, Mancini S, Cabrera P (2001) Ovine Echinococcus granulosus transmission dynamics in the province of Rio Negro, Argentina, 1980–1999. Vet Parasitol 98:263–272
Velho PENF, Faria AV, Cintra ML, Souza. EM, Moraes AM (2003) Larva Migrans: a case report and review. Revista do Instituto de Medicina Tropical de São Paulo 45:167–171
Gebre B, Alemayehu T, Girma M, Ayalew F, Tadesse BT, Shemelis T (2019) Cryptosporidiosis and Other Intestinal Parasitic Infections and Concomitant Threats Among HIV-Infected Children In Southern Ethiopia Receiving First-Line Antiretroviral Therapy. HIV/AIDS -. Res Palliat Care 11:299–306
Zida A, Yacouba A, Sawadogo MP, Diallo I, Sangare I, Bamba S, Ouattara B, Guiguemde TR (2017) Opportunistic and other intestinal parasites infections among HIV-positive patients in the era of combination antiretroviral therapy and preventive treatment in Ouagadougou, Burkina Faso. J HIV Clin Sci Res 4(1):008–0014. http://doi.org/10.17352/2455-3786.000122
Mohandas K, Sehgal R, Sud A, Malla N (2002) Prevalence of intestinal parasitic pathogens in HIV-positive individuals in Northern India. Jpn J Infect Dis 55(3):83–84
Brandonosio O, Maggi MA, Panaso S, Lisi A (1999) Intestinal protozoa in HIV infected patients in Apulia, south Italy. Epidemiol Infect 123:457–462
Akinbo FO, Okaka CE, Omoregie R (2010) Prevalence of intestinal parasitic infections among HIV patients in Benin city, Nigeria. Libyan J Med 5:10
Obateru OA, Bojuwoye BJ, Olokoba AB, Fadeyi A, Fowotade A, Olokoba LB (2017) Prevalence of intestinal parasites in newly diagnosed HIV/AIDS patients in Ilorin, Nigeria. Alexandria J Med 53(2):111–116. 10.1016/j.ajme.2016.04.001
Amoo JK, Akindele. AA, Amoo AOJ, Efunshile AM, Ojurongbe TA, Fayemiwo SA, Thomas BN, Ojurongbe O (2018) Prevalence of enteric parasitic infections among people living with HIV in Abeokuta, Nigeria. Pan Afr Med J 30:66. 10.11604/pamj.2018.30.66.13160
Cheersbrough M (2005) Identification of Fecal Protozoan Trophozoites, Cysts and Oocysts. District Laboratory Practice in Tropical Countries, Part 1 Second Edition. Cambridge University Press, pp 200–208
Pavie J, Menotti J, Porcher R, Donay JL, Gallien S, Sarfati C, Derouin F, Molina JM (2012) Prevalence of opportunistic intestinal parasitic infections among HIV-infected patients with low CD4 cells counts in France in the combination antiretroviral therapy era. Int J Infect Dis 16:e677–e679
Sarfati C, Bourgeois A, Menotti J, Liegeois F, Moyou-Somo R, Delaporte E, Derouin F, Ngole EM, Molina JM (2006) Prevalence of intestinal parasites including microsporidia in human immunodeficiency virus-infected adults in Cameroon: a cross-sectional study. Am J Trop Med Hyg 74(1):162–164
Da silva CV, Farreira MS, Borges AS, Costa-Cruz JM (2005) Intestinal parasitic infections in HIV/AIDS patients: experience at a teaching hospital in central Brazil. Scan J Inf Dis 37(3):211–215
Mohandas K, Sehgal R, Sud A, Malla N (2002) Prevalence of intestinal parasitic pathogens in HIV-positive individuals in Northern India. Japanese J Infect Disease 55(3):83–84
Tiwari BR, Ghimire P, Malla S, Sharma B&, Karki S (2013) Intestinal parasitic infection among the HIV-infected patients in Nepal. J Infect Developing Ctries 7:550–555. 10.3855/jidc.2785
Adesiji YO, Lawal RO, Taiwo SS, Fayemiwo SA, Adeyeba OA (2007) Cryptosporidiosis in HIV infected patients with diarrhoea in Osun State south-western Nigeria. Eur J Gen Med 4(3):119–122
Oyedeji OA, Adejuyigbe E, Oninla SO, Akindele AA, Adedokun SA, Agelebe E (2015) Intestinal parasitoses in HIV infected children in a Nigerian Tertiary Hospital. J Clin Diagn Res 9:SC01–SC05
Ayinmode AB, Zhang, Dada-Adegbola HO, Xiao L (2014) Cryptosporidium hominis subtypes and Enterocytozoon bienusi genotypes in HIV-infected persons in Ibadan, Nigeria. Zoonoses Public Health 61:297–303
Erhabor O, Obunge O, Awah I (2011) Cryptosporidiosis among HIV-infected persons in the Niger Delta of Nigeria. Niger J Med 20(3):372–375
Ghimire P, Sapkota D, Manandhar SP (2004) Cryptosporidiosis: opportunistic infection in HIV/AIDS patients in Nepal. J Trop Med Parasitol 27:7–10
Abdel-Messih IA, Wierzba TF, Abu-Elyazeed R, Ibrahim AF, Ahmed SF, Kamal K, Sanders J, French R (2005) Diarrhoea associated with Cryptosporidium parvum among young children of the Nile River Delta in Egypt. J Trop Pediatr 51:154–159
Baldursson S, Karanis P (2011) Waterborne transmission of protozoan parasites: review of worldwide outbreaks—an update 2004–2010. Water Res 45:6603–6614
Fontanet AL, Sahlu T, Rinke de Wit T, Messele T, Masho W, Woldemichael T, Yeneneh H and., Coutinho RA (2000) Epidemiology of infections with intestinal parasites and human immunodeficiency virus (HIV) among sugar-estate residents in Ethiopia. Annal Trop Med Parasitol 94:269–278
Paboriboune P, Phoumindr N, Borel E, Sourinphoumy K, Phaxayaseng S et al (2014) Intestinal Parasitic Infections in HIV-Infected Patients, Lao People’s Democratic Republic. PLoS ONE 9:e91452. 10.1371/journal.pone.0091452
Gotuzzo E, Terashima A, Alvarez H, Tello R, Infante R, D.M.Watts, et al (1999) Strongyloides stercoralis hyperinfection associated with human T cell lymphotropic virus type-1 infection in Peru. Am J Trop Med Hyg 60:146–149
Marcos LA, Terashima A, Canales M, Gotuzzo E (2011) Update on strongyloidiasis in the immunocompromised host. Curr Infect Dis Rep 13:35–46
Paula FM, and., Costa-Cruz JM (2011) Epidemiological aspects of strongyloidiasis in Brazil. Parasitology 138:1331–1340
Gedle D, Gelaw B, Muluye D, Mesele M (2015) Prevalence of malnutrition and Its associated factors among adult people living with HIV/AIDS receiving antiretroviral therapy at Butajira Hospital, Southern Ethiopia. BMC Nutr 1:5
Hailemariam G, Kassu A, Abebe G, Abate E, Damte D, Mekonnen E et al (2004) Intestinal parasitic infections in HIV/AIDS and HIV- seronegative individuals in a Teaching Hospital in Ethiopia. Jpn J Infect Dis 57:41–43
WHO (1981) Tech Rep, Ser., No. 666
larcain P, Holland CV (2000) The public health importance of Ascaris lumbricoides. Parasitology 121:51–71
Dibua UM, Ejere VC, Lijoka I, Oti OA (2013) Intestinal Parasitic infestations among people living with HIV/AIDS in Nsukka, Southeast Nigeria. Int J Curr Microbiol Appl Sci 2:539–550
Pennap GR, Ajegena S, Dodo U (2015) Intestinal Parasitosis among HIV Positive Patients Accessing Healthcare in a Medical Centre in Norhtern Nigeria. Int J Curr Microbiol Appl Sci 4:768–777
Olsen A, Samuelsen H, Onyango-Ouma W (2001) A study of risk factors for intestinal helminth infections using epidemiological and anthropological approaches. J Biosoc Sci 33:569–584
Traub RJ, Robertson ID, Irwin P, Mencke N, Andrew Thompson RC (2004) The prevalence, intensities and risk factors associated with geohelminth infection in tea-growing communities of Assam. India Trop Med Int Health 9:688–701
Asaolu SO, Ofoezie IE (2003) The role of health education and sanitation in the control of helminth infections. Acta Trop 86:283–294
Mwanjali G, Kihamia C, Kakoko DVC, Lekule F, Ngowi H, Johansen MV et al (2013) Prevalence and Risk Factors Associated with Human Taenia Solium Infections in Mbozi District, Mbeya Region, Tanzania. PLoS Neglected Trop Disease 7e2102. https://doi.org/10.1371/journal.pntd.0002102
Fisseha B, Patros B, Woldemichael T, Mohammed H (1999) Diarrhoea associated parasitic infections agents in AIDS patients within selected Addis Ababa Hospitals. Ethiop J Health Dev. 13,169 – 74
Reeder PES, Palmer MM (2001) Imaging of Tropical Diseases: With Epidemiological, Pathological, and Clinical Correlation (2 (revised) ed.). Heidelberg, Germany: Springer-Verlag. pp. 641–642. ISBN 978-3-540-56028-9
Syadaf HS, Khan SS, Kanwal N, Tasawer BM, Ajmal SM (2013) Review on diarrhea causing Hymenolepis nana-dwarf tapeworm. Int Res Pharm 4:32–35
Communicable Disease Control and Infection Prevention (CDC). Cryptosporidiosis: sources of infection and risk factors (2015) http://wwwcdcgov/parasites/crypto/infectionsourceshtml

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Intestinal parasitic infections in HIV-infected patients and domestic animals in Ekiti State, Nigeria

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Abstract

Impacts

Introduction

Methods

Study design and Sampling location

Sample collection

Laboratory analysis

Statistical Analysis

Ethical Consideration

Results

Socio demographic characteristics of HIV-infected patients

Human study

Animal study

Discussion

Declarations

Competing interests:

References

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