Abstract.
The problem of intestinal parasitic infection in human immunodeficiency virus (HIV)–infected people requires careful consideration in the developing world where poor nutrition is associated with poor hygiene and several coinfecting diseases. Studies have addressed this issue in Cameroon, especially in the low HIV prevalence area. The current study was conducted to determine the prevalence of intestinal parasitosis in people living with HIV (PLHIV) in Adamaoua and to identify associated risk factors. Stool and blood specimens from study participants were screened for intestinal parasites and anti-HIV antibodies, respectively. Of 235 participants, 68 (28.9%) were HIV positive, 38 of them on antiretroviral treatment (ART). The overall prevalence of intestinal parasites was 32.3%. Of 68 PLHIV, 32.3% (22/68) were infected with intestinal parasites, compared with 32.3% (54/167) of the HIV-negative patients. Univariate analysis showed no difference between the prevalence of intestinal parasites among PLHIV and HIV-negative patients (P = 0.69). ART was not associated with the prevalence of intestinal parasites. Multivariate analysis showed that the quality of water and the personal hygiene were the major risk factors associated to intestinal parasitosis. The level of education was associated with HIV serostatus: the higher the level of education, the lower the risk of being infected with HIV (P = 0.00). PLHIV and the general population should be screened routinely for intestinal parasites and treated if infected.
INTRODUCTION
Human immunodeficiency virus (HIV)-associated immunodeficiency often results in the appearance of opportunistic infections. These opportunistic infections may be bacterial, viral, or parasitic and are associated with increased morbidity and mortality.1,2 Of these infections, copro-parasites are the leading cause of severe, chronic diarrhea.3 About 60% of the world population is infected with intestinal parasites. They have significant morbidity.4 The prevalence of these infections is remarkably high in sub-Saharan Africa where HIV is concentrated. In Cameroon, the prevalence of intestinal parasites have been shown to vary by study site and study years: 33% in 2006 in Yaounde,5 27.8% in 2012 in Douala,6 and 14.6% in 2013 in Dschang.7 Malnutrition prevailing in sub-Saharan Africa promote the spread of parasitic infections.8 Digestive disorders in individuals with HIV are extremely common and 90% of patients frequently consult for gastrointestinal disorders during the course of the disease.9 In people living with HIV (PLHIV), diarrhea caused by these parasites are responsible for electrolyte disorders and malabsorption of nutrients and oral drugs. These factors may result in anorexia, weight loss, and a general deterioration of the patient’s health.1 A study carried out in Calabar in Nigeria within a population of PLHIV on antiretroviral treatment (ART) showed a prevalence of 29% of copro-parasites with a prevalence of 12% among HIV negative.10 Similar studies have been done in Cameroon in the Center region, in the West, and in the Littoral. No such study has been performed in the northern part of Cameroon. The goals for this study were to determine the prevalence rates for intestinal parasites in PLHIV in the Adamaoua Region of Cameroon, and associated risk factors.
MATERIALS AND METHODS
Study area and population.
The study was conducted in the Regional Hospital of Adamaoua in Ngaoundere and other health facilities, where during the period from 2004 and 2011, HIV has decreased from 6.9% to 5.1%, but still high compared with the national prevalence (4.3%).11 Adamaoua is one of the 10 regions of Cameroon. It borders Nigeria in the west and the Central African Republic in the east. Its capital is Ngaoundere. This mountainous area marks the border between the forest in the south and the savannas of the north. The land is poor and sparsely populated. The main economic activity is cattle breeding (zebus).
Islam is the main religion. The Fulani form the main ethnic group of this region, but there are minorities like Tikar and Gbaya, as well as other smaller ethnic groups. The majority of participants recruited in this study live in Ngaoundere, an urban setting, some in peri-urban setting (Meiganga, Ngaoundal, and Tignere) and the rest live in rural setting (Dang, Bawa, beka, and Tamounagui).
Process of the survey.
Patients consulting at the hospitals were requested to participate in the study. After obtaining informed consent, a questionnaire was administered to each participant by the nurse who had been specifically trained for this task. At least one stool sample and one blood sample were collected from each of the participants and used for intestinal parasites and HIV testing, respectively. Only one stool sample was analyzed because individuals often only provided one of the three requested stool samples. Since there was a possibility of HIV misdiagnosis, HIV testing was performed for all our study participants according to the Cameroon national HIV testing algorithm. None of the participants were taking antiparasitic medications.
Laboratory procedures.
The blood samples of all participants were screened for anti-HIV antibodies using Determine HIV 1/2 HIV rapid test (Alere, Chiba, Japan). Reactive samples were subjected to confirmation using Oraquick rapid test (OraSure Technologies, Thailand).
Stool samples were analyzed by direct microscopy with physiological saline and iodine, and after concentration by the formalin ether method coupled with the Ziehl–Neelsen modified technique for the detection of Cryptosporidium sp. and Isospora belli.12 Giemsa staining was also performed on the concentrated parasites for the identification of microsporidies.13
Statistical analysis.
Data were registered in Microsoft Excel 2016 and analyzed with R 3.2.5 statistical software. χ2 test (or Fisher’s test when necessary) was used to compare the prevalence of intestinal parasites according to HIV status. Multivariate analysis was used to perform and visualize the profile of patients infected with protozoa and helminths. And then, multivariate logistic model was used to evaluate the risk of parasitic infections by HIV infection status, hygienic conditions, and other variables (marital status, age, sex, educational level, etc.).
Ethics statement.
The study protocol was approved by the “Cameroon Bioethics Initiative” (CAMBIN) under the registration N° CBI/320/ERCC/CAMBIN. The confidentiality of each participant was respected.
Written informed consent was obtained prior to questionnaire administration and samples collection.
Patients newly diagnosed HIV positive were referred to HIV Treatment Center for counseling, care and management. Those diagnosed with intestinal parasites were offered appropriate medications.
RESULTS
Demographic characteristic of study population.
The majority of participants (85.9%) recruited in this study live in Ngaoundere (202/235), 5.5% (13/235) in peri-urban setting (Meiganga, Ngaoundal, and Tignere) and the rest (8.5%; 20/235) live in rural area (Dang, Bawa, beka, and Tamounagui).
A total of 235 people 16 to 90 years of age (mean 31.6 ± 12) were recruited. The number of female participants was higher (158; 67.2%) than that of male participants (77; 32.8%); thus, a sex ratio F/M of 2.1. Complete data were collected from all participants who had provided stool and blood samples as well as answered the questionnaires (see Table 1).
Table 1.
Overall population demographic, clinical and laboratory data
| Variable | Overall population N (%) | HIV-infected patients N (%) | Non-HIV-infected patients N (%) | P value between HIV-infected and noninfected patients | Infected with protozoans/helminths N (%) | HIV patients infected by parasites N (%) | Non-HIV patients infected by parasites N (%) | P value between HIV and non-HIV infected by parasites |
|---|---|---|---|---|---|---|---|---|
| N (%) | 235 | 68 (28.94) | 167 (71.06) | × | 76 (32.34) | 22 (32.35) | 54 (32.34) | 0.99 |
| Sex | ||||||||
| Male | 77 (32.77) | 21 (30.88) | 56 (33.53) | 0.69 | 26 (34.21) | 6 (27.27) | 20 (37.04) | 0.41 |
| Female | 158 (67.23) | 47 (69.12) | 111 (66.47) | 0.69 | 50 (65.79) | 16 (72.73) | 34 (62.96) | 0.41 |
| Average age ± SD (year) | 31.61 ± 11.96 | 32.62 ± 8.90 | 31.2 ± 13 | 0.017 | 32.66 ± 12.21 | 31.86 ± 7.56 | 32.98 ± 13.71 | 0.41 |
| Marital status | ||||||||
| Single | 74 (31.49) | 14 (20.59) | 60 (35.93) | 0.02 | 19 (25.00) | 4 (18.18) | 15 (27.78) | 0.38 |
| Married | 133 (56.6) | 39 (57.35) | 94 (56.29) | 0.88 | 46 (60.53) | 13 (59.09) | 33 (61.11) | 0.87 |
| Cohabitation | 4 (1.70) | 1 (1.47) | 3 (1.80) | 1.00 | 1 (1.32) | 0 (0.00) | 1 (1.85) | 1.00 |
| Widowed | 11 (4.68) | 6 (8.82) | 5 (2.99) | 1.00 | 3 (3.95) | 0 (0.00) | 3 (5.56) | 1.00 |
| Divorcee | 13 (5.53) | 8 (11.76) | 5 (2.99) | 1.00 | 7 (9.21) | 5 (22.73) | 2 (3.70) | 1.00 |
| Education level | ||||||||
| Illiterate | 50 (21.28) | 24 (35.29) | 26 (15.57) | 0.00 | 19 (25.00) | 8 (36.36) | 11 (20.37) | 0.14 |
| Primary | 57 (24.26) | 24 (35.29) | 33 (19.76) | 0.01 | 17 (22.37) | 6 (27.27) | 11 (20.37) | 1.0 |
| Secondary | 86 (36.6) | 18 (26.47) | 68 (40.72) | 0.04 | 25 (32.89) | 7 (31.82) | 18 (33.33) | 0.90 |
| Postsecondary | 42 (17.87) | 2 (2.94) | 40 (23.95) | 0.00 | 15 (19.74) | 1 (4.55) | 14 (25.93) | 1.00 |
| Occupation | ||||||||
| Student | 44 (18.72) | 3 (4.41) | 41 (24.55) | 0.00 | 12 (15.79) | 1 (4.55) | 11 (20.37) | 1.00 |
| Farming | 9 (3.83) | 7 (10.29) | 2 (1.20) | 0.00 | 1 (1.32) | 0 (0.00) | 1 (1.85) | 1.00 |
| Housewife | 83 (35.32) | 35 (51.47) | 48 (28.74) | 0.00 | 28 (36.84) | 11 (50.00) | 17 (31.48) | 0.13 |
| Official | 21 (8.94) | 1 (1.47) | 20 (11.98) | 0.01 | 2 (2.63) | 0 (0.00) | 2 (3.70) | 1.00 |
| Others | 78 (33.19) | 22 (32.35) | 56 (33.53) | 0.86 | 33 (43.42) | 10 (45.45) | 23 (42.59) | 0.82 |
| Personal hygiene wash of hands | ||||||||
| Always | 167 (71.06) | 50 (73.53) | 117 (70.06) | 0.59 | 43 (56.58) | 12 (54.55) | 31 (57.41) | 0.82 |
| Sometimes | 67 (28.51) | 18 (26.47) | 49 (29.34) | 0.65 | 33 (43.42) | 10 (45.45) | 23 (42.59) | 0.82 |
| Not at all | 1 (0.43) | 0 (0.00) | 1 (0.60) | 1.00 | 0 (0.00) | 0 (0.00) | 0 (0.00) | |
| Nail cleaning | ||||||||
| Always | 118 (50.21) | 37 (54.41) | 81 (48.50) | 0.41 | 33 (43.42) | 10 (45.45) | 23 (42.59) | 0.82 |
| Sometimes | 106 (45.11) | 28 (41.18) | 78 (46.71) | 0.44 | 41 (53.95) | 11 (50.00) | 30 (55.56) | 0.66 |
| Not at all | 11 (4.68) | 3 (4.41) | 8 (4.79) | 1.00 | 2 (2.63) | 1 (4.55) | 1 (1.85) | |
| Cleaning after defecation | ||||||||
| Wash with water | 78 (33.19) | 25 (36.76) | 53 (31.74) | 0.46 | 39 (51.32) | 12 (54.55) | 27 (50.00) | 0.72 |
| Use toilet paper | 95 (40.43) | 13 (19.12) | 82 (49.10) | 2.164e-05 | 22 (28.95) | 4 (18.18) | 18 (33.33) | 0.18 |
| Others methods | 62 (26.38) | 30 (44.12) | 32 (19.16) | 8.27e-05 | 15 (19.74) | 6 (27.27) | 9 (16.67) | 1.00 |
| Source of water consumed | ||||||||
| Borehole | 61 (25.96) | 14 (20.59) | 47 (28.14) | 0.23 | 32 (42.11) | 7 (31.82) | 25 (46.30) | 0.25 |
| Tap | 174 (74.04) | 54 (79.41) | 120 (71.86) | 0.23 | 44 (57.89) | 15 (68.18) | 29 (53.70) | 0.25 |
| ART | ||||||||
| Yes | 38 (16.17) | 38 (55.88) | 0 (0.00) | < 2.2e-16 | 11 (14.47) | 11 (50) | 0 (0.00) | 1.00 |
| No | 197 (83.83) | 30 (44.12) | 167 (100) | < 2.2e-16 | 65 (85.53) | 11 (50) | 54 (100) | 1.00 |
ART = antiretroviral treatment; HIV = human immunodeficiency virus; SD = standard deviation.
HIV testing.
Sixty-eight patients were HIV positive (28.9%) and 167 HIV negative (71.1%). Thirty-eight infected patients were on ART, whereas 30 were treatment naïve (see Table 1).
Parasitic infections.
Fresh stool analyses showed prevalence of parasites of 14% (33/235). After concentrating the stools, a prevalence of 25.5% (60/235) was found. This prevalence rose to 32.3% (76/235) after specific histologic stains. No difference was observed in the prevalence of intestinal parasitic infection according to the HIV status. Also, there was no association between density of parasites and HIV status (Table 2).
Table 2.
Parasites density with respect to HIV status
| Density | PLHIV N (%) | HIV-negative patients N (%) |
|---|---|---|
| Nul | 46 (67.65) | 114 (68.26) |
| Light | 2 (2.94) | 11 (6.58) |
| Moderate | 11 (16.18) | 29 (17.37) |
| Heavy | 9 (13.23) | 13 (7.78) |
| Total | 68 | 167 |
HIV = human immunodeficiency virus; PLHIV = people living with HIV. P = 0.43.
The following parasites were identified in the study population: Blastocystis hominis (18.3%), Entamoeba histolytica/dispar (6.4%), Entamoeba coli (5.96%), Endolimax nana (3.8%), Crystosporidium parvum (3%), Iodamoeba buetschlii (2.1%), Trichomonas intestinalis (1.7%), Giardia lamblia (1.3%), Embadomonas intestinalis (0.4%), Cyclospora cayetanensis (0.4%), Ascaris lumbricoides (0.4%), and hookworm (0.4%). More specifically, B. hominis was the most frequently identified parasites equally in PLHIV (16.2%) and HIV-negative (19.2%) participants. Six cases of C. parvum were identified, three among PLHIV and three among HIV-negative participants. Two participants were infected with microsporidies, one PLHIV, and the other HIV negative. No case of I. belli was detected.
Multiparasitism.
Multiple parasitism was rare in our population. In the HIV-infected group, 47 (69.1%) patients were not infected by intestinal parasites; one parasite was identified in 15 (22%) patients, two parasites in four (5.9%) patients, and three parasites in two (2.9%) patients.
Risk factors associated with intestinal parasite infection and with HIV infection.
No association was found between the sex, the matrimonial status, the level of education, the HIV serostatus, and the presence of intestinal parasites. Furthermore, no statistical difference was found between HIV status and the parasites density and presence of multiples parasites as shown in Table 2. The only variables associated with prevalence of intestinal parasites were the quality of water (odds ratio [OR] = 2.58 [1.28–5.22]), the personal hygiene/hand washing (OR = 2.64 [1.37–5.15]), and the cleaning after defecation (OR = 2.60 [1.19–5.86]) as presented in Table 3. No association was found between the ART treatment and the density of the intestinal parasites (P = 0.51). On the other hand, HIV status was inversely associated with the educational level (P < 0.05); (see Table 4).
Table 3.
Association between personal hygiene and parasitic infection
| Presence of parasites | Absence of parasites | P value | |
|---|---|---|---|
| Hands washing | 0.00 | ||
| Always | 43 (56.58) | 124 (77.99) | |
| Sometimes | 33 (43.42) | 34 (21.38) | |
| Not at all | 0 (0.00) | 1 (0.63) | |
| Nail cleaning | 0.14 | ||
| Always | 33 (43.42) | 85 (53.46) | |
| Sometimes | 41 (53.95) | 65 (40.88) | |
| Not at all | 2 (2.63) | 9 (5.66) | |
| Cleaning after defecation | 0.00 | ||
| Washing with water | 39 (51.32) | 39 (24.53) | |
| Use of toilet paper | 22 (28.95) | 73 (45.91) | |
| Others methods | 15 (19.74) | 47 (29.56) | |
| Source of drinking water | 9.471e-05 | ||
| Borehole | 32 (42.11) | 29 (18.24) | |
| Tap | 44 (57.89) | 130 (81.76) | |
HIV = human immunodeficiency virus.
Table 4.
Association between educational level and HIV status
| HIV-infected patients | HIV-noninfected patients | P value | |
|---|---|---|---|
| Education level | |||
| Illiterate | 24 (35.29) | 26 (15.57) | |
| Primary school | 24 (35.29) | 33 (19.76) | 3.20158e-06 |
| Secondary school | 18 (26.47) | 68 (40.72) | |
| Postsecondary school | 2 (2.94) | 40 (23.95) | |
| Total | 68 | 167 | |
HIV = human immunodeficiency virus.
DISCUSSION
The primary goal of this study was to determine the frequency of HIV-intestinal parasites coinfection in the Adamaoua and to evaluate the risk factors associated with this coinfection.
The proportion of new HIV infections identified among the participants was 9.3%, which was higher than the 5.1% found during the demographic survey.11 This may be due to the fact that we recruited the participants in the hospital, whereas the demographic survey recruited the participants from the community. Up to 44.1% of the HIV-positive patients were not yet on treatment, and this is not in agreement with the new 2015 World Health Organization recommendations.14 The prevalence of intestinal infections in Adamaoua was the same for HIV-positive and HIV-negative patients. Parasites like Cryptosporium parvum known as opportunistic parasites were identified in the overall population, but not specific to PLHIV which reflected the overall poor hygiene conditions of the entire population. Even the parasite density was the same in the two groups. This finding was contradictory to what has been found in other studies, where the prevalence of parasitic diseases was higher in PLHIV.2,5–7
The 32.3% prevalence of parasitic infections found in the Adamaoua general population was greater than 14.6% in West Region of Cameroon,7 but less than 57.5% in the Center Region.15 Note that the techniques used for biological analyzes of the study conducted in the West Region were the same as those used in Ngaoundere. The only difference was that in the West, concentrated stools were not analyzed microscopically before the modified Ziehl–Neelsen staining. A prevalence of 12.3% was obtained in fresh wet mount microscopy, 23.5% after concentration, and 32.3% after concentration and staining. In the Center Region, in addition to KATO concentration technique, the same techniques of biological analysis as used in Adamawa were performed. Gold concentration formalin-ether takes into account the cysts and oocysts but not helminth eggs as the KATO technique.
Contrary to the results found by Nkenfou and others,7 no association (χ2 = 0.00) was found between parasitic infection and HIV status; 31.9% of parasitic infections in PLHIV compared with 32.5% in HIV-seronegative participants. However, a strong link was found between parasitic status and personal hygiene/hand washing (χ2 = 17.57; OR = 3.73 with 7.06; 1.97 at 95% confidence interval). Also, subjects with HIV have poor hygiene practice compared with HIV-negative subjects (19.1% of PLHIV against 49.1% of HIV-negative patients use toilet tissue after defecation; Table 1). Service providers at the treatment centers should educate PLHIV on hygienic living conditions. This is opposite to what was found in the West Region. Care providers should strive to educate PLHIV to adhere to ART treatment and to have a healthy lifestyle to minimize the risk of contracting opportunistic diseases.
Similarly, no association between intestinal parasitosis/parasite density and ART treatment was found: χ2 = 0.56, P = 0.51; 35.5% of patients ART naive had a parasite infection and 28.9% of subjects on ART had an intestinal infection. The same results were obtained by Inyang-Etoh and others in Calabar, Nigeria.10 Using the same biological techniques, namely direct microscopy, concentration formalin-ether and modified Ziehl–Neelsen coloring, they got 29% (116/400) of parasitic infections in HIV patients taking ART. But this result is opposite to those found by Nkenfou and others in the West Region of Cameroon, and Missaye and others in Ethiopia.16 This could be explained by the overall poor hygienic conditions of the study population.
Dwellers of Adamaoua Region harbored mostly protozoa among which the most frequent one was B. hominis (18.3%). Infections by helminths were rarely detected (0.4% for A. lumbricoides). The proposed explanation for this is that inhabitants of Adamaoua were mainly animal breeders who do not eat raw meat and have less contact with soil compared with farmers. Monoinfection by protozoa was the rule compared with other studies where polyparasitism was more frequent.17–21 The speculation for this observation may be linked to the main limitation of our study, the analysis of only one stool sample per patient with thus limited sensitivity for the detection of other parasites. The prevalence of monoinfection may also be due to constant competition in the microbiota, leading a particular organism to be dominant.
The clinical spectrum caused by intestinal parasites especially protozoa in HIV-positive patients ranged from asymptomatic infection to severe infection resulting in chronic diarrhea, dehydration, and malabsorption.22 These could reduce the effectiveness of oral ART in case of intestinal parasites due to drug malabsorption. As factors associated to intestinal parasitic infections, three variables were identified: hand hygiene, cleaning after defecation, and water quality.
After Giemsa coloration, no microsporidia was found. In 2010, Anane and others in Tunisia have obtained an overall prevalence of 2.4% (14/572) microscoporidies. In PLHIV, the prevalence was 3.6% (10/279) and 1.4% (4/293) in seronegative patients.23 The result obtained in our study could be explained by the fact that all participants had no evidence of disease worsening. Microsporidia are generally present in patients whose CD4 counts are low.24
A major limitation in our study was the fact that only one stool sample was analyzed per patient. This could affect the data as the sensitivity of the microscopy is limited in case of light infection. This can then underestimate the prevalence, the intensity of infection, as well as the degree of multiparasitism.
CONCLUSIONS
PLHIV have a depressed immune system and are susceptible to infections called opportunistic infections that can be bacterial, viral, fungal, or parasitic. In this work, we evaluated the prevalence of parasitic infections in people with or without HIV. The results showed that PLHIV and HIV-negative patients had similar prevalence rates for intestinal parasitic infections. The prevalence and parasite density were similar both in patients on ART and ART-naïve patients. As part of the fight against HIV, the inverse correlation between HIV status and level of education suggests the importance of developing a strategy for improving educational opportunities in the Adamaoua Region. As protective factors against intestinal parasitic infections, personal hygiene should be promoted and safe water made available to the populations.
Acknowledgments:
We thank the study participants for their collaboration.
REFERENCES
- 1.Konaté A, Minta D, Diarra M, Dolo A, Dembele M, Diarra B, Maiga MY, Traore HA, Doumbo O, 2005. Parasitoses digestives au cours de la diarrhée du sida. Bull Soc Pathol Exot 98: 33–35. [PubMed] [Google Scholar]
- 2.Wumba R, Enache-Angoulvant A, Develoux M, Mulumba A, Mulumba PM, Hennequin C, Odio TW, Biligui S, Sala J, Thellier M, 2007. Prévalence des infections opportunistes digestives parasitaires à Kinshasa (République Démogratique du Congo), Résultats d’une enquête préliminaire chez 50 patients au stade SIDA. Med Trop 67: 145–148. [PubMed] [Google Scholar]
- 3.Assefa S, Erko B, Medhin G, Assefa Z, Shimelis T, 2009. Intestinal parasitic infections in relation to HIV/AIDS status, diarrhea and CD4 T-cell count. BMC Infect Dis 9: 155–160. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 4.OMS, 1987. Interrelations entre les maladies tropicales et les infections à VIH: rapport d’une consultation informelle de l’OMS. Kenya Medical Research Institute (KEMRI): World Health Organization Press, 63 Available at: http://books.google.cm/books/about/Interrelations_Entre_Les_Maladies_Tropic.html. [Google Scholar]
- 5.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: 162–164. [PubMed] [Google Scholar]
- 6.Lehman LG, Kangam L, Nguepi E, Mbenoun ML, Bilong Bilong CF, 2013. Study of intestinal parasitic infections associated with HIV infection in Douala, Cameroon. Retrovirology 9 (Suppl 1): 48. [DOI] [PubMed] [Google Scholar]
- 7.Nkenfou CN, Nana CT, Payne VK, 2013. Intestinal parasitic infections in HIV infected and non-infected patients in a low HIV prevalence region, West-Cameroon. PLoS One 8: e57914. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 8.UNAIDS, 2013. Global Report 2013: UNAIDS. Available at: http://files.unaids.org/en/media/unaids/contentassets/documents/epidemiology/2013/gr2013/UNAIDS_Global_Report_2013_en.pdf.
- 9.Ilboudo D, Sanou J, Traoré LK, 1997. Parasitoses digestives et infection par le virus de l’immunodéficience humaine à Ouagadougou. Med Afr Noire 44: 69–72. [Google Scholar]
- 10.Inyang-Etoh PC, Udonkang MI, Adeboboye AO, 2015. Occurrence of intestinal parasites amongst persons on highly active antiretroviraldrugtherapy in Calabar, Cross River State, Nigeria. Vet Sci Dev 5: 5794. [Google Scholar]
- 11.National Institute of Statistics, 2012. Demographic and Health survey and Multiple Indicators Cluster Survey DHS-MICS Preliminary Report. February 2012. Calverton, MD: INS et ICF International.
- 12.Henriksen S, Pohlenz J, 1981. Staining of Cryptosporidia by a modified Ziehl-Neelsen technique. Acta Vet Scand 22: 594–596. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Galeazzi G, 1992. Microsporidies. Anale du contrôle de qualité Colombes, Hôpital Louis Mourier, 1–3. Available at: http://www.laboratoire-defrance.com. [Google Scholar]
- 14.WHO recommendations, 2015. Treat All People Living with HIV, Offer Antiretrovirals as Additional Prevention Choice for People at “Substantial” Risk. News release September 30, 2015, Geneva, Switzerland: Available at: http://www.who.int/mediacentre/news/releases/2015/hiv-treat-all-recommendation/en/. [Google Scholar]
- 15.Vouking ZM, Enoka P, Tamo CV, Tadenfok CN, 2014. Prevalence of intestinal parasites among HIV patients at the Yaoundé Central Hospital, Cameroon. Pan Afr Med J 18: 136. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Missaye A, Dagnew M, Alemu A, Alemu A, 2013. Prevalence of intestinal parasites and associated risk factors among HIV/AIDS patients with pre-ART and on-ART attending dessie hospital ART clinic, northeast Ethiopia. AIDS Res Ther 10: 7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Hotez PJ, Molyneux DH, Fenwick A, Kumaresan J, Ehrlich Sachs S, Sachs JD, Savioli L, 2007. Control of neglected tropical diseases. N Engl J Med 357: 1018–1027. [DOI] [PubMed] [Google Scholar]
- 18.Hotez PJ, Bundy DAP, Beegle K, Brooker S, Drake L, de Silva N, Montresor A, Engels D, Jukes M, Chitsulo L, Chow J, Laxminarayan R, Michaud C, Bethony J, Correa-Oliveira R, Shuhua X, Fenwick A, Savioli L, 2006. Chapter 24. Helminth infections: soil-transmitted helminth infections and schistosomiasis. Jamison DT, Breman JG, Measham AR, Alleyne G, Claeson M, Evans DB, Jha P, Mills A, Musgrove P, eds. Disease Control Priorities in Developing Countries, 2nd edition Washington, DC: World Bank, 467–482. [Google Scholar]
- 19.Savioli L, Smith H, Thompson A, 2006. Giardia and Cryptosporidium join the “neglected diseases initiative.” Trends Parasitol 22: 203–208. [DOI] [PubMed] [Google Scholar]
- 20.Utzinger J, Becker SL, Knopp S, Blum J, Neumayr AL, Keiser J, Hatz CF, 2012. Neglected tropical diseases: diagnosis, clinical management, treatment and control. Swiss Med Wkly 142: w13727. [DOI] [PubMed] [Google Scholar]
- 21.Becker SL, Lohourignon LK, Speich B, Rinaldi L, Knopp S, N’Goran EK, Cringoli G, Utzinger J, 2011. Comparison of the Flotac-400 dual technique and the formalin-ether concentration technique for diagnosis of human intestinal protozoon infection. J Clin Microbiol 49: 2183–2190. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Babatunde SK, Salami AK, Fabiyi JP, Agbede OO, Desalu OO, 2010. Prevalence of intestinal parasitic infestation in HIV seropositive and seronegative patients in Ilorin. Nigeria Ann Afr Med 9: 123–128. [DOI] [PubMed] [Google Scholar]
- 23.Anane S, Attouchi H, Kaouech E, Belhadj S, Ben Chaabane T, Ben Abdallah N, Ben Othman T, Samoud A, Ben Hriz M, Kallel K, Chaker E, 2010. Caractéristiques épidémiologiques et cliniques de la microsporidiose intestinale chez les immunodéprimés vus à Tunis. Cahier Santé 20: 21–29. [DOI] [PubMed] [Google Scholar]
- 24.Asmuth DM, DeGirolami PC, Federman M, Ezratty CR, Pleskow DK, Desai G, Wanke CA, 1994. Clinical features of microsporidiosis in patients with AIDS. Clin Infect Dis 18: 819–825. [DOI] [PubMed] [Google Scholar]