Non-Opportunistic Intestinal Parasitic Infections in People Living with HIV Undergoing Antiretroviral Therapy in Brazzaville, Republic of Congo

Introduction: HIV infection remains a major public health problem. It is associated with co-infections, including intestinal parasitic infections. The aim of this study was to investigate intestinal parasitic infections in people living with HIV undergoing antiretroviral therapy. Materials and methods: This was a descriptive cross-sectional study conducted from October 2024 to June 2025 in outpatient treatment centers in Brazzaville. It involved PLHIV undergoing antiretroviral therapy, with or without diarrhea, who had given their informed consent. The stool samples collected were subjected to parasitological examination using a concentration technique in the Parasitology Laboratory of the Faculty of Health Sciences. Results: The total number of PLHIV included was 261. The median age was 49.0 years (42, 72). The prevalence of intestinal parasitic infections was 19.5% (51/261). They mainly affected women (20.2%, 41/203), with no significant difference (p = 0.617). PLHIV were exclusively carriers of monoparasitism. The intestinal parasites identified were E. histolytica/dispar (14.90%), E. coli (2.7%), 1 case of G. intestinalis, 1 case of T. intestinalis, 1 case of S. stercoralis, 1 case of A. lumbricoides, and 1 case of hookworm. Conclusion: Intestinal parasitic infections in PLHIV are dominated by protozoan infections, with the presence of strongyloids and hookworms.

• PLHIV
• Intestinal Parasitic Infections
• Protozoan Infections
• Monoparasitism
• Brazzaville

1. Introduction

HIV infection remains a major public health problem worldwide. It has caused more than 44.1 million deaths, with 630,000 deaths in 2024. Although diagnostic methods are becoming increasingly sophisticated and treatments increasingly effective, HIV infection continues to affect a large number of people. This infection has become a chronic condition that can be associated with longevity in affected patients [1] .

However, whether or not the patient is undergoing treatment, and whether or not they have a satisfactory CD4 count, other diseases may be associated with the infection. This is the case with intestinal parasitic infections. These can cause diarrhea, which can be severe in debilitated individuals, particularly those living with HIV (PLHIV). As HIV is an infection that causes cellular immune depletion, the ability of PLHIV to fight intestinal parasitic infections is reduced [2] . These intestinal parasitic infections can be caused by opportunistic and non-opportunistic parasites [3] .

In the case of non-opportunistic intestinal parasitic infections, protozoa and helminths have been identified as etiological agents in PLHIV. However, clinical manifestations vary from asymptomatic cases to severe intestinal damage [4] [5] .

This co-infection of HIV and intestinal parasitic infections has been studied in several countries. This is the case in India, where the prevalence of intestinal parasitic infections in PLHIV varied from one region to another. For example, it was 14.86% with hookworms as the predominant parasite according to Namaji MAAS et al. [6] , and 8.7% for Seema K et al. with A. lumbricoides as the dominant parasite [7] . In Africa, the prevalence of this co-infection also varied from one region to another, and even within the same region. In Ethiopia, Gedle D et al. found a prevalence of intestinal parasitic infections of 31.8%, with Taenia spp as the dominant species [8] .

In the Central African subregion, in Cameroon and the Democratic Republic of Congo, the prevalence rates were 59.52% and 24.6% respectively [9] [10] . However, in Brazzaville, the Republic of Congo, although HIV is a real public health problem, information on this co-infection is very scarce. We did not find any studies on intestinal parasitic infections or diarrhoea in HIV-immunocompromised individuals that provided information on intestinal parasites. However, a clinical case of strongyloidiasis in an immunocompromised patient was reported by Atipo-Ibara BI et al. [11] . This is why we wanted to carry out this study with the aim of investigating intestinal parasitic infections in PLHIV monitored in outpatient treatment centers in Brazzaville.

2. Patients and Method

This was a descriptive cross-sectional study conducted from October 1, 2024, to June 30, 2025, in outpatient treatment centers for people living with HIV/AIDS (PLWHA) in Brazzaville, notably the Brazzaville University Hospital Center (CHUB) and the Talangaï referral hospital (HRT). It involved all PLHIV patients being monitored, with or without diarrhea, who had not taken antihelminthic treatment in the four weeks prior to the study. Patients were systematically sampled when they arrived at the outpatient treatment center. Patients were informed about the study and were only included in the study if they gave their consent. Patients who had not yet started treatment and who were visiting the center for the first time were not included. The samples were analyzed at the Parasitology Laboratory of the Faculty of Health Sciences at Marien Ngouabi University in Brazzaville. For each patient, socio-demographic information and the results of the analysis of a stool sample collected in a transparent stool container were recorded on a form. Each sample underwent macroscopic examination to assess its consistency and check for the presence of mucus or blood; direct examination of the stool diluted in a physiological saline solution; and examination after performing the modified Ritchie concentration technique using a formalin-ether mixture. The examination under an optical microscope was performed by two microscopists looking for cysts, eggs, and vegetative forms of intestinal parasites.

The data were entered using Microsoft Excel 2010 software and analyzed using IBM SPSS 2025 software. The results were presented as means, medians, frequencies, and proportions.

The study was authorized by the management of the CHUB and HRT hospital HIV care centers.

3. Results

The total number of patients who participated in the study was 261.

Sociodemographic characteristics of PLHIV

Women (203/261) were more represented than men (58/261), with a sex ratio (M/F) of 0.29.

The median age of PLHIV was 49.00 years (42, 72). The extreme ages were 16 and 72 years.

Figure 1 shows the distribution of PLHIV by age group. It shows that the majority of PLHIV belonged to the [46 - 55 years] age group (34.9%), followed by those aged [36 - 46 years] (24.1%) and [56 - 65 years] (20.7%). PLHIV aged [16 - 25] represented the last category of patients with intestinal parasitic infections.

Frequency of non-opportunistic intestinal parasitic infections among PLHIV

Analysis of stool samples from PLHIV revealed a frequency of intestinal parasitic and fungal infections of 42.9% (112/261). Intestinal parasitic infections alone accounted for 19.5% (51/261).

The frequency of non-opportunistic intestinal parasitic infections by age group is shown in Table 1 . They were found more frequently in the [36 - 45 years] and [46 - 55 years] age groups, with a non-significant difference (p = 0.647).

Figure 1

Figure 1. Distribution of people living with HIV by age groups.

Table 1

Table 1. Distribution of intestinal parasitic infections according to age groups of people living with HIV.

		Non-opportunistic Intestinal parasitosis
		Negative	Positive
Age groups	[16 - 25 years]	7 (3.3%)	3 (5.9%)	10 (3.8%)
	[26 - 35 years]	25 (11.9%)	4 (7.8%)	29 (11.1%)
	[36 - 45 years]	51 (24.3%)	12 (23.5%)	63 (24.1%)
	[46 - 55 years]	73 (34.8%)	18 (35.3%)	91 (34.9%)
	[56 - 65 years]	45 (21.4%)	9 (17.6%)	54 (20.7%)
	[66 - 75 years]	9 (4.3%)	5 (9.8%)	14 (5.4%)
		210 (80.1)	51 (19.9%)	261 (100%)

PLHIV were carriers of monoparasitism in 35.2% of cases (92/261). Polyparasitism was observed in 7.7% of cases (20/261).

The different parasites that were found are shown in Figure 2 . It should be noted that Candida (30.7%; 80/261) was mainly isolated in the stools of PLHIV. Intestinal parasites themselves were mainly represented by protozoa, particularly amoeba cysts (17.6%; 46/261), dominated by E. histolytica/dispar cysts (14.90%) and E. coli (2.7%; 7/261), one case of Giardia intestinalis cysts (0.4%), and one case of Trichomonas intestinalis (0.4%). Helminths were found in equal proportions: 1 case of Strongyloides stercoralis (0.4%), 1 case of hookworm (0.4%) and 1 case of Ascaris lumbricoides (0.4%).

For intestinal parasitic infections, there was no link between the presence of parasites and age groups.

Women living with HIV (20.2%, 41/203) were more affected by intestinal parasitic infections than men (17.2%, 10/58), but without a statistically significant difference (p = 0.617). Monoparasitism was also more common in women (80.3%, 41/51) than in men (16.6%, 10/51), but the difference was not significant (p = 0.674).

Figure 2

Figure 2. Intestinal parasites detected in PLHIV undergoing treatment and monitored in Brazzaville.

4. Discussion

This study only looked at non-opportunistic intestinal parasitic infections in PLHIV. The viral loads of PLHIV were not investigated. This could be a significant drawback, as it would have been interesting to check the viral load of each patient in order to establish a possible link between intestinal parasitic infections and viral load. However, in a context where intestinal parasitic infections represent a public health problem in developing countries such as Congo [12] , understanding the role of these infections in PLHIV is of paramount importance, especially given that some of these diseases can cause serious symptoms in this population group.

The prevalence of intestinal parasitic infections in this study was 19.4%. This prevalence is similar to that reported by Nkenfou NC et al. in Dschang, Cameroon [9] [13] .

However, it is lower than that found by Vouking MZ in Yaoundé, Lar PM in Vom, and Aliyo A in Guji [14] - [16] .

Nevertheless, the frequency of non-opportunistic intestinal parasitic infections in our study was higher than that found by Taheu CN et al. in a peri-urban area of Yaoundé [17] , by Akinbo FO et al. in Benin City [18] , and by Namaji MAAS et al. in northeast India [6] .

This analysis shows that the frequency of intestinal parasitic infections among PLHIV varies from one country to another and from one environment to another within the same country. This can be explained by the fact that the frequency of intestinal parasitic infections may depend on the quality of life of patients, the quality of care provided to PLHIV, and the environment in which PLHIV live.

In this study, the type of parasitism identified was exclusively monoparasitism. Several studies on intestinal parasitic infections in PLHIV have shown that they were carriers of monoparasitism, as we observed [19] [20] . However, some authors report not only the existence of multiparasitism but also its predominance [3] .

With regard to the parasites identified, we also note a diversity of parasites. Helminths were not the most commonly observed parasites among PLHIV in Brazzaville. The species identified were A. lumbricoides, S. stercoralis, and Ankylostoma duodenale. In Bobo-Dioulasso, Sangaré I et al. also found a predominance of protozoa over helminths [21] [22] . Similarly, Ajayi OT et al. in Jos found a predominance of protozoa, with E. histolytica as the most commonly observed intestinal parasite [23] . In Laos, however, helminths were the most commonly observed parasites, followed by protozoa. These were S. stercoralis (dominant species) followed by hookworms in Laos [24] [25] . In Cape Town, helminths were the most common intestinal parasites, with A. lumbricoides being the most dominant [26] . Intestinal parasite ecology is often dependent on species dynamics in a given environment. Thus, PLHIV living in an environment where protozoan infections are dominant due to policies to combat geohelminthiasis through the mass administration of antihelminthics in accordance with World Health Organization strategies are more likely to be affected by protozoan infections [27] . This is the case in our country, where mass screening campaigns against geohelminthiasis have certainly helped to reduce the frequency of these parasites, leaving protozoa, most of which are not eliminated by the molecules used in deworming campaigns, to become more prevalent in the environment. On the other hand, it is important to note the modernisation of the city with the construction of modern latrines, which reduce contact between potential vectors of geohelminthiasis, contaminated soil and humans, thereby reducing the spread of geohelminths. A significant part of this reduction is also attributable to PLHIV’s compliance with hygiene rules.

Women were more likely to be carriers of intestinal parasitic infections than men, but without significant difference. The diversity of results in the literature regarding the most affected gender shows that this pathology is not related to gender, although some studies have found a link between the presence of intestinal parasites and gender [7] [28] .

5. Conclusion

Intestinal parasitic infections are a real problem among PLHIV. They are dominated by protozoa capable of causing serious damage in this population. Although helminth infections are relatively rare, emphasis must be placed on all these conditions in order to ensure comprehensive and integrated care for PLHIV.

References

1. World Health Organization (2024) Global HIV/AIDS Report.

2. Sow, D., Kandé, S., Diouf, J.B.N., Manga, I.A., Lelo, S., Fall, C.B.F., Sylla, K., Ndiaye, M., Tine, R.C., Ndiaye, J.L. and Faye, B. (2023) Prevalence of Soil-Transmitted Helminthiasis in a Cohort of Infected Children in Guediawaye Hospital, Suburb of Dakar, Senegal. African Journal of Parasitology Research, 11, 1-7

3. Eshetu, T., Sibhatu, G., Megiso, M., Abere, A., Baynes, H.W., Biadgo, B., et al. (2017) Intestinal Parasitosis and Their Associated Factors among People Living with HIV at University of Gondar Hospital, Northwest-Ethiopia. Ethiopian Journal of Health Sciences, 27, 411-420. >https://doi.org/10.4314/ejhs.v27i4.12

4. Salami, A., Babatunde, S., Fabiyi, J., Agbede, O. and Desalu, O. (2010) Prevalence of Intestinal Parasitic Infestation in HIV Seropositive and Seronegative Patients in Ilorin, Nigeria. Annals of African Medicine, 9, 123-128. >https://doi.org/10.4103/1596-3519.68356

5. Goon, D., Abaver, D., Nwobegahay, J., Iweriebor, B. and Anye, D. (2011) Prevalence of Intestinal Parasitic Infections among HIV/AIDS Patients from Two Health Institutions in Abuja, Nigeria. African Health Sciences, 11, S24-S27. >https://doi.org/10.4314/ahs.v11i3.70066

6. Namaji, M.A.A.S., Pathan, S.H. and Balki, A.M. (2020) Profile of Intestinal Parasitic Infections in Human Immunodeficiency Virus/Acquired Immunodeficiency Syndrome Patients in Northeast India. Indian Journal of Sexually Transmitted Diseases and AIDS, 41, 93-96. >https://doi.org/10.4103/ijstd.IJSTD_115_17

7. Seema, K., Kumar, A., Boipai, M., Kumar, M. and Sharma, A.K. (2023) Prevalence of Intestinal Parasites in HIV/Aids-Infected Patients with Correlation to CD4+ T-Cell Count at Hospital in Eastern India. Journal of Family Medicine and Primary Care, 12, 2884-2887. >https://doi.org/10.4103/jfmpc.jfmpc_806_23

8. Gedle, D., Kumera, G., Eshete, T., Ketema, K., Adugna, H. and Feyera, F. (2017) Intestinal Parasitic Infections and Its Association with Undernutrition and CD4 T Cell Levels among HIV/AIDS Patients on HAART in Butajira, Ethiopia. Journal of Health, Population and Nutrition, 36, 15-26. >https://doi.org/10.1186/s41043-017-0092-2

9. Nkenfou, C.N., Nana, C.T. and Payne, V.K. (2013) Intestinal Parasitic Infections in HIV Infected and Non-Infected Patients in a Low HIV Prevalence Region, West-cameroon. PLOS ONE, 8, e57914. >https://doi.org/10.1371/journal.pone.0057914

10. Wumba, R., Longo-Mbenza, B., Mandina, M., Odio Wobin, T., Biligui, S., Sala, J., et al. (2010) Intestinal Parasites Infections in Hospitalized AIDS Patients in Kinshasa, Democratic Republic of Congo. Parasite, 17, 321-328. >https://doi.org/10.1051/parasite/2010174321

11. Atipo-Ibara, B.I., Ahoui-Apendi, C.P., Gassaye, D., Bossali, F., Ossibi-Ibara, B.R., Ngami, R.S., et al. (2015) Anguillulose digestive révélée par un abdomen aigu. Journal Africain d’Hépato-Gastroentérologie, 9, 136-137. >https://doi.org/10.1007/s12157-015-0602-z

12. Expert Committee on Prevention WHO Control of Intestinal Parasitic Infections, (World Health Organization) (1987) Control of Intestinal Parasitic Infections: Report of a WHO Expert Committee. >http://www.who.int/iris/handle/10665/36941

13. Bissong, M., Nguemain, N., Ng’awono, T. and Kamga, F. (2015) Burden of Intestinal Parasites Amongst HIV/AIDS Patients Attending Bamenda Regional Hospital in Cameroon. African Journal of Clinical and Experimental Microbiology, 16, 97-103. >https://doi.org/10.4314/ajcem.v16i3.3

14. Vouking, M.Z., Enoka, P., Tamo, C.V. and Tadenfok, C.N. (2014) Prevalence of Intestinal Parasites among HIV Patients at the Yaoundé Central Hospital, Cameroon. Pan African Medical Journal, 18, Article 136. >https://doi.org/10.11604/pamj.2014.18.136.3052

15. Lar, P., Pam, V., Ayegba, J. and Zumbes, H. (2016) Prevalence and Distribution of Intestinal Parasite Infections in HIV Seropositive Individuals on Antiretroviral Therapy in Vom, Plateau State Nigeria. African Journal of Clinical and Experimental Microbiology, 17, 18-24. >https://doi.org/10.4314/ajcem.v17i1.3

16. Aliyo, A. and Gemechu, T. (2022) Assessment of Intestinal Parasites and Associated Factors among HIV/AIDS Patients on Antiretroviral Therapy at Bule Hora General Hospital, West Guji, Ethiopia. SAGE Open Medicine, 10, 1-7. >https://doi.org/10.1177/20503121221124685

17. Taheu, C.N., Meliedje, C.D.T., Bong, G.G.B., Ngo Likeng, J.L., Ghomsi, F.M., Nkoth, A.F., et al. (2021) Intestinal Parasites Infestation among People Living with HIV under Antiretroviral Therapy in Peri-Urban Area of Yaoundé, Cameroon. European Journal of Medical and Health Sciences, 3, 59-64. >https://doi.org/10.24018/ejmed.2021.3.4.929

18. Akinbo, F.O., Okaka, C. and Omoregie, R. (2010) Prevalence of Intestinal Parasitic Infections among HIV Patients in Benin City, Nigeria. Libyan Journal of Medicine, 5, Article 5506. >https://doi.org/10.3402/ljm.v5i0.5506

19. Aviles, J., Yombi, J.C., Erostegui, C., Torrico, M., Yanez, R., Rojas, M., Illanes, D. and Robert, A. (2020) Intestinal Parasitic Infections in Adult Living with HIV in Cochabamba, Bolivia. Infectious Diseases Diagnosis&Treatment, 4, Article 136.

20. Santos, V., Maia, F., Silva, L., Morais, A., Silva, J. and Wanderley, F. (2024) Parasitoses intestinais em pacientes com AIDS e/ou HTLV: Resultados de um hospital de referência em doenças infecciosas. Revista de Epidemiologia e Controle de Infecção, 14, 318-324. >https://doi.org/10.17058/reci.v14i2.18715

21. Sangaré, I., Bamba, S., Cissé, M., Zida, A., Bamogo, R., Sirima, C., et al. (2015) Prevalence of Intestinal Opportunistic Parasites Infections in the University Hospital of Bobo-Dioulasso, Burkina Faso. Infectious Diseases of Poverty, 4, 32-37. >https://doi.org/10.1186/s40249-015-0065-x

22. Nsagha, D.S., Njunda, A.L., Assob, N.J.C., Ayima, C.W., Tanue, E.A., Kibu, O.D., et al. (2016) Intestinal Parasitic Infections in Relation to CD4+ T Cell Counts and Diarrhea in HIV/AIDS Patients with or without Antiretroviral Therapy in Cameroon. BMC Infectious Diseases, 16, Article No. 9. >https://doi.org/10.1186/s12879-016-1337-1

23. Ajayi, O.T., Makanjuola, O.B., Olayinka, A.T., Olorukooba, A., Olofu, J.E., Nguku, P. and Fawole, O.I. (2021) Predictors of Intestinal Parasite Infection among HIV Patients on Antiretroviral Therapy in Jos, Plateau State, Nigeria, 2016: A Cross-Sectional Survey. Pan African Medical Journal, 38, Article 306.

24. Paboriboune, P., Phoumindr, N., Borel, E., Sourinphoumy, K., Phaxayaseng, S., Luangkhot, E., et al. (2014) Intestinal Parasitic Infections in HIV-Infected Patients, Lao People’s Democratic Republic. PLOS ONE, 9, e91452. >https://doi.org/10.1371/journal.pone.0091452

25. Roka, M., Goñi, P., Rubio, E. and Clavel, A. (2012) Prevalence of Intestinal Parasites in HIV-Positive Patients on the Island of Bioko, Equatorial Guinea: Its Relation to Sanitary Conditions and Socioeconomic Factors. Science of The Total Environment, 432, 404-411. >https://doi.org/10.1016/j.scitotenv.2012.06.023

26. Ifeoma, A., Apalata, T., Aviwe, B., Oladimeji, O. and Abaver, D.T. (2022) Prevalence of Intestinal Parasites in HIV/Aids-Infected Patients Attending Clinics in Selected Areas of the Eastern Cape. Microbiology Research, 13, 574-583. >https://doi.org/10.3390/microbiolres13030040

27. World Health Organization (2022) Geohelminthiasis. >https://www.who.int/fr/news-room/fact-sheets/detail/soil-transmitted-helminth-infections

28. Zeynudin, A., Hemalatha, K. and Kannan, S. (2013) Prevalence of Opportunistic Intestinal Parasitic Infection among HIV Infected Patients Who Are Taking Antiretroviral Treatment at Jimma Health Center, Jimma, Ethiopia. European Review for Medical and Pharmacological Sciences, 17, 513-516.