Prevalence of intestinal parasites in a cohort of HIVinfected patients from Antioquia, Colombia

Jorge Botero-Garcés, Esteban Villegas-Arbeláez, Sofía Giraldo, Johanna Urán-Velásquez, Laura Arias-Agudelo, Juan Carlos Alzate-Ángell, Gisela María García-Montoya, Ana Luz Galván-Díaz, .

Keywords: Intestinal diseases, parasitic, HIV, AIDS-related opportunistic infections, diarrhea, prevalence, Colombia

Abstract

Introduction: HIV infection is still a public health problem worldwide and co-infections with other infectious agents including intestinal parasites are of particular concern, mainly in developing countries like Colombia.
Objective: To conduct a cross-sectional study in patients attending an HIV care program in Antioquia given that there have been few intestinal parasites prevalence studies among the HIV population in the country.
Material and methods: We evaluated stool samples from 192 patients by direct wet mount and concentration, modified Ziehl Neelsen staining, and agar plate culture. Univariate and correlation analyses were done to explore the association between socio-demographic and clinical characteristics and parasitological data.
Results: The overall prevalence of intestinal parasites in HIV-positive subjects was 29.2% (56/192; 95% CI: 22.8% - 35.6%). Entamoeba histolytica/dispar/moshkosvkii with 13.0% (25/192; 95% CI: 8.2% - 17.8%) and Blastocystis with 12.0% (23/192; 95% CI: 7.4% - 16.6%) were the most frequent. Opportunistic parasites like Cryptosporidium spp. and Cystoisospora belli were less prevalent, each one with 0.5% of positive samples (1/192; 95% CI: 0.1% - 1.5%). Commensal protozoa were also detected with a prevalence of 18.8% (36/192; 95% CI: 13.3% - 24.3%). Most of the individuals in the study had a controlled viral load and an LTCD4 count greater than 200 cel/μL. A small percentage (9.3%) had diarrhea. Bivariate analysis and multivariate logistic regression showed that only age and having pets had a significant association with intestinal parasites in this cohort.
Conclusions: Our results confirmed that the evaluated population is at high risk of intestinal parasite infection, which highlights the need for routine screening of gastrointestinal parasites to provide prompt treatment and reduce possible complications.

Downloads

Download data is not yet available.
  • Jorge Botero-Garcés Unidad de Investigación Clínica, Corporación para Investigaciones Biológicas, Medellín, Colombia; Grupo de Parasitología, Facultad de Medicina, Corporación Académica para el Estudio de las Patologías Tropicales, Universidad de Antioquia, Medellín, Colombia https://orcid.org/0000-0002-3478-0194
  • Esteban Villegas-Arbeláez Unidad de Investigación Clínica, Corporación para Investigaciones Biológicas, Medellín, Colombia https://orcid.org/0000-0001-7025-5760
  • Sofía Giraldo Unidad de Investigación Clínica, Corporación para Investigaciones Biológicas, Medellín, Colombia https://orcid.org/0000-0001-7384-9599
  • Johanna Urán-Velásquez Grupo de Parasitología, Facultad de Medicina, Corporación Académica para el Estudio de las Patologías Tropicales, Universidad de Antioquia, Medellín, Colombia; Centro Nacional de Secuenciación Genómica, Sede de Investigación Universitaria, Universidad de Antioquia, Medellín, Colombia https://orcid.org/0000-0003-0187-4917
  • Laura Arias-Agudelo Centro Nacional de Secuenciación Genómica, Sede de Investigación Universitaria, Universidad de Antioquia, Medellín, Colombia https://orcid.org/0000-0001-8869-3515
  • Juan Carlos Alzate-Ángell Unidad de Investigación Clínica, Corporación para Investigaciones Biológicas, Medellín, Colombia; Unidad de Micología Médica y Experimental, Corporación para Investigaciones Biológicas-Universidad de Santander, Medellín, Colombia https://orcid.org/0000-0003-0319-0623
  • Gisela María García-Montoya Grupo Pediaciencias, Facultad de Medicina, Universidad de Antioquia, Medellín, Colombia https://orcid.org/0000-0002-2193-1360
  • Ana Luz Galván-Díaz Grupo de Microbiología Ambiental, Escuela de Microbiología, Universidad de Antioquia, Medellín, Colombia https://orcid.org/0000-0002-2127-4209

References

Nwosu FC, Avershina E, Wilson R, Rudi K. Gut microbiota in HIV infection: Implication for disease progression and management. Gastroenterol Res Pract. 2014;2014:1-6. https://doi.org/10.1155/2014/803185

Tian L-G, Wang T-P, Lv S, Wang F-F, Guo J, Yin X-M, et al. HIV and intestinal parasite co-infections among a Chinese population: An immunological profile. Infect Dis Poverty. 2013;2:18. https://doi.org/10.1186/2049-9957-2-18

Botero JH, Castaño A, Montoya MN, Ocampo NE, Hurtado MI, Lopera MM. A preliminary study of the prevalence of intestinal parasites in immunocompromised patients with and without gastrointestinal manifestations. Rev Inst Med Trop Sao Paulo. 2003;4:197-200. https://doi.org/10.1590/S0036-46652003000400004

Valbuena AM, Ramírez PX, Castillo JC, Trujillo SJ. Situación del VIH Sida en Colombia 2019. Fondo Colombiano de Enfermedades de Alto Costo. Cuenta Alto Costo. Consulted: Oct 30 2020. Available from: https://cuentadealtocosto.org/site/wp-content/uploads/2020/08/VIH2019.pdf.

Ministerio de Salud y Protección Social, Universidad de Antioquia. Encuesta Nacional de Parasitismo Intestinal en Población Escolar, Colombia, 2012-2014. 2015. p. 1-174. Accessed on: October 30, 2020. Available from: https://www.minsalud.gov.co/sites/rid/Lists/BibliotecaDigital/RIDE/VS/PP/ET/encuesta-nacional-de-parasitismo-2012-2014.pdf

Agudelo-González S, Murcia-Sánchez F, Salinas D, Osorio J. Infecciones oportunistas en pacientes con VIH en el hospital universitario de Neiva, Colombia. 2007-2012. Infectio. 2015;19:52-9. https://doi.org/10.1016/j.infect.2014.11.008

Navarro-i-Martínez L, Da Silva AJ, Botero-Garcés JH, Montoya-Palacio MN, Del Águila C, Bornay-LLinares FJ. Cryptosporidiosis in HIV-positive patients from Medellín, Colombia. J Eukaryot Microbiol. 2006;53(Suppl.1):S37-9. https://doi.org/10.1111/j.1550-7408.2006.00167.x

García LS, Arrowood M, Kokoskin E, Paltridge GP, Pillai DR, Procop GW, et al. Practical Guidance for Clinical Microbiology Laboratories: Laboratory diagnosis of parasites from the gastrointestinal tract. Clin Microbiol Rev. 2018;31. https://doi.org/10.1128/CMR.00025-17

Flórez AC, García DA, Moncada L, Beltrán M. Prevalence of microsporidia and other intestinal parasites in patients with HIV infection, Bogotá, 2001. Biomédica. 2003;23:274-82. https://doi.org/10.7705/biomedica.v23i3.1221

Botero JH, Montoya MN, Vanegas AL, Díaz A, Navarro-i-Martínez L, Izquierdo F, et al. Frecuencia de microsporidiosis intestinal en pacientes positivos para VIH mediante las técnicas de Gram cromotropo rápido y PCR. Biomédica. 2004;24:375. https://doi.org/10.7705/biomedica.v24i4.1287

Costa-Cruz JM, Ferreira MS, Rossin IR. Intestinal parasites in AIDS and +HIV patients in Uberlândia, Minas Gerais, Brazil. Mem Inst Oswaldo Cruz. 1996;91:685-6. https://doi.org/10.1590/S0074-02761996000600004

Barcelos NB, Silva L de F e, Dias RFG, Menezes Filho HR de, Rodrigues RM. Opportunistic and non-opportunistic intestinal parasites in HIV/ AIDS patients in relation to their clinical and epidemiological status in a specialized medical service in Goiás, Brazil. Rev Inst Med Trop Sao Paulo. 2018;60:1-9. https://doi.org/10.1590/s1678-9946201860013

Rivero-Rodríguez Z, Hernández A, Bracho Á, Salazar S, Villalobos R. Prevalencia de microsporidios intestinales y otros enteroparásitos en pacientes VIH positivos de Maracaibo, Venezuela. Biomédica. 2013;33:538-45. https://doi.org/10.7705/biomedica.v33i4.1468

Silva-Díaz H, Failoc-Rojas VE. Frequency and etiology of enteroparasitosis in patients with human immunodeficiency virus at a hospital of Lambayeque, Perú. Rev Habanera Ciencias Médicas. 2019;18:418-27.

Shirley D-AT, Farr L, Watanabe K, Moonah S. A Review of the global burden, new diagnostics, and current therapeutics for amebiasis. Open Forum Infect Dis. 2018;5:ofy161. https://doi.org/10.1093/ofid/ofy161

Moran P, Ramos F, Ramiro M, Curiel O, González E, Valadez A, et al. Entamoeba histolytica and/or Entamoeba dispar: Infection frequency in HIV+/AIDS patients in México city. Exp Parasitol. 2005;110:331-4. https://doi.org/10.1016/j.exppara.2005.03.023

Samie A, Barrett LJ, Bessong PO, Ramalivhana JN, Mavhandu LG, Njayou M, et al. Seroprevalence of Entamoeba histolytica in the context of HIV and AIDS: The case of Vhembe district, in South Africa’s Limpopo province. Ann Trop Med Parasitol. 2010;104:55-63. https://doi.org/10.1179/136485910X12607012373911

Cheng X, Tachibana H, Chen Y, Zhang Y, Yang B, Qi T, et al. Seroprevalence of Entamoeba histolytica infection in HIV-infected patients in China. Am J Trop Med Hyg. 2007;77:825-8. https://doi.org/10.4269/ajtmh.2012.11-0626

Abdollahi A, Saffar HH, Saffar HH, Sheikhbahaei S, Rasoulinejad M. Is the evaluation of Entamoeba histolytica infection in HIV-positive patients of any clinical significance? Acta Med Iran. 2015;53:46-50.

Skotarczak B. Genetic diversity and pathogenicity of Blastocystis. Ann Agric Environ Med. 2018;25:411-6. https://doi.org/10.26444/aaem/81315

Kumarasamy V, Anbazhagan D, Subramaniyan V, Vellasamy S. Blastocystis sp., Parasite associated with gastrointestinal disorders: An overview of its pathogenesis, immune modulation, and therapeutic strategies. Curr Pharm Des. 2018;24:3172-5. https://doi.org/10.2174/1381612824666180807101536

Fontanelli-Sulekova L, Gabrielli S, Furzi F, Milardi GL, Biliotti E, De Angelis M, et al. Molecular characterization of Blastocystis subtypes in HIV-positive patients and evaluation of risk factors for colonization. BMC Infect Dis. 2019;19:876. https://doi.org/10.1186/s12879-019-4537-7

Laksemi DA, Suwanti LT, Mufasirin M, Suastika K, Sudarmaja M. Opportunistic parasitic infections in patients with human immunodeficiency virus/acquired immunodeficiency syndrome: A review. Vet World. 2020;13:716-25. https://doi.org/10.14202/vetworld.2020.716-725

Wang Z-D, Liu Q, Liu H-H, Li S, Zhang L, Zhao Y-K, et al. Prevalence of Cryptosporidium, microsporidia and Isospora infection in HIV-infected people: A global systematic review and meta-analysis. Parasit Vectors. 2018;11:28. https://doi.org/10.1186/s13071-017-2558-x

Arzuza O, Arroyo B, Villegas S, Rocha A, Díaz H. Infecciones parasitarias intestinales en pacientes positivos para el virus de la inmunodeficiencia humana (VIH) en la ciudad de Cartagena de Indias, Colombia. Infectio. 2003;7:58-63.

Siuffi M, Angulo M, Velasco CA, López P, Dueñas VH, Rojas C. Relación entre los niveles de carga viral y los niveles de linfocitos CD4 en el diagnóstico de Cryptosporidium spp. en heces de niños de la Clínica pediátrica de VIH/SIDA del Hospital Universitario del Valle, Cali, Colombia. Colomb Med. 2006;37:15-20. https://doi.org/10.25100/cm.v37i1.407

Velasco CA, Méndez F, López P. Cryptosporidiosis in Colombian children with HIV/AIDS infection. Colomb Med. 2011;42:1-13. https://doi.org/10.25100/cm.v42i4.942

Montúfar Andrade F, Quiroga A, Builes C, Saldarriaga C, Aguilar C, Mesa M, et al. Epidemiología de la infección por el virus de inmunodeficiencia humana en pacientes hospitalizados en una institución de alta complejidad y enseñanza universitaria en Medellín, Colombia. Infectio. 2016;20:9-16. https://doi.org/10.1016/j.infect.2015.05.004

López MC, Moneada LI, Murcia MI, Saravia J, Nicholls RS. Frecuencia de parásitos intestinales en pacientes VIH+ en la ciudad de Santa Fe de Bogotá. Rev Fac Med. 1999;47:9-12.

Schär F, Trostdorf U, Giardina F, Khieu V, Muth S, Marti H, et al. Strongyloides stercoralis: Global distribution and risk factors. PLoS Negl Trop Dis. 2013;7:e2288. https://doi.org/10.1371/journal.pntd.0002288

Feitosa G, Bandeira AC, Sampaio DP, Badaró R, Brites C. High prevalence of giardiasis and strongyloidiasis among HIV-infected patients in Bahia, Brazil. Brazilian J Infect Dis. 2001;5:339-44. https://doi.org/10.1590/S1413-86702001000600008

Pinlaor S, Mootsikapun P, Pinlaor P, Pipitgool V, Tuangnadee R. Detection of opportunistic and non-opportunistic intestinal parasites and liver flukes in HIV-positive and HIV-negative subjects. Southeast Asian J Trop Med Public Health. 2005;36:841-5.

Aru RG, Chilcutt BM, Butt S, DeShazo RD. Novel findings in HIV, immune reconstitution disease and Strongyloides stercoralis infection. Am J Med Sci. 2017;353:593-6. https://doi.org/10.1016/j.amjms.2016.05.021

Barnes AN, Davaasuren A, Baasandagva U, Gray GC. A systematic review of zoonotic enteric parasitic diseases among nomadic and pastoral people. PLoS ONE. 2017;12:e0188809. https://doi.org/10.1371/journal.pone.0188809

Harvey TV, Tang AM, da Paixao Sevá A, Albano dos Santos C, Santos Carvalho SM, Magalhães da Rocha CMB, et al. Enteric parasitic infections in children and dogs in resource-poor communities in northeastern Brazil: Identifying priority prevention and control areas. PLoS Negl Trop Dis. 2020;14:e0008378. https://doi.org/10.1371/journal.pntd.0008378

Lowenstein C, Vasco K, Sarzosa S, Salinas L, Torres A, Perry MJ, et al. Determinants of childhood zoonotic enteric infections in a semirural community of Quito, Ecuador. Am J Trop Med Hyg. 2020;102:1269-78. https://doi.org/10.4269/ajtmh.19-0690

Witkowski JM, Bryl E, Fulop T. Should we try to alleviate immunosenescence and inflammaging - Why, how, and to what extent? Curr Pharm Des. 2019;25:4154-62. https://doi.org/10.2174/1381612825666191111153016

Suleiman BA, Yahaya M, Olaniyan FA, Sule AG, Sufiyan MB. Determinants of healthrelated quality of life among human immunodeficiency virus-positive (HIV-positive) patients at Ahmadu Bello University teaching hospital, Zaria, Nigeria- 2015. BMC Public Health. 2020;20:531. https://doi.org/10.1186/s12889-020-08659-9

Abange WB, Nkenfou CN, Gonsu-Kamga H, Nguedia CA, Kamgaing N, Lozupone C, et al. Intestinal parasites infections among HIV infected children under antiretrovirals treatment in Yaounde, Cameroon. J Trop Pediatr. 2020;66:178-86. https://doi.org/10.1093/tropej/fmz048

Zorbozan O, Quliyeva G, Tunali V, Ozbilgin A, Turgay N, Gokengin AD. Intestinal protozoa in HIV-infected patients: A retrospective analysis. Turkish J Parasitol. 2018;42:187-90. https://doi.org/10.5152/tpd.2018.5835

Taye B, Desta K, Ejigu S, Dori GU. The magnitude and risk factors of intestinal parasitic infection in relation to human immunodeficiency virus infection and immune status, at ALERT Hospital, Addis Ababa, Ethiopia. Parasitol Int. 2014;63:550-6. https://doi.org/10.1016/j.parint.2014.02.002

How to Cite
1.
Botero-Garcés J, Villegas-Arbeláez E, Giraldo S, Urán-Velásquez J, Arias-Agudelo L, Alzate-Ángell JC, et al. Prevalence of intestinal parasites in a cohort of HIVinfected patients from Antioquia, Colombia. Biomed. [Internet]. 2021 Oct. 15 [cited 2025 Apr. 5];41(Sp. 2):153-64. Available from: https://revistabiomedicaorg.biteca.online/index.php/biomedica/article/view/5992

Some similar items:

Published
2021-10-15

Altmetric

Article metrics
Abstract views
Galley vies
PDF Views
HTML views
Other views
QR Code

Funding data