SciELO - Scientific Electronic Library Online

 
vol.48 issue1Clinical outcomes and complications following percutaneous closure of patent foramen ovaleThe script clinical reasoning test An internal medicine educational practice perspective author indexsubject indexarticles search
Home Pagealphabetic serial listing  

Services on Demand

Journal

Article

Indicators

Related links

  • On index processCited by Google
  • Have no similar articlesSimilars in SciELO
  • On index processSimilars in Google

Share


Acta Medica Colombiana

Print version ISSN 0120-2448

Acta Med Colomb vol.48 no.1 Bogotá Jan./Mar. 2023  Epub Mar 28, 2024

https://doi.org/10.36104/amc.2023.2327 

ORIGINAL PAPERS

Opportunistic infections according to the CD4+ T lymphocyte count in patients with HIV at a tertiary care referral center

OSWALDO ENRIQUE AGUILAR-MOLINAa 

RAÚL ANDRÉS VALLEJO-SERNAa 

MARIA ANTONIA ESCOBAR-MERAb  * 

DANIEL BARONA-ROMYa 

ESTEFANÍA GARTNER-LÓPEZc 

LORENA MATTA-CORTÉSd 

aEspecialistas en Medicina Interna y Docentes Universidad del Valle Cali (Colombia).

bResidente de Medicina Interna Universidad Libre Cali (Colombia).

cEspecialista en Medicina Interna Hospital Universitario del Valle Cali (Colombia).

dEspecialista en Medicina Interna Hospital Universitario del Valle. Vicedecana de Investigación Universidad del Valle. Cali (Colombia).


Abstract

Opportunistic infections (OIs) have marked the prognosis in the natural course of patients with human immunodeficiency virus (HIV) infection.

Objective:

identifying the most common OIs and determining their relationship with the CD4+ lymphocyte count (CD4+TL) can improve our clinical practice and facilitate early diagnosis, the use of empiric treatments and prompt targeted treatment.

Materials and methods:

an observational, retrospective study aimed at describing the characteristics and variations of the OIs diagnosed clinically, using direct or indirect methods, which occur in patients with HIV (related to their CD4+TL count) who are admitted to a tertiary care center in Cali, Colombia. Adult patients hospitalized from January 2018 to January 2019 with a diagnosis of HIV/AIDS and a history or current diagnosis of OI were included. Individuals under the age of 18 and pregnant women were excluded.

Results:

a sample of 190 patients with at least one opportunistic infection was obtained, of whom 65.3% were men with a median age of 37 years (29.0-46.0), and the rest were women with a median age of 35.5 years (31.2-43.0). Eighty-three percent had a C3 classification on admission, 86% with a CD4+TL count ≤ 200 cells/mm3. The most frequent OIs included tuberculosis, with 28.4%, pneumocystosis with 27.9% and toxoplasmosis with 27.4%.

Conclusions:

in our population, despite advances in and greater availability of highly-effective antiretroviral therapy, most patients with HIV are hospitalized in advanced stages with opportunistic infections, in some cases with two or more concomitant infections, and with evidence of severe virological and immunological involvement. (Acta Med Colomb 2022; 48. DOI:https://doi.org/10.36104/amc.2023.2327).

Key words: HIV; opportunistic; CD4TL; Colombia

Resumen

Las infecciones oportunistas (IO) han marcado el pronóstico en la evolución natural de los pacientes con infección por virus de inmunodeficiencia humana (VIH).

Objetivo:

conocer las IO más frecuentes y establecer su relación con el conteo de linfocitos T CD4+ (LTCD4+) puede mejorar nuestra práctica clínica y favorecer un diagnóstico temprano, uso de terapias empíricas y tratamiento dirigido oportuno.

Material y métodos:

estudio observacional, retrospectivo, con el propósito de describir las características y variaciones de las IO diagnosticadas por clínica, métodos directos o indirectos, que se desarrollan en los pacientes con VIH en relación con su conteo LTCD4+ que ingresan a una institución de tercer nivel de atención en Cali (Colombia). Se incluyeron pacientes adultos hospitalizados entre enero 2018 a enero 2019 con diagnóstico de infección por VIH/SIDA y con antecedente o IO al momento del ingreso; se excluyeron menores de 18 años y gestantes.

Resultados:

se obtuvo una muestra de 190 pacientes con al menos una infección oportunista, del cual 65.3% eran hombres con una edad mediana de 37 años (29.0-46.0), para las mujeres de 35.5 años (31.2-43.0). El 83% se encontraba en clasificación C3 al ingreso, 86% con recuento de LTCD4+ ≤ 200 cels/mm3. De las IO las más frecuentes fueron, tuberculosis con 28.4%, neumocistosis con 27.9% y toxoplasmosis con 27.4%.

Conclusiones:

en nuestra población, pese al avance y mayor disponibilidad de terapia antirretroviral de alta efectividad, la mayoría de los pacientes con infección por VIH se hospitalizan en estadios avanzados con infecciones oportunistas, en algunos casos dos o más de manera concomitante y con evidencia de compromiso virológico e inmunológico severo. (Acta Med Colomb 2022; 48. DOI:https://doi.org/10.36104/amc.2023.2327).

Palabras clave: VIH; oportunista; LTCD4; Colombia

Introduction

Opportunistic infections (OIs) are an important cause of morbidity and mortality, especially in severely immunocompromised people 1-3. Patients with HIV infection who have a low CD4+ T cell count may develop a variety of OIs with a significant impact on their wellbeing, quality of life, medical care costs and survival 4. In regions like North America, Europe and Australia, Pneumocystis jirovecii pneumonia (PJP), Kaposi sarcoma (KS), esophageal candidiasis, cytomegalovirus (CMV), and disseminated Mycobacterium avium complex (MAC) infection and related disease were the prevalent OIs prior to the antiretroviral therapy (ART) era 5,6. In developing regions, the predominant HIV-related OIs prior to the introduction of ART were tuberculosis (TB), candidiasis, infectious diarrhea, bacterial meningitis and recurrent herpes simplex infections 7,8.

The substantial decrease in OIs with the introduction of ART is evident; however, there are significant differences in the burden of OIs between high-income and limited resource settings. It is important to have information on the reasons for hospital admissions among HIV patients and the type of OIs related to the CD4+ T cell count, in order to improve our clinical practice and favor early diagnosis, the use of empiric therapies and timely targeted therapy, considering that the described epidemiological changes entail different empirical coverage to what is currently used, which can also be influenced by geographic location.

Methodology

This was an observational, descriptive study with retrospective data collection. Adult hospitalized patients with an HIV/AIDS diagnosis and a history of OIs, or at least one OI at the time of admission, from January 1, 2018, to January 1, 2019, were included. The data were taken from the medical chart database at our institution. Those under the age of 18, pregnant women, those with incomplete medical charts, and cases without a confirmed or presumptive diagnosis of OI were excluded. The sociodemographic conditions, clinical characteristics, reasons for hospitalization, type of OIs and cancers were determined, as well as immunovirological markers (CD4+ T cell count and HIV viral load). The study was approved by the Research and Ethics Committee at Hospital Universitario del Valle (HUV). Body mass index (BMI) was calculated as weight in kilograms divided by the square of height in meters (kg/m2).

For the initial analysis, BMI was stratified according to the WHO criteria: <17 kg/m2 (moderate to severe undernutrition), 17 to <18.5 kg/m2 (mild undernutrition), >18.5-25 kg/m2 (normal nutrition) and > 25 kg/m2 (overweight and obesity) 9. The definitions of HIV infection/AIDS, opportunistic infections and HIV/AIDS-related cancers were those established by the United States Centers for Disease Control and Prevention (CDC). De novo HIV was defined as those diagnosed for less than three months. The current European definition of late diagnosis (LD) in an individual is a CD4+ T cell count of less than 350 cells/mm3 and/or an AIDS-defining illness at the time of diagnosis (10, 11). We chose to use WHO's definition of LD: a CD4+ T cell count under 200 cells/mm3 or a WHO clinical stage 3 or 4 at the time of diagnosis 12.

Imaging (radiology, tomography), microbiological (Gram, India ink, Cryptococcus capsular antigen, Ziehl-Neelsen, cultures), serum (VDRL), enzyme (ADA) and histopathological methods allowed the diagnosis of OIs. Studies of lavage and brushing samples were performed in the microbiology laboratory, including Gram, KOH, India ink, Ziehl-Neelsen, aerobic, fungal and mycobacterial cultures, as well as molecular biology for Mycobacterium tuberculosis (MTB) and cytomegalovirus. The pathology laboratory processed histopathology and cytology studies using immunohistochemistry, Ziehl-Neelsen, and PAS stains, along with molecular biology studies. For mycobacterial infection diagnoses, direct stains for acid-alcohol fast bacilli were performed, like Ziehl-Neelsen and modified Ziehl-Neelsen, along with Mycobacterium cultures and PCR for MTB. Sample seeding for microbiological isolation during the study period was done on solid culture medium (in duplicate for each sample).

To improve sensitivity, molecular identification tests for MTB were run using the Abbott m2000 Real Time MTB® detection test. To determine the disease stage, the most commonly used system is the CDC>s 1993 revision which substitutes the 1986 classification:

  • Clinical category A applies to primary infections and asymptomatic patients with or without persistent generalized lymphadenopathy (PGL).

  • Category B applies to patients with symptoms of diseases which do not belong to category C, but are related to HIV infection (oral candidiasis; persistent vulvovaginal candidiasis; cervical dysplasia; fever or diarrhea for more than one month; oral hairy leukoplakia; herpes zoster; immune thrombocytopenia; listeriosis; pelvic inflammatory disease; peripheral neuropathy).

  • Category C includes patients who have the diseases included in the AIDS-defining illnesses. Patients in categories C1, C2, C3, A3 and B3 are considered to have AIDS 13.

Results

A sample of 444 patients with an HIV diagnosis was obtained during the study period, after applying the exclusion criteria; 190 patients had HIV infection with at least one OI (Figure 1). Of the observed population, 65.3% were men, with a median age of 37 years (29.0-46.0), and 35.5 years (31.2-43.0) for women. Altogether, 81.6% of the patients were from Valle del Cauca Department, and 5.3% were from Cauca Department.

Figure 1 Patient sample. 

The patients' most common nutritional status was severe undernutrition, with 37.9%; we found an adequate nutritional status in 23.2% of the cases (Table 1). A total of 45.8% of the patients had been diagnosed for less than three months (de novo), and 69% of the cases had a late diagnosis (CD4+ T cell count less than 200 cells/mm3). Of the patients with a prior HIV diagnosis, only 7.76% were found to use OI prophylaxis.

Table 1 General characteristics of the population. 

Variables Female Male General
Sex 66 (34.7) 124 (65.3) 190
Age 35.5 (31.2 - 43.0) 37.0 (29.0 - 46.0) 37.0 (30.0 - 44.8)
Place of origin
Valle 57 (86.4) 98 (79.0) 155 (81.6)
Cauca 2 (3.0) 8 (6.5) 10 (5.3)
Nariño 2 (3.0) 4 (3.2) 6 (3.2)
Other 5 (7.6) 14 (11.3) 19 (10.0)
Time since diagnosis
Novo 26 (39.4) 61 (49.2) 87 (45.8)
Less than one year 9 (13.6) 18 (14.5) 27 (14.2)
1 - 5 years 11 (16.7) 17 (13.7) 28 (14.7)
5 - 10 years 10 (15.2) 14 (11.3) 24 (12.6)
More than 10 years 10 (15.2) 13 (10.5) 23(12.1)
Vertical 0 1 (0.8) 1 (0.5)
Nutritional status
Adequate 20 (30.3) 24 (19.4) 44 (23.2)
Mild undernutrition 0 1 (0.8) 1 (0.5)
Severe undernutrition 17 (25.8) 55 (44.4) 72 (37.9)
No data 29 (43.9) 44 (35.5) 73 (38.4)

The CD4+ T cell count was less than 200 cells/mm3 in 86.8% of the cases, with a count lower than 50 cells/mm3 in 54.7% of the patients, 50-100 cells/mm3 in 17.4% of the cases, and only 2.1% of the patients having a CD4+ T cell count over 500 cells/mm3. In 8.4%, the HIV viral load (VL) was undetectable, and in 8.9%, the VL was not reported in the chart (Table 2). Regarding their initial classification, C3 was the most frequent stage, with 87.8% of the cases.

Altogether, 42.1% (80) of the patients were on ART, but only 31% of these adhered to the instated treatment; among the patients who had ART ordered, the two most frequently used schemes were a combination of a non-nucleoside reverse transcriptase inhibitor (NNRTI) and two nucleoside reverse transcriptase inhibitors (NRTIs), and a combination of two NRTIs with a potentiated protease inhibitor. One hundred sixty-five patients (86.8%) had had an OI on their last recorded hospitalization.

Table 2. Virological and immunological status. 

Variables Female Male General (%)
Stage on admission
C1 2 (3.0) 2 (1.6) 4(2.1)
C2 13 (19.7) 8 (6.5) 21 (11.1)
C3 51(77.2) 114 (91) 165 (86.8)
Viral load (Copies/mL)
50 - 10,000 6 (9.1) 18 (14.5) 24 (12.6)
10,000- 100,000 14 (21.2) 37 (29.8) 51 (26.8)
100,000 - 500,000 17 (25.8) 29 (23.4) 46 (24.2)
More than 500,000 15 (22.7) 21 (16.9) 36 (18.9)
Undetectable 8(12.1) 8 (6.5) 16 (8.4)
No data 6 (9.1) 11 (8.9) 17 (8.9)
Count (CD4 cells/mm3)
Less than 50 31 (47.0) 73 (58.9) 104 (54.7)
50 - 100 9 (13.6) 24 (19.4) 33 (17.4)
100 - 200 11 (16.7) 17 (13.7) 28 (14.7)
200 - 500 13 (19.7) 8 (6.5) 21(11.1)
More than 500 2 (3.0) 2 (1.6) 4(2.1)

The most common OIs in the whole group were tuberculosis with 28.4%, pneumocystosis with 27.9%, and toxoplasmosis with 27.4%; oral candidiasis, histoplasmosis and crypotcoccosis were reported in 4.2%, 11.1%, and 11.6%, respectively. The least common OIs were CMV with 3.7% and MAC with 0.5% of the cases (Table 3). Altogether, 223 OIs were recorded, with 48 patients having more than one OI; in this group, the most frequent associations were his-toplasmosis associated with pneumocystosis, tuberculosis associated with pneumocystosis, and tuberculosis associated with toxoplasmosis.

Table 3 Opportunistic infections. 

Variables Female Male Total
Type of presentation
History of OI 11 (16.7) 14 (11.3) 25 (13.2)
Prior OI on admission 55 (83.3) 110 (88.7) 165 (86.8)
Toxoplasmosis
Not present 46 (69.7) 92 (74.2) 138 (72.6)
Present 20 (30.3) 32 (25.8) 52 (27.4)
Pneumocystosis
Not present 49 (74.2) 88 (71.0) 137 (72.1)
Present 17 (25.8) 36 (29.0) 53 (27.9)
Cryptococcosis
Not present 59 (89.4) 109 (87.9) 168 (88.4)
Present 7 (10.6) 15 (12.1) 22 (11.6)
Histoplasmosis
Not present 57 (86.4) 112 (90.3) 169 (88.9)
Present 9 (13.6) 12 (9.7) 21 (11.1)
Candidiasis
Not present 63 (95.5) 119 (96.0) 179 (94.2)
Present 3 (4.5) 5(6.2) 8 (4.2)
Tuberculosis
Not present 48 (72.7) 88 (71.0) 136 (71.6)
Present 18 (27.3) 36 (29.0) 54 (28.4)
CMV infection
Not present 64 (97.0) 119 (96.0) 183 (96.3)
Present 2 (3.0) 5 (4.0) 7 (3.7)
MAC infection
Not present 66(100) 123 (99.2) 189 (99.5)
Present 0 1 (0.8) 1 (0.5)
Coccidia infections
Not present 64 (97.0) 121 (97.6) 185 (97.4)
Present 2 (3.0) 3 (2.4) 5 (2.6)
Defining neoplasm
Not present 59 (89.4) 106 (85.5) 165 (86.8)
Present 7 (10.6) 18 (14.5) 25 (13.2)
Non-defining neoplasm
Not presente 65 (98.5) 122 (98.4) 187 (98.4)
Present 1 (1.5) 2 (1.6) 3 (1.6)

Regarding the association of OIs in relation to the CD4+ T cell count, 91% of the OIs occurred in patients with fewer than 200 cells/mm3 and only 1.8% of the OIs in those with lymphocyte counts greater than 500 cells/mm3.

Sixty-three percent of the cerebral toxoplasmosis cases were found in patients with CD4+ T cell counts less than 100 cells/mm3 and 62% of the pneumocystosis cases were found in patients with CD4+ T cell counts less than 50 cells/mm3, as were 100% of the Histoplasma infections (21). Tuberculosis was found in all ranges, with more patients in the CD4+ T cell range of less than 50 cells/mm3 (52%) (Table 4, Figure 2).

Discussion

Human immunodeficiency virus infection is a public health problem due to its high economic impact 14. In the described population, OIs were more frequent in men (65.3 vs. 34.7%) and at a general age ranging from 33 to 44 years, similar to populations described in other cities in our country and other countries in Latin America and Europe 4-16. The overall prevalence of undernutrition was high (37.9%), comparable to the undernutrition rate of patients hospitalized with AIDS in similar groups 18,19, probably due to most of the admitted patients being severely immunocompromised, with a CD4+ T cell count <200 cells/mm3, which is known to be related to undernutrition 20.

Most AIDS diagnoses and deaths are preventable, and one of the main predictors of HIV morbidity and mortality is late diagnosis of HIV infection. Altogether, 69.6% met the definition of LD, much higher than the 53% recorded in the European population, but similar to some African registers 10,21. A total of 86.8% of the patients with OIs had a CD4+ T cell count <200 cells/mm3; counts under 50 cells/ mm3 were found in 54.7% of the patients, and only 42.1% were on an ART scheme at the beginning of the study, very far from the 90-90-90 WHO 2020 objective and from the 81% reported in some cohorts in industrialized countries 22. For ART to be effective (reach undetectable plasma VLs), at least 95% of the daily doses must be taken; in our study, treatment adherence was measured with a patient survey which indicated that only 31% of the patients had adequate adherence, which could explain the very low percentage of undetectable VLs (8%).

Our study shows that the most common OIs were tuberculosis with 28.4%, followed by pneumocystosis with 27.9% and toxoplasmosis with 27.4%; oral candidiasis, histoplasmosis and cryptococcosis were reported in 4.2, 11.1 and 11.6%, respectively. This spectrum has varied widely from population to population and depends on some factors like access to ART or adequate affiliation to a social security system. Tuberculosis has already been described as the main OI in other data published in our country 23. Human immunodeficiency virus infection is known to have fostered a dramatic increase in the incidence of TB in many areas of the world, in some of which it is 10 times greater in people infected with HIV than in the general population 24.

In other countries, for example the United States, Djawe et al. describe pneumocystosis and Kaposi sarcoma as the most frequently reported OIs of all times (prior to and after the beginning of effective ART) 25. Among the systemic mycoses, cryptococcosis is most often found in patients with AIDS, especially in the form of meningoencephalitis. One of the most significant risk factors for opportunistic mycotic infections in patients with HIV infection is a CD4+ T cell count less than or equal to 200 cells/mm3 (26, which was corroborated in our study.

Table 4 Opportunistic infections according to CD4 T cell count. 

Opportunistic infections CD4 T lymphocyte count
Less than 50 50 - 100 100 - 200 200 - 500 More than 500
Toxoplasmosis 24 (17.9) 9 (22.5) 15 (51.7) 3 (18.7) 1 (25)
Pneumocystosis 33 (24.6) 12 (30) 5 (17.2) 2 (12.5) 1 (25)
Cryptococcus 15 (11.1) 5 (12.5) 0 1 (6.25) 1 (25)
Histoplasma 21 (15.7) 0 0 0 0
Candida 6 (4.5) 0 0 2 (12.5) 0
Tuberculosis 28 (20.9) 11 (27.5) 6 (20.7) 8 (50) 1 (25)
CMV 3 (2.2) 3 (7.5) 1 (3.4) 0 0
MAC 0 0 1 (3.4) 0 0
Coccidia 4 (2.9) 0 1 (3.4) 0 0
Total 134 29 4
A total of 223 OIs were recorded; 48 patients had more than one OI and the three most common associations were histoplasmosis associated with pneumocystosis, tuberculosis associated with pneumocystosis and tuberculosis associated with toxoplasmosis.

Figure 2 Opportunistic infections according to CD4 T cell count. 

In our study, 22 cases of Cryptococcus infection were documented, 20 of which were in patients with CD4+ T cell counts under 200 cells/mm3, which corresponds to 12.1% of all patients in this CD4+ T cell range; only two cases were documented in patients with CD4+ T cell counts greater than 200 cells/mm3. We underscore a low percentage of OIs due to Candida, which suggests a low rate of diagnosis at our center. These data are similar to local studies in which a prevalence of Candida infection of up to 5.5% has been estimated in patients with HIV 27.

We highlight the fact that patients with CD4 counts <50 cells/mm3 were more prone to having more than one OI (often three), compared with all the patients studied, which concurs with other reviews 28-29.

Conclusions

Despite the availability of highly-effective ART, OIs continue to cause considerable morbidity and mortality in patients infected with HIV. Accessibility to ART should be improved, delayed diagnosis reduced, and above all, lack of adherence to treatment should be impacted (the latter derived from psychosocial and economic factors, including low educational level, poverty and unemployment) 30. Instating certain measures like regular medical visits, evaluating barriers prior to beginning ART, using ART with a high genetic resistance barrier, simplified dosing schemes (including the single-pill regimen), and multidisciplinary approaches including social work, are important strategies which need to be disseminated more 31,32.

In our population, most patients are hospitalized in advanced stages with OIs and with evidence of severe viral and immunological compromise. Our study contributes valid information regarding the main OIs affecting this population, which should therefore be thoroughly checked for, along with cancers, when evaluating patients with HIV infection.

References

1. Holmes, C. B.; Losina, E.; Walensky, R. P.; Yazdanpanah, Y.; Freedberg, K A. Review of Human Immunodeficiency Virus Type 1-Related Opportunistic Infections in Sub-Saharan Africa. Clin.Infect. Dis. 2003, 36(5), 652-662. https://doi.org/10.1086/367655. [ Links ]

2. Kouanfack, O. S. D.; Kouanfack, C.; Billong, S. C.; Cumber, S. N.; Nkfusai, C. N.; Bede, F.; Wepngong, E.; Hubert, C.; Nguefack-Tsague, G.; Singwe, M. N. Epidemiology of Opportunistic Infections in HIV Infected Patients on Treatment in Accredited HIV Treatment Centers in Cameroon. Int. J. Matern. Child Health AIDS 2019, 8 (2), 163-172. https://doi.org/10.21106/ijma.302. [ Links ]

3. Dereje, N.; Moges, K.; Nigatu, Y.; Holland, R. Prevalence And Predictors Of Opportunistic Infections Among HIV Positive Adults On Antiretroviral Therapy (On-ART) Versus Pre-ART In Addis Ababa, Ethiopia: A Comparative Cross-Sectional Study. HIVAIDSAuckl . NZ 2019, 11, 229-237. https://doi.org/10.2147/HIV.S218213. [ Links ]

4. O Iroezindu, M. Prevalence and Risk Factors for Opportunistic Infections in HIV Patients Receiving Antiretroviral Therapy in a Resource-Limited Setting in Nigeria. J. AIDS Clin. Res. 2013, 01 (S3). https://doi.org/10.4172/2155-6113.S3-002. [ Links ]

5. Iroezindu, M. Disparities in the Magnitude of Human Immunodeficiency Virus-Related Opportunistic Infections between High and Low/Middle-Income Countries: Is Highly Active Antiretroviral Therapy Changing the Trend? Ann. Med. Health Sci. Res. 2016, 6 (1), 4. https://doi.org/10.4103/2141-9248.180234. [ Links ]

6. Rosenblum, L.; Buehler, J. W.; Morgan, M. W.; Costa, S.; Hidalgo, J.; Holmes, R.; Lieb, L.; Shields, A.; Whyte, B. M. The Completeness of AIDS Case Reporting, 1988: A Multisite Collaborative Surveillance Project. Am. J. Public Health 1992, 82 (11), 1495-1499. https://doi.org/10.2105/AJPH.82.11.1495. [ Links ]

7. Rubaihayo, J.; Tumwesigye, N. M.; Konde-Lule, J. Trends in Prevalence of Selected Opportunistic Infections Associated with HIV/AIDS in Uganda. BMC Infect. Dis. 2015, 15 (1), 187. https://doi.org/10.1186/s12879-015-0927-7. [ Links ]

8. Rubaihayo, J.; Tumwesigye, N. M.; Konde-Lule, J.; Wamani, H.; Nakku-Joloba, E.; Makumbi, F. Frequency and Distribution Patterns of Opportunistic Infections Associated with HIV/AIDS in Uganda. BMC Res. Notes 2016, 9 (1), 501. https://doi.org/10.1186/s13104-016-2317-7. [ Links ]

9. World Health Organization. Nutrition Requirements for People Living with HIV/AIDS: Report of a Technical Consultation. Geneva: WHO; 2003. [ Links ]

10. European Centre for Disease Prevention and Control/WHO Regional Office for Europe. (2019). HIV/AIDS Surveillance in Europe 2019-2018 Data. [ Links ]

11. Late presenters working group in COHERE in EuroCoord; Mocroft, A.; Lundgren, J.; Antinori, A.; Monforte, A. d'Arminio; Brannström, J.; Bonnet, F.; Brockmeyer, N.; Casabona, J.; Castagna, A.; Costagliola, D.; De Wit, S.; Fätkenheuer, G.; Furrer, H.; Jadand, C.; Johnson, A.; Lazanas, M.; Leport, C.; Moreno, S.; Mussini, C.; Obel, N.; Post, F.; Reiss, P.; Sabin, C.; Skaletz-Rorowski, A.; Suarez-Loano, I.; Torti, C.; Warszawski, J.; Wittkop, L.; Zangerle, R.; Chene, G.; Raben, D.; Kirk, O. Late Presentation for HIV Care across Europe: Update from the Collaboration of Observational HIV Epidemiological Research Europe (COHERE) Study, 2010 to 2013. Euro Surveill. Bull. Eur. Sur Mal. Transm. Eur. Commun. Dis. Bull. 2015, 20 (47). https://doi.org/10.2807/1560-7917.ES.2015.20.47.30070. [ Links ]

12. Ngongo, N. M.; Nani-Tuma, H. S.; Mambimbi, M. M.; Mashi, M. L.; Izizag, B. B.; Ndolumingu, F. K.; Maes, N.; Moutschen, M.; Darcis, G. Decrease in Late Presentation for HIV Care in Kinshasa, DRC, 2006-2020. AIDS Res. Ther. 2021, 18, 41. https://doi.org/10.1186/s12981-021-00366-8. [ Links ]

13. Ward, M., Buehler, M. J. W., Jaffe, M. H. W., & Berkelman, R. L. (1993). 1993 Revised Classification System for HIV Infection and Expanded Surveillance Case Definition for AIDS among Adolescents and Adults. [ Links ]

14. Fondo Colombiano de Enfermedades de Alto Costo, Cuenta de Alto Costo (CAC). Situación del VIH en Colombia 2019; Bogotá D.C. 2020. [ Links ]

15. Agudelo-Gonzalez, S.; Murcia-Sanchez, F.; Salinas, D.; Osorio, J. Infecciones Oportunistas En Pacientes Con VIH En El Hospital Universitario de Neiva, Colombia. 2007-2012. Infectio 2015, 19 (2), 52-59. https://doi.org/10.1016/j.infect.2014.11.008. [ Links ]

16. Montalvo, R. H.; Mejía, J. R.; Ramírez, P.; Rojas, E.; Serpa, H.; Tiza, V. Infecciones Oportunistas Post Inicio de Tratamiento Antirretroviral En Pacientes Con VIH/SIDA En Un Hospital Público de Perú. Rev. Fac. Cienc. Salud UDES 2018, 5 (1), 19. https://doi.org/10.20320/rfcsudes.v5i1.103. [ Links ]

17. Gueler, A.; Moser, A.; Calmy, A.; Günthard, H. F.; Bernasconi, E.; Furrer, H. ; Fux, C. A.; Battegay, M.; Cavassini, M.; Vernazza, P.; Zwahlen, M.; Egger, M. Life Expectancy in HIV-Positive Persons in Switzerland: Matched Comparison with General Population. Aids 2017, 31 (3), 427-436. https://doi.org/10.1097/QAD.0000000000001335. [ Links ]

18. Hailemariam, S.; Bune, G. T.; Ayele, H. T. Malnutrition: Prevalence and Its Associated Factors in People Living with HIV/AIDS, in Dilla University Referral Hospital. Arch. Public Health 2013, 71 (1), 13. https://doi.org/10.1186/0778-7367-71-13. [ Links ]

19. Alebel, A.; Demant, D.; Petrucka, P.; Sibbritt, D. Effects of Undernutrition on Mortality and Morbidity among Adults Living with HIV in Sub-Saharan Africa: A Systematic Review and Meta-Analysis. BMC Infect. Dis. 2021, 21, 1. https://doi.org/10.1186/s12879-020-05706-z. [ Links ]

20. Mulu, H.; Hamza, L.; Alemseged, F. Prevalence of Malnutrition and Associated Factors among Hospitalized Patients with Acquired Immunodeficiency Syndrome in Jimma University Specialized Hospital, Ethiopia. Ethiop. J. Health Sci. 2016, 26 (3), 217. https://doi.org/10.4314/ejhs.v26i3ALinks ]

21. Assen, A.; Molla, F.; Wondimu, A.; Abrha, S.; Melkam, W.; Tadesse, E.; Yilma, Z.; Eticha, T.; Abrha, H.; Workneh, B. D. Late Presentation for Diagnosis of HIV Infection among HIV Positive Patients in South Tigray Zone, Ethiopia. BMC Public Health 2016, 16 (1), 558. https://doi.org/10.1186/s12889-016-3263-y. [ Links ]

22. Sezgin, E.; Van Natta, M.; Thorne, J.; Puhan, M.; Jabs, D. Secular Trends in Opportunistic Infections, Cancers and Mortality in Patients with AIDS during the Era of Modern Combination Antiretroviral Therapy. HIV Med. 2018, 19 (6), 411-419. https://doi.org/10.1111/hiv.12609. [ Links ]

23. Montúfar Andrade, F.; Quiroga, A.; Builes, C.; Saldarriaga, C.; Aguilar, C.; Mesa, M.; Zuleta Tobón, J. 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 (1), 9-16. https://doi.org/10.1016/j.infect.2015.05.004. [ Links ]

24. Corbett, E. L.; Watt, C. J.; Walker, N.; Maher, D.; Williams, B. G.; Raviglione, M. C.; Dye, C. The Growing Burden of Tuberculosis. Arch. Intern. Med. 2003, 163 (9), 1009. https://doi.org/10.1001/archinte.163.9.1009. [ Links ]

25. Djawe, K.; Buchacz, K.; Hsu, L.; Chen, M. J.; Selik, R. M.; Rose, C.; Williams, T.; Brooks, J. T.; Schwarcz, S. Mortality Risk after AIDS-Defining Opportunistic Illness among HIV-Infected Persons-San Francisco, 1981-2012. J. Infect. Dis. 2015, 212 (9), 1366-1375. https://doi.org/10.1093/infdis/jiv235. [ Links ]

26. González Ángel, Tobón Ángela María. Infecciones micóticas oportunistas en pacientes con VIH/SIDA. Infect. [Internet]. 2006 Dec [cited 2022 Mar 08] ; 10(4): 279-287. [ Links ]

27. Martinez LL, Cardona-Arias JA. Infecciones fúngicas en un hospital público de referencia para la atención de personas con VIH/SIDA, Medellín 2013-2017. MÉD.UIS. 2020;33(2): 17-24. doi: 10.18273/revmed.v33n2-2020002 [ Links ]

28. Tilak, A.; Shenoy, S.; Varma, M.; Kamath, A.; Tripathy, A.; Sori, R.; Saravu, K. Opportunistic Infection at the Start of Antiretroviral Therapy and Baseline CD4+ Count Less than 50 Cells/Mm3 Are Associated with Poor Immunological Recovery. J. Basic Clin. Physiol. Pharmacol. 2019, 30 (2), 163-171. https://doi.org/10.1515/jbcpp-2018-0105. [ Links ]

29. Gautam, H.; Bhalla, P.; Saini, S.; Uppal, B.; Kaur, R.; Baveja, C. P.; Dewan, R. Epidemiology of Opportunistic Infections and Its Correlation with CD4 T-Lymphocyte Counts and Plasma Viral Load among HIV-Positive Patients at a Tertiary Care Hospital in India. J. Int. Assoc. Physicians AIDS Care Chic . Ill 2002 2009, 8 (6), 333-337. https://doi.org/10.1177/1545109709346881. [ Links ]

30. Benson, C.; Wang, X.; Dunn, K. J.; Li, N.; Mesana, L.; Lai, J.; Wong, E. Y.; Chow, W.; Hardy, H.; Song, J.; Brown, K. Antiretroviral Adherence, Drug Resistance, and the Impact of Social Determinants of Health in HIV-1 Patients in the US. AIDSBehav. 2020, 24 (12), 3562-3573. https://doi.org/10.1007/s10461-020-02937-8. [ Links ]

31. Guidelines for the Use of Antiretroviral Agents in HIV-1-Infected Adults and Adolescents I AIDS Education and Training Centers National Coordinating Resource Center (AETC NCRC) Guidelines for the Use of Antiretroviral Agents in HIV-1-Infected Adults and Adolescents I AIDS Education and Training Centers National Coordinating Resource Center (AETC NCRC) https://aidsetc.org/resource/guidelines-use-antiretroviral-agents-hiv-1-infected-adults-and-adolescents (accessed 2021 -08 -22). [ Links ]

32. Holmes, C. B.; Losina, E.; Walensky, R. P.; Yazdanpanah, Y.; Freedberg, K. A. Review of Human Immunodeficiency Virus Type 1-Related Opportunistic Infections in Sub-Saharan Africa. Clin. Infect. Dis. 2003, 36(5), 652-662. https://doi.org/10.1086/367655. [ Links ]

Received: September 13, 2021; Accepted: July 22, 2022

*Correspondencia: Dra. María Antonia Escobar-Mera. Cali (Colombia). E-Mail: antoniaescobarmera@hotmail.com

Creative Commons License This is an open-access article distributed under the terms of the Creative Commons Attribution License