Clinical management of patients with advanced HIV disease at The AIDS Support Organization, Mbarara clinic in Southwestern Uganda: a retrospective review of patient records

doi:10.21203/rs.3.rs-5005696/v1

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Clinical management of patients with advanced HIV disease at The AIDS Support Organization, Mbarara clinic in Southwestern Uganda: a retrospective review of patient records

https://doi.org/10.21203/rs.3.rs-5005696/v1

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Introduction: Uganda has made significant progress in expanding access to ART over the years, however, currently up to 50% of PLHIV still enroll into HIV care with AHD. PLHIV who present with AHD continue to have a greater mortality risk and the risk rises as CD4 counts drop, particularly if they fall below 100 cells per cubic millimeter. This study therefore seeks to evaluate the clinical management practices for AHD at a high volume not for profit health facility in an urban setting in Southwestern Uganda.

Methods: A cross-sectional analysis of secondary data from a large volume, nonprofit health facility in Southwestern Uganda was done. An analysis included patient records of 994 new and 76 virologically non suppressed patients. Descriptive analysis of data was done, and the two groups (treatment naïve and non-suppressed) were compared using chi-square tests or Fisher’s exact test for categorical data and the Mann Whitney U test for numerical data. The analysis was done using StatsDirect.

Results: The prevalence of ADH as defined by a CD4 cell count below 200 cells/µl or WHO clinical stage 3 or 4 disease was 20.4% (95% CI: 18.0—23.0). The prevalence of AHD was considerably higher among males 30.3% (95% CI: 26.1—35.0%) compared to females: 13.9% (95% CI: 11.2—17.0%). Access to CD4 as a diagnostic test for AHD was 74.5% (741/994) among newly enrolled patients compared to 77.6% (59/76) among virally non suppressed patients. Access to serum CrAg screening among patients with AHD was higher among the newly enrolled HIV clients at 60.6% (131/216) compared to non-suppressed clients; 22.2% (6/27) (p < 0.001). Additionally, there was no significant difference in administration of fluconazole between the two groups (p = 0.476). Among the patients with AHD, the proportion of patient tested for TB using urine TB_LAM was higher among the newly enrolled patients (45.9%) compared to the non-suppressed clients (21.4%), and this difference was statistically significant (p = 0.010).

Conclusion: This study demonstrates that much as significant strides have been made in the achievement of the UNAIDS 95 95 95 targets, the prevalence of AHD remains high, and the implementation of the AHD intervention package remains sub-optimal. The Ministry of Health and partners need to strengthen processes for the screening, diagnosis, and management of AHD.

Clinical trial number: Not applicable.

Advanced HIV Disease

prevalence

management

Uganda has made significant strides towards achieving the Joint United Nations Program on HIV/AIDS (UNAIDS) 95, 95, 95 targets, which aim to achieve 95% of people living with HIV (PLHIV) knowing their HIV status, 95% of those who know their HIV status beginning lifelong antiretroviral treatment (ART), and 95% of those on ART achieving viral suppression [1]. According to the 2020 Uganda Population-based HIV Impact Assessment (UPHIA), 80.9% of HIV-positive adults and adolescents over the age of 15 were aware of their HIV status. Of these, 96.1% had begun antiretroviral therapy (ART), and 92.2% had a suppressed viral load [1, 2]. Additionally, as ART has become more widely available, HIV/AIDS-related mortality and morbidity have decreased over time [3]. Since 2003, there have been 43% fewer deaths per year from complications associated with AIDS. Despite this decline the trend has lately plateaued, and up to 50% of patients with HIV continue to present with advanced HIV disease (AHD) [3].

Advanced HIV disease is defined by the World Health Organization (WHO) as having a CD4 cell count of less than 200 cells per mm3 or a WHO clinical stage three or four condition in adults, adolescents, and children older than five years [3]. In addition, all HIV-positive children under the age of five who have never had ART or who have taken it for less than a year are considered to have advanced HIV disease [4]. AHD can affect people who are new on ART or those who have received treatment before [5].

Despite the WHO recommendation for universal access to ART regardless of CD4 cell count, it is estimated that 30 to 40 percent of HIV patients beginning ART in low- and middle-income countries have a CD4 less than 200 cells per mm³ and 20 to 25% have severe immunosuppression with CD4 counts less than 100 cells/mm³ [3, 6]. Additionally, about 10% of patients initiating ART with severe immunosuppression die within the first three months of treatment [6]. Adults with AHD are more likely to die from tuberculosis (TB), cryptococcal meningitis, severe bacterial infections, toxoplasmosis and Pneumocystis jirovecii pneumonia [3, 5]. On the other hand, the most common causes of death in children with AHD include tuberculosis, severe bacterial infections, Pneumocystis jirovecii pneumonia, diarrheal illnesses, and malnutrition [3]. The emergence or worsening of symptoms associated with these infections is primarily caused by Immune Reconstitution Inflammatory Syndrome, which majorly affects patients who start ART with low CD4 counts [6].

Ever since the introduction WHO Guidelines for Managing Advanced HIV Disease and Rapid Initiation of Antiretroviral Therapy in 2017, there has been little research on the current clinical practices in the management of AHD in outpatient settings in Africa. Only five published studies have examined the management practices of AHD in Africa (Senegal, Tanzania, Botswana, Zambia and Malawi) [7–11]. Three of the studies were conducted in an outpatient setting while two of then assessed AHD management practices in the inpatient medicine units [7]. Overall, the quality of AHD care was worse in outpatient HIV clinics than inpatient care. Specifically, the study conducted in Malawi by Heller et al to evaluate AHD care at Kamuzu Central Hospital medical ward found a much better quality of AHD care than all the other studies [9]. This was attributed to formation of a dedicated space (AHD room) with dedicated staff for screening handling patients diagnosed with AHD [9]. There is a dearth of published literature evaluating implementation of the WHO package of interventions and current practices for AHD management in Uganda. This study will therefore add to the existing body of knowledge on the management of AHD in Uganda and Africa in general.

Despite progress made in expanding access to ART over the years, up to 50% of PLHIV still enroll into HIV care with AHD [3]. PLHIV who present with AHD continue to have a greater mortality risk and the risk rises as CD4 counts drop, particularly if they fall below 100 cells per cubic millimeter [3]. It is crucial that the WHO package of interventions be put into practice in order to improve early diagnosis of individuals with AHD and prompt delivery of preventive, diagnostic, and therapeutic services for the major causes of death [12]. Efforts to curb mortality associated with AHD cannot succeed without guideline adoption, and access to key diagnostic and treatment services. This study therefore seeks to evaluate the prevalence and clinical management practices for AHD at a high volume not for profit health facility in an urban setting in Uganda. This study will inform the Uganda Ministry of Health about the adoption and diffusion of AHD package of interventions to guide planning and implementation.

Study design: This study used a retrospective review of patient records to determine the prevalence and clinical management of AHD in a large non-profit health facility in southwestern Uganda. In this review, a descriptive cross-sectional analysis of HIV patient-level data from the Uganda Electronic Medical Records system was done.

Study setting: This study was carried out in the Southwestern Ugandan at a Private Not for Profit (PNFP) health facility known as The AIDS Support Organization (TASO) Mbarara Centre of Excellence (TASO Mbarara COE). This health center was established by TASO, a non-profit organization that was started in 1987 by a group of volunteers to provide assistance to PLHIV [13]. There are 11 such HIV clinics in Uganda operated by TASO, and they all provide basic HIV care package, including HIV testing, prevention of mother to child transmission services, voluntary medical male circumcision, care, treatment, and support services [13]. The TASO Mbarara clinic receives most of its funding from the United States President’s Emergency Plan for AIDS Relief (PEPFAR) through the United States Agency for International Development (USAID). This clinic was chosen because of its high volume of PLHIV and its location in Mbarara city in Southwestern Uganda, a region with the third highest (6.3%) prevalence of HIV [1]. The facility currently serves about 6,145 clients (Source: Program data) majority of them coming from Ankole region.

Study population: The study population included all the newly identified HIV patients at TASO Mbarara COE between January 2020 and December 2022. This time frame was chosen because it followed the adoption and incorporation of AHD guidelines into the consolidated HIV/AIDS prevention, care, and treatment guidelines published by the Uganda Ministry of Health during this time. The analysis included all records for newly diagnosed PLHIV older than five years of age who engaged in HIV care and were assigned a unique identification between January 2020 and December 2022. Clients transferred to TASO Mbarara COE after initiating ART from another health facility were excluded from this analysis.

Sample size and sampling: All records for patients newly enrolled in the HIV clinic at TASO Mbarara COE between January 2020 and December 2022 and all the active virally non-suppressed were included in this analysis. In total, medical records of 994 new and 76 non-suppressed HIV patients were included in the analysis.

Study variables and operational definitions

The study variables which were used in this study to answer the research question are illustrated in Table S1. For purposes of this study, AHD was defined as having a CD4 cell count less than 200 cells per mm³ or a WHO clinical stage 3 or 4 for children, adolescents, and adults above the age of five years old. Clinical management of AHD covered screening for AHD, diagnosis, prophylaxis, and treatment of the common OIs such as tuberculosis, cryptococcal disease, PJP among others. A patient was regarded as having undergone AHD screening if they underwent a CD4 test or clinical staging. TB screening was considered done if the patient had a documented symptom screen at the first clinical contact while TB diagnosis was considered assessed if the patient had a documented urine TB Lipoarabinomannan (TBLAM), Xpert MTB/LF or chest X ray result. In addition, cryptococcal disease was considered done if the patient had a documented serum or CSF CrAg result. Treatment for any of the identified OIs was considered done if the patient had documented medication for the respective OIs.

Data collection

This study used secondary data from the TASO Mbarara COE HIV program, a busy HIV clinic in southwestern Uganda. Data were extracted from the Uganda Electronic Medical Records (Uganda EMR) system by the facility data manager who has already had a series of trainings and mentorship in the usage of this electronic system. Uganda EMR is a national electronic medical records system which is used to record, monitor, and track patient data as well as to inform program decisions and enhance performance.

The data used in this analysis were already generated during routine patient care by the clinic team. Every newly registered patient's information is documented on the HIV care card by the attending team, which included the counselor who offered pre- and post-test counseling, the doctor or clinical officer who conduct clinical assessments and prescription and the pharmacist or dispenser who issues out medicines to the patient. In cases where laboratory investigations are requested, patients were sent to the laboratory which was housed within the same building and tests are done and results documented in the laboratory register and a slip is provided to the patient to take to the clinician’s room for clinical decision making.

The HIV care cards and the linkage and PreART register were used capture all the AHD related data, including the dates of HIV diagnosis and ART initiation, CD4 counts, TBLAM results, serum CrAg results, TB screening and diagnosis, ART regimen, and prophylactic treatment for OIs. At the close of the clinic day, the data clerk collects all the filled-out HIV care cards and enters this data into the Uganda EMR, typically within the same week.

Laboratory procedures

All investigations were done at the clinic by a professional laboratory technician who was authorized by the Allied Health Professionals Council of Uganda. The BD FACSPresto or PIMA CD4 analyzer was used for CD4 testing, while a GeneXpert equipment was used for the Xpert MTB/RIF assay for TB diagnosis. The TBLAM and CrAg testing were done using simple strips with minimal training requirements and biosafety hazards. External quality assurance testing for HIV tests, CD4 and TB tests is conducted by the Uganda Virus Research Institute and the National TB and Leprosy Program.

Data management and analysis

The researcher checked the dataset for accuracy, completeness, and consistency after extracting it from the Uganda EMR and putting it into a spreadsheet. To validate and rectify the errors, the electronic data were triangulated with patient charts, PreART registers and laboratory registers to check for duplicates, missing entries, or outliers in the data.

The data were imported into Stats Direct analysis software and was summarized using descriptive statistics. The proportion of clients who had AHD as defined by a CD4 less than 200 cells/mm3 or clinical stage 3 or 4 was determined. While categorical variables were reported using proportions or percentages together with 95% confidence intervals (CI), continuous variables were summarized using mean, median, and standard deviation. The means and proportions were presented in the form of a cascade. Bar charts were used to visualize frequencies of categorical data. A chi-square test was used to compare the characteristics of study participants, prevalence as well as the management practices of AHD between the newly enrolled and non-suppressed patients. This test was used because it is the preferred statistical test for comparing proportions between two independent populations [14]. In cases where the groups being compared were small, we used the Fisher’s exact test which is the recommended test for analysis of small samples especially when over 20% of the cells have expected frequencies less than five [14].

Additionally, the Mann Whitney U test (Wilcoxon Rank Sum test) was used to compare the median CD4 counts between the two independent samples. This test was used because the data were numeric and they did not meet the assumptions for the parametric alternative, the independent t-test i.e., the test for normality of the data and the test for homogeneity of variance in the two groups being compared [15].

Ethical considerations

Ethical approval

was obtained from TASO Research Ethics Committee (TASO-2023-220) while administrative approval to obtain the dataset was obtained from the Executive Director of TASO Uganda through the TASO REC administration. All patient-identifying information such as names, telephone contacts, or physical addresses that would allow patient identification was removed from the dataset prior to analysis. To protect patient privacy, distinct identification numbers (ART numbers) were used for each individual record. The dataset was pass-word protected and stored in a secure computer accessible to only the researcher.

Characteristics of study participants

In total, 994 new HIV positive patients were enrolled in the clinic between January 2020 and December 2022 all the records of the 994 clients were included in the analysis (Table 1). Overall, 57.8% (575/994) of the new HIV patients were female, while 41.9% (419/994) were male. In addition, the majority (94.6%) of the newly enrolled HIV patients were adults. Only 31 (3.1%) adolescents and 23 (2.3%) children under 10 years old were enrolled during the same period. The overall median age of the patients was 30 (IQR: 25–37) years. Among males and females, the median age was 34 (IQR: 29–41) and 28 (IQR: 23–33) years, respectively.

In addition, there were 76 active virally non-suppressed clients in the HIV clinic at the time of data collection. Of these, 51% (38/76) were female. The overall median age among the non-suppressed clients was 37.5 (IQR: 26.5—46).

Table 1

Characteristics of study participants
	Newly enrolled	Non suppressed	Total	p-value
N	994 (92.9%)	76 (7.1%)	1,070 (100.0%)
Category by age
Adolescent	31 (3.1%)	7 (9.2%)	38 (3.6%)	0.021
Adult	940 (94.6%)	67 (88.2%)	1,007 (94.1%)
Child	23 (2.3%)	2 (2.6%)	25 (2.3%)
Gender
Female	575 (57.8%)	39 (51.3%)	614 (57.4%)	0.267
Male	419 (42.2%)	37 (48.7%)	456 (42.6%)
WHO Clinical stage at enrolment
WHO STAGE 1	392 (39.4%)	27 (35.5%)	419 (39.2%)	0.087
WHO STAGE 2	567 (57.0%)	43 (56.6%)	610 (57.0%)
WHO STAGE 3	26 (2.6%)	3 (3.9%)	29 (2.7%)
WHO STAGE 4	9 (0.9%)	3 (3.9%)	12 (1.1%)
Baseline ART regimen.
0	12 (1.2%)	6 (7.9%)	18 (1.7%)	< 0.001
ABC/3TC/DTG	30 (3.0%)	4 (5.3%)	34 (3.2%)
TDF-3TC-EFV	60 (6.0%)	0 (0.0%)	60 (5.6%)
TDF/3TC/DTG	892 (89.7%)	66 (86.8%)	958 (89.5%)

Prevalence of AHD among newly enrolled and virally non-suppressed patients.

The CD4 coverage among eligible PLHIV was 74.5% (741/994) among newly enrolled patients and 77.6% (59/76) among virally non suppressed patients. Of the 994 newly enrolled patients enrolled in the clinic in the study period, 741 new patients who had a CD4 test and all the 994 (100%) had a documented WHO clinical stage. The prevalence of ADH as defined by a CD4 cell count below 200 cells/µl or WHO clinical stage 3 or 4 disease was 20.4% (95% CI: 18.0—23.0). Among the males, the prevalence of AHD was 30.3 (95% CI: 26.1—35.0%) which was considerably higher than the females at 13.9% (95% CI: 11.2—17.0%).

The CD4 coverage among virally unsuppressed patients was 77.6% (95% CI: 66.6—86.4%), while all the 76 clients had a documented WHO clinical stage. Majority of the non-suppressing clients were classified as WHO clinical stage 1 (35.5%) or 2 (56.6%) with WHO clinical stage3 and 4 contributing the smallest number, both at 3.9%. Among the non-suppressed patients with a documented CD4 test and a WHO clinical stage, the prevalence of AHD was 43.5% (27/62), and it was higher among the males at 45.6% compared to females (41.4%) as shown in Table 2.

Table 2

Prevalence of AHD among new and non-suppressed patients at TASO Mbarara
	Newly enrolled HIV patients		Non suppressed patients
Variable	Prevalence of AHD % (n/N)	95% Confidence Interval	Prevalence of AHD % (n/N)	95% Confidence Interval
Overall	21.7 (216/994)	19.2—24.4%	35.5 (27/76)	31.0—56.7%
Gender
Male	32.5 (136/419)	28.0—37.2%	45.6 (15/33)	28.1—63.6%
Female	13.9 (80/575)	11.2—17.0%	41.4 (12/29)	23.5—61.1%
Age category
Children (< 10 yrs.)	65.2 (15/23)	42.7—83.6%	50.0 (1/2)	1.3—98.7%
Adolescents (10–19)	16.1 (5/31)	5.5—33.7%	25.0 (1/4)	0.6—80.6%
Adults (Above 19).	20.9 (196/840)	18.3—23.6%	46.4 (26/56)	33.0—60.3%

AHD management practices

All the 994 (100%) new clients identified at TASO clinic were initiated on ART within 14 days in line with the WHO test and treat recommendations. The most prescribed regimen for newly enrolling HIV patients was TDF/3TC/DTG at 89.7% (892/994) followed by TDF-3TC-EV at 6.0% (60/994) (Table 3). WHO clinical staging was documented for all the new clients enrolled in the clinic with majority (96.5%) of these being in either WHO clinical stage one or two and only 3.5% (35/994) of the patients being in clinical stage 3 of 4 (Fig. 1). Of the 994 new patients enrolling into the HIV clinic from January 2020 to December 2022, only 74.5% (741/994) had a baseline CD4 test done with a median CD4 count was 417 cells/µl (IQR: 196—721). Of the 216 newly enrolled patients who had AHD, only 44.4% (96/216) had laboratory evaluation using TBLAM, and 23 TB patients were diagnosed and 100% (23/23) were initiated on TB treatment in line with the World Health Organization AHD management guidelines.

Also, of the 216 patients with AHD, only 60.6% (131/216) had a serum CrAg test done for diagnosis of cryptococcal antigenemia and 12 patients were found to have a positive serum CrAg result. None of the patients had a record of lumber puncture with CSF CrAg results. However, all the 12 patients received pre-emptive treatment for cryptococcal disease with fluconazole.

Table 3

Baseline ART regimes for newly enrolled HIV patients
ART Regimen	Frequency	Relative %	Cumulative	Cumulative Relative %
ABC-3TC-ATV/r	1	0.1	1	0.1
ABC-3TC-EFV	1	0.1	2	0.2
ABC-3TC-LPV/r	5	0.5	7	0.7
ABC-3TC-DTG	30	3.0	37	3.7
AZT-3TC-ATV/r	1	0.1	38	3.8
AZT-3TC-DTG	3	0.3	41	4.1
TDF-3TC-ATV/r	1	0.1	42	4.2
TDF-3TC-EFV	60	6.0	102	10.2
TDF-3TC-DTG	892	89.7	994	100

Management of AHD among virally unsuppressed patients.

At the time of data collection, the clinic had 76 virally unsuppressed HIV patients. Of these, 77.6% (59/76) had a CD4 test and 100% (76/76) had a documented WHO clinical stage to support the diagnosis of AHD. Among those who had CD4 and WHO clinical staging, 43.5% (27/62) had AHD, and only five of these had a TB_LAM or Xpert MTB assay done, and one TB patients was diagnosed giving a yield of 20%; and this patient was initiated on TB treatment according to the MOH TB treatment guidelines.

Screening and OI Prophylaxis

All the 994 (100%) new patients had a TB symptom screen conducted at enrolment, and 118 of them had a sample collected for Xpert MTB/RIF assay or urine TB_LAM testing, however, TB results were available for only 86.4% (102/118) of the patients. From the 102, tests that were conducted, 27 patients tested positive for tuberculosis representing a positivity of 26.5% and a prevalence of 2,716 TB cases per 100,000 new HIV patients. All the 27 identified TB patients were initiated on TB treatment.

Regarding prophylaxis of opportunistic infections, all the 100% (994/994) patients enrolled in the clinic were initiated on Trimethoprim-Sulfamethoxazole (cotrimoxazole) prophylaxis while 65.5% (651/994) of them were initiated on a six-month course of Isoniazid or combined Isoniazid and Rifapentine for TB prevention in line with the national guidelines. Ninety-seven of the new patients were not eligible for TB Preventive Treatment. The reasons for ineligibility include being presumed to have TB (91) or having active TB disease (6) at the time of enrolment.

The management of AHD between newly enrolled and virally non-suppressed clients was compared and the analysis of the findings is illustrated in Table 4, below. There was no statistically significant difference in access to CD4 testing between the two groups (p = 0.587) with a coverage of 74.5% and 77.6% among virally non suppressed and new clients respectively. The median CD4 count was higher at 417 (IQ4: 195—721) among newly enrolled clients compared to virally non-suppressed clients 246 (IQR: 153–507) (p-value—0.014).

Table 4

Comparing newly enrolled and virally non-suppressed patients
	Newly enrolled	Virally non- suppressed	p-value
N	994 (92.9%)	76 (7.1%)
CD4 Access
No	253 (25.5%)	17 (22.3%)	0.587
Yes	741 (74.5%)	59 (77.6%)
AHD Status
No	778 (78.3%)	35 (56.5%)	< 0.001
Yes	216 (21.7%)	27 (43.5%)
Median CD4 result/mm3 (IQR)	417 (195—721)	246(153—507)	0.014
Accessed a serum CrAg test
No	85 (39.4%)	21 (77.8%)	< 0.001
Yes	131 (60.6%)	6 (22.2%)	< 0.001
Serum CrAg result
NEG	119 (90.8%)	6 (100.0%)	0.438
POS	12 (9.2%)	0 (0.0%)
Received Fluconazole
No	119 (90.8%)	5 (100.0%)	0.478
Yes	12 (9.2%)	0 (0.0%)
Pre-emptively treated with Amphotericin B and Fluconazole
No	982 (98.8%)	76 (100.0%)	0.335
Yes	12 (1.2%)	0 (0.0%)
Accessed TB LAM
No	120 (54.1%)	22 (78.6%)	0.010
Yes	102 (45.9%)	6 (21.4%)	0.010
TB Screening result
Completed TB treatment	21 (2.1%)	1 (1.3%)	0.555
Currently on TB treatment	3 (0.3%)	0 (0.0%)
No signs or symptoms of TB	876 (88.1%)	67 (88.2%)
Suspect TB - referred or sputum sent	94 (9.2%)	8 (10.5%)
Pre-emptive treatment for cryptococcal disease
No	75 (73.5%)	5 (83.3%)	> 0.999
Yes	27 (26.5%)	1 (16.7%)
Treated for TB
No	75 (73.5%)	5 (83.3%)	> 0.999
Yes	27 (26.5%)	1 (16.7%)
TB Assessment result
NEG	75 (73.5%)	5 (83.3%)	> 0.999
POS	27 (26.5%)	1 (16.7%)
Diagnosed OIs at enrolment
No	139 (93.9%)	7 (100.0%)	> 0.999
Yes	9 (6.1%)	0 (0.0%)
Medicines for OIs given?
No	139 (93.9%)	7 (100.0%)	> 0.999
Yes	9 (6.1%)	0 (0.0%)

None received Lumber Puncture

Serum CrAg testing and management of cryptococcal disease

Access to serum CrAg screening was higher among the newly enrolled HIV clients at 60.6% (131/216) compared to non-suppressed clients; 22.2% (6/27) (p < 0.001). Additionally, there was no significant difference administration of fluconazole between the two groups (p = 0.476). In both groups, the proportion of eligible HIV patients who received fluconazole for pre-emptive treatment of cryptococcal disease very low at 9.2% (12/131) for the newly enrolled and 0% (0/5) among the non-suppressed clients. None of the eligible patients received a lumber puncture for the diagnosis cryptococcal meningitis and none of the 12 patients with a positive serum CrAg received combination pre-emptive treatment with Amphotericin B or Flucytosine as recommended by the Ministry of Health AHD guidelines.

TB diagnosis and management

Symptom screening for TB was widely done for 100% of patients among both the newly enrolled and non-suppressed patients. Among the patients with AHD who had their CD4s less than 200 cell/ml, the proportion of patients who were tested for TB using urine TB_LAM assay was higher among the newly enrolled patients (45.9%) compared to the non-suppressed clients (21.4%), and this difference was statistically significant (p = 0.010). All the newly enrolled TB, HIV co-infected patients were initiated on TB treatment. There were no diagnosed cases of TB among the non-suppressed patients.

Prevalence of Advanced HIV Disease

Ever since the adoption of the WHO guidelines for clinical management of AHD in Uganda in 2020, this is the first published study to evaluate the prevalence and clinical management of new and non-suppressed HIV patients with AHD in Uganda. From the analysis of a sample of 994 treatment naïve HIV patients at a non-profit health facility in Western Uganda, the prevalence of ADH as defined by a CD4 cell count below 200 cells/µl or WHO clinical stage 3 or 4 disease was 20.4%. However, the prevalence differed in different groups, with males having a higher prevalence than the females (30.3% versus 13.9%) and children under 10 years having the highest prevalence at 65.2% while the least prevalence of AHD was among the adolescents 16.1%. These findings are consistent with those from several other studies which have demonstrated that males are more likely than males to present with AHD [8, 16–18]. A national HIV cohort study conducted in South Africa from 2004 to 2016 found that men were almost than twice as likely to enrol into care with AHD (23.1% vs 12.6%) [16]. The high AHD prevalence among men adds to the existing regional data revealing the failure of HIV programs to attract men [11].

This study also found that there was no difference in access to CD4 testing between the two groups is explained by similar quality of care between the treatment naïve and non-suppressed patients. This similar access to CD4 testing is attributed to Uganda Ministry of Health guidelines which highlight the importance of AHD screening in both the treatment naïve and non-suppressed patients because these groups are the ones who are at risk of subclinical OIs and require CD4 testing and comprehensive clinical examination to determine if they have stage 3 or 4 disease for further management [12].

Additionally, the high AHD prevalence among men is attributed to delayed diagnosis of HIV infection and linkage to care and treatment services. Several initiatives have been put in place throughout Africa to promote HIV testing and patient enrolment in ART, but little progress has been made in locating and enlisting men for HIV treatment. Attracting men for HIV testing has been the main barrier because very few men are found and consented to HIV testing services [19]. Even the increase of HIV testing and treatment under the test and treat strategy has mostly benefited more women than men, widening the gap between male and female life expectancy [19].

The high prevalence of AHD among both treatment naïve and non-suppressed patients is attributed to the fact that they are not on treatment, or they are non-adherent to the treatment or on ineffective treatment [18]. With the current Ministry of Health test and treat policy [20], where all HIV positive patients are started on HAART the prevalence of AHD is expected to reduce. Additionally, interventions for viral re-suppression for patients already on ART are within the policy in Uganda, therefore it is critical that these are implemented to fidelity to achieve HIV epidemic control. For-example, the WHO recommends that patients who are virologically unsuppressed receive at least three Intensive Adherence Counselling (IAC) to achieve viral suppression again [21]. This intervention is known to achieve viral suppression in over 70.5% of HIV patients with viraemia [21].

Management of Advanced HIV Disease

In this study conducted in the private not for profit facility in South Western Uganda, the prevalence of AHD was relatively high and this warrants provision of the WHO AHD care package [3]. The WHO package of care for AHD includes rapid ART initiation, screening, diagnosis and management TB and cryptococcal disease, cotrimoxazole prophylaxis, Isoniazid prophylaxis as well as adherence support [3]. In line with these recommendations, Meya et al, published guidance on the indicators and targets for monitoring implementation of the AHD package [12]. For-example, every patient with a positive HIV test should receive a CD4 count [12]. In addition, serum CrAg screening and LAM or Xpert MTB assay should be done for all those with s CD4 count less than 200 cells/ml and all those positive tests should started on the appropriate treatment in line with the national guidelines [12].

The findings from this study demonstrate an average access to AHD screening using CD4 testing among both the ART naïve (74.5%) and virally unsuppressed patients (77.6%). These finding are consistent with those from inpatient settings in Malawi (65.1%) and Botswana (85.9%) [9, 11]. Increasing access to CD4 testing is a great opportunity in the management of AHD as it helps in identifying asymptomatic patients with AHD and therefore prompt clinicians to initiate timely interventions [12]. To improve the diagnosis and management of AHD, HIV control programs ought to expand access to CD4 testing using interventions such as the Point of Care (POC) such as the VISITECT lateral flow assay, a semi-quantitative assay that reports CD4 results as a binary measure of less than 200 or greater than 200 cells/ml [22, 23].

This study also found that 100% of all newly diagnosed patients started ART within seven days from the date of diagnosis. In addition, 93% of the patients initiating ART received a dolutegravir-based regime which is the preferred first-line medication according to the WHO recommendations. ART is the most important intervention for preventing AHD related deaths [22]. It is critical to quickly start or restart ART with regimens that rapidly reduce viral load with low side effects, such as integrating inhibitor-based regimens regardless of the CD4 count or WHO clinical stage. Our findings differ from those from a similar study in Senegal where only about 33% of newly diagnosed patients-initiated ART within seven days of diagnosis [8]. This is largely attributed to differences in the study setting; whereas significant gains have been made on the UNAIDS 95 95 95 targets in Uganda and other East African countries, there has been slow progress in West and Central African countries where it is estimated that only about 48% of PLHIV know their HIV status [8].

Regarding prophylaxis of opportunistic infections, all the new enrolled HIV patients received Sulphamethoxazole-Trimethoprim (cotrimoxazole) prophylaxis while 6 in 10 patients who did not have TB symptoms received a six-month course of Isoniazid for TB prophylaxis in line with the national guidelines. These findings differ from those from a similar cross-sectional study in Senegal where only 65% new PLHIV received cotrimoxazole prophylaxis and none (0%) received Isoniazid Preventive Treatment [8]. The barriers to optimal Isoniazid uptake include Isoniazid stock-out, concerns about the development of Isoniazid drug resistance, low patient acceptance, provider concerns about drug interactions, limited of awareness of the eligibility criteria and a lack of commitment on the part of health managers to scale up the intervention [8, 24].

Uganda TB guidelines recommend the use of urine TBLAM in patients with AHD who are very ill and have CD4 counts less than 200 cells/ml [25]. Our findings also demonstrate that whereas access to TB symptom screening is universally done (100%), there is sub-optimal access to urine TBLAM testing with only 44.4% (96/216) laboratory evaluation and 23 TB patients diagnosed and treatment initiated. These findings are consistent with those from a 2022 Tanzanian retrospective cohort study of 2624 patient records, which assessed the implementation of the WHO TB-related AHD care package and its impact on HIV patient outcomes [10]. In Tanzania, among the 716 HIV patients with AHD, only 5% had diagnostic assessment using Xpert MTB assay; urine TBLAM assay was generally not done (0%) [10]. These findings illustrate that despite being a user-friendly test, pain-free and safe, TBLAM testing is not optimally done.

Evidence from a Randomised Controlled Trial in Tanzania and Zambia suggests that targeted CrAg screening and pre-emptive treatment with fluconazole reduces the incidence and mortality from cryptococcal meningitis [26]. However, the findings from this study in Uganda demonstrate that 6 in 10 patients with AHD had CrAg screening done, of which 12 patients were found to have a positive serum CrAg result and they all received pre-emptive treatment with fluconazole. Despite the Ministry of Health recommendation to conduct a lumber puncture and CSF CrAg for all patients with a positive serum CrAg, none of the patients had a lumber punctured done. These findings are consistent with those from another study in Uganda which evaluated implementation of a cryptococcal antigen screening program in Central and Southwestern Uganda which found that CrAg screening was done for 71% of the AHD patients, 83.9% were initiated on pre-emptive treatment with fluconazole, and 69.6 had a lumber puncture done [27]. These findings demonstrate significant successes in CrAg screening as well as some gaps along the cryptococcal disease management cascade.

Integration of routine CrAg screening for patients with AHD and pre-emptive treatment with fluconazole into HIV programs is cost effective and is associated with reduced occurrence of cryptococcal meningitis and an overall reduction of HIV related deaths [27]. In a Uganda cost-effectiveness analysis model for evaluating the national cryptococcal screening program, it was found that, CrAg screening and treatment saved 7320 lives at a cost of $459 per life saved. On the other hand, without CrAg screening, the cost of one week treatment of a patient with cryptococcal meningitis using Amphotericin B and Flucytosine is $1861 [28]. This makes CrAg screening and pre-emptive treatment with fluconazole more cost-effective than treatment of established meningitis [12, 28].

Barriers and facilitators to AHD Screening and management

A qualitative study conducted at a secondary referral hospital in Malawi found the following to be barriers to optimal delivery of a complete AHD package including screening, prophylaxis, diagnosis and management [29]. These include complexity of the intervention, weak coordination of work, inadequate resources to scale-up point of care diagnostic services for AHD, and knowledge and information gaps among service providers [29]. Implementation of AHD was reported by providers to be cumbersome requiring the involvement of different departments, several laboratory investigations which prolong patient waiting time. Each newly diagnosed HIV patient had to go through several tests including CrAg and TBLAM if CD4 is less than 200 cell/ml; before they were linked to treatment [29].

The lack of resources of AHD screening and management was also reported as a barrier by Mithi et al. These resources included posters, testing algorithms or Standard Operating Procedures, laboratory equipment such as centrifuges, pipettes, and waste management facilities as well as lack of training on how to conduct point of care tests such as TBLAM and CrAg [29]. Furthermore, in Uganda, Lofgren et al, found challenges of inadequate supply of medicines including fluconazole which affected the quality of AHD care [30].

Still, in Malawi, the inadequate coordination of work was attributed to the long distance between the ART clinic and the laboratory which caused loss of patients between the two departments. Additionally, the absence of communication systems such as a telephone hindered communication between the different teams and departments thus compromising service delivery [29]. This information is helpful for health managers to identify where the bottlenecks are and guides in the development of a mitigation plan to address the barriers.

The possible facilitators for optimal implementation of AHD screening, diagnosis and management include availability of policy documents including guidelines and Standard Operating Procedures, adequate external support by the Ministry of Health and PEPFAR implementing partners in the form of human resources, data collection tools, program review meetings, as well integrated mentorships and supportive supervision [29].

Additionally, the presence of trained AHD implementation leads who also served as ART focal persons helps to facilitate successful implementation [29]. Similarly, in Uganda, selecting a focal point person for CrAg testing at each health facility was helpful. This staff was responsible for following up patients who tested positive for CrAg for timely assessment and treatment [30].

The other facilitators reported in health facilities in Uganda include having an appropriate quantity of CrAg testing kits, having positive interactions between trainers and clinic staff, and training of providers about cryptococcal disease [30]. This information on the facilitators is helpful for health managers and policy makers to identify areas which need to be enhanced for successful implementation of the intervention.

Study strength and limitations

This study had several strengths, first, this study used a representative sample of 994 of treatment naïve patients who were enrolled at the TASO clinic. The study utilized secondary data which was routinely collected and entered the national electronic medical records system and updated weekly. This made the process of data acquisition easier considering the short research timeline.

Secondly, the data were valid because they were generated by a team of qualified and trained health workers including medical officers, clinical officers, counsellors, laboratory staff and nurses. These health workers had training in advanced HIV disease management and had medical licenses by their respective professional bodies. Additionally, validity of the tests conducted was ensured through internal and external quality assurance mechanisms coordinated through the Uganda Virus Research Institute and the National TB and Reference Laboratory.

There is no published study in Uganda that has evaluated the current practices in the management of AHD considering the WHO and Ministry of Health recommendations. This study elucidates the level of implementation and adherence to current standards for AHD and highlights the gaps along the cascade that the government need to address to improve implementation of these guidelines to fidelity.

Limitations

This study had some limitations. This study being a descriptive cross-section study means that the study utilized data at one specific point in time from January 2020 to December 2022 after the integration and roll-out of AHD guidelines. This therefore means that findings of this study are likely to change with time as the AHD interventions are scaled-up and adopted at more health facilities. Also, this being a retrospective review of patient records, is subject to information bias because of incorrect documentation or missing data (lack of documentation). This challenge was mitigated by verifying the electronic data with paper-based registers and any missing entries were filled.

Additionally, some categories of clients, such as those re-engaging into care after interruption in treatment were not included in this analysis since there was no standardized system of capturing AHD screening and management data for this category of clients in health facilities. Lastly, this study was conducted in only one high volume nonprofit health facility, therefore, the findings of this study may not be generalizable nor be used to make inferences about the status of AHD screening and management practices in other settings in Uganda, because: first, patients attending nonprofit health facilities may have different characteristics than those attending public health facilities, second, the clinical practices may also differ in different settings; third, urban and rural implementation may also differ due to unique health system challenges in the rural settings.

This study assessed the prevalence and clinical management of advanced HIV disease at an urban high volume non-profit health facility in Southwestern Uganda. We found that although the prevalence of AHD was high especially among the males, several missed opportunities were found in the AHD package of care which could slow progress in reducing HIV related morbidity and mortality. Interventions for reducing HIV related morbidity and mortality need to integrate the screening, identification and treatment of PLHIV with AHD, provide prophylaxis, diagnosis and treatment of OIs, track HIV patients who are lost from care, and strengthening mortality surveillance [22]. Such efforts include strengthening clinical assessments and diagnostics to be able to differentiate those with low CD4 counts and provide tailored package for those with AHD, scale-up integrase inhibitor-based ART regimes as dolutegravir, and strengthen the prevention and management of tuberculosis and cryptococcal disease which are the leading causes of HIV-related deaths among patients with AHD [22].

Recommendations

It is necessary to increase access to AHD services at lower-level healthcare facilities by increasing AHD screening, diagnosis, and treatment at primary healthcare facilities. Using point-of-care diagnostics like TBLAM strips, serum CrAg strips, PIMA or VISITECT CD4 tests, which distinguish between CD4 counts below and above 200cells/ml using a strip, is one way to do this. These exams are simple to use and don't require extensive training to administer.

Our findings of the relatively high prevalence of AHD suggest that HIV control programs need to purposefully implement targeted HIV case finding approaches to maximize early diagnosis and treatment initiation, and these interventions should be customized to the target populations to be reached to close the ART coverage gaps. For example, the high prevalence of AHD among men calls for client centred interventions such as health education for men about HIV, community-based HIV testing, testing men who escort their partners for antenatal care, self-testing and HIV testing incentives [19].

Need for further research.

There is a need for further research on the barriers and facilitators to implementation of AHD management guidelines in Uganda to guide policy makers at the Ministry of Health and health managers at lower levels to develop strategies to mitigate these bottlenecks as well as enhance the facilitators to implementation.

Also, further research is needed on the health system readiness to support implementation of these WHO recommendations. Our study picks-up areas around the AHD cascade where there are gaps, but it doesn’t go into the health system issues affecting implementation. For an intervention to be effective, it must be carried out within the framework of a strong health system, one that has sufficient and trained human resources, a strong supply chain management system for essential commodities, funding, strong health information systems, and the leadership to move the intervention forward. Therefore, more research is needed to understand the health system readiness to support implementation of the AHD intervention package.

Lastly, there is insufficient evidence on cost-effectiveness of the AHD package of interventions. Two studies in Uganda and one in Malawi have so far evaluated the cost-effectiveness of implementing a cryptococcal antigen screening program, which is only one of the packages of AHD care [9, 28]. Therefore, more research is needed on the cost-effectiveness of AHD screening and management, covering the entire package of care.

AHD

Advanced HIV Disease

ART

Antiretroviral Therapy

CrAg

Cryptococcal Antigen

PLHIV

People Living with HIV

TASO

The AIDS Support Organization

TBLAM

TB Lipoarabinomannan assay

Ethics approval and consent to participate.

Ethics clearance was obtained from TASO Research Ethics Committee (TASO-2023-220) while administrative approval to obtain the dataset was obtained from the Executive Director of TASO Uganda through the TASO REC administration. All patient-identifying information such as names, telephone contacts, or physical addresses that would allow patient identification was removed from the dataset prior to analysis. To protect patient privacy, distinct identification numbers (ART numbers) were used for each individual record.

Consent for publication.

Not applicable.

Availability of data and materials

The dataset used in the current study are available from the corresponding author on reasonable request.

Competing interests

All authors declare no competing interests.

Acknowledgement

I am grateful for the University of Manchester Equity and Merit Scholarship program support in funding my masters training. Without this training, this research would not have been possible. We also thank The AIDS Support Organization for providing the necessary support in accessing the approvals and data required for the study.

Authors contributions

PT and IG conceptualized and designed the research study. PT pursued all approvals for the study and analyzed the data with technical assistance from IG. PT also developed the initial version of the manuscript, and the final version was approved by both authors. IG provided overall oversight of the study.

Funding

This study was funded through personal savings.

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No competing interests reported.

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Clinical management of patients with advanced HIV disease at The AIDS Support Organization, Mbarara clinic in Southwestern Uganda: a retrospective review of patient records

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Version 1

Abstract

Figures

Background

METHODOLOGY

Study variables and operational definitions

Data collection

Laboratory procedures

Data management and analysis

Ethical considerations

RESULTS

Characteristics of study participants

AHD management practices

Screening and OI Prophylaxis

None received Lumber Puncture

Serum CrAg testing and management of cryptococcal disease

TB diagnosis and management

DISCUSSION

Prevalence of Advanced HIV Disease

Management of Advanced HIV Disease

Barriers and facilitators to AHD Screening and management

Study strength and limitations

Limitations

Conclusion

Recommendations

Abbreviations

Declarations

References

Additional Declarations

Supplementary Files

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