ABSTRACT.
Tuberculosis (TB) is the leading cause of death among people living with HIV (PLWH). Limited TB knowledge has been associated with delayed TB diagnosis and low adherence to TB treatment. A cross-sectional study was conducted among PLWH at the largest HIV-referral center in Lima, Peru, to describe TB knowledge among PLWH and potential associated sociodemographic factors. Participants answered a self-administered survey on TB knowledge, which consisted of five questions about TB cure, transmission, treatment, symptoms, and prevention. Of 179 PLWH enrolled, most participants did not know that isoniazid (85%) and antiretrovirals (78%) are preventive measures for TB, and 56 (31.3%) knew that TB can be asymptomatic in PLWH. We did not find statistical differences in TB knowledge based on gender, education, marital status, and time on HIV care. We identified important gaps in TB knowledge among PLWH. Addressing these gaps could empower PLWH to reduce their TB risk.
In 2020, tuberculosis (TB) was the second leading cause of death by a single infectious agent worldwide.1 Approximately 10 million people developed TB, and TB caused 214,000 deaths among people living with HIV (PLWH).1 In Peru, 38,000 new cases of TB and 2,400 cases of TB-HIV coinfection were estimated in 2020.2
Even though TB accounts for one-third of HIV related deaths, 61% of the people diagnosed with TB knew their HIV status, and 39% of newly diagnosed PLWH received TB preventive treatment in 2020.1 Studies among PLWH in Indonesia,3 Thailand,4 and India5 have reported limited knowledge on TB symptoms, treatment, and prognosis and lack of knowledge of TB. Limited TB knowledge among PLWH has been associated with delay in TB diagnosis6 and poor adherence to TB medication,7 which can increase morbidity and mortality. Furthermore, gender, education, and marital status have been associated with lack of knowledge of TB among PLWH.5 In Peru, studies have described poor knowledge on TB among hospital outpatients and among household contacts of TB patients.8,9 However, TB knowledge has not been quantified among PLWH in Peru, despite their increased risk of TB. This study measured TB knowledge among PLWH in Lima, Peru, and explored statistical differences between sociodemographic factors.
This study was part of a cross-sectional study carried out at a large third level hospital located in a peri-urban area in Lima, Peru (catchment area of 2,682,608 inhabitants), and it provides care to the largest number of PLWH in Peru.10 Adult PLWH enrolled at the HIV program were invited to participate between November 2016 and July 2017, while they waited for viral load and CD4 tests (routine tests for all PLWH in Peru). We included those who consented to participate completed a self-administered survey of five questions addressing TB knowledge. The questions were based on published studies4,5 and in consultation with infectious diseases specialists who recommended adding two questions: one on TB prevention and one on TB transmission. The questions were piloted with six PLWH to determine clarity, any potential discomfort, or alternative responses. We inquired on the recognition of TB risk in presence or absence of specific symptoms, the risk of TB transmission TB prevention, and TB treatment and cure. Percentages were used to describe categorical variables (gender, education status, marital status, and time on HIV care) and median and interquartile ranges (IQR) for continuous variables (TB knowledge, age and time on HIV care).
A score was created to explore statistical differences between TB knowledge and some sociodemographic characteristics of participants. Participants received 2 points for replying correctly to the questions with a single correct answer (on TB cure, transmission, and treatment). For the questions with more than one correct answer (on symptoms and prevention), participants received 2 points if all correct items were marked, 1 point if they marked some but not all correct options, and 0 points if they marked an incorrect answer. The maximum possible score was 10. Nonparametric tests (Mann–Whitney and Kruskal–Wallis tests) were used to compare statistical differences between the TB knowledge of sociodemographic characteristics of participants (gender, education status, marital status, and time on HIV care, categorized as < 12 months and ≥ 12 months).5 Associations with a P < 0.05 were considered significant.
The study was approved by the Ethics Committees from Universidad Peruana Cayetano Heredia and Hospital Cayetano Heredia. All participants gave their written informed consent and received a booklet with the correct answers upon completion of the survey.
Of 255 eligible participants who were invited to participate, 50 (19.6%) declined participation and 26 (10.2%) did not complete the TB questionnaire and were not included in the analysis. Of the 179 participants included, 53 (29.6%) were female, the median age was 36 years (IQR 27–44), 50 (27.9%) were married or cohabiting, six (3.4%) divorced, 111 (62.0%) single, and 12 (6.7%) widowed. Most participants (49.7%, N = 89) had completed high school, 13 (7.3%) had completed primary school, and 77 (43.0%) had completed higher education. The median time between the participant’s enrollment in the HIV program and the study interview was 4 years (IQR: 1.7–7.6).
The answers to each question regarding TB knowledge are presented in Table 1. Seventy-three (40.8%) participants recognized at least two symptoms related to TB, and 16 (8.9%) recognized all of them. The most common combination of TB symptoms recognized was cough with weight loss (N = 99, 55.3%). Isoniazid preventive therapy (IPT), antiretroviral therapy, and avoiding contact with a person with active TB were all three recognized as strategies to prevent TB by six (3.4%) participants; eight (4.5%) recognized IPT and antiretroviral therapy. Table 2 shows the analysis of the sociodemographic characteristics associated with TB knowledge. We found no statistical differences in TB knowledge and participants’ gender, marital status, and educational status. Participants who were in HIV care ≥ 12 months had slightly higher TB knowledge than participants who were on HIV care < 12 months, although this was not significant (P = 0.07).
Table 1.
Knowledge related to TB among people living with HIV in a referral center in Lima, Peru, 2016–2017 (N = 179)
| Knowledge related to TB | n (%) |
|---|---|
| Is TB is a curable illness | |
| Yes | 149 (83.2) |
| No | 11 (6.2) |
| Did not know | 17 (9.5) |
| Did not answer | 2 (1.1) |
| TB can produce the following symptoms* | |
| Cough for 15 days or more | 144 (80.5) |
| Cough even for some days | 22 (12.3) |
| Night sweats | 71 (39.7) |
| Fever | 76 (42.5) |
| Weight loss | 90 (50.3) |
| TB can be asymptomatic | 56 (31.3) |
| Does not know | 6 (3.4) |
| TB can be transmitted by* | |
| Being in contact with an untreated TB patient | 127 (71.0) |
| Poor nutrition | 91 (50.8) |
| Did not know | 14 (7.8) |
| TB can be prevented through* | |
| Vaccination | 55 (30.7) |
| Good nutrition | 110 (61.5) |
| Antiretrovirals | 39 (21.8) |
| Avoiding contact with TB patients | 86 (48.1) |
| Taking isoniazid preventive therapy | 27 (15.1) |
| It is not possible to prevent TB | 3 (1.7) |
| Did not know | 19 (10.6) |
| TB is cured by | |
| Long treatment with multiples pills | 138 (77.1) |
| It cannot be cured | 10 (5.6) |
| Antitussive medication (cough medication) | 4 (2.2) |
| Without medication | 2 (1.1) |
| Did not know | 28 (15.6) |
TB = tuberculosis.
Participants could mark more than one answer; therefore, sum does not add to 100%.
Table 2.
TB knowledge score by participants’ sociodemographic characteristics among people living with HIV in Lima, Peru (N = 179)
| Sociodemographic characteristic | TB knowledge score median (IQR) | Two-sided P value* |
|---|---|---|
| Gender | ||
| Male | 7 (5–8) | 0.86 |
| Female | 7 (5–8) | |
| Education | ||
| No higher education (primary or secondary) | 7 (5–8) | 0.82 |
| Higher education | 7 (5–8) | |
| Civil status | ||
| Partnered (married or cohabitant) | 7 (5–8) | 0.87 |
| Not partnered (single, divorced, or widow) | 7 (5–8) | |
| Time in HIV care† | ||
| < 12 months | 6 (4–7) | 0.07 |
| ≥ 12 months | 7 (5–8) | |
IQR = interquartile range; TB = tuberculosis.
Calculated using the Mann–Whitney test.
Defined as time between HIV program enrollment and study interview.
This study, among PLWH in Lima, Peru, where TB incidence is moderate, found important knowledge gaps related to TB risk and care: most participants did not know that IPT (85%) and antiretrovirals (78%) are preventive measures for TB, and only 31% knew that TB can be asymptomatic in PLWH. Since 1998, Peruvian national guidelines recommends TB chemoprophylaxis with isoniazid for all PLWH for 12 months after being diagnosed with HIV and after ruling out active TB disease, which should be done even in the absence of TB symptoms.11
No statistical differences in TB knowledge were found between participants’ sociodemographic characteristics. This differs with previous studies among PLWH, which reported that gender and education were associated with lack of knowledge of TB among PLWH in India.5 The lack of statistical differences of TB knowledge between participants’ characteristics in our study may have alternative explanations related to the study design. It may have been due to measurement bias (because TB knowledge differs from knowing about TB and our survey was different that the one used in India) or sample bias (PLWH who are not enrolled in care may have better/worse TB knowledge), although almost 50% of PLWH enrolled in this study completed high school, similar to the percentage of adults living in Lima reported in the last national census (43%).12 Furthermore, we may have had insufficient sample size to detect statistical differences for these two factors.
Tuberculosis clinical manifestations among PLWH vary from classic symptoms (fever, night sweats, productive cough and weight loss) to subclinical TB (having none or almost no TB symptoms), the latter being more frequent in advanced HIV immunosuppression.13 In our study, only 31% of participants identified that TB can be asymptomatic, which is important considering that a recent review of found a 50% of subclinical TB in the general population, and this percentage may be higher among PLWH.14 Peruvian HIV guidelines recommend TB screening with sputum analysis, a chest X-ray, and a tuberculin skin test upon initiation of antiretrovirals11 and, thereafter, TB symptom screening (cough, fever, night sweats, and weight loss) and TB contact elicitation at every health facility encounter.11 If active TB is suspected, a chest X-ray and a sputum sample are taken.11 In our study, we found a high percentage of PLWH who did not know of the asymptomatic presentation of TB; healthcare providers should adhere to guidelines and perform periodic TB screening despite the absence of symptoms.
We found important gaps in TB prevention knowledge. Isoniazid preventive therapy is the only TB preventive therapy for PLWH recommended by Peruvian guidelines and is fundamental in preventing TB in PLWH because it reduces the risk in up to 60%.15 However, 85% of PLWH in our study lacked this knowledge, which can place a barrier to IPT uptake and adherence.16 Suboptimal adherence to IPT has been reported in PLWH in Lima: 47% of PLWH discontinued IPT before 6 months of initiation,17 and only 22% of the study participants knew that TB can be prevented through antiretrovirals, despite the decrease in TB incidence by the use of antiretrovirals.15 The limited knowledge about IPT and antiretrovirals among the study participants may have alternative explanations. Some patients may be more familiar with “antituberculosis drugs” or “TB preventive therapy” instead of “isoniazid preventive therapy,” and some participants may recognize the role of antiretrovirals on HIV specific outcomes (such as viral suppression) and in the prevention of opportunistic infections, but not on TB specifically. However, when the survey was piloted with six PLWH, they did not report any misunderstanding or alternative responses to these questions. We recommend interventions to improve this knowledge aiming to strengthen adherence to IPT and to antiretrovirals.
In this study, PLWH had gaps in TB knowledge. The WHO recognizes that improving health literacy is fundamental to empower patients in their own care and improve their health.18 This highlights the need to improve patient’s health literacy and disease-specific knowledge, especially in key populations such as PLWH. Interventions that inform on knowledge, attitudes, and practices regarding TB transmission, prevention, risk factors, and misconceptions have been found to be effective in increasing knowledge in trials in Nigeria and Indonesia.19,20 Considering the gaps in TB knowledge found in our study, the Peruvian HIV program and other organizations working to prevent and control HIV could implement interventions to improve TB knowledge on PLWH in Lima, Peru.
Our study was limited by our convenience sampling of PLWH retained in care. Persons who felt more comfortable with their knowledge might have been more likely to participate in the study and to finish the survey, which could have overestimated TB knowledge, and PLWH not retained in care may have lower knowledge than those retained. Furthermore, the TB knowledge score was not formally validated. Yet we developed the questions based on validated surveys that explored TB knowledge in PLWH4,5 and in consultation with infectious diseases specialists. Also, potential confounding factors, that have been associated with poor TB knowledge among PLWH (such as TB stigma)3,4 were not measured and could have impacted the associations explored in the analysis. Finally, the external validity of these results is limited, and the findings may be generalizable to PLWH retained in care in Lima, Peru. However, the findings from this study could be used for future studies in different populations and settings.
In Lima, where TB incidence is moderate and HIV prevalence is low, HIV-infected individuals that are coinfected with TB are 5 times more likely to die and less likely to be cured compared with noninfected individuals.21 This study found TB knowledge gaps among PLWH, emphasizing the need to implement educational interventions targeting PLWH in our settings to improve TB symptoms recognition and understand the importance of IPT, antiretrovirals, and general TB prevention care.
ACKNOWLEDGMENT
The American Society of Tropical Medicine and Hygiene (ASTMH) assisted with publication expenses.
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