Tuberculosis Stigma and Its Correlates among HIV-Positive People who Inject Drugs in Ukraine

Abstract

Background.

Tuberculosis (TB) is commonly stigmatized. Correlates of perceived TB stigma have not been assessed specifically among HIV-positive people who inject drugs (PWIDs). It is also unclear how perceived TB stigma intersects with other forms of stigma affecting this population. We aimed to evaluate perceived TB stigma, its correlates and its intersection with HIV and substance use stigma among HIV-positive PWIDs in Ukraine.

Methods.

Among 191 participants at three sites across Ukraine, we assessed stigma scores, socio-demographic, behavioral and health-related variables by TB status (history of active TB infection, history of latent TB treatment, no history of TB infection). We used self-reported history of latent TB treatment as a proxy for latent TB infection status. We used ordinary least squares to estimate factors associated with perceived TB stigma.

Results.

Lower perceived TB stigma scores were associated with latent TB treatment status (adjusted beta (aβ)=−0.2 [−0.3; 0.0], p=0.032). Higher perceived TB stigma scores were associated with higher substance use stigma scores (aβ=0.1 [0.0; 0.2], p=0.004). Depressive symptoms were common in this sample, though not significantly associated with TB status.

Conclusion.

History of latent TB treatment appears to impact beliefs about perceived TB stigma. Individuals who endorse higher substance use stigma are more likely to hold stigmatizing perceptions about people with TB. HIV-positive PWIDs with history of active TB infection or latent TB treatment commonly experience mental health distress. This stigma intersection needs further exploration in this population, including of its relation with mental health, to provide further insights for targeted interventions.

INTRODUCTION

Stigma is a social determinant of health that negatively impacts outcomes and perpetuates disparities.^1,2 Commonly stigmatized conditions, including tuberculosis (TB), HIV, and substance use disorders, are associated with significant unmet treatment needs.^3–5 Impacts of stigma from multiple stigmatized conditions are often correlated and synergistic; this construct is described as intersectional stigma.^2,6 For example, individuals with both HIV and TB report greater HIV-related stigma than individuals with HIV alone.⁷ Current literature calls for further work to better understand the effects of intersectional stigma on TB prevention and treatment success.⁶ Attention to stigma and its impacts can help make progress towards person-centered care (i.e., awareness of the personhood and priorities of patients, as well as the contexts in which they live). Building knowledge of how stigma impacts care is an important step in targeting interventions that empower marginalized patients.⁸

Stigma is a major barrier to eliminating TB.⁹ Common causes of TB-associated stigma include negative perceptions of TB’s relationship with HIV diagnosis,¹⁰ fear of infection,⁹ and perceived incurabilty.¹¹ TB stigma is associated with worsened socioeconomic outcomes¹² and social exclusion.¹¹ Different forms of stigma exist; one is perceived stigma, defined as an individual’s feelings about their stigmatized condition and their perceived experiences of being stigmatized by others.⁶ With some exceptions, investigations into perceived TB stigma are limited.^7,11,13 We posit that perceived TB stigma may also impact individuals with latent TB infection¹⁴ (i.e., no clinically manifested evidence of active disease), particularly those with other stigmatized conditions such as HIV¹⁵ and thus are potentially impacted by intersectional stigma.⁶ While impacts of perceived TB stigma on mental health are not well-articulated, general TB-related stigma is significantly associated with worsened mental illness.^16,17 Ongoing efforts to evaluate TB stigma in varying cultural contexts is needed.¹⁸

Understanding impacts of TB stigma is relevant in Ukraine, which has an estimated TB incidence of approximately 77 cases per 100,000 individuals.¹⁹ Ukrainians diagnosed with TB consider it a shameful disease and report socially isolating and withdrawing in order to cope with its effects.²⁰ Further, Ukraine has a HIV epidemic with increasing incidence rates, which results in a serious public health challenge when combined with its TB rates.²¹ Injection drug use accounts for a large proportion of HIV transmission in Ukraine, and people who inject drugs (PWIDs) are at heightened risk for TB infection.

This study aimed to investigate perceived TB stigma among a population of HIV-positive PWIDs across Ukraine. We described demographic, behavioral, and mental health characteristics among individuals by TB status. We hypothesized that negative mental health outcomes are associated with active TB infection or latent TB treatment status, as well as with higher perceived TB stigma levels.

METHODS

Study Setting

Data were collected at seven healthcare facilities (i.e., opioid agonist treatment (OAT) sites) in six regions of Ukraine. This project is a sub-study of a project that assessed care delivery methods of HIV and substance use treatments and their associations with stigma.²²

Participants

Three sub-groups of participants were eligible for inclusion: 1) HIV positive PWIDs with a self-reported a history of active TB infection treatment (diagnosed and received treatment); 2) HIV positive PWIDs who self-reported a history of latent TB treatment (i.e., received isoniazid preventive treatment but have never been diagnosed with active TB); and 3) HIV positive PWIDs that have never been diagnosed either with active or latent TB infection by self-report. Participants were allocated to sub-groups based upon responses to the following: Have you ever been diagnosed with TB? Which type of TB were you told you had? Have you ever received preventive therapy for tuberculosis with Isoniazid?

Eligibility criteria included age ≥18 years; lifetime history of drug injection (by self-report); HIV-positive status (by self-report); receiving opioid agonist treatment (OAT); and fluency in Russian or Ukrainian. The exclusion criterion was cognitive impairment.

Procedures

Data were collected from July through September 2017. An research assessor screened patients, obtained informed consent, and administered a survey at the OAT site. Data collected included demographic, behavioral (e.g., illicit drug use, alcohol use) and clinical (e.g., history of TB, CD4 cell count) characteristics of participants, in addition to perceptions of health care services and social support.²² Participants received 200 Ukrainian hryvnia as compensation for their time and transportation expenses.

Variables

The primary outcome was perceived TB stigma measured using the TB stigma scale.²³ We adapted the scale’s 11 item sub-scale that evaluated perceived community perspectives of TB (e.g., “some people may not want to eat or drink with friends who have TB”). As used by the scale developers,²³ aggregated raw TB stigma score was standardized to lie between 0 and 50, with higher scores representing higher levels of stigma.

In addition to demographic variables (see Table 1), we collected behavioral variables such as illicit drug use and unhealthy alcohol use (Alcohol Use Disorders Identification Test, short version (AUDIT-C) score²⁴). Mental health characteristics included questions about 1) past suicide attempts and 2) perceptions of feeling sad or depressed. We assessed HIV stigma (Berger Scale²⁵), substance use stigma (Substance Abuse Stigma Scale²⁶), and social support (modified version of the Duke University-University of North Carolina Functional Support Questionnaire²⁷). All variables were based on self-report.

Table 1.

Demographics, behavior variables, and mental health characteristic of study participants by TB history (active, latent, or no diagnosis) and comparisons by group.

Characteristic	Total (n=191) n (Column %)	A. History of active TB (n=45) n (Column %)	B. History of latent TB (n=76) n (Column %)	C. No TB history (n=70) n (Column %)	Group differences (p)
					Overall	A vs. B	A vs. C	B vs. C
Sex					0.39	0.62	0.90	0.62
Male	143 (75%)	36 (80%)	53 (70%)	54 (77%)
Female	48 (25%)	9 (20%)	23 (30%)	16 (23%)
Mean age (SD)	40 (7)	41 (6)	40 (7)	39 (7)	0.14	0.59	0.12	0.48
Marital Status					0.13	0.16	0.16	1.00
Married/partnered	80 (42%)	13 (29%)	35 (46%)	32 (46%)
Living alone	111 (58%)	32 (71%)	41 (54%)	38 (54%)
Education					0.17	0.30	0.30	0.84
Secondary or less	75 (39%)	23 (51%)	26 (34%)	26 (37%)
College or higher	116 (61%)	22 (49%)	50 (66%)	44 (63%)
Employment					0.08	0.15	0.14	0.78
Employed	78 (41%)	12 (27%)	33 (43%)	33 (47%)
Unemployed	113 (59%)	33 (73%)	43 (57%)	37 (53%)
Monthly income per capita ($)					0.65	0.85	0.85	0.85
$0–64	104 (54%)	27 (60%)	39 (51%)	38 (54%)
$64–385	87 (46%)	18 (40%)	37 (49%)	32 (46%)
Daily income below poverty line (≤$1.90)					0.06	0.11	0.12	0.84
Yes	77 (40%)	25 (56%)	26 (34%)	26 (37%)
No	114 (60%)	20 (44%)	50 (66%)	44 (63%)
Stable housing					1.00	1.00	1.00	1.00
Yes	179 (94%)	42 (93%)	71 (93%)	66 (94%)
No	12 (6%)	3 (7%)	5 (7%)	4 (6%)
Drinking behavior (AUDIT-C)					0.52	0.94	0.75	0.75
Hazardous drinking (score ≥3 for females and ≥4 for males)	46 (24%)	9 (20%)	17 (22%)	20 (29%)
No hazardous drinking	145 (76%)	36 (80%)	59 (78%)	50 (71%)
Opioid/stimulant use in the past 30 days					0.46	1.00	0.66	0.66
Yes	87 (46%)	19 (42%)	32 (42%)	36 (51%)
No	104 (54%)	26 (58%)	44 (58%)	34 (49%)
Median social support [25th percentile; 75th percentile]  (Scale from 10 to 40; higher score equals greater social support)	32 [28;38]	33 [28;38]	32 [27;38]	32 [28;36]	0.58	0.70	0.68	0.68
Do you often feel sad or depressed?					0.79	1.00	1.00	1.00
Yes	135 (71%)	33 (73%)	55 (72%)	47 (67%)
No	55 (29%)	12 (27%)	21 (28%)	22 (31%)
Missing*	1 (1%)	0 (0%)	0 (0%)	1 (1%)
Have you ever attempted suicide?					0.73	1.00	1.00	1.00
Yes	54 (28%)	12 (27%)	20 (26%)	22 (31%)
No	136 (71%)	33 (73%)	56 (74%)	47 (67%)
Missing*	1 (1%)	0 (0%)	0 (0%)	1 (1%)
How much of the time in the past 4 months have you felt “downhearted and blue”?					0.37	0.57	0.40	0.57
All/most of the time	70 (37%)	13 (29%)	27 (36%)	30 (43%)
Some of the time	67 (35%)	15 (33%)	28 (37%)	24 (34%)
A little/none of the time	53 (28%)	17 (38%)	21 (28%)	15 (21%)
Missing*	1 (1%)	0 (0%)	0 (0%)	1 (1%)
Mean perceived TB stigma (SD)  (Scale from 0 to 50; higher score equals greater stigma)	35 (7)	36 (6)	34 (7)	37 (7)	0.05	0.18	0.97	0.06
Mean HIV stigma (SD)  (Scale from 10 to 40; higher score equals greater stigma)	25 (4)	25 (4)	25 (3)	24 (4)	0.47	0.94	0.49	0.61
Mean substance use stigma (SD)  (Scale from 21 to 105; higher score equals greater stigma)	63 (12)	63 (11)	64 (12)	63 (12)	0.85	0.87	0.99	0.90

^*Missing data was excluded during hypothesis testing.

Measures were pilot tested among five participants in Kyiv prior to the study. We estimated reliability and factor validity for the perceived TB stigma scale in Ukraine (one factor, 11 items) with confirmatory factor analysis and Cronbach’s alpha: α= 0.89; comparative fit index (CFI) = 0.980, Tucker‐Lewis index (TLI) = 0.975, standardized root mean square residual (SRMR) = 0.109). Measures of factor validity and reliability for HIV stigma, substance use stigma, and social support scale were presented elsewhere. ²²

Data Analysis

We compared selected socio-demographic, behavioral and health-related variables among three sub-groups of participants representing different TB status using chi-square tests for categorical variables, t-tests for normally distributed numeric variables, and Kruskal-Wallis tests for numeric variables deviating from normal distribution. Ordinary least squares (OLS) were used to estimate factors associated with perceived TB stigma. We started with binary regressions. As sample size would not allow us to conduct adjusted analysis for all selected covariates, the adjusted model includes variables significant at p<0.05 in binary models, in addition to age, sex, employment and income that are common confounders. We assessed model assumptions to ensure that the OLS procedure produced the best possible estimates. Variance Inflation Factors (VIF) were estimated to test for multicollinearity using VIF>5 threshold. Level of significance was set at 5%. Analysis was done in R, version 3.5.2.²⁸

Ethics Approval

The Institutional Review Boards at Boston University Medical Campus, Miriam Hospital, and the Ukrainian Institute on Public Health Policy approved the study protocol and instruments. All study staff were trained on the study protocol, human subjects protection and participant assessment prior to recruitment.

RESULTS

Participant Demographic, Behavioral, and Mental Health Characteristics

We screened 198 PWIDs living with HIV for the study; 191 were eligible and included in the analysis (Table 1).²² Typical for the regional population, the sample was predominantly male (75%) with a mean age of 40 years (SD: 7 years). The majority of the sample reported living alone (58%), having a technical school degree or higher (61%), and were unemployed (59%). Median score for social support was 32 (interquartile range 28–38). There were no significant differences in participant demographic or behavioral characteristics either overall or by subgroup (active, latent, or no history of TB).

A majority of participants reported feeling frequently sad or depressed (71%) or downhearted (most of the time=37%; some of the time=35%). Over a quarter (28%) of the sample endorsed a past suicide attempt. There were no significant differences related to mental health characteristics either overall or by TB subgroup.

Perceived TB Stigma

Across all participant groups, the mean standardized TB stigma score was 35 out of 50 (SD: 7). Perceived TB stigma scores were lower among people with a history of latent TB treatment, compared to people with a history of active TB infection or without TB history; mean differences had marginal significance (p=0.05).

Factors Associated with TB Stigma

In binary regressions, higher perceived TB stigma score was associated with suicide attempts (β=3.5 [1.4; 5.6], p=0.001); feeling frequently downhearted and blue (β=3.1 [0.7; 5.5], p=0.011); social support (β=−0.2 [−0.3; 0.0], p=0.032); HIV stigma (β=0.5 [0.2; 0.7], p=0.001); and substance use stigma (β=0.2 [0.1; 0.3], p<0.001) (Table 2).

Table 2.

Factors associated with perceived TB stigma scores among HIV-positive PWIDs: OLS (n=191).

		Perceived TB stigma score
		Crude beta (95% CI), p-value	Adjusted beta (95% CI), p-value
TB history	History of latent TB (ref. history of active TB)	−2.2 [−4.7; 0.2], p=0.076	−2.6 [−5.0; −0.2], p=0.034
	Neither history of active TB nor latent TB (ref. history of active TB diagnosis)	0.3 [−2.2; 2.8], p=0.822	−0.2 [−2.6; 2.3], p=0.898
Sex	Male (ref. female)	0.6 [−1.6; 2.8], p=0.609	0.1 [−1.2; 3.2], p=0.371
Age, years		0.0 [−0.2, 0.1], p=0.546	0.0 [−0.1; 0.1], p=0.920
Marital status	Living alone (ref. married/partnered)	0.4 [−1.6; 2.3], p=0.714	-
Education	Secondary or less (ref. college or higher)	1.1 [−0.9; 3.1], p=0.276	-
Employment	Unemployed, student, home maker (ref. Employed full/part-time)	−0.1 [−2.1; 1.9], p=0.931	−0.9 [−2.9; 1.1], p=0.362
Monthly income	0–64 USD per household member (ref. 64–385 USD)	−0.3 [−2.2; 1.6], p=0.766	−0.7 [−2.7; 1.2], p=0.452
Poverty	Daily income per household member ≤1.90 USD (ref. >1.90 USD)	−0.3 [−2.3; 1.7], p=0.766	-
Stable housing	Yes (ref. no)	−3.0 [−7.0; 0.9], p=0.135	-
Drinking behavior (AUDIT-C)	Hazardous drinking: score ≥3 for females and ≥4 for males (ref. no hazardous drinking)	0.7 [−1.6; 2.9], p=0.568	-
Any opioid or stimulant drug use in the past 30 days	Yes (ref. no)	0.4 [−1.6; 2.3], p=0.717	-
Do you often feel sad/depressed?	Yes (ref. no)	1.8 [−0.3; 4.0]. p=0.089	-
Have you ever tried to kill yourself or attempt suicide?	Yes (ref. no)	3.5 [1.4; 5.6], p=0.001	1.7 [−0.5; 3.9], p=0.124
How much of the time in the past 4 months have you felt “downhearted and blue”?	All/most/a good bit of the time (ref. a little/none of the time)	3.1 [0.7; 5.5], p=0.011	1.3 [−1.2; 3.7], p=0.320
	Some of the time (ref. a little/none of the time)	0.8 [−1.6; 3.2], p=0.495	−0.2 [−2.6; 2.2], p=0.857
Social support		−0.2 [−0.3; 0.0], p=0.032	−0.1 [−0.2; 0.1], p=0.425
HIV stigma		0.5 [0.2; 0.7], p=0.001	0.2 [−0.1; 0.5], p=0.182
Substance use stigma		0.2 [0.1; 0.3], p<0.001	0.1 [0.0; 0.2], p=0.004

^*Values in bold indicate statistically significant associations.

After adjustment for age, sex, employment, income, mental health and social support, perceived TB stigma was linked to TB status (adjusted beta (aβ)=−0.2 [−0.3; 0.0], p=0.032 for history of latent TB treatment compared to history of active TB infection) and substance use stigma (aβ=0.1 [0.0; 0.2], p=0.004).

DISCUSSION

In this sample of PWIDs living with HIV, participants’ demographic and behavioral variables did not significantly differ by TB status. Variables of interest (sex, age, marital status, education, employment, monthly income, poverty level, stable housing, drinking behavior, drug use, and social support) were not associated with perceived TB stigma. This contrasts with previous findings that female sex,⁷ poor social support,¹³ and substance use¹³ are associated with perceived TB stigma. Unlike other studies, not all participants had direct, lived experience of TB diagnoses, which may account for this difference. However, all participants reported positive HIV diagnoses and were actively engaged in OAT; it is possible that these factors overshadowed the salience of TB diagnosis.

Individuals with history of latent TB treatment reported lower perceived TB stigma versus people either with a history of active TB infection or without TB. While individuals with latent TB infection commonly endorse internalized and perceived TB stigma,¹⁴ the perceived TB stigma scale might perform differently among PWIDs living with HIV who have had active TB infection and more experience with associated stigma (i.e., experiences that impact response patterns). Alternatively, as compared to individuals without history of TB infection, individuals with latent TB infection may have received TB education after engaging in treatment or may have had contact with others similarly diagnosed; both of these mechanisms have been shown to possibly mitigate stigma perceptions.²⁹ At the same time, individuals with diagnoses of latent TB infection may have been prevented from developing the more apparent, stigmatizing symptoms of active TB infection. Work to evaluate perceived TB stigma and its intersection with other forms of stigma among individuals with latent TB infection, with emphasis on scale psychometrics and measurement invariance, is an important next step.

Higher perceived TB stigma scores were not associated with poorer mental health outcomes. Others have suggested that individuals in stigmatized groups may find solidarity among their communities that buffers some of stigma’s negative impacts.³⁰ Resiliency, developed over time after managing intersectional stigma, may also impact these findings.³¹ The interplay of these factors may have particular relevance among this sample, as all participants had multiple stigmatized identities and yet were engaged in care; this may have strengthened perceptions of community support and taught strategies to cope with stigma.

Independent of perceived TB stigma, over 70% of individuals with a history of active TB infection or latent TB treatment reported feeling frequently sad or depressed. Respondents in these same groups also reported a history of past suicide attempts (27% and 26%, respectively). These high rates of mental health distress are noteworthy, particularly in consideration of the complex relationship between mental health, TB infection, and intersectional stigma. Stigma consistently has been shown to correlate with depressive symptoms,⁹ and co-occurring TB infection and depressive disorders results in worsened health outcomes compared to TB infection alone.³² In response to the sample’s high rates of mental health distress, we suggest that individuals diagnosed with TB infection receive improved routine screening of mental health symptoms through validated instruments and that treatment facilities assess the possibility of integrating mental health services in clinical settings. This might include offering brief psychoeducation and develop of referral mechanisms for severe cases of mental illness. Currently, there are extreme challenges accessing mental health care services in Ukraine, as less than 5% of individuals with a psychiatric disorder accesses treatment.³³ Thus, individuals diagnosed with TB infection in Ukraine will likely struggle to receive mental health care without increased research and funding.

We found that higher perceived TB stigma scores were associated with higher substance use stigma scores. In this specific population, perceived TB stigma intersects with substance use stigma not merely in an additive way.⁶ Individuals who experience stigma associated with one condition may be increasingly likely to report stigma associated with a second, in part due to sensitivity to stigma experiences.⁶ This may be relevant among this population, as stigma associated with substance use strongly affects individuals from the former Soviet Union,³⁴ and thus may have made participants increasingly likely to also endorse perceived TB stigma. Alternatively, intersectional stigma may be influenced by perceived (though not necessarily present) characteristics;⁶ in this sample, individuals who use substances may more readily perceive that the community assumes related diagnoses of HIV and TB infection. Finally, higher levels of perceived TB stigma may have different links with mental health impacts when other forms of stigma, such as HIV stigma, are also high.⁷

Limitations

There are several limitations that bear consideration. First, this study included only brief mental health measures that did not fully capture the breadth of relevant psychiatric symptoms. Nevertheless, even our limited measures found that participants endorsed symptoms of mental health distress, suggesting that ongoing efforts to treat mental illness is an important facet of effective TB treatment. Constructs related to mental health³⁵ and stigma¹⁸ are highly influenced by cultural knowledge, perspective, and language, and thus the measures may have imprecisely gathered data. While we assessed the psychometric properties of the tools used in this study, we recognize the need for continued validation of these measures.

We further note that participants self-reported their TB infection and treatment status. As we were unable to verify TB diagnosis by medical record review, it is possible that participants incorrectly reported their TB history or status. Additionally, history of receipt of preventive treatment for TB was used as a proxy to assign participants to the latent TB sub-group; it is possible that some participants may have conflated receipt of preventive treatment with active TB infection diagnosis. This could have impacted allocation to sub-group and subsequent outcomes in the analysis.

Some participants may have been reticent to disclose health information about TB infection, which could have similarly affected allocation to sub-groups. Nevertheless, the majority of participants in the study did report past TB infection status and other highly personal information, suggesting an overall willingness to report sensitive data. Finally, we did not evaluate the timing of participants’ TB infection diagnosis, and it is feasible that timing of diagnosis may impact recollection of experience of stigma.

Efforts that evaluate perceived TB stigma and mental health impacts in other settings, such as in TB-specific treatment programs, will be important to fully understand these relationships. Future efforts should also ensure adequate sample size, as we were not able to adjust for all potential confounders in our models.

Conclusions and Future Directions

Findings indicate that perceived TB stigma intersects with other stigma forms, specifically substance use stigma. Individuals diagnosed with TB infection, including latent TB infection, indicated experiencing mental health distress. Improved understanding of risk factors among vulnerable populations, specifically through the use of qualitative approaches, will inform targeted, contextualized future interventions. Addressing the burden of TB, HIV, and injection drug use will require innovative, integrated treatment mechanisms to improve general health and mental health outcomes across disorders, particularly as effective TB prevention and treatment is increasingly aligned with person-centered care.