Multidrug-resistant tuberculosis in Ho Chi Minh City: a retrospective study of 2,267 cases from 2011 to 2015

doi:10.21203/rs.2.12034/v1

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Multidrug-resistant tuberculosis in Ho Chi Minh City: a retrospective study of 2,267 cases from 2011 to 2015

https://doi.org/10.21203/rs.2.12034/v1

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published 22 Feb, 2020

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Background

Multidrug resistant tuberculosis (MDR-TB) remains a serious public health problem with poor treatment outcome. Predictors of poor outcomes vary in different health-care settings. Vietnam is among the 30 countries with high burden of MDR-TB. We aim to describe demographic characteristics and identify risk factors for poor outcome of MDR-TB in Ho Chi Minh City (HCMC), the most populous city in Vietnam.

Methods

This retrospective study included 2,267 patients who initiated MDR-TB treatment from 2011 to 2015 in HCMC. Treatment outcomes were available in 2,241 patients. Data was collected from standardized paper-based treatment cards and electronic records. Statistical analysis was performed using R program.

Results

Among 2,267 eligible cases, 60.2% were failure of category I or II regimen, 57.7% were underweight, 30.2% had diabetes mellitus and 9.6% were HIV positive. Notification rate increased 24.7% from 2011 to 2015.Treatment success rate was 73.3%. Risk factors for poor treatment outcome included HIV co-infection (odds ratio (OR): 2.92), advanced age (OR: 1.47 for every increase of 5 years for patients older than 60), having history of MDR-TB treatment (OR: 5.65), sputum smear grade scanty and 1+ (OR: 1.48), smear grade 2+ or 3+ (OR: 2.07), low BMI (OR: 0.84 for every increase of 1kg/m2 of BMI for patients with BMI<21).

Conclusion

Our study describes the increasing burden of MDR-TB in HCMC and the need for better drug resistance screening for all TB patients. Patients with HIV, high smear grade, malnutrition and history of previous MDR-TB treatment should receive additional care.

Infectious Diseases

multidrug resistant tuberculosis

retrospective

treatment outcome

risk factors

Vietnam

Multidrug resistant tuberculosis (MDR-TB), defined as tuberculosis (TB) with resistance to at least rifampicin and isoniazid, is a serious public health problem. In 2017, there were an estimated 558,000 incident cases and 230,000 deaths due to MDR/Rifampicin resistant (RR)-TB worldwide. Treatment of MDR-TB is lengthy, toxic and expensive, with success rates reported at 55% in 2017 [1]. HIV co-infection, low body mass index (BMI) and positive sputum smear are predictors of poor MDR-TB outcomes, but these predictors may vary in different health-care settings [3] [2] [4] [5] [6].

Vietnam is among high TB and MDR-TB burden countries. Its estimated incidence of TB in 2017 was 129 per 100,000 people. A national survey in 2011 showed resistance to any drug was 32.7% in new TB patients and 54.2% in previously treated patients [7]. The prevalence of MDR-TB was 4.1% in new patients and 17% in previously treated patients with 4900 estimated new cases annually countrywide [1]. Ho Chi Minh City (HCMC) is the most populous city in Vietnam (around 8 million people) and also the center for TB and drug-resistant TB management in Southern Vietnam. In 2009, the Vietnam National TB Programme initiated the Programmatic Management of Drug-resistant TB (PMDT) under the support of Global Fund (Switzerland) to provide free treatment and support for MDR-TB patients [3]. Pham Ngoc Thach hospital (PNTH) is a tertiary referral center for TB and lung diseases in Southern Vietnam, which provided treatment for 81% of registered MDR-TB patients in Vietnam in 2010 [8]. The number of patients enrolled in PMDT rapidly increased from 2010 to 2014; yet, the total number of MDR-TB patients enrolled for treatment in Vietnam in 2014 was still very low, with only a third of the estimated 5100 cases receiving treatment [3]. From 2011, all 24 district TB units (DTUs) of HCMC participated in the MDR-TB management. However, until now, there has been no information about the notification trend, treatment outcome and factors associated with poor treatment outcome of MDR-TB patients in HCMC. In this study, we retrospectively investigated the demographic characteristics and risk factors for poor treatment outcomes of MDR-TB in HCMC from 2011 to 2015.

Study setting and population

Patients were hospitalized in PNTH for 7 to 14 days to initiate treatment, and then referred to DTUs for outpatient follow-up. Treatment modalities did not change during the study time, with the standardized combination of 6 drugs for a total of 18 to 24 months of treatment [3].

Sputum samples from suspected MDR-TB patients or from patients with MDR/RR-TB detected by XpertMTB/RIF or line probe assay (LPA) were sent to the laboratory in PNTH for confirming MDR-TB by drug susceptibility testing (DST). Culture and DST in solid and liquid media were the main initial diagnostic method prior 2012. Pyrazinamide and ethambutol were components of standardized MDR-TB regimen, but detecting these drugs’ resistance were challenging because of unreliable phenotypic DST results [9]. Since 2012, GenoType MTBDRplus (Hain Lifescience GmbH, Germany - LPA) and XpertMTB/RIF (Cepheid, USA) were used to detect MDR/RR-TB.

We included all patients who initiated treatment with second-line drugs in HCMC under PMDT from January 2011 to December 2015. Patients who started their MDR-TB treatment after 2015 might not have treatment outcomes available at the time of data collection. We then excluded the patients who 1) had evidence of irrelevant diagnosed MDR either by DST, Xpert or LPA test, or 2) were enrolled in the STREAM trial [10] to receive a 9-month regimen, or 3) did not start treatment (Figure 1).

Data collection

Demographic and clinical information, radiographs, acid-fast bacilli (AFB) staining, DST results, treatment regimens and treatment outcomes were recorded into structured paper forms. To improve reliability, we collected data from both standardized paper-based treatment cards and electronic records and verified data during the data collection, entry and analysis processes.

Statistical analysis

Data analysis was performed using R program version 3.5.2 [11]. The baseline characteristics were summazied as number of cases and percentage for categorical variables and median with interquartile range (IQR) for continuous variables. We used Kruskal Wallis test to identify the change of median of age and BMI over 5 years, and Wilcoxon test to compare median BMI of diabetes mellitus (DM) and non-DM patients. Chi squared test was used to compare categorical variables.

We evaluated the association between poor treatment outcome and HIV co-infection, history of previous MDR-TB treatment, AFB smear grade and BMI by using a multivariable logistic regression model. The outcome is a binary treatment outcome variable with “success” (cured, completed) and “non-success” (death, failure, lost to follow-up ) as defined in [12]. The covariates were all the preceding risk factors. The model adjusted for potential risk factors of male gender, age and DM status. For variable age and BMI, the univariate analysis of the effect of age and BMI on treatment outcomes suggested to model them by index variable for age less than 60 years old and BMI greater than 21 kg/m², and linear patterns for age greater than 60 years old and BMI less than 21 kg/m². To minimize bias caused by missing data, we imputed them by using multiple imputation by chained equation (“mice” package in R[13]) and we performed multivariate logistic regression models using both imputed data analysis and complete case analysis. There were only small differences in the results between the two analyses. Therefore, we presented the results of imputed data analysis and provided non-imputed results in the supplementary data

Ethical approval

The study was approved by Institutional Review Board at PNTH and Oxford Tropical Research Ethics Committee, UK. Individual written informed consent was waived by the Institutional Review Board because this is a retrospective collection and data were recorded and analyzed anonymously.

Characteristics of MDR/RR-TB patients

From 2,395 electronic records and 1,913 paper-based records available, 2,267 MDR/RR-TB cases were included (Figure 1). Twenty-three patients had 2 episodes of treatment during the study time, including 8 relapse cases, 13 retreatment after lost to follow-up cases and 2 retreatment after failure cases. Baseline characteristics are presented in Table 1. Of 2,267 cases, the median age was 43 years (IQR: 33-53 years) and did not change during 2011 to 2015 (p = 0.481), 1,716 (75.7%) were male, 128 (5.6%) were registered as new patients, 679 (30%) were relapse cases, 1,364 (60.2%) were failure of either category 1 or 2 treatment regimens. A total of 205 patients (9.6% of tested patients) were HIV co-infected; of these, 33 (16.1%) were registered as new patients, 22 (10.7%) had extra-pulmonary MDR-TB including 10 MDR-TB meningitis cases (4.9%), which was higher than in non-HIV patients (p<0.001). Among 1,816 cases with BMI information available, 57.8% was classified as underweight with 25.1% severe underweight. Median of BMI did not differ during 5 years (p = 0.966). DM status was available for 1,189 patients (52.5%), 359 of whom (30.2%) had DM. Median BMI of DM patients (20.0 kg/m²) was higher than non-DM patients (17.8 kg/m²) (p<0.001) and HIV co-infection in DM patients (0.9%) was lower than in non-DM patients (9.8%) (p<0.001).

Drug resistance pattern

Table 2 outlines the drug resistance pattern of MDR-TB patients. Of the 503 DST results from 491 patients that were retrievable, 10 patients had 2 DST at different time points, 1 patient had 3 DST. Of 491 patients with DST, 55.0% and 63.0% had resistance to pyrazinamide and ethambutol, respectively. Fluoroquinolone resistance and any injectable agent resistance accounted for 12.7% and 8.1%, respectively. Among 378 patients with DST for second-line drugs, there were 63 (16.7%) pre extensively drug-resistant (XDR) TB and 8 (2.1%) XDR-TB patients.

MDR-TB trend

Figure 2 shows increasing temporal trend from 2011 to 2015 for both the absolute number of cases and the notification rate per 100,000 population. Numbers of notified MDR/RR-TB patients decreased by 9% between 2011 and 2012, and increased an average of 15.9% annually from 2012 to 2015. Number of MDR-TB cases and notification rate increased 41.0% and 24.7% from 2011 to 2015, respectively.

Treatment outcomes

Table 3 summarizes the treatment outcomes of 2,241 MDR-TB patients whose treatment outcomes were retrievable. Successful outcomes were achieved in 1,642 (73.3 %) patients, including 55.6% cured and 17.7% completed. Among those with unsuccessful outcomes, 10.1% died, 5% failed treatment and 11.6% lost to follow-up. In HIV patients, 49 (23.0%) died, 8 (3.9%) failed the treatment and 42 (20.5%) lost to follow-up. The success rate for 64 pre-XDR-TB patients was 53.1% while 14.1% died, 23.4% failed treatment and 7.8% lost to follow-up. Of 8 XDR-TB patients, 1 (12.5%) cured with a bedaquiline regimen, 2 (25%) died including 1 who received bedaquiline regimen and 5 (62.5%) failed.

Risk factors for poor outcomes

We evaluated the association between poor treatment outcome and HIV co-infection, history of previous MDR-TB treatment, AFB smear grade and BMI. We also included potential risk factors of male gender, age and DM status into multivariate logistic regression model.

Independent risk factors for poor outcomes were older age (OR for every increase of 5 years when patients are older than 60: 1.47, 95% CI: 1.19-1.80, p<0.001), HIV co-infection (OR: 2.92, 95% CI: 2.06-4.14, p<0.001), a history of MDR-TB treatment (OR: 5.65, 95% CI: 2.93-10.93, p<0.001), AFB positive (OR: 1.48 for low smear grade (1+ and <1+), 95%CI: 1.08-2.03, p=0.01 and OR: 2.07 for high smear grade (2+ and 3+), 95%CI: 1.49-2.89, p<0.001), and low BMI (OR: 0.84 for every increase of 1kg/m2 for patients with BMI<21, p<0.001) (Figure 3).

This is the first study to describe the characteristics and identify the risk factors for poor outcomes of MDR-TB in HCMC, Vietnam. Although the incidence of TB in Vietnam has been declining [1], MDR-TB cases are on the rise. The improvement in diagnostic technologies with the introduction of Xpert in the end of 2012 and changes in MDR-TB diagnostic policies might be part of the reasons for the increasing numbers of notified cases, together with the ongoing transmission of drug-resistant TB. High rates of failure of regimen 1 (22.6%) and regimen 2 (37.6%) in MDR-TB patients reflect the insufficient screening for drug resistance prior treatment of new and retreated patients, and highlight the need for drug resistance screening for all TB patients regardless of their TB history.

We found high rates of resistance to pyrazinamide (55.0%) and ethambutol (63.0%) in our MDR-TB cohort, as reported by other studies [14] [15]. This may reflect the fact that the majority of MDR-TB patients (94.3%) already had exposure to first line anti-TB drugs and might have developed resistance to pyrazinamide and ethambutol during previous treatment. This questions the effectiveness of emperical use of these two drugs in the standardized MDR-TB regimen [16] and emphasizes the need for an approved genotypic DST to rapidly detect pyrazinamide resistance.

Resistance rates to fluoroquinolones (12.7%) and injectable agents (8.1%) were comparable to those of the survey in Vietnam in 2011 [17] but lower than in South Korea [14] and average global rates [1]. Resistance to second-line drugs were high although they are not used in the regimen 1 and 2. It might partly due to easy access to antibiotics without prescription in Vietnam [18].

HIV co-infection, positive baseline AFB smear, older age and previous treatment with second-line drugs are main risk factors for poor treatment outcomes in our cohort, which were also observed in cohorts in Estonia, Latvia, Philippines, Russia, Peru [4], Ukraine [2]. Malnutrition was common (57.8%) and also a risk factor for poor outcome (OR: 0.81 for every 1kg/m² increase of BMI). Low BMI might be a consequence of severe disease and low social-economic status, which are well-known risk factors for poor outcome of TB. PMDT should focus on nutrition support to improve treatment outcomes.

The prevalence of DM in our cohort (30.2%) was double that of other TB patients (13.7%) in Hanoi, Vietnam [19] and was almost 6 times higher that of general Vietnamese population in 2013 (5.4%) [20]. Although DM is a known risk factor for poor treatment outcome of TB, developing MDR-TB and reducing sputum conversion rate during MDR-TB treatment [21] [22] [23], whether DM also leads to poor treatment outcome of MDR-TB is still controversial [21] [24] [25]. After adjusted for other factors, DM was not an independent risk for poor outcomes in our cohort, which agrees with pooled data analysis from cohorts in Latvia, Korea and Italy [26]. Due to the unavailability of DM treatment information, we do not know whether the effect of DM on MDR-TB treatment was influenced by the use of metformin, a hypoglycemic agent that might improve TB treatment outcomes [27] [28]. Despite this limitation, DM is a common but neglected comorbidity in MDR-TB patients and should be screened for prior MDR-TB treatment.

This study has several limitations. This is a retrospective study and some records were irretrievable at the study time. Demographic information and records of smear, culture and DST was not completely recorded on the electronic database. The majority of patients (78.4%) did not have DST results, and we could not include drug resistance information into multivariate logistic regression models. Finally, the information on smoking and alcohol use were not available in our cohort, although they are known risk factors for poor outcome [29] [30]. Therefore, a prospective study is necessary to provide a comprehensive assessment of risk factors for poor treatment outcome of MDR-TB.

Despite these limitations, the present study emphasizes the increasing trend of MDR-TB in HCMC between 2011 and 2015 and the need for drug resistance screening for all TB patients. Patients with HIV, high smear grade, malnutrition and history of previous MDR-TB treatment are at high risk of poor outcomes and should receive additional medical care.

MDR: Multidrug resistant tuberculosis TB: tuberculosis RR: Rifampicin resistant BMI: body mass index HCMC: Ho Chi Minh City PNTH: Pham Ngoc Thach Hospital PMDT: Programmatic Management of Drug-resistant Tuberculosis DTU: district tuberculosis unit LPA: line probe assay DST: drug susceptibility testing AFB: acid-fast bacilli IQR: interquartile range OR: odds ratio DM: diabetes mellistus XDR: extensively drug resistantce

Acknowledgements

We would like to thank Le Van Ngo, Tran Minh Khuyen, Pham Thi Thuy Lieu, Nguyen Ngoc Phat, Nguyen Van Hoi, Nguyen Van Thom, Nguyen Van Nghia, Phan Hong Liem, Ly Hong An, Chung Thi Bich Dao, Hoang Van Thang, Nguyen Thi Nguyet Thu, Truong Ngoc Dai, Nguyen Chi Thien, Nguyen Hong Nguyen, Vo Van Tam, Nguyen Trung Hoa, La Duc Du, Nguyen Hoang Tu, Tran Dinh Thu, Tran Quynh Ly, Tran Thi Mai An, Truong Thi Nhu Thuy, Ho Van Nho, Phan Thi Minh Tan, Vo Van Hung and all their staff in 24 DTUs in HCMC; all doctors and nurses of PNTH; and Nguyen Lam Vuong for his helpful advice on statistical analysis.

Funding

This work was supported by the Wellcome Trust Intermediate Fellowship [206724/Z/17/Z to N.T.T.T] and the Wellcome Trust Major Overseas Program Funding [106680/B/14/Z to G.T].

Availability of data and materials

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

Authors’ contributions

GET and NTTT conceptualized, designed and revised the manuscript. LHV designed the study, collected, interpreted the data, and draft the manuscript. NHL, TVV, NTMT and DTMH participated in the design and data collection. PTP, VTS and NTH coordinated the study and collected the data. DNV and LTHN participated in data analysis and revised manuscript. All authors read and approved the final manuscript.

Ethics approval and consent to participate

The study was approved by Institutional Review Board (IRB) at PNTH and Oxford Tropical Research Ethics Committee (OxTREC), UK.

Competing interests

All authors declare no competing interests.

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Due to technical limitations, tables are only available as a download in the supplemental files section.

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Journal Publication

published 22 Feb, 2020

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Editorial decision: Major revision
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Review #3 received at journal
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Reviewer #3 agreed at journal
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Review #1 received at journal
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Review #2 received at journal
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Reviewer #2 agreed at journal
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Reviewer #1 agreed at journal
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You are reading this older preprint version

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Multidrug-resistant tuberculosis in Ho Chi Minh City: a retrospective study of 2,267 cases from 2011 to 2015

Status:

Journal Publication

Version 1

Abstract

Figures

Background

Methods

Study setting and population

Data collection

Statistical analysis

Ethical approval

Results

Characteristics of MDR/RR-TB patients

Drug resistance pattern

MDR-TB trend

Treatment outcomes

Risk factors for poor outcomes

Discussion

Conclusion

Abbreviations

Declarations

References

Tables

Supplementary Files

Status:

Journal Publication

Version 1