Burden of COVID-19 pandemic on tuberculosis hospitalisation patterns at a tertiary care hospital in Rajasthan, India: a retrospective analysis

Abstract

Objective

This study aimed to investigate the burden of the COVID-19 pandemic on tuberculosis (TB) trends, patient demographics, disease types and hospitalisation duration within the Respiratory Medicine Department over three distinct phases: pre-COVID-19, COVID-19 and post-COVID-19.

Design

Retrospective analysis using electronic medical records of patients with TB admitted between June 2018 and June 2023 was done to explore the impact of COVID-19 on patients with TB. The study employed a meticulous segmentation into pre-COVID-19, COVID-19 and post-COVID-19 eras.

Setting

National Institute of Medical Science Hospital in Jaipur, Rajasthan, India.

Primary and secondary outcome measures

Primary outcome includes patients admitted to the Respiratory Medicine Department of the hospital and secondary outcome involves the duration of hospital stay.

Results

The study encompassed 1845 subjects across the three eras, revealing a reduction in TB incidence during the post-COVID-19 era compared with the pre-COVID-19 period (p<0.01). Substantial demographic shifts were observed, with 5.2% decline in TB incidence among males in the post-COVID-19 era (n=529) compared with the pre-COVID-19 era (n=606). Despite the decrease, overall TB incidence remained significantly higher in males (n=1460) than females (n=385), with consistently elevated rates in rural (65.8%) as compared with the urban areas (34.2%). Extended hospital stays were noted in the post-COVID-19 era compared with the pre-COVID-19 era (p<0.01).

Conclusion

The study underscores the influence of the COVID-19 pandemic on the TB landscape and hospitalisation dynamics. Notably, patient burden of TB declined during the COVID-19 era, with a decline in the post-COVID-19 era compared with the pre-COVID-19 era. Prolonged hospitalisation in the post-COVID-19 period indicates the need for adaptive healthcare strategies and the formulation of public health policies in a post-pandemic context. These findings contribute to a comprehensive understanding of the evolving TB scenario, emphasising the necessity for tailored healthcare approaches in the aftermath of a global health crisis.

Correspondence to Dr Nalin Joshi; [email protected]

STRENGTHS AND LIMITATIONS OF THIS STUDY

• This study contributes to the understanding of the intricate dynamics between the COVID-19 pandemic and tuberculosis (TB).

• Focusing on a single tertiary care hospital may limit the generalisability of findings to broader populations.

• The precise causes underlying the observed increase in hospitalisation duration for patients with TB in the post-COVID-19 era remain speculative.

Background

Since its emergence in 2019, the COVID-19 pandemic has posed multifaceted challenges, affecting governmental responses, economic stability and healthcare systems, and instigating widespread societal disruption on a global scale. This unprecedented crisis has garnered the attention of healthcare providers, scientists and researchers, making the year 2020 particularly memorable for its overshadowing by the COVID-19 pandemic. In an effort to decrease the transmission of SARS-CoV-2 and manage healthcare infrastructures, numerous countries implemented population-wide lockdowns.¹

As of the period from 8 January to 4 February 2024, the WHO’s COVID-19 epidemiological update reports a noteworthy decline in the number of new cases by 58% and new deaths by 31%,² with the majority of prevalence in the male population.³ While the spotlight understandably focused on COVID-19, it is imperative not to overlook the broader impact this pandemic has exerted on other communicable diseases.

This study, set in the context of the prevailing global scenario, directs attention to tuberculosis (TB), which stands as the second leading cause of death following COVID-19.⁴ In 2022, a staggering 10.6 million individuals worldwide were diagnosed with TB. Notably, India carries the highest burden of TB, contributing to 26% of the global TB incidence and 32% of the global TB mortality in 2022. The country also grapples with a considerable burden of drug-resistant TB, with an estimated 124 000 cases of rifampicin-resistant TB in 2022.⁵ Despite significant progress made by India in scaling up TB diagnosis and treatment prior to the pandemic, the disruptive influence of COVID-19 led to a sharp decline in TB notifications during 2020 and 2021. Consequently, there was a surge in TB incidence and mortality between 2020 and 2022, reversing the previously observed downward trend.^{6 7}

Modelling studies by Cilloni et al and Hogan et al indicate a substantial impact of the COVID-19 pandemic on TB transmission, death and incidence in the forthcoming years.^{8 9} The rapid escalation of COVID-19 cases necessitated the diversion of resources, both human and infrastructural, to combat the novel virus.

This resource shift raised concerns about the continuity and quality of care for individuals with chronic conditions, particularly those undergoing treatment for TB. The management of TB necessitates a systematic and sustained approach, involving regular medical supervision, consistent medication adherence and timely follow-ups. However, the disruptions caused by the COVID-19 pandemic introduced significant barriers to maintaining this delicate balance. Lockdowns, social distancing measures and the fear of contracting the virus deterred many patients with TB from seeking essential medical attention.¹⁰ This study examines how the COVID-19 pandemic has influenced the pattern of TB with respect to hospitalisation stay in northern (Rajasthan, Haryana and Uttar Pradesh) and central states (Madhya Pradesh) of India.

Methodology

This study examines the impact of COVID-19 on patients with TB who sought treatment at the Respiratory Medicine Department of the National Institute of Medical Science (NIMS) Hospital in Jaipur, Rajasthan, India. The geographical scope encompasses patients from the states of Rajasthan, Uttar Pradesh, Haryana and Madhya Pradesh.

Using a retrospective design, the study draws data from meticulously maintained electronic medical records archived by the Medical Record Department of NIMS Hospital spanning from June 2018 to June 2023.

In adherence to carefully crafted inclusion criteria, the study includes subjects registered between June 2018 and June 2023 who received a clear diagnosis of TB. Only individuals with complete demographic profiles and clinical characteristics are incorporated into the analysis. Importantly, the study focuses exclusively on patients who visited NIMS Hospital in Jaipur, Rajasthan, to maintain geographical consistency.

To uphold the rigour of the research, exclusion criteria are established, refining the selection process. Subjects falling outside the June 2018–June 2023 time frame are excluded to ensure temporal coherence. Additionally, individuals lacking comprehensive demographic and clinical data are respectfully omitted from the study population.

Statistical analysis

IBM SPSS V.28.0 (IBM Corp) was used to analyse data. After data cleaning and managing missing data, descriptive analysis was performed to summarise the data. The continuous variables were presented as mean±SD and categorical variables reported as frequency and percentage. The data were divided into three distinct phases: pre-COVID-19 era spanning from June 2018 to 2019, the COVID-19 era encompassing 2020–2021, and finally, the post-COVID-19 era spanning 2022–June 2023.¹¹ The percentage change between these eras was calculated by dividing the difference between new and old cases by the old cases multiplied by 100. The mean difference between data was calculated using the analysis of variance and Χ² test and p value of <0.05 was considered statistically significant. Microsoft Excel V.2021 was used for representing data in graphical form.

Patient and public involvement

There was no direct involvement of patients and the public in the design, conduct, reporting or dissemination plans of this research.

Result

A total of 1845 patients were diagnosed with TB at the NIMS Hospital, Rajasthan, India with varying proportions across the three eras: 732 (39.7%) in the pre-COVID-19 era, 453 (24.6%) in the COVID-19 era and 660 (35.8%) in the post-COVID-19 era—with the shortest hospital stay during the pre-COVID-19 era, followed by the post-COVID-19 era and the longest in the COVID-19 era. Majority of TB cases were pulmonary TB, and the distribution varied significantly across eras with highest cases (37.2%) in the pre-COVID-19 and lowest (20.5%) in the COVID-19 era. The most prevalent types of TB include TB of the lungs; pneumoconiosis associated with TB; TB of the bones and joints; TB of the intestines, peritoneum and mesenteric glands; and tuberculous meningitis. The distribution of these types varied significantly across the three eras (table 1 and figure 1).

Table 1

Demographic variable of tuberculosis cases stratified according to pre-COVID-19, COVID-19 and post-COVID-19 eras

Variables	Pre-COVID-19 era	COVID-19 era	Post-COVID-19 era	Total	P value
Total patients, n (%)	732 (39.7)	453 (24.6)	660 (35.8)	1845 (100)	<0.01
Age (mean±SD)	49.59±15.85	42.69±18.52	45.65±17.34	46.49±17.28	<0.01
Area of residence, n (%)					<0.001
Rural	607 (82.9)	321 (70.9)	377 (57.1)	1305 (65.8)
Urban	125 (17.1)	132 (29.1)	283 (42.9)	540 (34.2)
Length of hospital stay, mean±SD	5.93±3.73	7.61±5.058	6.42±3.77	6.52±4.16	<0.01
Form of tuberculosis, n (%)					<0.01
Pulmonary tuberculosis	687 (37.2)	378 (20.5)	587 (31.8)	1652 (89.5)
Extrapulmonary tuberculosis	45 (2.4)	75 (4.1)	73 (4.0)	193 (10.5)
Total	732 (39.7)	453 (24.6)	660 (35.8)	1845 (100)
Type of tuberculosis, n (%)					<0.01
Lungs	564 (30.6)	340 (18.4)	582 (31.5)	1486 (80.5)
Pneumoconiosis associated with TB	123 (6.7)	42 (2.3)	6 (0.3)	171 (9.3)
TB of bones and joints	28 (1.5)	37 (2.0)	31 (1.7)	96 (5.2)
TB of intestines, peritoneum and mesenteric glands	11 (0.6)	24 (1.3)	35 (1.9)	70 (3.8)
Tuberculous meningitis	6 (0.3)	10 (0.5)	6 (0.3)	22 (1.2)
Total	732 (39.7)	453 (24.6)	660 (35.8)	1845 (100)

All the continuous variables are presented as mean±SD and categorical variables are presented as number (%). P value was significant at less than 0.05 or 0.01.

Figure 1. Number of patients with tuberculosis admitted over the last 5 years.

The patients were geographically distributed among states, with the majority from Rajasthan, followed by other states which include Uttar Pradesh, Madhya Pradesh and Haryana. A salient observation surfaced during our examination of TB incidence from Rajasthan, revealing a marginal decline in patient visits to hospital in the post-COVID-19 era as compared with the pre-COVID-19 era (figure 2).

Figure 2. Geographical distribution of patients who visited the Respiratory Medicine Department of the National Institute of Medical Science Hospital from June 2018 to June 2023.

Examining gender-wise distribution across the phases, we observed a 41.5% representation of males during the pre-COVID-19 era, a decline during the COVID-19 era of 22.3% and a subsequent rate of 36.2% during the post-COVID-19 era. The male population has a higher TB incidence, which decreased by 5.3% in the post-COVID-19 era compared with the pre-COVID-19 era (figure 3). Across all three phases, a consistent trend emerged: higher TB incidence in rural areas compared with urban areas. Notably, a substantial 29.3% spike was detected in urban populations from pre-COVID-19 to post-COVID-19 phases, reaching 52.4% (figure 4).

Figure 3. Gender-wise distribution of the patient population in the pre-COVID-19, COVID-19 and post-COVID-19 eras.

Figure 4. Area-wise distribution (urban and rural) of patients with TB in the pre-COVID-19, COVID-19 and post-COVID-19 eras.

Discussion

The inception of COVID-19 in India, marked by its first report on 27 January 2020, has catalysed a global healthcare crisis.¹² In response, the Indian government implemented a 21-day nationwide lockdown from March 24 to minimise transmission. The initial wave exhibited a modest infectivity rate, attributed to rigorous lockdown measures and social distancing adherence, primarily impacting the economic and socioeconomic domains while sparing the healthcare system from substantive stress.¹³

A paradigm shift occurred in March 2021 with the onset of a devastating second wave, intensified by ‘pandemic fatigue’, resulting in widespread transmission and significant societal upheaval.¹⁴ The subsequent third wave in January 2022 differed markedly, characterised by the diminished virulence of the omicron variant, heightened transmissibility and widespread administration of COVID-19 vaccines to adults, affirming vaccine efficacy.¹⁵ Globally, the COVID-19 pandemic has impeded TB control, causing setbacks in diagnosis, delays in treatment initiation and elevated TB-related mortality rates, jeopardising TB elimination targets by 2030. The shared pulmonary impact and symptomatic similarities of both COVID-19 and TB accentuate respiratory health challenges, manifesting as cough, cold, fatigue and fever, underscoring the intricate challenges posed by their coexistence.¹⁶

The pandemic’s disruption of healthcare services has led to diminished TB testing, treatment and prevention coverage. Analyses of TB centres worldwide consistently reveal a substantial reduction in patients with TB during the pandemic’s first year, notably in countries with high TB burdens such as Italy, France and Spain.¹⁶ The indirect impact of COVID-19 on TB care is evident in resource-constrained, high TB burden settings, exemplified by a 52% drop in TB notifications in Jiangsu Province, China, in 2020 compared with 2015–2019. Delays in reporting, rather than detection, were noted, with reductions in TB cases in the first half of 2020 anticipated to rebound by the second half of 2020 or early 2021. Despite some recovery after the initial COVID-19 wave, TB cases globally regressed to 2012 levels by the end of 2020, with significant shortfalls reported in countries like India, Indonesia, the Philippines and China. The Global Fund Results Report underscored the severe impact of the pandemic on TB treatment, revealing a substantial drop in the number of people treated for drug-resistant TB and HIV-positive patients with TB on antiretroviral treatment in 2020.^16–18

Our findings revealed a discernible 3.9% reduction in TB incidence during the post-COVID-19 period, with an overall prevalence rate of 35.8%, as opposed to the pre-COVID-19 era, where the incidence stood at 39.7%. This corroborates with the observations presented in the Global Tuberculosis Report 2022 by the WHO, which documented a decline in patient numbers during the post-COVID-19 era compared with the pre-COVID-19 era.¹⁹

The reduction in TB incidence during the COVID-19 era was notably ascribed to the widespread adoption of masks within the population, demonstrating a pivotal role in mitigating TB transmission dynamics.²⁰ Furthermore, our investigation noted a marginal decline in the patient count at our tertiary care hospital during the post-COVID-19 era relative to the pre-COVID era, contrasting with an increase observed in the post-COVID-19 era compared with the height of the COVID-19 pandemic. This fluctuation may be attributed to the implementation of free treatment camps designed to reach a wider demographic. Geographical disparities were apparent, with a higher influx of patients from urban areas compared with rural regions in the post-COVID-19 era, a phenomenon attributed to the logistical constraints imposed by lockdown measures during the pandemic period, restricting accessibility to our hospital located on the outskirts of the city.²¹ Remarkably, gender-based distinctions persisted, revealing a higher incidence of TB in men than women across both study eras. This predisposition may be attributed to various lifestyle factors, including heightened tobacco and alcohol consumption, increased susceptibility to lung injury, and extensive travel and community interactions among males.^22–25 Despite the existence of a century-old TB vaccine, its impact remains confined to mitigating severe disease in children without influencing overall prevalence. Modelling endeavours were undertaken to assess the confluence of COVID-19 and TB coinfections, with the joint implementation of COVID-19 prevention and coinfection management measures yielding the most favourable outcomes among various control strategies.²⁶ The primary focus of our study was on the duration of hospitalisation for patients with TB, revealing an increase in the post-COVID-19 era compared with the pre-COVID-19 era, with a concomitant rise in the average length of hospital stay. While the precise aetiology of this phenomenon remains elusive, it is posited that post-COVID-19 complications may contribute to the observed prolongation of hospitalisation for patients with TB.

Conclusion

This study provides valuable insights into the impact of the COVID-19 era on TB landscape and hospitalisation patterns. We observed a noteworthy 3.9% decline in TB during the post-COVID-19 period, aligning with global trends documented in the WHO’s Global Tuberculosis Report 2022. An upward trajectory in the length of hospital stay was observed in the post-COVID-19 era compared with the pre-COVID-19 era. The prolonged hospital stays in the post-COVID-19 era may reflect the pandemic’s lasting impact on the healthcare system. These findings highlight the need for adaptive healthcare strategies to manage TB and public health policy formulation in a post-pandemic world.

Strengths and limitations

While our study contributes valuable insights, several limitations warrant consideration. First, the focus on a single tertiary care hospital may limit the generalisability of findings to broader populations. Additionally, the retrospective design of our study, reliant on electronic medical records, is subject to data completeness and accuracy limitations inherent to such retrospective analyses. The impact of socioeconomic factors on healthcare-seeking behaviour and access to diagnostic services remains a potential confounder not fully explored in our study. Furthermore, the precise causes underlying the observed increase in the post-COVID-19 era hospitalisation duration for patients with TB remain speculative, necessitating further investigation. Despite these limitations, our study contributes to the understanding of the intricate dynamics between the COVID-19 pandemic and TB, laying a foundation for future research and targeted public health interventions (online supplemental file 1).

We would like to thank the Medical Record Department (MRD) workers of NIMS Hospital for their cooperation during data extraction.

Data availability statement

Data are available upon reasonable request.

Ethics statements

Patient consent for publication

Not applicable.

Ethics approval

Ethical considerations are paramount in research endeavours. Accordingly, the study adheres to the principles outlined in the Declaration of Helsinki (1975). Ethical clearance was obtained from the Institutional Ethics Committee of NIMS University (approval number # NIMSUR/IEC/2023/685) to ensure the protection of participants' rights and confidentiality. Individual informed consent was waived due to no direct involvement of human participants.

Footnote

Contributors Conceptualisation—MS and SR. Methodology—PR, PS and NJ. Software—SR and SM. Validation—MS, NJ and DN. Formal analysis—AKS, SR, HB and SM. Investigation—MS, HB and SR. Resources—DN and NJ. Data curation—SR, AKS, SD and PN. Writing (original draft preparation)—SR, PR and PS. Writing (review and editing)—MS, AS and SR. Visualisation—SR and PR. Supervision—BST, DN, NJ and MS. Project administration—DN. Funding acquisition—BST and DN. Guarantor- NJ. All authors contributed to the article and approved the submitted version.

Funding Financial support was provided by NIMS University Rajasthan, Jaipur, India. No funding has been provided for the study.

Disclaimer All other decisions on design, data collection, analysis, interpretation and publication were independent of the funding sources.

Map disclaimer The depiction of boundaries on this map does not imply the expression of any opinion whatsoever on the part of BMJ (or any member of its group) concerning the legal status of any country, territory, jurisdiction or area or of its authorities. This map is provided without any warranty of any kind, either express or implied.

Competing interests None declared.

Patient and public involvement Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.

Provenance and peer review Not commissioned; externally peer reviewed.

Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.

References

¹ Duma Z, Chuturgoon AA, Ramsuran V, et al. The challenges of severe acute respiratory syndrome Coronavirus 2 (SARS-Cov-2) testing in low-middle income countries and possible cost-effective measures in resource-limited settings. Global Health 2022; 18: 5. doi:10.1186/s12992-022-00796-7

² Programme GT. Global tuberculosis report 2021. World Health Organization; 2021. Available: https://www.who.int/publications/digital/global-tuberculosis-report-2021/covid-19

³ Bwire GM. Coronavirus: why men are more vulnerable to COVID-19 than women? SN Compr Clin Med 2020; 2: 874–6. doi:10.1007/s42399-020-00341-w

⁴ World Health Organization. Newsroom, fact sheets, detail, tuberculosis. 2023. Available: https://www.who.int/news-room/fact-sheets/detail/tuberculosis

⁵ World Health Organization. Global tuberculosis report 2023. 2023.

⁶ Varshney K, Patel H, Kamal S. Trends in tuberculosis mortality across India: improvements despite the COVID-19 pandemic. Cureus 2023; 15: e38313. doi:10.7759/cureus.38313

⁷ Ponnampalli S, Birudukota NVS. The impact of COVID-19 pandemic in high-burden countries for tuberculosis: a systematic review. Health Sciences Review 2023; 9: 100128. doi:10.1016/j.hsr.2023.100128

⁸ Cilloni L, Fu H, Vesga JF, et al. The potential impact of the COVID-19 pandemic on the tuberculosis epidemic a modelling analysis. EClinicalMedicine 2020; 28: 100603. doi:10.1016/j.eclinm.2020.100603

⁹ Hogan AB, Jewell BL, Sherrard-Smith E, et al. Potential impact of the COVID-19 pandemic on HIV, tuberculosis, and malaria in low-income and middle-income countries: a modelling study. Lancet Glob Health 2020; 8: e1132–41. doi:10.1016/S2214-109X(20)30288-6

¹⁰ Togun T, Kampmann B, Stoker NG, et al. Anticipating the impact of the COVID-19 pandemic on TB patients and TB control programmes. Ann Clin Microbiol Antimicrob 2020; 19: 21. doi:10.1186/s12941-020-00363-1

¹¹ Guo BC, Chen YJ, Huang WY, et al. Psychological disorders and suicide attempts in youths during the pre-COVID and post-COVID era in a Taiwan pediatric emergency department. Front Psychol 2023; 14: 1281806. doi:10.3389/fpsyg.2023.1281806

¹² Andrews MA, Areekal B, Rajesh KR, et al. First confirmed case of COVID-19 infection in India: a case report. Indian J Med Res 2020; 151: 490–2. doi:10.4103/ijmr.IJMR_2131_20

¹³ Lamba I. Why India needs to extend the nationwide lockdown. Am J Emerg Med 2020; 38: 1528–9. doi:10.1016/j.ajem.2020.04.026

¹⁴ Asrani P, Eapen MS, Hassan MI, et al. Implications of the second wave of COVID-19 in India. Lancet Respir Med 2021; 9: e93–4. doi:10.1016/S2213-2600(21)00312-X

¹⁵ Lahariya C. Third wave of the COVID-19 pandemic in India: what lies ahead. Health Express, 2022.

¹⁶ Migliori GB, Thong PM, Alffenaar J-W, et al. Gauging the impact of the COVID-19 pandemic on tuberculosis services: a global study. Eur Respir J 2021; 58: 2101786. doi:10.1183/13993003.01786-2021

¹⁷ Goudiaby MS, Gning LD, Diagne ML, et al. Optimal control analysis of a COVID-19 and tuberculosis co-dynamics model. Inform Med Unlocked 2022; 28: 100849. doi:10.1016/j.imu.2022.100849

¹⁸ Geric C, Saroufim M, Landsman D, et al. Impact of COVID-19 on tuberculosis prevention and treatment in Canada: a multicentre analysis of 10,833 patients. J Infect Dis 2022; 225: 1317–20. doi:10.1093/infdis/jiab608

¹⁹ Ministry of Health and Family Welfare. Available: https://tbcindia.gov.in/WriteReadData/l892s/56467

²⁰ Dharmadhikari AS, Mphahlele M, Stoltz A, et al. Surgical face masks worn by patients with multidrug-resistant tuberculosis: impact on infectivity of air on a hospital ward. Am J Respir Crit Care Med 2012; 185: 1104–9. doi:10.1164/rccm.201107-1190OC

²¹ Arega B, Negesso A, Taye B, et al. Impact of COVID-19 pandemic on TB prevention and care in Addis Ababa, Ethiopia: a retrospective database study. BMJ Open 2022; 12: e053290. doi:10.1136/bmjopen-2021-053290

²² Watkins RE, Plant AJ. Does smoking explain sex differences in the global tuberculosis epidemic? Epidemiol Infect 2006; 134: 333–9. doi:10.1017/S0950268805005042

²³ Arcavi L, Benowitz NL. Cigarette smoking and infection. Arch Intern Med 2004; 164: 2206–16. doi:10.1001/archinte.164.20.2206

²⁴ Imtiaz S, Shield KD, Roerecke M, et al. Alcohol consumption as a risk factor for tuberculosis: meta-analyses and burden of disease. Eur Respir J 2017; 50: 1700216. doi:10.1183/13993003.00216-2017

²⁵ le Polain de Waroux O, Cohuet S, Ndazima D, et al. Characteristics of human encounters and social mixing patterns relevant to infectious diseases spread by close contact: a survey in Southwest Uganda. BMC Infect Dis 2018; 18: 172. doi:10.1186/s12879-018-3073-1

²⁶ TB/COVID-19 Global Study Group. TB/COVID-19 global study group. tuberculosis and COVID-19 co-infection: description of the global cohort. Eur Respir J 2022; 59: 2102538. doi:10.1183/13993003.02538-2021