Prevalence and Factors Associated with Tuberculosis Among Healthcare Workers: A Systematic Review with Meta-Analysis

1. Introduction

Tuberculosis (TB) is an infectious disease caused by Mycobacterium tuberculosis and is considered one of the main communicable diseases of global public health concern. [1,2] Early detection and control of TB represent a challenge for health services, especially for low-income countries with high levels of social inequality. [3]

Brazil is on the list of 30 countries with a high TB burden, accounting for 87% of all TB cases worldwide. [4] TB also results in 1.5 million deaths annually and is classified as the second leading cause of death from a single infectious agent, second only to COVID-19. The disease is also the ninth leading cause of death globally. [5,6] The global annual incidence of TB is estimated at 142 cases per 100,000 inhabitants. [6] In Brazil, 78,057 cases were reported in 2022, resulting in 36.3 cases per 100,000 inhabitants. [7] TB often affects vulnerable groups, [8] including healthcare workers, whether in primary care, outpatient, or hospital settings. [9,10] These professionals are exposed to aerosols produced by infected patients during coughing or sneezing while providing care. [2,9,11] It is estimated that healthcare workers are 1.9 to 5.7 times more likely to develop TB compared to the general population. This risk increases according to the TB burden in the country and the levels of infection control measures. [12] This reality makes the disease an important occupational problem of global concern. [2]

To address this challenge and provide a safer working environment for healthcare workers, the World Health Organization (WHO) established the “End TB” Strategy in 2015, which aims to reduce the incidence of TB by 95% by 2030. To achieve this goal, infection control in healthcare settings was included as a priority component. [13] In Brazil, the Ministry of Health (MoH), in 2014, included in the Notifiable Diseases Information System (SINAN) a field referring to specific populations in which there is a category for healthcare workers, allowing the monitoring of cases in this population. [9]

According to the Ministry of Health, in 2022, 1,141 cases of TB were reported among health workers in Brazil. [7] However, it is important to highlight that these professionals can be infected with M. tuberculosis and not develop the disease, as the bacillus can remain in a latent state for decades. This condition is called Latent Tuberculosis Infection (LTBI), and its prevalence exceeds 30% among healthcare workers. Furthermore, the risk of illness in this group is nearly three times higher than in the general population. [14]

Systematic reviews have been conducted on the subject [15,16,17], most of which present an analysis of prevalence in the general population but do not distinguish among healthcare workers. As mentioned, healthcare workers are considered a risk group for TB, as they are often in direct contact with large loads of the bacillus, depending on their area of work. Particularly healthcare workers in countries with high TB prevalence are at increased risk of TB infection and disease development due to their frequent, prolonged, and close exposure to infectious TB cases. [18]

Therefore, this study becomes relevant because it proposes to understand the prevalence of the disease in this specific population, as well as its related factors, aiming to minimize this knowledge gap still present in the current literature. It is, therefore, essential to carry out a systematic review that updates the evidence on the subject, allowing a critical reflection on the occurrence of TB among health service workers, especially considering the cascade of care. This study aims to analyze the prevalence and factors associated with tuberculosis among healthcare workers.

2. Materials and Methods

Protocol and Registration

This is a systematic literature review with meta-analysis, [19] conducted according to the recommendations and criteria of the Joanna Briggs Institute (JBI)[20] and reported following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines. [21] The protocol for this review was registered on York University’s International Prospective Register of Systematic Review (PROSPERO) platform under number CRD42022320153 on April 27, 2022.

Research Question and Eligibility Criteria

The research question was: What is the prevalence and the factors associated with tuberculosis among healthcare workers? The acronym CoCoPop (Condition, Context, and Population) was used. [20] The chosen condition was TB, the context considered was healthcare settings, and the population was healthcare workers.

The inclusion criteria were studies involving healthcare workers (of technical or higher education level) working in healthcare settings, regardless of the level of care. Studies that presented partial results and/or did not directly address the research question were excluded, as were those that investigated associations between TB and other health conditions; those in which it was not possible to access the full data after three attempts to contact the authors by e-mail. It is worth mentioning that there were no time or language restrictions.

Data Source Search

The database search took place in December 2023, covering the following databases: SCOPUS (Elsevier), Web of Science (WoS), MEDLINE (PubMed), CINAHL (Cumulative Index to Nursing and Allied Health Literature), and LILACS (Latin American and Caribbean Health Sciences Literature).

Search Strategy

The search strategy was developed based on terms from the Medical Subject Headings (MeSH). After defining the search terms, the Boolean operators “AND” and “OR” were used. Initially, a pilot test was conducted in MEDLINE. Thus, the following high-sensitivity search strategy was applied to all databases, taking into account the specificities of each source: (Tuberculosis[Title] OR Latent Tuberculosis[Title]) AND (Health Care[Title] OR Health Care Workers[Title] OR Healthcare[Title] OR Physical Therapists[Title] OR Nursing Assistants[Title] OR Patient Care Team[Title] OR Nurse Midwives[Title] OR Nurse Anesthetists[Title] OR Nurses[Title] OR Community Health Workers[Title] OR Physician Assistants[Title] OR Physicians Hospitalists[Title] OR Family Nurse Practitioners[Title] OR Allied Health Personnel Health Occupations[Title] OR Occupational Health Nursing[Title] OR Public Health Nursing Occupational Health[Title] OR Nurses, Community Health[Title] OR Nurses, Public Health[Title] OR Nutritionists[Title] OR Health Services Accessibility[Title] OR Hospital Care[Title] OR Prehospital Care[Title] OR Day Care, Medical[Title] OR Home Care Services, Hospital-Based[Title] OR Health Centers[Title] OR Primary Health Care[Title] OR Healthcare workes[Title] OR Emergency Medical Services[Title] OR Family Health Strategy[Title] OR Intensive Care Units[Title] OR Primary Nursing[Title] OR Mental Health Services[Title] OR Mobile Health Units[Title] OR Radiology Department, Hospital[Title] OR Ambulatory Care[Title] OR Essential Public Health Functions[Title] OR Health Facilities, Proprietary[Title] OR Home Care Services[Title] OR Community Health Services[Title] OR Delivery of Health care[Title] OR Women’s Health Service[Title] OR Secondary Care[Title] OR Tertiary Healthcare[Title] OR Health Services, Indigenous[Title] OR School Health Service[Title] OR Student Health Services[Title] OR Basic Health Services[Title] OR Maternal Health Service[Title] OR Urban Health Services[Title] OR Suburban Health Service[Title] OR Rural Health Services[Title] OR Occupational Health Service[Title] OR Health Services for the Aged[Title] OR Laundry Service, Hospital[Title] OR Adolescent Health Service[Title] OR Public Health Services[Title] OR Emergency Service, Hospital[Title])

Study Selection Process

After screening the articles in the databases, the studies were imported into the literature citation manager Start of the Art through Systematic Review. Subsequently, the references of all the selected studies were searched to identify additional relevant studies. The studies were selected independently and blindly by two reviewers/authors, both with experience in systematic review and the study area. A first reading of titles and abstracts was conducted, with the selected materials being fully reviewed later. Consensus meetings were held regarding the inclusion of articles, and any disagreements were discussed with the participation of a third reviewer/author of the study.

Data Extraction, Processing, and Analysis Process

The results were synthesized in a Microsoft Excel® spreadsheet, taking into account the following variables for extraction: study characteristics (author, year, title, journal, country of origin), methodological aspects (study type, level of care, professionals, and sample), and prevalence results and factors associated with tuberculosis, as well as objectives, main findings, and conclusions.

Evaluation of Methodological Quality

The eligible studies underwent a methodological quality assessment, using the JBI recommendations, by two independent reviewers/authors. In cases of disagreement, the opinion of a third reviewer/author was requested. On a scale consisting of nine criteria, the studies were classified as follows: zero to three criteria (low quality), four to six criteria (medium quality), and seven or more (high quality). [22]

Subsequently, all the articles, regardless of their methodological quality, were subjected to data extraction and narrative synthesis.

Meta-Analysis

To assess the prevalence of TB among health professionals, random effects models were used to present the prevalence as a percentage, together with 95% confidence intervals. Heterogeneity between studies was assessed using the I² test, in which values above 50% and p-values less than 0.05 indicate high heterogeneity. [23]

For a study to be included in the meta-analysis, it had to provide both the number of workers with TB and the total sample size. In cases where the studies only provided prevalence data, they studied the sample size. The years of data collection for each study were considered to analyze the trend in TB prevalence. [24] Subgroup analyses were conducted considering age, sex, education level, and years of service. The analysis was performed using the R program, with the Meta package.

3. Results

Descriptive Characteristics and Quality of Included Studies

Using the search strategies, 7,392 articles were initially identified, 706 of which were duplicates, 146 records were marked as ineligible by automation tools and 72 records were removed for other reasons. Leaving 6,468 for screening. Next, 5,589 articles that did not meet the inclusion criteria were excluded, including 879 full-text studies. After reading all the articles, 32 were included in the review, as shown in Figure 1.

When evaluating the methodological quality of the studies, 21 articles (65.6%) scored between seven and nine, that is, high quality; of these, eight scored nine, covering all items analyzed for excellence in methodological quality, as described in Table 1.

When analyzing the characterization of the studies included, the majority were published in 2023 (six publications), the first being published in 1985. The investigations were carried out in different countries, including Germany, Saudi Arabia, South Korea, Spain, India, Portugal, and Japan, published in international journals and with a cross-sectional epidemiological design. The characteristics of the articles reveal groups composed mainly of doctors and nurses, developed in high complexity, with an average population of 803.06 health professionals (maximum 4,735 and minimum 35 professionals), As described in Table 2.

Table 3 identified risk factors for developing TB among health workers, such as educational level below higher education (ID: 1372), length of service of more than ten years, absence of BCG (Bacille Calmette-Guérin) vaccination, occupational exposure to TB, female gender, advanced age (workers over 50), smoking, presence of comorbidities such as diabetes mellitus (DM) and hepatitis (ID: 1372; 1376; 1417; 1455; 2020; 2491; 3784; 4336; 4478; 5481; and 6145). The pulmonary clinical form was the most frequently identified (ID: 4572; 6015).

Concerning the type of worker, it was found that the incidence of TB is high among nurses and doctors (ID: 1417; 1448; 4478; 6015; 6145). The incidence of ILTB among health workers is high in the occupational environment, and the main contamination environments for these professionals are wards, the Intensive Care Unit (ICU), the Emergency Room, and Primary Care (ID: 1448; 4478; 6145 and 6328).

The high prevalence of ILTB among healthcare workers means that studies (ID: 1448;1455; 2234; 3784; 4075; 4271; 4478; 5503; 5829) emphasize the need for preventive measures such as pre-employment screening, especially for those employed in areas of high endemicity, annual screening, regular infection control training, frequent use of hand rubbing and use of N95 masks as Personal Protective Equipment, as well as maintaining surveillance programs and adopting and stricter preventive strategies against infection.

Prevalence of Tuberculosis Among Healthcare Workers

In the analysis of prevalence, 23 studies were included, highlighting high heterogeneity between the studies, with an I² value of 99% = 2.5350, p = 0. The result of the meta-analysis showed an active TB prevalence of 15.98% [9.00 – 26.78], with a total population across all studies of 63,371 healthcare workers (Figure 2).

The meta-analysis of associated factors revealed that the older the professional, the greater the chance of developing TB 1.47 [95% CI 1.19 – 1.82 I2 = 88%, p = 0.01] (figure B/ 3), being a graduate was 1.57 more likely [95% CI 1.01 – 2.43 I2 = 0%, p = 0.49] (figure C/3) and having ten years or more of professional experience increased the chances at 1.08 [95% CI 1.02 - 1.14 I2 = 48%, p = 0.08] (figure D/3).

Figure 3. Factors related to tuberculosis among health professionals. Rio Grande do Sul, Brazil, 2024.

Figure 3. Factors related to tuberculosis among health professionals. Rio Grande do Sul, Brazil, 2024.

4. Discussion

Through the synthesis of this review, the prevalence and associated factors of TB in healthcare workers were found. The meta-analysis revealed that the prevalence of active TB among workers was 15.98% [9.00 – 26.78], and when analyzing the associated factors, female sex showed 1.27 times higher chances of developing TB, while older age and more than 10 years of professional experience had 2.48 and 1.08 times higher chances, respectively, of developing the disease.

These results corroborate the systematic review, which showed a prevalence of TB among health workers of 28% (95% CI 21-36) and occupational risk factors are related to direct contact with patients with active TB and having more professional experience, i.e., the longer the time in the health service, the greater the chances of developing the disease. [25]

TB, being a serious public health problem in health services, directly affects workers in these service institutions. This problem has been forgotten or minimized for a long time by health institution managers and/or government representatives but is back in the discussion today by incorporating health workers as a target population, that is, a priority for combating and eliminating TB in the world. [9,18,26]

These results are in line with the proposals made by the WHO [13] in conjunction with the Ministry of Health, [9] which include health workers as a population with a higher probability of developing TB due to exposure and work characteristics, i.e., workers have direct and indirect contact with Mycobacterium tuberculosis during patient care. [27,28] Furthermore, the risk of exposure and acquisition of TB in the workplace is a concrete factor, and professional categories such as nursing, medicine, and physiotherapy are more exposed to infection, considering their duties. [29]

It is worth noting that TB is transmitted via the respiratory tract through inhaling aerosols produced by the coughing, talking, or sneezing of a patient with active TB. Thus, when the bacilli are expelled, they remain dispersed in the occupational environment in the form of aerosols for a period that depends on the environmental characteristics of the location, i.e., ventilation conditions and direct sunlight. [30] Bacillus is highly contagious and has serious effects on workers’ health. Signs and symptoms can take a long time to manifest in the airways, which poses a challenge for early prevention measures to eliminate the bacteria. [29]

In addition, the transmission of the bacteria to healthcare workers depends on different factors, such as the type of job they do, the length of time they have been exposed to it in the workplace, and the number of years they have worked, i.e., the longer they have worked, the greater the risk of developing the disease. [31]

It is also worth noting that the transmission of TB within healthcare services is related to the effectiveness of preventive interventions carried out by managers, as well as the implementation of ongoing education among workers and the use of personal protective equipment. [26] Healthcare professionals use personal protective equipment to shield themselves from cough droplets, sneezes, or other bodily fluids from infected patients and contaminated surfaces that could infect them. Therefore, using such equipment helps reduce the chances of contamination. [32]

A study carried out in Nepal, which sought to assess the knowledge and practice of nurses in preventing and controlling TB infection, found that most nurses had an inadequate level of knowledge and poor practice of TB prevention and control. In terms of practice, none of the nurses reported using an N95 mask or respirator when caring for TB patients. [33]

Therefore, health workers are vulnerable to TB infection, Labor laws mention that TB is considered a disease related to the work environment and, in Brazil, it is an occupational disease that is compulsorily notifiable to the SINAN. [34]

Concerning the categories of health workers and their expectation of TB infection compared to the general population, the literature shows a risk 3 to 20 times higher among nursing staff, 6 to 11 times higher among clinical pathologists, four to eight times higher among students (nursing, physiotherapy, and medicine); and two to nine times higher among bacteriology laboratory technicians. [35]

A study of nurses in China found that the prevalence of TB among nurses working in TB-related departments is 5.1 times higher than in the general population, and the incidence of LTBI among healthcare workers is between 17 and 36%. [27] In a study of 1,870 healthcare workers in South Korea, 12% (229) tested positive for TB, and those of advanced age were 0.96 times more likely to develop the disease. [33] In a cross-sectional study assessing the burden of LTBI among health workers in Afghanistan, with 4,648 health workers, the prevalence of latent TB infection was 47.2% (1,738 workers). [37] In Germany, the prevalence of LTBI is estimated at 10% based on examinations carried out in connection with the country’s occupational and preventive medicine. [38]

Authors have found that nursing staff in hospitals are the most at risk of contracting TB, which corroborates the results of this review, which shows that nursing staff are the most likely to fall ill with TB. In addition, the disease is highly prevalent among other professional categories, such as healthcare assistants and maintenance workers, radiology technicians, pharmacists, physiotherapists, nutritionists, and medical students. [28]

Health workers, in addition to being at increased risk of developing TB due to their working environment, as already noted, are also at risk of developing drug-resistant TB compared to the general population. [40]

However, when analyzing Brazilian studies on TB in health workers, there is a gap in knowledge, in other words, invisibility. [41] Furthermore, controlling TB effectively is a matter of extreme concern since the lack of research in a given area of knowledge makes this population invisible to public health policies, leading to negative consequences for workers’ health and a lack of health coverage and prevention.

In order to achieve the ambitious targets set by the WHO through the End TB by 2035 strategy, countries need to incorporate innovation, investment, and the authority of effective public policies that reach vulnerable populations, including health workers. [9,13] The burden of TB on healthcare workers is a negative labor-related factor and, due to its nosocomial transmission, can make it difficult to achieve the goals of eliminating and eradicating TB since healthcare workers act as a reservoir of the bacillus, thus contributing to maintaining the cycle of transmission of the disease in society. [28]

The transmission of TB in health services to workers is related to non-existent or inadequate infection control measures, especially in places with few material and physical resources. [28,31] This risk is proportionally more alarming in low- and middle-income countries due to increased exposure and the lack of preventive measures, such as poor ventilation in the workplace and inadequate precautions during sputum collection and bronchoscopy. [38]

Other occupational risk factors associated with LTBI include being a nurse, a diabetic, a smoker, being over 35 years old, working in cleaning services, hospitalization units with high patient turnover, assisting people living with HIV, not having been vaccinated with Bacille Calmette-Guérin or being immunocompromised. [37]

Thus, investment in research, policies and programs aimed at this high-priority population must be implemented and incorporated, especially in countries that have a high burden of circulating TB. In addition, by incorporating measures in health services to protect against ILTB through TB Preventive Therapy (TPT), with the implementation of this measure in health services, there is a potential reduction in the risk of progression of the disease by up to 90%; TPT aims to eliminate bacteria during their dormant state, thus maintaining a low rate of progression of the bacillus in the work environment, which consequently reduces transmission among health workers. [38]

To reduce the rate of contamination among healthcare workers, it is recommended to implement screening and treatment of ILTB to prevent TB development among workers and transmission to other individuals. [42] Furthermore, a systematic review [43] highlighted the need to standardize methods for researching TB recurrence, promote actively seeking prevention of drug resistance, facilitate treatment retention and provide integrated care for patients with HIV that can reduce recurrence rates. Some countries, such as China, include in their institutional policies annual screening for ILTB among workers at high risk of exposure, as well as treatment. [36]

Therefore, to invest in data reduction measures associated with the risk of bacillus contamination in the occupational environment, it is essential that managers recognize the risk factors and develop actions and strategies for minimizing, reducing, and eliminating the risk of developing and maintaining TB in the occupational environment.

It should be noted that studies have pointed to weaknesses in the implementation of infection control measures in health services, resulting in health professionals understanding that only the use of personal protective equipment is sufficient for individual and collective protection. There is still a lack of knowledge on the part of many health professionals about the importance of screening as a biosafety measure. [41]

Health institutions must carry out periodic screening programs to identify and monitor TB among health workers and establish effective administrative, environmental, and individual protection measures to prevent infection in professionals at risk of exposure to M. tuberculosis. These measures are necessary because they contribute to achieving the targets set by the WHO. [33]

Considering the above, it should be emphasized that the risk of acquiring TB in the workplace among health workers, especially those on the front line, is real. As such, joint actions are needed between these workers and managers to implement TB prevention strategies, reduce the number of illnesses, and provide appropriate treatment.

Finally, it is important to emphasize that systematic reviews are at the top of the levels of evidence and that this study rigorously followed the JBI recommendations to find evidence on the prevalence and factors associated with TB in healthcare workers. However, as a limitation of the study, it is important to mention that this meta-analysis should be interpreted considering the methodological quality of the studies included, and another limitation is the heterogeneity of the studies, which made further comparisons impossible.

5. Conclusions

This review provided relevant data on TB in health workers and helped to identify the risk factors associated with its infection. There is a need for early diagnosis of TB in the workplace and ongoing education with a rigorous preventive strategy to control contamination and spread, both in the workplace and in the social environment where the professional is inserted.