In October 2015, the World Health Organization (WHO) reported that tuberculosis now ranks alongside human immunodeficiency virus (HIV) as the leading cause of death worldwide, with >1.5 million deaths and 9.6 million new active cases in 2014. The majority of these tuberculosis cases occur in the 22 high-burden countries, where the healthcare systems are often fragile and underresourced. It comes as no surprise that healthcare workers (HCWs) are disproportionately affected by contagious conditions such as Ebola virus disease, influenza virus, and tuberculosis. The emergence of multidrug-resistant (MDR) tuberculosis, which now accounts for 3.3% of new tuberculosis cases and 20% of repeat tuberculosis cases, and extremely drug-resistant tuberculosis, which accounts for 10% of MDR tuberculosis, also increases the risk to HCWs, especially in areas of high HIV seroprevalence. In this supplement, many of the risks, issues, and possible solutions to the ongoing problem of transmission of tuberculosis to the healthcare workforce are addressed.
Verkuijl et al [1] discuss the main pillars of the approach to tuberculosis infection control: managerial and administrative, environmental, and utilization of personal protective equipment (PPE). They present data that in underresourced settings, the initial step of a managerial plan, including policy setting, facility assessment, and annual planning, is only rarely implemented [2]. Likewise, administrative work practices such as triage, redeployment of HIV-infected staff to lower-risk settings, and practice guidelines for diagnoses, are equally rarely followed [3]. In surveys in sub-Saharan Africa, environmental controls that extend beyond using open ventilation, such as the implementation of ultraviolet germicidal irradiation, are generally not even acknowledged or known, much less practiced. Verkuijl et al further contend that there is an overemphasis on the role of PPE, despite the fact that it is intermittently used, not appropriately fit-tested, and frequently too expensive to be readily available. Encouragingly, they describe a test case program in Eastern Cape Province, South Africa, where all the pillars are implemented with little monetary infusion, but to a greater extent due to the will of management and staff.
Van Cutsem et al [4] point out the inadequacy of the worldwide DOTS (directly observed treatment, short-course) program to address the issue of MDR tuberculosis, with <20% of the 450 000 annual cases receiving treatment [5]. They highlight the fallacy that in high-burden countries, tuberculosis is contained and only occurs in tuberculosis clinics and wards. They point out studies in which HCWs in other areas are as vulnerable to tuberculosis risk as those who are confined to work in tuberculosis areas [6, 7]. The potential broadened use of a specific tool for infection control, the FAST approach (Find cases Actively, Separate safely, and Treat effectively) is emphasized, although difficult when <10% of the Mycobacterium tuberculosis isolates from hospitalized patients undergo drug sensitivity testing. The rapid rise in MDR tuberculosis [8], and the fact that MDR and XDR tuberculosis are rarely identified and thus appropriately treated, only compound the problem. One solution is decentralized care with universal precautions, rather than targeted ones, in high-incidence settings. They point out that the cost of MDR tuberculosis, at US$8300 per case in South Africa, or single case of XDR tuberculosis, which in the United States approaches US$500 000 per person [9], and which is massively impacting multiple countries' healthcare budgets, justifies the cost of implementing such measures. As with the findings of other authors in this series, an overemphasis on PPE has led to complacency in addressing the issue more systematically.
One issue with many of the needed policies and procedures is the stigma associated with either tuberculosis, HIV, or both in the healthcare setting. Most everyone may agree on the need to address the issue, but woefully little work has been done to develop appropriate tools to measure stigma in order to study the impact of any given intervention. Wouters and colleagues begin to address this gap by examining stigma in the hospital setting that is both internalized and externalized [10]. The 7 quantitative scales they develop address the relationship between internal and external stigma, and will be a useful starting point to examine the new tools and interventions that would decrease the risk of nosocomial transmission of tuberculosis to the HCW.
Tudor et al examine the risk factors for tuberculosis disease in HCWs over a 5-year period in KwaZulu-Natal, South Africa [11]. They point out that 11%–16% of the HCWs in South Africa are infected with HIV, and that HIV is the single greatest risk factor for tuberculosis in HCWs in this region. Contact in the tuberculosis ward in their setting is also a risk, and they emphasize the need to identify, help, and not stigmatize those who are living with HIV.
The WHO has acknowledged that the elimination of tuberculosis in general, and the associated risk to HCWs, cannot be achieved without the effective deployment of interventions that work as well as development of new tools, such as novel diagnostics and vaccines. In addition, a better understanding of latent infection is also urgently needed. Hatherill et al review the history of tuberculosis and vaccines in HCWs, and point out that most HCW infections are not acquired in the community [12]. They call attention to the data supporting the use of BCG vaccine in those who are BCG naive, not latently infected, and entering a high-risk setting, and note that many countries have adopted such a policy for their HCWs who provide care in high-risk environments [13]. The issue and potential role of revaccination in certain populations is also explored [14, 15]. The authors cover some of the issues concerning enrolling HCWs into clinical trials, and emphasize the extraordinarily high rates of new infection in naive HCWs such as residents or newly graduated nurses just entering the workforce.
These public health challenges also raise bioethical and legal issues. A timely article by Boulanger et al [16] provides an overview of some of the most important ethical considerations related to tuberculosis prevention from the perspective of HCWs: fairness in ensuring equal pay for community workers or family members who provide care in a nonprofessional setting; the concept of duty to serve and administer healthcare when one puts one's own life at risk; and the use of HCWs as subjects in clinical trials.
Last, von Delft et al [17] remind us that the issue of tuberculosis in HCWs is not about numbers, controls, policies, and finances, but about human beings who are our friends and coworkers. Individuals entering the field of healthcare are young, and often carry a sense of invincibility and an indifference to the threat of their surroundings. They work in a setting where there is a scarcity of trained HCWs, and where there is no financial compensation to students (vs employees) for occupational health and safety. The authors discuss the sense of stigma—even shame—and the inability to cope with the demands of treatment while continuing to work or train.
The world responded to the Ebola epidemic, which in the entire 2014–2015 outbreak killed as many people as die in 3 days from tuberculosis, with an infusion of funds estimated at US$4 billion. The United States responded to the crisis of MDR tuberculosis in New York City in the early 1990s with a similarly massive influx of funding, estimated to be nearly US$1 billion. A person dies every 21 seconds from tuberculosis, some of whom are frontline caregivers, DOTS supporters, and healthcare professionals. The end of the tuberculosis epidemic, as called for by the WHO, will require a proactive and urgent mobilization of resources, political will, and innovation, which must start with active protection of our health workforce.
Notes
Supplement sponsorship. This article appears as part of the supplement “Healthcare Workers and Tuberculosis Prevention,” sponsored by Aeras.
Potential conflict of interest. T. G. E. has received funding from Aeras. L.-G. B. has received funding from the National Institutes of Health, South Africa Department of Science and Technology, Aeras, and the Bill & Melinda Gates Foundation. Both authors have submitted the ICMJE Form for Disclosure of Potential Conflicts of Interest. Conflicts that the editors consider relevant to the content of the manuscript have been disclosed.
References
- 1.Verkuijl S, Middelkoop K. Protecting our front-liners: occupational tuberculosis prevention through infection control strategies. Clin Infect Dis 2016; 62(suppl 3):S231–7. [DOI] [PubMed] [Google Scholar]
- 2.Gupta S, Granich R, Date A et al. Review of policy and status of implementation of collaborative HIV-TB activities in 23 high-burden countries. Int J Tuberc Lung Dis 2014; 18:1149–58. [DOI] [PubMed] [Google Scholar]
- 3.Naidoo S, Seevnarain K, Nordstrom DL. Tuberculosis infection control in primary health clinics in eThekwini, KwaZulu-Natal, South Africa. Int J Tuberc Lung Dis 2012; 16:1600–4. [DOI] [PubMed] [Google Scholar]
- 4.van Cutsem G, Isaakidis P, Farley J, Nardell E, Volchenkov G, Cox H. Infection control for drug-resistant tuberculosis: early diagnosis and the treatment is the key. Clin Infect Dis 2016; 62(suppl 3):S238–43. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.World Health Organization. Global tuberculosis report 2014. Geneva, Switzerland: WHO, 2014. [Google Scholar]
- 6.Tudor C, Van der Walt M, Margot B et al. Tuberculosis among health care workers in KwaZulu-Natal, South Africa: a retrospective cohort analysis. BMC Public Health 2014; 14:891. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Escombe AR, Huaroto L, Ticona E et al. Tuberculosis transmission risk and infection control in a hospital emergency department in Lima, Peru. Int J Tuberc Lung Dis 2010; 14:1120–6. [PubMed] [Google Scholar]
- 8.World Health Organization. Multidrug-resistant tuberculosis (MDR-TB): 2014 update. Geneva, Switzerland: WHO, 2014. [Google Scholar]
- 9.Cox H, Ramma L, Wilkinson L, Azevedo V, Sinanovic E. Cost per patient of treatment for rifampicin-resistant tuberculosis in a community-based program in Khayelitsha, South Africa. Trop Med Int Health 2015; 20:1337–45. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Wouters E, Rau A, Engelbrecht M et al. The developing and piloting of parallel scales measuring external and internal HIV and tuberculosis stigma among healthcare workers in the free state province, South Africa. Clin Infect Dis 2016; 62(suppl 3):S244–54. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11.Tudor C, Van der Walt M, Margot B et al. Occupational risk factors for tuberculosis among healthcare workers in KwaZulu-Natal, South Africa. Clin Infect Dis 2016; 62(suppl 3):S255–61. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12.Hatherill M, Scriba TJ, Udwadia ZF et al. BCG and new preventive tuberculosis in vaccines: implications for healthcare workers. Clin Infect Dis 2016; 62(suppl 3):S262–7. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Bjartveit K. Olaf Scheel and Johannes Heimbeck: their contribution to understanding the pathogenesis and prevention of tuberculosis. Int J Tuberc Lung Dis 2003; 7:306–11. [PubMed] [Google Scholar]
- 14.Dye C. Making wider use of the world's most widely used vaccine: Bacille Calmette-Guerin revaccination reconsidered. J R Soc Interface 2013; 10:20130365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 15.Mangtani P, Abubakar I, Ariti C et al. Protection by BCG vaccine against tuberculosis: a systematic review of randomized controlled trials. Clin Infect Dis 2014; 58:470–80. [DOI] [PubMed] [Google Scholar]
- 16.Boulanger RF, Hunt MR, Benatar SR. Where caring is sharing: evolving ethical considerations in tuberculosis prevention among healthcare workers. Clin Infect Dis 2016; 62(suppl 3):S268–74. [DOI] [PubMed] [Google Scholar]
- 17.von Delft A, Dramowski A, Sifumba Z et al. Exposed, but not protected: more is needed to prevent drug-resistant tuberculosis in healthcare workers and students. Clin Infect Dis 2016; 62(suppl 3):S275–80. [DOI] [PubMed] [Google Scholar]
