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SUPPLEMENT ARTICLE
Tuberculosis Infection Control in Resource-Limited
Settings in the Era of Expanding HIV Care
and Treatment
Naomi N. Bock,1 Paul A. Jensen,2 Bess Miller,1 and Edward Nardell3,4
1
Global AIDS Program and 2Division of Tuberculosis Elimination, Centers for Disease Control and Prevention, Atlanta, Georgia; 3Division of Social
Medicine and Health Inequalities, Brigham and Women’s Hospital, Harvard Medical School, and 4Partners In Health, Boston, Massachusetts
The opportunities for human immunodefiency virus (HIV) care and treatment created by new treatment
initiatives promoting universal access are also creating unprecedented opportunities for persons with HIVassociated immunosuppression to be exposed to patients with infectious tuberculosis (TB) within health care
facilities, with the attendant risks of acquiring TB infection and developing TB disease. Infection control
measures can reduce the risk of Mycobacterium tuberculosis transmission even in settings with limited resources,
on the basis of a 3-level hierarchy of controls, including administrative or work practice, environmental
controls, and respiratory protection. Further research is needed to define the most efficient interventions. The
importance of preventing transmission of M. tuberculosis in the era of expanding HIV care and treatment in
resource-limited settings must be recognized and addressed.
After decades of mounting mortality from an unchecked HIV epidemic in some of the poorest countries
of the world, the 21st century has begun with an unprecedented goal of “universal access to treatment for
all who need it by 2010” [1]. Numerous governments
and nongovernmental organizations are providing
technical and financial resources to make this goal a
reality [2–6]. The irony is that the opportunities for
HIV care and treatment created by their initiatives are
also creating unprecedented opportunities for persons
with HIV-associated immunosuppression to be exposed
to infectious tuberculosis (TB) within health care facilities, with the attendant risks of acquiring infection
with Mycobacterium tuberculosis and of progression to
Potential conflicts of interest: none reported.
Financial support: Centers for Disease Control and Prevention. Supplement
sponsorship is detailed in the Acknowledgments.
The findings and conclusions in this report are those of the authors and do not
necessarily represent the views of the Centers for Disease Control and Prevention.
Reprints or correspondence: Dr. Naomi N. Bock, Centers for Disease Control
and Prevention, 1600 Clifton Rd., Mail Stop E-04, Atlanta, GA 30333 (neb2@
cdc.gov).
The Journal of Infectious Diseases 2007; 196:S108–13
2007 by the Infectious Diseases Society of America. All rights reserved.
0022-1899/2007/19604S1-0012$15.00
DOI: 10.1086/518661
S108 • JID 2007:196 (Suppl 1) • Bock et al.
TB. Health care workers themselves might have HIV
infection and, thus, might be subject to these increased
risks [7]. Thus, the importance of preventing the transmission of M. tuberculosis in the era of expanding HIV
care and treatment in resource-constrained settings
must be recognized and addressed.
Little research and limited resources have been expended on TB infection control during the past 50
years. Infection control is not a prominent feature of
the current global strategy to control TB [8]. The global
TB effort needs plans, structure, goals, indicators, and
a budget, to address the ongoing issue of institutional
transmission. The increase in the incidence of multidrug-resistant TB (MDR-TB) and the emergence of extensively drug-resistant TB (XDR-TB) among HIV-infected populations may generate the political will to
focus attention on the spigots that are producing TB
cases faster than they can be identified and treated [9,
10]. Despite growing evidence that institutional transmission is a critical factor in epidemic HIV-associated
TB and MDR-TB, many argue that the evidence proving that community transmission is not playing an
equally important role in resource-constrained settings
is not available. A top priority, then, should be to obtain
that evidence, so that resources will be directed toward
protecting workers, patients, and other occupants in buildings,
including but not limited to health care facilities, residential
AIDS facilities, prisons, refugee camps, and worker hostels.
RISK OF M. TUBERCULOSIS TRANSMISSION
The occupational risk of TB for health care workers has been
reported since the early 20th century. In 1928, an investigation
in Norway found that 95% of 220 student nurses acquired TB
infection, as documented by tuberculin skin test conversion,
by their graduation, and 22% developed TB disease [11]. Other
studies from the United States during the preantibiotic era
confirmed that health care workers were at increased risk of
developing TB disease, compared with the general population
[12, 13]. With the introduction of anti-TB chemotherapy and
ambulatory (in place of inpatient) treatment, both the overall
incidence rate in the general population and the occupational
risk of TB declined in the United States and other developed
countries until the mid-1990s. At that time, the HIV epidemic,
among other factors, led to increasing TB rates [14], and this
resurgence of TB was associated with many hospital-based TB
outbreaks. These outbreaks affected not only health care workers but also patients, most of whom had HIV infection. Most
outbreaks also involved MDR-TB [15–19].
Little information about occupational risks for TB among
health care workers in resource-constrained settings in subSaharan Africa, Asia, or Latin America was published until the
mid-1990s. At that time, reports from Thailand and Côte
d’Ivoire documented high rates of TB infection among health
care workers, with stratification showing an association of
higher infection rates with longer duration of work in health
care settings or with more patient contact [20, 21]. In Malawi
in 1996, the relative risk for TB disease among the clinical staff
of 43 hospitals providing services for patients with TB was 11.9
times that in the general population of comparable age [22].
More recently, an investigation of TB among staff at a large
urban hospital in Kenya found that, from 2001 through 2005,
TB case rates among the staff were 2–3.5 times higher than
rates in the general population [23]. In that investigation, 2
hospital-related exposures were significantly associated with TB
among staff: (1) the number of hours of patient contact and
(2) working in hospital settings where patients with TB receive
care, including inpatient medical wards, the emergency department, and the TB clinic. Factors unrelated to work, including self-reported HIV infection and living in an urban
slum, were also significantly associated with TB.
Some of the increased risk for TB disease among health care
workers in these reports is likely related to the HIV epidemic.
Health care workers have been documented to have increasing
rates of HIV infection in settings with generalized HIV epidemics [7]. HIV-infected health care workers are more likely
than health care workers without HIV infection to develop TB
from activation of preexisting latent infection [24]. They are
also, however, more likely to experience rapid progression to
disease after new infection or reinfection, which can occur in
the health care setting [25–27]. HIV-associated immunopathology has not been shown to increase the incidence of acquisition of initial infection with M. tuberculosis. Thus, the reports
of increased prevalence of infection associated with patient contact and duration of employment provide evidence of likely
transmission within health care settings.
Most of the reports cited above involve hospital inpatient
wards as sites of M. tuberculosis transmission to health care
workers and patients. However, as new HIV service settings are
established in resource-constrained areas, other potential sites
of transmission are appearing. For instance, studies in areas
with high rates of TB and HIV infection have shown that,
among persons with HIV infection accessing voluntary counseling and testing (VCT) or antenatal services, up to 11% have
previously undiagnosed TB disease [28–30]. Up to half of these
persons may have infectious TB.
In addition, several recent reports document that the incidence of TB disease remains high even after HIV-infected patients begin receiving antiretroviral therapy (ART). In Abidjan,
129 patients receiving highly active ART (HAART) had an overall incidence of TB of 4.8 cases/100 person-years [31]. In rural
Uganda, an incidence density of 3.6 cases/100 person-years was
documented among almost 1000 persons receiving HAART
[32]. Patients such as these are attending HIV care clinics and
other HIV care services, such as community support programs,
and can be a source of M. tuberculosis transmission in those
settings. Because of the dual morbidity of TB and HIV infection,
some programs are attempting to provide TB and HIV care in
one clinical setting [33]. This can improve clinical management
and is convenient for the patients affected by both diseases,
but careful attention to infection control will be necessary so
that program integration does not increase the risk of M. tuberculosis transmission.
Although M. tuberculosis transmission has not been documented frequently in the outpatient setting, in the Malawi
study, the site of work (i.e., inpatient wards vs. outpatient departments) was not significantly different between health care
workers with TB and those without TB [23]. Also, because the
diagnosis of TB disease in persons with HIV-associated immunosuppression is often delayed, particularly in those with
negative acid-fast bacilli sputum-smear results, there may be
more time for potential exposure for health care workers and
other patients [34].
TB INFECTION CONTROL
As noted above, the likelihood of persons with unsuspected
infectious TB spending time in HIV care facilities currently
being established in resource-constrained settings, with the atTB Infection Control in HIV Care Settings • JID 2007:196 (Suppl 1) • S109
tendant risk of spread of M. tuberculosis to other immunocompromised patients or to staff, is high. These settings include
any outpatient facility where HIV-infected persons receive diagnosis, care, treatment, and support, such as VCT centers,
clinics for the management of opportunistic infections, ART
clinics, and support clubs for people living with HIV infection.
Also, in some areas, primary health care clinics serve patient
populations with a high prevalence of HIV infection, as well
as with a high prevalence of TB, both recognized and undiagnosed. Inpatients on hospital medical and pediatric wards
are also likely to have a high prevalence of HIV infection.
Infection control measures can reduce the risk of M. tuberculosis transmission even in settings with limited resources [35–
37]. TB infection control is based on a 3-level hierarchy of
controls, including administrative or work practice, environmental controls, and respiratory protection [38]. Some aspects
of the controls will differ between inpatient and outpatient
settings, but the priorities and basic approaches are the same.
The Appendix contains multiple references with information
and tools for implementing TB infection control programs in
HIV care settings in resource-constrained settings. The general
principles are described here.
Work practice and administrative control measures are the
first line of defense against M. tuberculosis transmission within
facilities caring for people with HIV infection. Their goals are
to prevent exposure of staff and patients to TB and to reduce
the spread of infection by ensuring rapid and appropriate diagnostic investigation and treatment for patients and staff suspected or known to have TB. This can best be accomplished
through the prompt recognition and separation of persons with
potentially infectious TB disease, followed by prompt provision
of TB and HIV services. Components to good work practice
and administrative controls include the following [37]:
• An infection control plan
• Administrative support for procedures in the plan, including quality assurance
• Training of staff
• Education of patients and increasing community awareness
• Coordination and communication between the HIV and
TB programs
Environmental controls are the second line of defense for
preventing the spread of TB in HIV care settings; however,
administrative controls must be in place to ensure the proper
operation and sustainability of these environmental controls.
It is important to recognize that if work practice or administrative controls are inadequate, environmental controls may not
reduce risk as effectively. Environmental controls include ventilation (natural and mechanical), room air cleaners (generally
filters or UV germicidal irradiation [UVGI]), or UVGI in the
upper room. The optimal use of interior space to reduce crowding is both an administrative and environmental issue.
S110 • JID 2007:196 (Suppl 1) • Bock et al.
Some environmental control measures are technologically
complex and expensive and, thus, more appropriate for referral
hospitals. However, well-designed natural ventilation can reduce the risk of spreading TB. Natural ventilation relies on
“free movement” of air through open doors and windows. Even
in warm climates, however, windows and doors are often closed
tight for security and warmth at night, when patients are most
likely to be indoors, thereby limiting the efficacy of natural
ventilation unless the building is designed with consideration
of natural ventilation. Fans (exhaust and mixing) or “open
ventilation channels” may also assist in this process and distribute the air. If patients are asked to provide sputum specimens for TB diagnosis on site, they should always do so outside
in the open air and away from other people or in a specially
ventilated booth, not in small rooms such as bathrooms or
other enclosed areas.
Under high-risk conditions, where ventilation alone is estimated to be insufficient, the use of upper-room UVGI may be
indicated. Studies show that M. tuberculosis organisms are killed
if they are exposed sufficiently to UVGI, although efficacy is
reduced when relative humidity is 170%, which is a common
condition in many resource-limited settings. The goal in the
design and installation of upper-room UVGI is to maximize
the UVGI in the upper room and maintain the UVGI at a level
in the occupied space that will cause no harm to occupants.
Financial investment is required for initial installation costs,
but maintenance costs are relatively low. With poor maintenance, such as allowing dust to cover the lamps or not replacing
lamps on schedule, efficacy may be reduced.
With a slight increase in resources over UVGI, a ventilation
system can supply air at one location in a room; this air is
swept across the room and exhausted at the other end. This is
quite cost-effective in areas with moderate climates. In some
regions, however, air must be heated in the winter to ensure
that the ventilation provides tempered air to occupied spaces;
if it is not, then the ventilation will not be a sustainable intervention, because of staff or patients turning it off.
The last tier of protection for health care workers is respiratory protection. If fitted and used properly to prevent faceseal leaks, a personal respirator can, in theory, greatly reduce
the chance that inhaled air will contain infectious tubercle bacilli. Even a poor respirator or face mask that filters only 50%
of inhaled particles has the equivalent effect, in theory, of a
doubling of room ventilation, and at a fraction of the cost.
Perhaps the greatest limitation of respiratory protection, however, is that it cannot be worn continuously and is unlikely to
be in place when treating a patient with unsuspected infectious
TB. Respirator use is clearly indicated during high-risk procedures, such as sputum induction, bronchoscopy, or postmortem examinations. Under those circumstances, formal
training and periodic fit testing has been recommended for
maximum performance [38].
One final issue critical to TB infection control is that of
increasing access to VCT and to HIV care—including ART, if
indicated—among health care workers. Encouraging and enabling health care workers and all staff to know their HIV
infection status should be a priority of all health care services
and of HIV care programs, in particular. The rate of HIV infection among health care workers and staff may be similar or
even higher than that in the broader community [7]. In the
past, stigma, lack of confidentiality, and lack of treatment options have contributed to failure of health care workers to know
their HIV infection status. These conditions are changing [1].
Encouraging and enabling health care workers and all institutional staff to know their HIV infection status can be facilitated by providing accessible, acceptable, and confidential VCT.
Policies that prioritize ART for health care workers and staff
who need it can motivate such individuals to know their HIV
infection status. Similarly, training and policies should be in
place to enable health care workers and staff to recognize early
symptoms of TB in themselves and to seek clinical evaluation
without fear of stigma in the workplace. Health care workers
are a valuable resource, and they must receive adequate care
and treatment to remain healthy and in the workforce. Furthermore, HIV-infected health care workers and other staff are
at increased risk of developing TB disease if exposed in the
workplace, and additional precautions should be taken to protect them. Immunocompromised health care workers should
be given opportunities to work in areas with a lower risk of
exposure to TB.
THE NEED FOR ADDITIONAL RESEARCH
The current level of knowledge about the most effective TB
infection control practices in resource-limited settings is far
from complete. However, operational research can further inform practice. Areas in which carefully collected and analyzed
data would be useful include the following:
• Screening tools and algorithms to quickly identify potentially infectious patients with TB presenting for HIV
services
• Strategies for increasing the proportion of health care
workers who know their HIV infection status and are
able to access adequate care, including ART and isoniazid
preventive therapy
• Designs for enhancing total air flow and air flow direction
through semicontrolled natural ventilation
• Utility of UVGI in resource-limited settings
• Feasibility of prolonged treatment with isoniazid or other
effective agents for prevention of TB in immunocompromised health care workers
• Interventions with health care workers that reduce stig-
•
ma toward patients with HIV infection and TB/HIV
coinfection
Cost-benefit analyses of infection control interventions
in resource-limited settings
BEYOND HEALTH CARE SETTINGS
Although this discussion focuses on health care settings in an
era of expanding ART, these same persons come together in
many other institutional settings where transmission is as likely
and where similar interventions are possible. These congregate
settings include but are not limited to residential AIDS facilities,
prisons, jails, and refugee camps. Specific recommendations for
some of these settings are included in the Appendix.
Acknowledgments
Supplement sponsorship. This article was published as part of a supplement entitled “Tuberculosis and HIV Coinfection: Current State of
Knowledge and Research Priorities,” sponsored by the National Institutes
of Health Division of AIDS, the Centers for Disease Control and Prevention
Division of TB Elimination, the World Bank, the Agence Nationale de
Recherches sur le Sida et les Hépatites Virales, and the Forum for Collaborative HIV Research (including special contributions from the World
Health Organization Stop TB Department, the International AIDS Society,
and GlaxoSmithKline).
APPENDIX
ADDITIONAL RESOURCES
TUBERCULOSIS INFECTION CONTROL
•
•
•
•
Centers for Disease Control and Prevention. Guidelines
for preventing the transmission of Mycobacterium tuberculosis in health-care facilities. MMWR Recomm Rep
1994; 43(RR-13):1–132. Available at: http://www.cdc.gov/
mmwr/preview/mmwrhtml/00035909.htm. Accessed 6
June 2007.
World Health Organization (WHO). Guidelines for the
prevention of tuberculosis in health care facilities in resource-limited settings. Geneva: WHO, 1999. Available at:
http://www.who.int/docstore/gtb/publications/healthcare/
PDF/WHO99-269.pdf. Accessed 6 June 2007.
Jensen PA, Lambert LA, Iademarco MF, Ridzon R, for
the Centers for Disease Control and Prevention. Guidelines for preventing the transmission of Mycobacterium
tuberculosis in health-care settings, 2005. MMWR Recomm Rep 2005; 54(RR-17):1–141. Available at: http://
www.cdc.gov/mmwr/preview/mmwrhtml/rr5417a1.htm.
Accessed 6 June 2007.
World Health Organization, Centers for Disease Control
and Prevention (CDC). Tuberculosis infection control in
the era of expanding HIV care and treatment: addendum
TB Infection Control in HIV Care Settings • JID 2007:196 (Suppl 1) • S111
to WHO Guidelines for the Prevention of Tuberculosis
in Heath Care Facilities in Resource-Limited Settings,
1999. Atlanta: CDC, 2007. Available at: http://www.cdc
.gov/nchstp/od/gap/docs/InfectionControlAddendum_2
-20-07.pdf. Accessed 14 June 2007.
The following guidelines were developed for the US domestic
situation but contain useful material:
• Francis J. Curry National Tuberculosis Center, Institutional Consultation Services. A guideline for establishing
effective practices: identifying persons with infectious
TB in the emergency department. 1998. Available at:
http://www.nationaltbcenter.edu/catalogue/downloads/
emergencyRoomGuidelines.pdf. Accessed 6 June 2007.
• Francis J. Curry National Tuberculosis Center, Institutional Consultation Services, and California Department
of Health Services. TB in homeless shelters: reducing the
risk through ventilation, filters, and UV. 2000. Available
at: http://www.nationaltbcenter.edu/catalogue/downloads/
tbhomelessshelters.pdf. Accessed 6 June 2007.
TB/98.255; UNAIDS/98.34. Geneva: WHO, 1998. Available at: http://www.who.int/docstore/gtb/publications/
TB_HIV_polstmnt/PDF/tbhivpolicy.pdf. Accessed 6 June
2007.
MULTIDRUG-RESISTANT TUBERCULOSIS
•
•
•
TUBERCULOSIS AND HIV INFECTION
•
•
•
•
World Health Organization (WHO). Strategic framework to decrease the burden of TB/HIV. Geneva: WHO,
2002. Available at: http://www.who.int/docstore/gtb/
publications/tb_hiv/2002_296/pdf/tb_hiv_2002_296_en
.pdf. Accessed 6 June 2007.
World Health Organization (WHO). Report of a “Lessons
Learnt” workshop on the six ProTEST pilot projects in
Malawi, South Africa and Zambia. WHO/HTM/TB/
2004.336. Geneva: WHO, 2004. Available at: http://
whqlibdoc.who.int/hq/2004/WHO_HTM_TB_2004.336
.pdf. Accessed 6 June 2007.
World Health Organization (WHO). A guide to monitoring and evaluation for collaborative TB/HIV activities:
field test version. Geneva: WHO, 2004. Available at: http:
//whqlibdoc.who.int/hq/2004/WHO_HTM_TB_2004.342
.pdf. Accessed 6 June 2007.
World Health Organization (WHO). TB/HIV: a clinical
manual. 2nd ed. Geneva: WHO, 2004. Available at: http:
//whqlibdoc.who.int/publications/2004/9241546344.pdf.
Accessed 6 June 2007.
South African Medical Research Council/National Department of Health. The management of multi-drug resistant tuberculosis in South Africa. 2nd ed. South African
Medical Research Council/National Department of Health,
1999.
South African Medical Research Council/National Department of Health. DOTS-Plus for standardized management of multi-drug resistant tuberculosis in South Africa—policy guidelines. South African Medical Research
Council/National Department of Health, 2004.
World Health Organization (WHO)/International Union
Against Tuberculosis and Lung Disease Global Project on
Anti-tuberculosis Drug Resistance Surveillance. Anti-tuberculosis drug resistance in the world: report no. 3.
WHO/HTM/TB/2004.343. Geneva: WHO, 2004. Available at: http://www.who.int/tb/publications/who_htm_tb
_2004_343/en/index.html. Accessed 6 June 2007.
CORRECTIONAL INSTITUTIONS
•
World Health Organization (WHO). Tuberculosis control
in prisons: a manual for programme managers. WHO/
CDS/TB/2000.281. Geneva: WHO, 2000. Available at: http:
//www.who.int/docstore/gtb/publications/prisonsNTP/
PDF/tbprisonsntp.pdf. Accessed 6 June 2007.
The following guidelines were developed for US domestic
situation but contain useful material:
• Francis J. Curry National Tuberculosis Center, California
Department of Health Services. Tuberculosis infection control plan template for jails. 2002. Available at: http://www
.nationaltbcenter.edu/jailtemplate/docs/tb_section1.pdf.
Accessed 7 June 2007.
LABORATORY ISSUES
ISONIAZID PREVENTIVE THERAPY
•
World Health Organization (WHO) Global Tuberculosis
Programme, Joint United Nations Programme on HIV/
AIDS (UNAIDS). Policy statement on preventive therapy
against tuberculosis in people living with HIV: report of
a meeting held in Geneva 18–20 February 1998. WHO/
S112 • JID 2007:196 (Suppl 1) • Bock et al.
•
World Health Organization (WHO). Strategic approach for
the strengthening of laboratory services for tuberculosis
control, 2006–2009. WHO/HTM/TB/2006.364. Geneva:
WHO, 2006. Available at: http://whqlibdoc.who.int/hq/
2006/WHO_HTM_TB_2006.364_eng.pdf. Accessed 7 June
2007.
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