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SUPPLEMENT ARTICLE
Optimizing the Protection of Research Participants and
Personnel in HIV-Related Research Where TB Is Prevalent:
Practical Solutions for Improving Infection Control
Jason E. Farley, PhD, MPH, CRNP,*†Timothy F. Landers, PhD, CNP,‡
Catherine Godfrey, MD, FRACP,§ Virginia Lipke, RN, MHA, ACRN, CIC,k
and Jeremy Sugarman, MD, MPH, MA¶#†
Abstract: Tuberculosis (TB) is a leading cause of death among
persons with HIV globally. HIV-related research in TB endemic
areas raises some unique and important ethical issues in infection
control related to protecting both research participants and personnel.
To address such concerns, this article provides practical guidance to
help research teams develop strategies to prevent TB transmission in
studies involving persons with HIV in TB endemic settings.
Key Words: infection control, TB, HIV, clinical research, human
subjects protections, ethics
(J Acquir Immune Defic Syndr 2014;65:S19–S23)
Tuberculosis (TB) caused by Mycobacterium tuberculosis
is a leading cause of death among persons with HIV.
1
Molecular epidemiologic evaluations clearly demonstrate
hospital-associated transmission of TB in settings with high
HIV prevalence.
2,3
Research participants and personnel con-
ducting HIV-related research may be exposed to TB, includ-
ing drug-resistant TB strains through airborne exposure.
Gathering participants for research purposes in some settings
may therefore increase risk of transmission to research par-
ticipants and personnel. Visit frequency, duration, the prox-
imity to other participants, and many environmental factors
affect this risk. Indeed, incident TB is often a primary out-
come of clinical trials attempting to define the best strategies
for preventing HIV infection or treating those who are in-
fected.
4,5
Even in the best of circumstances with active case
finding and policies which require isolating individuals with
cough,
6
crowded waiting rooms, long study visits, and facil-
ities with poor ventilation bring potentially infectious people
in close contact with research personnel and research partic-
ipants who are at high risk for developing TB. HIV-infected
patients are more commonly sputum smear negative for TB
than HIV-uninfected patients, but they remain infectious and
the diagnosis of TB may be delayed.
7
In settings where TB is prevalent, trial design and
conduct should account for factors that may pose additional
risks to research participants and take measures to minimize
them. Incorporating TB infection control (TBIC) into research
may be challenging because evidence-based infection control
practices have not been adopted in many clinical and
community settings where HIV-related research may be
conducted.
8–13
The AIDS Clinical Trials Group has adopted
a guideline for TB prevention at its clinical sites, but it is
unclear whether similar approaches are being implemented
in other research settings. Furthermore, there remains a pau-
city of literature on the implementation of TBIC measures
14
and infection control measures
15
specifically in HIV-related
research settings.
16–19
However, it is clear that biomedical
interventions that may be included in HIV-related research,
such as intensified case findings, rapid diagnostics, access to
isoniazid preventative therapy to prevent activation of TB,
and earlier antiretroviral therapy
20
confer TB prevention ben-
efits both directly to the recipient of the intervention and to
others as a result of decreased opportunities for exposure.
21,22
Regardless, to minimize risk of TB transmission, it is essential
that research teams implement comprehensive approaches to
TB prevention that incorporate both biomedical interventions
From the *Johns Hopkins University School of Nursing, Department of Com-
munity and Public Health, Baltimore, MD; †Johns Hopkins Center for
AIDS Research (CFAR), Baltimore, MD; ‡The Ohio State University Col-
lege of Nursing, Columbus, OH; §National Institute of Allergy and Infec-
tious Diseases (NIAID), National Institutes of Health, Bethesda, MD;
kDivision of Global HIV/AIDS (GAP), Centers for Disease Control and
Prevention, Atlanta, GA; ¶Johns Hopkins Berman Institute of Bioethics;
and #Johns Hopkins University School of Medicine, Baltimore, MD.
This publication proposal was made possible with help from the Johns
Hopkins University Center for AIDS Research, a National Institutes of
Health (NIH)–funded program (1P30AI094189), which is supported
by the following NIH cofunding and participating Institutes and
Centers: National Institute of Allergy and Infectious Disease, NCI,
National Institute of Child Health and Human Development, National
Heart, Lung, and Blood Institute, National Institute of Drug Abuse,
National Institute of Mental Health, National Institute on Aging, FIC,
and OAR. Work on this article was also supported in part by the
National Institute of Allergy and Infectious Disease, National Institute
of Drug Abuse and the National Institute of Mental Health under
Cooperative Agreement # UM1AI068619 to the HIV Prevention
Trials Network.
The findings and conclusions in this report are those of the author (V.L.) and
do not necessarily represent the official position of the Centers for
Disease Control and Prevention/the Agency for Toxic Substances and
Disease Registry.
The authors have no conflicts of interest to disclose.
This article was written by C.G. in her capacit y as an NIH employee, but the
views expressed in this paper do not necessarily represent those of the
NIH.
Correspondence to: Jason E. Farley, PhD, MPH, CRNP, Johns Hopkins
University School of Nursing, 525 N. Wolfe Street, Suite 525, Baltimore,
MD 21205 (e-mail: jfarley1@jhu.edu).
Copyright © 2013 by Lippincott Williams & Wilkins
J Acquir Immune Defic Syndr Volume 65, Supplement 1, January 1, 2014 www.jaids.com |S19
and system-level infection control interventions, including site-
level guidance to facilitate appropriate implementation.
In this article, we outline practical strategies for clinical
research teams in settings where TB is prevalent to follow
established TBIC practices and guidelines.
23–25
In addition to
antiretroviral therapy and appropriate biomedical management
of HIV disease, these infection control strategies are critical to
mitigate risk for research participants and personnel.
PROPOSED STEPS IN PROTECTING RESEARCH
PARTICIPANTS AND PERSONNEL
Risk Assessment
A comprehensive TB risk assessment is an essential
first step for TBIC. This begins with evaluating the settings
where initial contact with potential participants will occur.
Local TB epidemiology, administrative and environmental
controls (ECs) at the proposed sites, and available personal
protective equipment (PPE) should be reviewed. Baseline
knowledge of TBIC principles among research personnel
is a critical element in the initial assessment, and the level
of education regarding TBIC is a measurable outcome of
TBIC initiatives.
The Centers for Disease Control and Prevention has
developed a brief TBIC monitoring and evaluation checklist for
use in TB/HIV clinical settings. A modified version to facilitate
the completion of a research site risk assessment is shown in
Table 1.
26
This modified checklist for research includes the
following: (1) integrating TBIC procedures into research proto-
cols; (2) attending to managerial aspects of TBIC; (3) admin-
istrative controls; (4) ECs; and (5) promoting use of PPE among
research participants and study personnel. As delineated in
Table 1, the comprehensive approach to TBIC that is developed
should be incorporated into relevant parts of study protocols,
procedure manuals, and a managerial plan. Doing so helps to
ensure transparency, accountability, and implementation.
Administrative Controls
Administrative Controls are system-level changes
designed to decrease exposure to infectious patient-participants.
9
These standard TBIC activities include segregating coughing
participants, fast-tracking smear-positive participants, or requir-
ing participants to wear a surgical mask. Cough hygiene and use
of a simple surgical mask reduces airborne droplets
27
and
has been shown to be highly acceptable to patients in clinical
settings
28
; however, in a recent survey of research sites in
resource-limited settings, only 40% of sites had cough hygiene
information available to participants.
29
In clinical practice, these interventions are challenging
because they require oversight, adequate resources for appro-
priate implementation, and may require sensitivity training to
reduce stigma associated with mask use. Further, in many
settings, there are no enforcement requirements for these
interventions. Despite these challenges, efforts should be taken
to implement administrative controls in research sites. For
example, in designing recruitment plans, consideration should
be given to incorporating a risk reduction strategy to decrease
the likelihood of persons with active TB being in contact with
others. Sputum specimen collection should occur in a manner
that minimizes risk to others at the site, and follow-up visits
should minimize transmission risk. Consideration should also
be given toward adopting a robust TB diagnostic strategy,
intensified case finding and the ability to offer isoniazid
preventive therapy.
Environmental Controls
ECs include activities that decrease TB bacilli in the
clinical environment. Practical ECs do not require costly
renovations, and small environmental changes can make
a large difference. Adequate ventilation, measured in air
exchanges per hour (ACH), is the most commonly applied
EC and may have an important impact on infectivity. ACHs
can be determined through simple calculations, and stan-
dardized worksheets permit estimation in a variety of
clinical settings.
30
Twelve ACH are recommended in conditions requir-
ing airborne isolation and may be achievable with open
windows and cross-ventilation under the right circumstan-
ces. In determining the appropriate placement and use of
ECs, site staff should consider where study personnel meet
with potential participants, particularly those who have not
been screened or tested for TB or who are undergoing
diagnostic procedures. Examples of low-cost practical
solutions include providing a covered space for outdoor
sputum collection, covering a waiting area outdoors to
prevent long waiting time indoors, and ensuring open
window policies (including awnings that allow them to
remain open in rainy weather). Wind-driven roof turbines
are a less costly alternative to mechanical ventilation and
have been shown to meet minimum air exchange require-
ments.
31
Where funding is available, consideration should be
given to using upper-room ultraviolet germicidal irradia-
tion
32
with scheduled cleaning, working fans,
33
and a routine
maintenance plan to prevent dust and debris from collecting,
which reduces their effectiveness.
Personal Protective Equipment
Use of a simple paper mask by patients has been shown
to reduce TB transmission by more than 50% in a guinea pig
model in South Africa.
27
The use of N95 respirators in clinical
personnel (also known as FFP2 respirators) with appropriate
annual fit testing or seal checks before entering clinical areas
is a proven intervention for the prevention of nosocomial
spread of TB.
34
Although clinical settings in which drug-
resistant TB is common tend to have policies that require
PPE use, adherence to these policies may be limited, and
there are few regulatory controls regarding their enforce-
ment.
8
Research teams may be better positioned to enforce
such policies. For example, study personnel may be required
to attend annual infection control trainings and to use PPE;
failure to do so could result in a poor performance appraisal or
dismissal from duty. From the participants’perspective, im-
plemented correctly (ie, all persons attending the research site
wear a mask while inside the research setting), stigma or
Farley et al J Acquir Immune Defic Syndr Volume 65, Supplement 1, January 1, 2014
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disclosure of status is not propagated because it is an expec-
tation of everyone in the site.
PUTTING INFECTION CONTROL PLANS INTO
RESEARCH PRACTICE
Developing practical strategies for prevention of TB
transmission in HIV-related research in areas where TB is
prevalent can be accomplished with appropriate planning.
Figure 1 provides a schematic overview of the critical ele-
ments of the necessary steps in this process. Education of
personnel about TB transmission principles and personal risk
is also critical. Periodic occupational health evaluation and
training of staff can raise awareness of the importance of
TBIC.
35
As described above, internationally recognized guid-
ance for risk assessment and mitigation is available from the
Centers for Disease Control and Prevention and may be adap-
ted for the specific research study plans
26
and trainings for the
TABLE 1. TB Infection Control Monitoring and Evaluation Tool Modified for Research Sites
Scoring
Research protocol
1 The research protocol is designed with integrated measures to prevent TB transmission Y or N
2 The SOP manual or study manual identifies procedures that may increase risk of TB transmission for each team member based on their
specific duties within the study
YorN
3 The human subjects research section of the grant proposal and SOP, as appropriate, includes a plan to reduce transmission to participants and
research personnel
YorN
4 TBIC training for all personnel and investigators is complete and updated annually. Records are maintained Y or N
Managerial
5 The principal investigator has identified the individual who will regularly monitor TBIC at the research site Y or N
6 A written IC plan or checklist is available as part of the SOPs for this site Y or N
7 The facility design and participant flow have been assessed including best use of space and ventilation and documented in the IC plan in the
SOPs
YorN
8 Monitoring and evaluation of TBIC data forms are reviewed routinely and reported to the appropriate infection control personnel members
of the host facility
YorN
9 A tracking system for all TB suspects, referrals, and their sputum smear results is in place Y or N
10 A register is kept of all TB patients reported to the appropriate authority within the setting Y or N
11 All patients with TB are managed on DOT as per the national guidelines Y or N
12 Participant and visitor information on TBIC is available for all and offered by the personnel Y or N
13 Monitoring and evaluation to improve TBIC measures is conducted at this site Y or N
Administrative
14 Participants are routinely asked about cough upon entering site Y or N
15 Participants who are coughing are separated from others and “fast tracked”to the appropriate study team member Y or N
16 A “Cough Monitor”gives cough etiquette guidance and assists with triage Y or N
17 Signage for cough etiquette is present YorN
18 Sputum samples are collected in a designated area and away from others Y or N
19 Health care workers and study personnel who assist with sputum collection take necessary precautions Y or N
20 A confidential log of diagnosis and referral of all personnel who develop TB is maintained Y or N
21 Personnel receive a confidential evaluation for TB in an occupational health setting at least annually Y or N
22 Personnel are offered an HIV test annually and offered ART if positive through designated occupational health clinic or services Y or N
23 HIV-infected personnel are reassigned if requested by the worker Y or N
24 INH preventive treatment is offered to HIV-infected personnel through occupational health clinic Y or N
Environmental controls
25 Natural and/or mechanical airflow is monitored daily by personnel in all areas with infectious patients Y or N
26 Regular maintenance for directional and extractor fans is conducted and documented in a logbook Y or N
27 Signs are in place to keep doors and windows open when feasible Y or N
28 If UVGI is used, routine cleaning and maintenance is scheduled and documented Y or N
29 Participants are not crowded in hallways or waiting areas YorN
30 Outdoor area waiting is utilized YorN
Personal protective equipment
31 N-95 or FFP2 respirators are readily available for personnel and their use is required Y or N
32 Personnel have been trained on proper fit of respirators and documentation of testing is kept in a log Y or N
33 Supplies are available to coughing participants (tissues, cloths, paper masks, trash bins, etc) Y or N
34 Personnel are provided continuing education opportunities and annual exams on TBIC Y or N
35 Participants who are returning to the site for follow-up posttreatment are provided a respirator if smear or culture-positive patients will be
present at any time in the same area during the visit
YorN
DOT, directly observed therapy; IC, infection control; SOP, standard operating procedures; UVGI, ultraviolet germicidal irradiation; Y, yes; N, no.
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research team.
14
Although mathematical modeling exercises
36
provide some perspective on the relative benefit of concom-
itant interventions, the key TBIC strategy is the careful anal-
ysis of the individual circumstances of each research study
and the development of tailored standard operating proce-
dures to mitigate risk. While outside the scope of this article,
engaging local communities in TB and/or HIV research is an
important step in developing TBIC plans that have buy-in
within the targeted community.
37
CONCLUDING COMMENTS
Prevention of TB transmission in HIV-related clinical
research is an important means of helping to minimize risks
to research participants and personnel. Transmission of TB
in hospitals and clinical sites where care of patients with
HIV is given is well documented and usual practices in
research settings may be inadequate to protect against TB
transmission. To mitigate risk and protect research partic-
ipants and personnel, investigators should examine each
protocol carefully and the settings in which it will be
implemented. Conducting risk assessments during protocol
development should help to ensure that inadequacies in
TBIC could be addressed. Further research is needed on
TBIC implementation within research settings, and data on
the efficacy of these measures are required particularly given
the added costs incurred with implementation of both
biomedical and other TBIC strategies. Regulatory measures,
such as funder-driven requirements, may strengthen imple-
mentation of TBIC. Although there are emerging data on the
cost-effectiveness of biomedical interventions for TB pre-
vention,
38–40
such data for programmatic TBIC strategies
remain sparse within both clinical and research settings.
Nonetheless, until such data are available, it seems reason-
able to assume that having a keen understanding of biomed-
ical, administrative, and environmental aspects of TBIC
should help reduce the likelihood of TB transmission,
thereby optimizing the protection of research participants
and personnel.
REFERENCES
1. World Health Organization. Tuberculosis Fact Sheet [serial online].
2013. Available at: http://www.who.int/mediacentre/factsheets/fs104/en.
Accessed August 1, 2013.
2. Andrews JR, Gandhi NR, Moodley P, et al. Exogenous reinfection as
a cause of multidrug-resistant and extensively drug-resistant tuberculosis
in rural South Africa. J Infect Dis. 2008;198:1582–1589.
3. Gandhi NR, Moll A, Sturm AW, et al. Extensively drug-resistant
tuberculosis as a cause of death in patients co-infected with tuber-
culosis and HIV in a rural area of South Africa. Lancet. 2006;368:
1575–1580.
4. Severe P, Juste MA, Ambroise A, et al. Early versus standard antiretro-
viral therapy for HIV-infected adults in Haiti. N Engl J Med. 2010;363:
257–265.
5. Cohen MS, Gay CL. Treatment to prevent transmission of HIV-1. Clin
Infect Dis. 2010;50(suppl 3):S85–S95.
6. Burgess AL, Fitzgerald DW, Severe P, et al. Integration of tuberculosis
screening at an HIV voluntary counselling and testing centre in Haiti.
AIDS. 2001;15:1875–1879.
7. Kanaya AM, Glidden DV, Chambers HF. Identifying pulmonary tuber-
culosis in patients with negative sputum smear results. Chest. 2001;120:
349–355.
8. Farley JE, Tudor C, Mphahlele M, et al. A national infection control
evaluation of drug-resistant tuberculosis hospitals in South Africa. Int J
Tuberc Lung Dis. 2012;16:82–89.
9. Kompala T, Shenoi SV, Friedland G. Transmission of tuberculosis in
resource-limited settings. Curr HIV/AIDS Rep. 2013;10:264–272.
10. Reid MJ, Saito S, Nash D, et al. Implementation of tuberculosis infection
control measures at HIV care and treatment sites in sub-Saharan Africa.
Int J Tuberc Lung Dis. 2012;16:1605–1612.
FIGURE 1. Framework for risk assess-
ment, protocol, and SOP develop-
ment in TBIC activities in HIV-related
research.SOP,standardoperating
procedures; CAB, community advi-
sory board.
Farley et al J Acquir Immune Defic Syndr Volume 65, Supplement 1, January 1, 2014
S22 |www.jaids.com Ó2013 Lippincott Williams & Wilkins
11. Woith W, Volchenkov G, Larson J. Barriers and motivators affecting
tuberculosis infection control practices of Russian health care workers.
Int J Tuberc Lung Dis. 2012;16:1092–1096.
12. Chai SJ, Mattingly DC, Varma JK. Protecting health care workers from
tuberculosis in China: a review of policy and practice in China and the
United States. Health Policy Plan. 2013;28:100–109.
13. Menon S. Preventing nosocomial MDR TB transmission in sub Saharan
Africa: where are we at? Glob J Health Sci. 2013;5:200–210.
14. Cobelens F, van Kampen S, Ochodo E, et al. Research on implementa-
tion of interventions in tuberculosis control in low- and middle-income
countries: a systematic review. PLoS Med. 2012;9:e1001358.
15. Legido-Quigley H, Montgomery CM, Khan P, et al. Integrating tubercu-
losis and HIV services in low- and middle-income countries: a systematic
review. Trop Med Int Health. 2013;18:199–211.
16. Heilig CM, Chia D, El-Sadr W, et al. Unaccepatable, acceptable. “Jus-
tifying research risks in a clinical trial for treatment of multidrug-resistant
tuberculosis.”IRB. 2011;10–17.
17. Bayer R, Greco DB, Ramachandran R. The ethics of clinical and epide-
miological research. Int J Tuberc Lung Dis. 2011;15(suppl 2):S25–S29.
18. Davidow AL, Katz D, Reves R, et al. The challenge of multisite epide-
miologic studies in diverse populations: design and implementation of
a 22-site study of tuberculosis in foreign-born people. Public Health Rep.
2009;124:391–399.
19. Chiang CY, Glaziou P, Enarson DA, et al. Protecting patients’rights,
ensuring safety and quality assurance in tuberculosis prevalence surveys.
Int J Tuberc Lung Dis. 2009;13:27–31.
20. Wood R, Lawn SD. Antiretroviral treatment as prevention: impact of the
‘test and treat’strategy on the tuberculosis epidemic. Curr HIV Res.
2011;9:383–392.
21. Kufa T, Mngomezulu V, Charalambous S, et al. Undiagnosed tuberculosis
among HIV clinic attendees: association with antiretroviral therapy and
implications for intensified case finding, isoniazid preventive therapy,
and infection control. J Acquir Immune Defic Syndr. 2012;60:e22–e28.
22. Golub JE, Pronyk P, Mohapi L, et al. Isoniazid preventive therapy,
HAART and tuberculosis risk in HIV-infected adults in South Africa:
a prospective cohort. AIDS. 2009;23:631–636.
23. World Health Organization. WHO Policy on TB Infection Control in
Healthcare Facilities, Congregate Settings and Households [serial on-
line]. 2009. Available at: http://whqlibdoc.who.int/publications/2009/
9789241598323_eng.pdf. Accessed August 1, 2013.
24. LoBue P, Sizemore C, Castro KG. Plan to combat extensively drug-resistant
tuberculosis: recommendations of the Federal Tuberculosis Task Force.
MMWR Recomm Rep. 2009;58:1–43.
25. Centers for Disease Control and Prevention. Guidelines for Preventing
Transmission of Mycobacterium tuberculosis in Health-Care Settings
[serial online]. 2005. Available at: http://www.cdc.gov/mmwr/pdf/rr/
rr5417.pdf. Accessed August 1, 2013.
26. Centers for Disease Control and Prevention. TB Infection Control Monitor-
ing and Evaluation Tool [serial online]. 2010. Available at: resources/
pmtct-care/docs/focused-monitoring-tool.pdf. Accessed August 1, 2013.
27. Dharmadhikari AS, Mphahlele M, Stoltz A, et al. Surgical face masks
worn by patients with multidrug-resistant tuberculosis: impact on infec-
tivity of air on a hospital ward. Am J Respir Crit Care Med. 2012;185:
1104–1109.
28. Gonzalez-Angulo Y, Geldenhuys H, Van As D, et al. Knowledge and
acceptability of patient-specific infection control measures for pulmonary
tuberculosis. Am J Infect Control. 2013;41:717–722.
29. Godfrey C, Villa C, Dawson L, et al. Controlling healthcare-associated
infections in the international research setting. J Acquir Immune Defic
Syndr. 2013;62:e115–e118.
30. Tuberculosis Infection Control: A Practical Manual for Preventing TB
[serial online]. Curry International Tuberculosis Center at University of
California San Francisco; 2011. Available at: http://www.currytbcenter.
ucsf.edu/products/product_details.cfm?productID=WPT-12. Accessed
August 1, 2013.
31. Cox H, Escombe R, McDermid C, et al. Wind-driven roof turbines:
a novel way to improve ventilation for TB infection control in health
facilities. PLoS One. 2012;7:e29589.
32. Nardell E, Vincent R, Sliney DH. Upper-room ultraviolet germicidal
irradiation (UVGI) for air disinfection: a symposium in print. Photochem
Photobiol. 2013;89:764–769.
33. Zhu S, Srebric J, Rudnick SN, et al. Numerical investigation of upper-
room UVGI disinfection efficacy in an environmental chamber with
a ceiling fan. Photochem Photobiol. 2013;89:782–791.
34. Willeke K, Qian Y. Tuberculosis control through respirator wear: perfor-
mance of National Institute for Occupational Safety and Health-regulated
respirators. Am J Infect Control. 1998;26:139–142.
35. Torres CJ, Silva R, Sa R, et al. Results of five-year systematic screening
for latent tuberculosis infection in healthcare workers in Portugal.
J Occup Med Toxicol. 2010;5:22.
36. Basu S, Galvani AP. The transmission and control of XDR TB in South
Africa: an operations research and mathematical modelling approach.
Epidemiol Infect. 2008;136:1585–1598.
37. Boulanger RF, Seidel S, Lessem E, et al. Engaging communities in
tuberculosis research. Lancet Infect Dis. 2013;13:540–545.
38. Hausler HP, Sinanovic E, Kumaranayake L, et al. Costs of measures to
control tuberculosis/HIV in public primary care facilities in Cape Town,
South Africa. Bull World Health Organ. 2006;84:528–536.
39. Shrestha RK, Mugisha B, Bunnell R, et al. Cost-effectiveness of includ-
ing tuberculin skin testing in an IPT program for HIV-infected persons in
Uganda. Int J Tuberc Lung Dis. 2006;10:656–662.
40. Yaesoubi R, Cohen T. Identifying dynamic tuberculosis case-finding
policies for HIV/TB coepidemics. Proc Natl Acad Sci U S A. 2013;
110:9457–9462.
J Acquir Immune Defic Syndr Volume 65, Supplement 1, January 1, 2014 Tuberculosis Infection Control
Ó2013 Lippincott Williams & Wilkins www.jaids.com |S23
