Barriers to pediatric TB diagnosis 2015

INT J TUBERC LUNG DIS 19(10):000–000
Q 2015 The Union
http://dx.doi.org/10.5588/ijtld.15.0178
Barriers to the diagnosis of childhood tuberculosis: a qualitative
study
S. S. Chiang,*† S. Roche,‡ C. Contreras,§ V. Alarc ón,¶ H. del Castillo,# M. C. Becerra,†§** L. Lecca§
*Section of Infectious Diseases, Department of Pediatrics, Baylor College of Medicine, Houston, Texas,
†
Department of Global Health and Social Medicine, Harvard Medical School, Boston, ‡
Boston University School of
Public Health, Boston, Massachusetts, USA; §
Socios En Salud Sucursal Peru (Partners In Health), Lima, ¶
Estrategia
Sanitaria Nacional de Prevenci ón y Control de Tuberculosis, Ministerio de Salud, Lima, #
Instituto Nacional de Salud
del Ni ño, Lima, Peru; **Division of Global Health Equity, Brigham and Women’s Hospital, Boston, Massachusetts,
USA
S U M M A R Y
S E T T I N G : In 2012, Peru’s National Tuberculosis Pro-
gram (NTP) reported that children aged 0–14 years
accounted for 7.9% of the country’s tuberculosis (TB)
incidence. This figure is likely an underestimate due to
suboptimal diagnosis of childhood TB.
O B J E C T I V E : To identify barriers to childhood TB
diagnosis in Lima, Peru.
D E S I G N : Using semi-structured guides, moderators
conducted in-depth interviews with four NTP adminis-
trators and five pulmonologists specializing in TB and
10 focus groups with 53 primary care providers,
community health workers (CHWs), and parents and/
or guardians of pediatric TB patients. Two authors
independently performed inductive thematic analysis
and identified emerging themes.
R E S U LT S : Participants identified five barriers to child-
hood TB diagnosis: ignorance and stigma among the
community, insufficient contact investigation, limited
access to diagnostic tests, inadequately trained health
center staff, and provider shortages.
C O N C L U S I O N : Recent efforts to increase childhood TB
detection have centered on the development of new
technologies. However, our findings demonstrate that
many diagnostic barriers are rooted in socio-economic
and health system problems. Potential solutions include
implementing multimedia campaigns and community
education to reduce ignorance and stigma, prioritizing
contact investigation for high-risk households, and
training primary care providers and CHWs to recognize
and evaluate childhood TB.
K E Y W O R D S : focus group; in-depth interview; socio-
economic disparities; stigma; health care provider
training
IN 2012, PERU’S NATIONAL TB Program (NTP)
reported that children aged 0–14 years accounted for
7.9% of its tuberculosis (TB) incidence of 95 per
100 000 person-years (py).1,2 This figure is likely an
underestimate due to suboptimal diagnosis among
children. Childhood TB experts have long argued that
pediatric case notifications in low- and middle-
income countries (LMICs) such as Peru, underesti-
mate the true burden of disease.3–6 Two lines of
evidence support this assertion. First, the proportion
of childhood cases correlates directly with TB
incidence. Data from high-incidence regions with
rigorous surveillance demonstrate that childhood
cases comprise 15–39% of the total TB caseload.7–9
In contrast, the United States reported a 2011 TB
incidence of 3.4/100 000 py, and attributed 6% of its
cases to children.10 As Peru has a 28-fold higher TB
incidence, it is unlikely that children would account
for only 7.9% of its cases. Second, recent modeling
studies independently concluded that the World
Health Organization (WHO) underestimated the
2010 global childhood TB caseload by at least
30%.1,11,12 The WHO derived the annual estimate
from case notifications, and adjusted for under-
diagnosis and underreporting; however, the same
correction factor was used for adults and children. In
contrast, the modeling studies adjusted for additional
diagnostic challenges specific to childhood disease.
An important reason for the suboptimal diagnosis
of childhood TB is its paucibacillary nature, which
reduces the sensitivity of acid-fast smear microscopy
and mycobacterial culture.13 The inability of most
children to expectorate sputum further complicates
diagnosis. Although research efforts have increasingly
focused on the development of more sensitive
technologies, no new tool has demonstrated greater
Correspondence to: Silvia S Chiang, Section of Infectious Diseases, Department of Pediatrics, Baylor College of Medicine,
Suite 1120, 1102 Bates Street, Houston, TX 77030, USA. Tel: (þ1) 832 824 4330. Fax: (þ1) 832 825 4347. e-mail: schiang@
alumni.stanford.edu
Article submitted 24 February 2015. Final version accepted 25 May 2015.
//titan/production/j/jtld/live_jobs/jtld-19-10/jtld-19-10-08/layouts/jtld-19-10-08.3d Š 7 August 2015 Š 11:06 am Š Allen Press, Inc. Page 1

sensitivity than culture.14 In the absence of microbi-
ological confirmation, physicians make a clinical
diagnosis using the tuberculin skin test (TST),
epidemiologic clues, and clinical and radiographic
findings. Although clinical diagnosis also has limita-
tions, experienced clinicians have used it effectively
for decades.15–17
The challenges of childhood TB diagnosis have
been well described by clinical studies and expert
opinion.13,15,16,18,19 However, only one study has
reported the perspectives of front-line health care
providers or affected families.20 An understanding of
the experiences of these groups is crucial to increasing
case detection. In this qualitative study, we sought to
identify obstacles to childhood TB diagnosis faced by
primary care providers and patients’ families.
STUDY POPULATION AND METHODS
Setting
El Agustino and La Victoria, two of Lima’s 43
districts, were chosen as the setting due to their high
TB incidence, at respectively 224 and 195/100 000 py
(unpublished data, Peruvian NTP), which exceeded
Lima’s overall 2012 TB incidence of 148/100 000 py.2
In Peru, 78% of TB patients receive care through the
Ministry of Health (MOH),1 which runs neighbor-
hood-based primary health centers with designated
NTP providers. NTP physicians diagnose TB and
prescribe treatment; NTP nurses and nursing techni-
cians supervise treatment, educate patients, perform
contact investigations, and administer TSTs;21 and
volunteer community health workers (CHWs) assist
nurses and nursing technicians. Many NTP providers
also have non-TB-related responsibilities, such as
administering vaccines. When needed, health center
physicians refer patients to MOH hospitals to see
NTP-affiliated pulmonologists specialized in TB.
Methods
In June and July 2012, we conducted 10 focus group
discussions (FGDs) with 53 NTP health center
providers, CHWs, and parents and/or guardians of
TB patients aged 0–14 years. In-depth interviews with
four NTP administrators and five pulmonologists
added a broader perspective to the issues explored in
the FGDs. We conducted in-depth interviews instead of
FGDs to capture the depth and diversity of the key
informants’ professional experiences. (The administra-
tors had various functions within the NTP, and
pulmonologists practiced in different hospital settings.)
Four female Peruvian staff members of Socios En
Salud (SES), a non-governmental organization
(NGO) that has collaborated with Peru’s NTP since
1996, served as moderators for the FGDs and
conducted the interviews. Moderators had previous
experience in facilitating FGDs and no prior rela-
tionships with the participants. After explaining that
their goal should be to understand participants’
experiences with childhood TB, moderators conduct-
ed the sessions using semi-structured guides devel-
oped by the authors (Table 1).
We purposefully sampled NTP providers, CHWs,
and parents and/or guardians at the eight (of 16 total)
health centers in El Agustino and La Victoria with the
highest pediatric TB caseloads. Table 2 details the
eligibility criteria and composition of the FGDs. Key
informants for the nine in-depth interviews were
chosen because their administrative or clinical catch-
ment areas included El Agustino and/or La Victoria.
Moderators invited FGD participants in person,
and authors invited key informants by telephone. Of
64 invited FGD participants, 11 (17%) declined due
to time constraints. All invited key informants
participated. Due to budget and staffing limitations,
we could not employ an iterative process of data
collection and analysis to the point of saturation. The
number and size of sessions were therefore deter-
mined a priori based on previously established
guidelines.22,23 FGDs and in-depth interviews were
conducted in Spanish, lasted 60–90 min, and took
place in private in SES conference rooms. No repeat
interviews were conducted. With participant consent,
moderators took field notes and audio-recorded all
sessions; recordings were transcribed verbatim.
Participants signed written informed consent and
received reimbursement for round-trip travel to SES.
The Institutional Review Boards of the MOH
(Direcci´on de Salud IV Lima Este), Universidad
Peruana Cayetano Heredia, Lima, Peru, and Harvard
Medical School, Boston, MA, USA, approved the
study.
Data analysis
Audio recordings were transcribed and uploaded to
NVivo version 10 (QSR International, Melbourne,
VIC, Australia). SSC and SR, both fluent in Spanish,
independently analyzed the data in Spanish using
conventional content analysis, an inductive ap-
proach.24,25 These authors first read and listened to
the transcripts to obtain an overall understanding of
the data. Based on their initial impressions of the data,
they developed English-language codes that represent-
ed and organized the concepts expressed in the text.
The authors refined and finalized the codes after
testing them on a sample of the transcripts. They then
coded all transcripts and identified emerging themes
that represented similar ideas or different facets of the
same topic. To ensure inter-observer reliability, the
authors resolved coding discrepancies after each step
and reached a consensus on emerging themes. All
moderators reviewed and agreed with the findings.
RESULTS
Overall, there was consensus among participants that
2 The International Journal of Tuberculosis and Lung Disease

childhood TB was under-diagnosed in Peru, although
one pulmonologist and two NTP officials believed the
number of missed cases to be small. Five main
diagnostic barriers emerged from the discussions:
ignorance and stigma among the community, insuf-
ficient contact investigation, limited access to diag-
nostic tests, inadequately trained health center staff,
and provider shortages. While participants men-
tioned the challenge of sputum collection and the
low sensitivities of smear microscopy and culture,
these issues received less attention than the other five
barriers.
Ignorance and stigma
Participants identified two reasons why children with
symptomatic TB present to medical care late or not at
Table 1 Focus group and in-depth interview questions
Participants Questions (translated into English from the original Spanish)*
Pulmonologists and NTP
administrators (IDIs)
What is your general opinion about the childhood TB situation in Peru?
Do you think that the number of childhood TB cases that the MOH has reported is accurate? Do you think the
number is under-estimated or over-estimated? Please explain.
Do you think there are sufficient resources to diagnose children with TB in Peru? What is missing?
What is the evaluation process for a child suspected of having TB?
What problems have you observed in the diagnostic process for a child with TB?
Physicians only: Have you ever had doubts in deciding whether or not a child had TB? When this occurs, what
do you do?
Have you ever ordered a TB diagnostic test in a child that could not be obtained? Please explain why the test
could not be obtained and what you did to continue the diagnostic evaluation.
Physicians only: How often do you see cases of children suspected of having TB? Who referred these children
to you? Why do you think the health centers made these referrals? Have you ever thought that a referral was
made unnecessarily, that the diagnosis could have been made in the health center?
Do you think the MOH health centers have sufficient human resources and supplies to diagnose childhood TB?
What is your opinion of the current level of contact investigation?
What would you do to improve the diagnosis of childhood TB?
NTP physicians, nurses,
and nursing technicians
working at health
centers (FGDs)
Have you ever participated in a training session on childhood TB? If so, when and where?
Where did you learn what you know about childhood TB? Do you think you have sufficient knowledge to
diagnose children with this disease?
What methods are used in your health center to obtain a sputum sample from childhood TB suspects?
Have you ever ordered a TB diagnostic test in a child that could not be obtained? Please explain why the test
could not be obtained and what you did to continue the diagnostic evaluation.
Have you ever referred children suspected of having TB to a pulmonologist? Why? How easy is it to make this
referral?
Physicians only: Have you ever had doubts in deciding whether or not a child had TB? When this occurs, what
do you do?
What activities do you do in your health center to look for contacts of TB patients? Are there limitations to
contact tracing? If so, what?
Do you think there are childhood TB cases in your community that are not being identified? If so, why are these
cases not being identified?
In your opinion, how could the detection of childhood TB be improved? What type of support would you need
to improve the evaluation and diagnosis of childhood TB in your health center?
Community health
promoters (FGDs)
Have you ever participated in a training session on childhood TB? If so, when and where?
Where did you learn what you know about childhood TB? Do you think you have sufficient knowledge to
diagnose children with this disease?
Do you think the diagnostic process for children suspected of having TB is the same as for adults suspected of
having TB?
What would you do if there were children living in the same household as an adult TB patient in your
community? Do you think these children are at risk for contracting TB? When situations like this one occur in
your community, do the children generally present to the health center for evaluation?
Have you ever referred children suspected of having TB to the health center for evaluation? How easy was this
referral?
Do you think the health center you work with has sufficient human resources and supplies to diagnose
childhood TB?
What activities do you do in your health center to look for contacts of TB patients? Are there limitations to
contact tracing? If so, what?
Do you think there are childhood TB cases in your community that are not being identified? If so, why are these
cases not being identified?
In your opinion, how could the detection of childhood TB be improved? What type of support would you need
to improve the evaluation and diagnosis of childhood TB in your health center?
Parents of pediatric TB
patients (FGDs)
Who diagnosed your child with TB? Where was your child diagnosed?
What did you think of the care that your child received in the health center?
What specialists have seen your child and where?
Has your child seen a pulmonologist at a hospital? What did you think of the specialist care that your child
received?
There are many children who do not present to a health center for TB evaluation until they have severe
symptoms. In your opinion, what are the reasons for this delay in presenting to a health center?
* Questions were designed to elicit general impressions of barriers to childhood TB diagnosis and to explore health-system related challenges. Questions were not
piloted.
IDI ¼ in-depth interview; TB ¼ tuberculosis; MOH ¼ Ministry of Health; FGD ¼ focus group discussion; NTP ¼ National Tuberculosis Program.
Barriers to childhood TB diagnosis 3

all: parental ignorance about TB and pervasive stigma
against TB patients in the community. Parents may
not recognize symptoms or may attribute them to
minor ailments:
[Another] obstacle [to diagnosis] is that the mother
does not to bring the child because she does not
realize that her child is coughing. . .Sometimes
[patients] think that [children with cough] have
allergies or colds. . .They do not think of the
possibility of TB. They do not think TB will
happen to them as long as they eat well . . . (Nurse,
Focus Group 4).
This quote also illustrates the widespread belief
that good nutrition immunizes against TB, and this
belief—intertwined with social class—leads families
to deny their susceptibility to TB. As one nurse
explained, ‘Middle-class people do not believe that
their children can get tuberculosis. They say, ‘How
can my children get tuberculosis if they eat well?’’
(Nurse, Focus Group 4). One physician reported a
family that lost two persons to TB; nevertheless,
despite multiple home visits from social workers, the
remaining household members refused evaluation
because they did not believe members of their socio-
economic class were susceptible to TB (Focus Group
1).
Stigma can affect care-seeking behaviors even
among families who recognize their vulnerability to
TB. Household contacts of TB patients commonly
refuse TSTs ‘because they feel shame’ (Nursing
Technician, Focus Group 5). When asked why
families may not take symptomatic children for
evaluation, one mother replied, ‘It may be because
of shame that [the illness] might be TB’ (Focus Group
10). One father admitted using the back entrance to
the health center’s anti-tuberculosis treatment area to
avoid being seen (Focus Group 10). Although not all
families experienced TB-related discrimination, some
parents reported that because of the illness, they and
their children had been the subjects of disdainful
looks, gossip, and avoidance.
Insufficient contact investigation
Participants reported infrequent use of contact
investigation to identify childhood TB cases. Some
families refuse evaluation due to stigma or denial, but
others may not undergo assessment for logistical
reasons. A nurse estimated, ‘Of the [contacts] that I
report. . . 60% are evaluated, and the other 40% are
never evaluated for a thousand reasons. They do not
have time, they work all day, they cannot miss
school,’ (Focus Group 4).
Health center personnel conduct home visits to
evaluate contacts who do not show up at the health
center. However, barriers to home visits include
providers having to pay for their own transportation
and being unable to locate families who have moved.
Furthermore, several female staff members expressed
safety concerns, which are exacerbated by personnel
shortages:
The area [around my health center]. . .is danger-
ous. . .I cannot go out [to place TSTs] alone. . .
When I request that a colleague accompany me,
that person is administering vaccines. . .I also
cannot leave if there is no other NTP provider
[at the health center]. . .A nurse was robbed the
other day. (Nurse, Focus Group 4)
Frequent tuberculin shortages are another obstacle
to contact investigation. One physician tried to
circumvent the tuberculin shortage at his health
center by referring children to a nearby hospital for
TST placement; however, the children never returned
for test interpretation (Focus Group 1).
Table 2 Focus group eligibility criteria and composition
Focus
group Eligibility criteria*
Participants
n
Female
participants
n (%)
1 NTP physicians currently working at a health center in El Agustino for 73 months 6 2 (33)
2 NTP physicians currently working at a health center in La Victoria for 73 months 4 1 (25)
3 NTP nurses currently working at a health center in El Agustino for 73 months 7 7 (100)
4 NTP nurses currently working at a health center in La Victoria for 73 months 3 3 (100)
5 NTP nursing technicians currently working at a health center in El Agustino for 73 months 6 5 (83)
6 NTP nursing technicians currently working at a health center in La Victoria for 73 months 6 6 (100)
7 Currently active community health promoters in El Agustino with 76 months’ experience in TB control
activities
6 6 (100)
8 Currently active community health promoters in La Victoria with 76 months’ experience in TB control
activities
6 6 (100)
9 Parents and/or guardians of children who had received treatment for TB disease in the past 6 months;
treatment must have been administered at a health center in El Agustino
4 3 (75)
10 Parents and/or guardians of children who had received treatment for TB disease in the past 6 months;
treatment must have been administered at a health center in La Victoria.
5 4 (80)
* We required 73 months’ experience for NTP staff and 76 months’ experience for health promoters to ensure that participants had sufficient professional
experience to contribute to FGDs. The minimum experience for health promoters was longer because, unlike staff, they do not work regular hours. We recruited
parents or guardians of recently treated children for two reasons. First, participants recall recent events more accurately, and second, their experiences are more
likely to reflect current NTP policies and practices. Eligibility criteria for all groups included informed consent.
NTP ¼ National Tuberculosis Program; TB ¼ tuberculosis; FGD ¼ focus group discussion.

Limited access to diagnostic tests
Health centers often lack the necessary equipment to
diagnose childhood TB. In addition to tuberculin
shortages, participants reported a lack of properly
functioning radiograph machines. Physicians are
most likely to solve this problem by referring patients
to private facilities:
[The radiograph machine] broke about 3 years ago
and has not been fixed. . . We have the support of
[another] health center that does chest radio-
graphs. I asked for [a radiograph there] once but
never again because the quality was very low. . .It
is easier to tell the patient to go [to a private
facility] for the radiograph (Physician, Focus
Group 1).
Physicians related that they rarely send patients to
MOH hospitals for radiographs because of the long
wait for the patient and the large amount of
paperwork for the referring provider. Moreover,
some providers did not know that TB patients could
obtain free chest radiographs at MOH facilities. As
private facilities charge for radiographs, patients
often delay or forgo this test. A pulmonologist
explained: ‘Many patients do not come to their
appointments because they have not even one sol
[US$0.35] for transportation, much less for their
chest radiograph and [other] exams’ (Interview 6).
Parents also reported having to purchase gastric
aspirate supplies, sometimes with help from non-
governmental organizations or community groups.
According to one CHW, ‘The [families] are poor.
They do not have enough money for the gastric
aspirate . . .We raise money to buy [the supplies] for
them because otherwise they do not come [for the
procedure],’ (Focus Group 8).
Inadequately trained health center staff
Even when diagnostic tests are obtained, health
center providers may lack the training and confidence
to interpret the results. One NTP administrator
worried that ‘not everyone has the necessary exper-
tise’ to place and interpret TSTs correctly (Interview
8). Multiple health center physicians admitted feeling
uncomfortable reading pediatric radiographs. Nurses
also perceived this lack of skill:
Not all the [health center] physicians. . .know how
to read a [pediatric] chest radiograph. . .So. . .I
gather all my [pediatric] chest radiographs. . .and I
take them to Dr. [pulmonologist’s name omitted].
If he is not sure, then I call Dr. [second
pulmonologist’s name omitted] (Focus Group 3).
In general, providers found childhood TB diagnosis
difficult, but not one FGD participant had attended
childhood TB training because sessions occurred so
rarely. According to one physician, ‘TB trainings are
all about adults. . . We are used to taking care of
adults, but taking care of children is completely
different’ (Focus Group 2).
Provider shortages
Health center physicians do not regularly consult
pulmonologists to diagnose adult TB, but because
they lack the confidence to diagnose childhood TB,
they routinely refer children (Physicians, Focus
Groups 1 and 2). However, ‘the [physicians] who
have the most experience managing pediatric TB are
pediatric pulmonologists, and there are no more than
20 [in Peru]’ (NTP Administrator, Interview 5).
Moreover, not all pediatric pulmonologists see TB
patients (Nurses, Focus Groups 3 and 4). Therefore,
children may be evaluated by adult pulmonologists.
The delay to see a specialist may be 1–2 months
(Nurses and Nursing Technicians, Focus Groups 4
and 5).
Parents reported additional delays on the day of the
appointment: ‘At the hospital, they make us wait
hours. . .Sometimes you have to go look for the doctor
yourself. . ..’ (Focus Group 9). Moreover, hospitals
reject patients who do not have their referral forms
completed correctly or are not accompanied by health
center personnel, who provide the pulmonologist
with the patient’s history and test results. The latter
requirement is onerous for busy health center staff:
‘[We] arrive [at the hospital] in the morning and leave
in the afternoon. But if [we] are not present, the
doctor will not see the patient’ (Nurse, Focus Group
3).
Due to these obstacles, patients may be sent to
multiple health establishments multiple times before
receiving a proper evaluation. Both parents and
providers used the slang term pelotear—which means
‘to throw around like a ball’—to describe how
patients are treated by the health care system (Focus
Groups 1, 3, and 9).
Providers and parents expressed the need for more
childhood TB specialists, but the financial limitations
of the MOH make hiring more pulmonologists an
unlikely prospect. The MOH, which manages 78% of
Peru’s TB caseload,1 cannot compete with the salaries
at private medical facilities:
After a maximum of 11 hours at my job in the
[private] clinic, I earn more than my job here at the
[MOH] hospital as chief. . .The [name of private
clinic omitted] has. . . opened many branches.
With each branch opening, they hire away two
pulmonologists [from the MOH]. . .They have far
more pulmonologists than the Ministry [of
Health]. . . (Pulmonologist, Interview 6)
Provider shortages at the primary care level also
adversely affect childhood TB diagnosis. The low
number of smear microscopy technicians at health
centers jeopardizes the quality of test interpretation:
‘At the current rate, we are exceeding what a

technician can [properly] do. . .Samples are not being
processed well’ (Pulmonologist, Interview 2).
The workload also exceeds the capacity of NTP
physicians, nurses, and nursing technicians—partic-
ularly if they have other non-TB responsibilities. As
one NTP administrator related,
There is a lot of work and not just for TB. . .I ask
for information from the health center, and the
health center responds that the person in charge of
TB has gone out to work on other cam-
paigns. . .vaccines. . .dengue. . . (Interview 5)
Parents complained about lack of access to health
center physicians as well. One mother shared,
To date, the physician still has not examined my
daughter, and. . .every time I go to speak with her, I
am told that she does not have time, that she has
too many patients to see, that [NTP nurses and
nursing technicians] will see my daughter in the
afternoon... (Focus Group 9)
CHWs help health center staff with the workload,
but participants reported recent attrition in CHW
numbers because they no longer received incentives
(previously provided by NGOs) for their efforts. One
physician even witnessed ‘CHWs who come to the
health center. . .for medical attention for a relative,
and they are denied care. . .after that they often stop
volunteering’ (Focus Group 1).
DISCUSSION
The experiences described in this study illustrate
barriers at every step of the childhood TB diagnostic
process, from case finding to diagnostic testing and
clinical evaluation. Other reports from Lima corrob-
orate our findings of childhood TB knowledge
deficits among providers, insufficient sputum pro-
cessing capacity, significant out-of-pocket diagnostic
and transportation costs for patients, frequent diag-
nostic supply shortages, and TB stigma in the
community.26–30 We found one other qualitative
study that examined challenges to childhood TB
diagnosis. In that study, Tanzanian primary care
providers, like our participants, reported feeling
inadequately trained to recognize and diagnose
childhood TB.20
While participants acknowledged the challenge of
sputum collection in children and the low sensitivities
of smear microscopy and culture, these issues
received less attention than the five main barriers
identified in this study. Our results serve as a reminder
that with proper clinician training, childhood TB can
be diagnosed clinically, and that most barriers to its
detection are rooted in the socio-economic charac-
teristics of TB-affected communities and the health
systems that serve them. A more sensitive assay may
not be available for many years. In the meantime,
community education and health system improve-
ments may increase detection of this disease.
First, interventions that address TB-related igno-
rance and stigma may encourage health care-seeking
behaviors. Case detection in Pakistan and Colombia
increased after multimedia public service announce-
ments were made encouraging individuals with
prolonged cough to seek medical attention.31,32 In
Ethiopia, TB clubs (support groups for TB patients)
identified and referred 69% of all new cases over a 6-
month period.33 This low-cost, community-led ini-
tiative reduced TB stigma in both Ethiopia and
Nicaragua.34,35 These and other interventions, such
as a TB stigma reduction toolkit,36 could be adapted
for childhood TB and Peru. To establish best
practices, their efficacy should be assessed with
standardized knowledge and stigma scales.35,37–41
Second, household contact investigation, a high-
yield and cost-effective case-finding strategy for
childhood TB, should be strengthened.15,42–46 Peru’s
NTP mandates contact investigation, but resource
restraints limit its implementation.21,47 The NTP may
consider prioritizing high-risk households, such as
those with a sputum-positive index case, drug-
resistant disease, or children aged ,5 years.42 Other
ways to strengthen contact investigation include
improving the index patient’s TB literacy, a factor
associated with increased adherence to contact
investigation,48 and using text messaging to remind
patients to take household members for evaluation.
Lima-area focus groups indicated that TB patients
would accept the latter approach.49 Moreover, the
ubiquity of mobile phones, present in 88.5% of Lima
households in 2013, and the minimal cost of text
messaging, would increase feasibility and cost-effi-
ciency.
Third, Peru should reinforce its national policy
guaranteeing free TB evaluation and care at MOH
facilities.21,47 Peru has taken steps to improve access
to these services, as patients previously had to show
proof of health insurance. Although individuals living
at or below the poverty line qualified for free public
health insurance, they could not register for this
coverage without a national identification card,
which many poor people lack.50 As of December
2014, patients no longer need to show national
identification or health insurance documentation to
access TB care.51 This is a step forward, but more
diagnostic supplies and functioning equipment are
also needed.
Fourth, training health center providers to detect
childhood TB may shorten the time to diagnosis and
avoid the cost and inconvenience of referral to
hospitals. Accessible reference materials and contin-
ued monitoring may be important components of
training. Childhood case notifications in Bangladesh
and Pakistan increased when health worker training
was accompanied by continued monitoring and the

distribution of clinical reference guides, which
presented practical tips relevant to medical practice
in a clear, concise format.52,53 In contrast, in South
Africa, an isolated 1-day course to teach pediatric
chest radiograph interpretation met with limited
success.54 More work is needed to identify the most
effective approaches to training primary care provid-
ers to recognize and evaluate childhood TB.
Finally, given the shortage in health center person-
nel, CHWs could help identify and evaluate TB
suspects. There is growing evidence that well-trained
CHWs improve various health outcomes, including
increased TB case detection, in diverse settings.55–58
Furthermore, community members may be more
effective than health providers in referring individuals
with TB symptoms.33,56 Previous experiences have
shown that CHWs facilitate community-based hu-
man immunodeficiency virus (HIV) and TB treatment
programs in Lima,57,58 and sustainable strategies are
needed to incentivize and retain this workforce.
Our study had limitations. It was conducted in a
single location, and findings may not be generalizable
to other settings. In addition, we were unable to
collect and analyze data continuously to the point of
saturation.59 However, we established the number of
sessions a priori, and the amount of new information
contained in the last few transcripts was minimal.
Moreover, previously established guidelines suggest-
ed that our sample size would achieve the point of
data saturation.60 Finally, the majority of participants
in all but the physician focus groups were women
(Table 2). The dearth of fathers/male guardians may
have resulted in an under-appreciation of diagnostic
barriers that affect men more than women. For
example, because they are frequently employed
outside of their communities, men may experience
greater inconvenience due to travel time and the
inflexible hours of health care facilities.61 Male
nurses, nursing technicians, and CHWs may also
face obstacles not captured in our study. However, we
believe that the gender distribution of the focus
groups represents the local workers and primary care
givers for children.
CONCLUSION
This qualitative study described obstacles to child-
hood TB diagnosis faced by primary care providers
and patients’ families. Our findings demonstrate that
many barriers to childhood TB detection stem from
socio-economic and health system problems, which
must be addressed alongside efforts to develop more
sensitive and setting-appropriate diagnostic technol-
ogies.
Acknowledgements
The authors thank the study participants; moderators S Soto, J
Jimenez, and K Tintaya; and Socios En Salud volunteers M
Lindeborg, L Ostrer, D Vyas, K Reifler, Y Leung, and N Tyagi. We
also thank J Starke and N Parker VanValkenburgh for their
valuable feedback on earlier versions of this manuscript.
Funding was provided by the David Rockefeller Center for Latin
American Studies at Harvard University, Boston, MA, USA.
Conflicts of interest: none declared.
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R E S U M E
C O N T E X T E : En 2012, le Programme National
Tuberculose (PNT) du Pérou a déclaré que les enfants
de 0–14 ans représentaient 7,9% de l’incidence de la
tuberculose (TB) dans le pays. Cette estimation est
probablement sous-évaluée en raison d’un diagnostic
insuffisant de la TB de l’enfant.
O B J E C T I F : Identifier les obstacles au diagnostic de la
TB de l’enfant à Lima, Pérou.
S C H E´ M A : Grâce à des guides semi-structurés, les
animateurs ont réalisé des entretiens approfondis avec
quatre administrateurs du PNT et cinq pneumologues
spécialisés dans la TB et 10 groupes focaux avec 53
soignants de premier niveau, des travailleurs de santé
communautaire (HCW) et les parents et/ou responsables
des enfants atteints de TB. Deux auteurs ont réalisé
indépendamment une analyse thématique inductive et
identifié des thèmes émergents.
R E´ S U LT A T S : Les participants ont identifié cinq
obstacles au diagnostic de la TB de l’enfant :
l’ignorance et la stigmatisation dans les communautés,
une investigation insuffisante des sujets contacts, un
accès limité aux tests de diagnostic, un personnel des
centre de santé insuffisamment formé, et la pénurie de
prestataires.
C O N C L U S I O N : Les efforts récents visant à augmenter
la détection de la TB de l’enfant ont été centrés sur
l’élaboration de techniques nouvelles. Cependant, nos
résultats montrent que de nombreux obstacles au
diagnostic sont enracinés dans des problèmes
socioéconomiques et liés au système de santé. Parmi les
solutions potentielles, on peut envisager la mise en
œuvre de campagnes multimédia et d’éducation sanitaire
des communautés afin de réduire l’ignorance et la
stigmatisation, de donner la priorité à l’investigation
des contacts dans les foyers à haut risque et de former des
prestataires de santé de niveau primaire et des HCW
pour reconnaˆıtre et évaluer la TB de l’enfant.
R E S U M E N
C O N T E X T O: En el 2012, la Estrategia Sanitaria
Nacional de Prevención y Control de la Tuberculosis
(ESN-PCT) de Perú informó que los niños entre 0–14
años representaban el 7,9% de la incidencia nacional de
la tuberculosis (TB). Esta cifra es probablemente
subestimado debido a las dificultades en el diagnóstico
de la TB pedia´trica.
O B J E T I V O: Identificar las barreras para el diagnóstico
de la TB pedia´trica en Lima, Perú.
D I S E ÑO: Utilizando gu´ıas semiestructuradas, un grupo
de moderadores realizaron entrevistas en profundidad a
cuatro administradores de la ESN-PCT y cinco
neum ólogos especializados en TB. As´ı mismo se
realiz ó 10 grupos focales con 53 proveedores de
atención primaria, agentes de salud comunitaria, y
padres y/o tutores de pacientes con TB pedia´trica. Dos
autores independientes realizaron el ana´lisis tema´tico
inductivo e identificaron los temas emergentes.
R E S U LT A D O S: Participantes identificaron cinco
barreras al diagnóstico de la TB pedia´trica: ignorancia
y estigma entre la comunidad, insuficiente uso de la
investigación de contactos, acceso limitado a estudios de
diagnóstico, capacitación inadecuada del personal de los
centros de salud, y la escasez de proveedores.
C O N C L U S I O´ N: Los recientes esfuerzos para aumentar la
detección de la TB pedia´trica se han enfocado en el
desarrollo de nuevas tecnolog´ıas. Sin embargo, nuestros
resultados demuestran que muchas barreras se basan en
problemas socioeconómicos y debilidades del sistema de
salud. Posibles soluciones incluyen realizar campañas
multimedia y educaci ón de la comunidad para
incrementar el conocimiento y disminuir el estigma,
priorización en los hogares de alto riesgo el estudio de
contactos, y la capacitación de proveedores de atención
primaria y a los agentes salud comunitario para
reconocer y evaluar la TB pedia´trica.
Barriers to childhood TB diagnosis i

Queries for jtld-19-10-08
1. Author: we found the following for reference 21: Ministerio de Salud. Norma te´cnica de salud para la atencio´n
integral de las personas afectadas por tuberculosis. NTS N8104-MINSA/DGSP V.01. Lima, Peru: Ministerio de
Salud, 2013. http://190.223.45.115/newtb/Archivos/NormaTecnica.pdf. Correct? Ed
//titan/production/j/jtld/live_jobs/jtld-19-10/jtld-19-10-08/layouts/jtld-19-10-08q.3d Friday, 7 August 2015 11:06 am Allen Press, Inc. Page 1

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