Paediatric tuberculosis (TB) has long been an evasive entity for public health practitioners striving to control the disease. Owing to difficulty in diagnosis of paediatric TB, incidence estimates based on current case detection fall short of actual rates. The four high-burden countries in South Asia (SA-HBC)—Afghanistan, Pakistan, India and Bangladesh—alone account for >75% of missed TB cases worldwide. It follows that these countries are also responsible for a large although unmeasured proportion of missed paediatric cases. In view of current Millennium Development Goals recommending a scale-up of paediatric TB detection and management globally, there is a dire need to improve paediatric TB programmes in these high-burden countries. Inherent problems with diagnosis of paediatric TB are compounded by programmatic and social barriers in SA-HBC. We have reviewed the current situation of TB control programmes in SA-HBC countries based on published statistics and performed a strengths, weaknesses, opportunities and threats situational analysis with a view towards identifying critical issues operant in the region posing barriers to improving paediatric TB control.
- South Asia
- National tuberculosis control programs
- health systems
Statistics from Altmetric.com
Of an estimated nine million new cases of tuberculosis (TB) occurring across the globe each year, children account for nearly half a million (490 000), with two-thirds residing in 22 high-burden countries (HBCs).1 In 2011 alone, 64 000 childhood deaths (among ≤15 years) were attributed to TB.2 Current WHO-recommended case detection methods (sputum smear positivity) identify only an estimated 5% of TB cases among children,3 a demographic with classically sputum smear-negative, and predominantly culture and Xpert negative, disease. It is therefore not surprising that children make up the majority of an estimated three million people with TB who remain undiagnosed and untreated.1 It is imperative that in the move towards zero TB deaths in children, programmes are strengthened and equipped to detect and control the disease in this ‘vulnerable’ subgroup in high-TB burden areas of the world.
Here, we review evidence on paediatric TB burden, and capacity of national TB control programmes (NTPs) for paediatric scale-up in four high-burden countries of South Asia (SA-HBC)1: Afghanistan, Pakistan, India and Bangladesh. The purpose of this review is to evaluate the current capacity of TB control programmes in these four countries to diagnose, treat and quantify childhood TB, and propose practical solutions to gaps in achieving integrated paediatric TB management.
Teasing apart the proportion of children in the TB epidemic in SA-HBC (Afghanistan, Pakistan, India and Bangladesh)
Paediatric cases (occurring in children aged 0–14 years) are an early indicator of ongoing transmission of TB among adolescents and adults aged 15–34 years, the demographic responsible for highest transmission rates.4 ,5 Children develop disease earlier and contract the disease through contact with adult cases.
South Asia houses half of the world's high TB-burden countries, two-third of which are also high incidence for multidrug-resistant (MDR)-TB.1 Table 1 presents information available on health and demographic indicators of relevance in Afghanistan, Pakistan, India and Bangladesh.1 ,6–11 Incidence estimates show that all four countries are high burden for TB (40–499 incident cases per 100 000 population), and sparing Afghanistan, also high burden for MDR-TB cases. Around one-quarter of the world's youth (the greatest proportion among all geopolitical regions) lives in this region.12 This skewed age demographic indicates that the TB epidemic in South Asia represents a large proportion of childhood TB cases in the world. The main programmatic challenge lies in capturing all incident childhood TB cases, despite sputum smear limitations in this age group.13
Case detection rates and missed paediatric TB cases
TB case detection rates (CDRs) for all age groups range from 49% to 65% in SA-HBC. These fall short of the 70% CDR global target.14 Pakistan, India and Bangladesh are among 12 countries where 75% of the three million ‘missed’ cases occurred in 2012, with India contributing to as much as 31%, Pakistan 5% and Bangladesh 6% to the total 75% cases.14 Figure 1 shows all reported TB cases in 2011 and 2012, disaggregated by site, and age.1 Although 29–47% of the population in these countries comprises children 0–14 years,7 paediatric cases comprise a very small proportion of total reported cases. A recent estimation of missed paediatric cases, based on a mathematical model built on household exposure to adult cases, reports that India alone accounts for 27% of the missed cases in 22 HBCs.15 Even this staggering proportion may be an underestimate as this model assumes that BCG confers protection against extrapulmonary TB and partial protection against pulmonary TB, a vaccine that we now know does not have protective efficacy more than 0–50%16 ,17 in high-prevalence populations.
To increase CDRs, some HBCs have declared TB to be a notifiable disease; however, compliance with this law remains far from satisfactory.18 Occasional studies of paediatric household contacts of adult TB cases have demonstrated that contact investigations may be a useful strategy to capture these missed cases.19 ,20
Factors contributing to missed paediatric cases
Traditionally, problems with paediatric pulmonary TB case detection have been paucibacillary and extrapulmonary disease,13 both not amenable to classic smear status detection. However, smear status as a measure of CDR has been widely criticised by several authorities on paediatric TB.3 ,21 The case definition employed by NTPs for paediatric CDRs therefore needs attention from WHO so that it is refined to include smear-negative and extrapulmonary cases. NTPs also miss children with disease who seek care at non-NTP facilities in the public and private health sector domain due to poor lateral data linkages between the programme and non-NTP caregivers to children. Not all cases seen in private clinics are reported to NTP authorities. Poverty and poor access to healthcare also account for a proportion of missed cases. More than half the world's paediatric population is reportedly deprived of at least one, and 30% of two or more severe basic needs globally.22 ,23 In South Asia, human needs deprivation rates are as high as 80% and serve as a surrogate for poor access to healthcare. While poverty itself is a major contributor to inadequate coverage, its consequences also add to missed cases .South Asia houses one-half of the world's food-deprived children,23 resulting in a high rate of malnutrition in children under 5 years of age (weight for age index, table 1). Malnutrition contributes to both a higher risk of TB and low likelihood of diagnosis by Mantoux testing. Anergy on Mantoux testing is often misinterpreted by physicians as a ‘negative’ test for TB.
Knowledge of disease pathogenesis and course, and, diagnostic hurdles,24 is also limited among physicians in low-resource SA-HBC settings. Low TB detection rates despite a high percentage of children under 5 years of age taken to a physician for acute respiratory illnesses (table 1) represent missed opportunities for physicians to suspect, screen for and diagnose TB in children, especially those with malnutrition or failure to thrive. Low clinical suspicion may contribute to poor capture and reporting of TB cases in children, contributing to an ever-increasing gap in data on incidence. Low health budgets in SA-HBC compound the problem of these missed cases by establishing a vicious cycle of low resources unable to cope with the increasing healthcare demands of vulnerable paediatric populations. Another emerging threat to paediatric TB control is the burgeoning epidemic of other infectious diseases including measles and varicella. A widespread and underdetected epidemic of these debilitating illnesses of childhood propagates malnutrition and functional immune deficiency among children, leading to a higher-than-expected incidence of TB in HBCs. Moreover, models of estimated paediatric cases do not account for these predisposing conditions. There is therefore a large proportion of unmeasured effect of such epidemics as risk factors for TB among children.
SA-HBC have low HIV prevalence (see table 1) and therefore a low probability of HIV and TB coinfections among children on a larger population-based scale. However, the epidemiology of HIV in South Asia involves concentrated epidemics in ‘high-risk’ groups, including sex workers, intravenous drug users and homosexuals,25 belonging to vulnerable populations and therefore less likely to access healthcare. The fact that children belonging to these high-risk groups would thus be even more likely to have undetected infectious disease, including TB, suggests that a special focus on HIV-TB coinfections in these special populations is critical.
A summary of contributing factors to missed cases is presented in box 1.
Factors contributing to missed paediatric tuberculosis
Poor data linkages between national TB control programmes (NTPs) and private practitioners
Poor coverage by NTPs for contact investigations and case detection
Poor reference diagnostic tests and unavailability of interferon gamma release assays in most laboratories
Lack of physician knowledge of diagnostic algorithms
Other ‘more visible’ infectious diseases
Poverty and malnutrition
Underdetected HIV burden
The above factors can be translated into substantial gaps in NTPs between control programme requirements and existing service provided. Box 2 identifies these service gaps.
Paediatric tuberculosis (TB) control service gaps in high-burden countries in South Asia
Lack of lateral linkages between national TB control programmes and Expanded Program forImmunisations (EPI)/Integrated Maternal and Child Health and private practitioners
Preventive measures such as isoniazid preventive therapy in contacts not implemented
Physician are not trained by NTPs in paediatric diagnostic algorithms
Notably, the prevention of paediatric TB in SA-HBC countries remains far from satisfactory. Prevention is the ultimate goal in the fight to control TB. Global efforts towards developing an effective vaccine and prevention of progression of latent to active TB continue.26 Although progress in vaccine development has been slow, successful TB control programmes have benefited from isoniazid preventive therapy (IPT) efforts, especially in low-endemic regions.27 Latent TB infection treatment with IPT in children under 5 years of age is recommended2 and is likely to have a high impact on the prevention of tuberculous disease in this high-risk exposed population in HBCs.28 Although national guidelines support the use of IPT in children,8–11 knowledge of and compliance with this practice is unsatisfactory,29 ,30 and high estimated paediatric TB incidences suggest that the desired endpoint of prevention is not being reached.15 Published literature shows district or facility-based IPT initiatives,31 ,32 but research-based implementation approaches produce patchy coverage. Such missed opportunities in prevention in a vulnerable population prone to severe disease create a service gap that must be addressed through robust programmatic strategies.
Another major gap is the lack of lateral linkages between various components of paediatric healthcare service in the region. Both EPI and Integrated Management of Neonatal and Childhood Illnesses (IMNCI) programmes lack linkages with private clinics and TB centres. Optimal coverage rates for three doses of the trivalent diphtheria, pertussis and tetanus vaccine in all four countries33 reflect that vaccination visits, especially in the first year, can be potential screening and contact-tracing opportunities provided primary healthcare providers are primed and appropriately trained.
The impact of physician training in paediatric TB algorithms has also not been assessed on a larger scale owing to a lack of routine training procedures for all general physicians and paediatricians. Such measures have been a part of operational research but are not programmatically implemented. However, NTPs are identifying the need to train physicians in paediatric TB increasingly and a positive move towards this goal is imminent.34 Additionally, training of other healthcare staff including community health workers, pharmacists, radiologists and nurses in various aspects of paediatric TB care will help improve case detection and management.
Several knowledge gaps exist that can be filled to inform future steps towards improvement in data reporting and surveillance.
Drug resistance data reported to WHO are not disaggregated by age.1 According to a recent review by Zignol et al,35 MDR cases have only been reported in Bangladesh, and not in Afghanistan, Pakistan or India. However, in view of high MDR burden, such cases doubtless occur among children, indicating a target area where surveillance and laboratory diagnostics can be improved for childhood TB.
Knowledge gaps also exist in the area of maternal TB with perinatal transmission leading to infant TB. The few studies on the subject from India have been limited because of poor follow-up rates.36 Integration of maternal and neonatal health programmes will serve to establish continuum of care while also ensuring that chronic illnesses such as TB when diagnosed in mothers are also sought in neonates.37 Information on number of empiric prescriptions for TB in children or adults will also be useful NTP indicators of not only accurate reporting but also possibly a need to revise case definitions and refresh physician training. Existing knowledge gaps are listed in box 3.
Drug-resistant tuberculosis (TB) rates among children unknown
Unknown burden of maternal and perinatal, neonatal and infant TB
Paucity of information on empiric anti-TB treatment prescribed to children
How useful these data will prove in assessing TB control among children may be answered by operational research then undertaken to evaluate such approaches in the public health context.
We reviewed efforts in all four countries in the four major areas of TB care according to the International Standards of Tuberculosis Care (ISTC): public health, diagnosis, treatment and HIV coinfections.38 Figure 2 shows publications originating from SA-HBC based on these four areas of care and the proportion of studies focused on paediatric TB.
Although medical research focuses heavily on TB in these HBCs (with the notable exception of Afghanistan), most research and publications have focused on adult TB. Probable reason for this is a lack of focus on childhood TB control by public health officials and physicians. Recently, however, with joint efforts of the Stop-TB Partnership and WHO to improve knowledge of childhood TB, models have been developed in Pakistan and India39–41 to control TB in this vulnerable population. While this recent focus is encouraging, there is a lack of unified effort leading to weak paediatric-centred TB health systems.
Overview of national TB control programmes in SA-HBC
Paediatric TB control initiatives in the region are new and underdeveloped, and cannot be assessed with rigour using the same indicators as adult control programmes.42 Therefore, to inform paediatric TB prevention and management strategies, it may be useful to examine NTP systems for capacity to scale-up existing services to include paediatric services. Table 2 presents national NTP features in SA-HBC according to six essential health system building blocks in WHO's health system framework.43 Review of NTPs in these areas serves to evaluate existing services and identify potential barriers to TB control.
SA-HBC have primary care-focused health systems, with vertical and decentralised NTPs in India and Pakistan,9 ,44 and plans to decentralise in Afghanistan.45 Bangladesh has a horizontal programme, which has central stewardship by its Health Population and Nutrition Sector Development Program (HPNSDP).46 This is commendable in view of the current WHO recommendation to integrate paediatric TB programmes in routine healthcare systems. India has the most adequately funded NTP with more than one-third of total budget emanating from domestic quarters. Afghanistan, Pakistan and Bangladesh provide only 3–5% domestic funding to NTPs,1 which leads to concerns regarding unsustainable financial support. There is a clear need to increase national health budget spending, cost-efficiency and equity. NTPs have shortage of workforce;47 however, no basic information regarding number of health workers, public sector and private sector centres was available for any of these countries. This may be due to weak health and information management systems resulting in a lack of coordinated activities. There are also a limited number of diagnostic laboratories,1 a direct result of weak health systems and limited domestic funding.
All four countries, while maintaining IMNCI programmes in their public health infrastructure,48 have not been able to introduce TB screening, testing, diagnostics and treatment among these programmes and disease control programmes remain vertical.
Programmatic barriers to developing and implementing paediatric TB control programmes in SA-HBC
In view of the deficiencies (and occasional strengths, viz., horizontal programmes in Bangladesh and domestic funding in India), in TB control programmes in SA-HBC, the main barriers to developing a paediatric TB control component in each of these programmes are a lack of lateral linkages with adequately scaled up healthcare initiatives for children such as IMNCI and a lack of indicators reflecting workforce needs to implement new initiatives strengthening existing services. Among the indicators for services delivery, inadequate vital registry systems and electronic databases in these countries1 add to the existing barriers in diagnosis of paediatric TB and hence contribute to inappropriate mobilisation of resources towards areas with higher TB incidence.
Paediatric TB treatment is registered under Directly Observed Therapy Shortcourse (DOTS) in SA-HBC countries.1 However, the DOTS reporting system in these countries is based on public–private partnership clinics that are not adequately linked by a central monitor. Therefore, there is uncertainty in assessing paediatric TB treatment completion rates and mortality and these figures as reported to WHO are not disaggregated by age. National standards for reporting and disaggregating data are required and implementation is needed before the limited resources that are available can be mobilised towards effective paediatric TB control.
These barriers may be surmounted by professional input from multiple relevant sources such as paediatric infectious disease clinicians, diagnostic laboratories and microbiologists, epidemiologists and information technology (IT) experts. A multidisciplinary taskforce such as this informing policy in NTPs will be key to resolving gaps in coverage, capture and programme self-evaluation.
SWOT situational analysis
Based on programme strengths and barriers described above, we have applied the strengths, weaknesses, opportunities and threats (SWOT) analysis49 to NTPs in SA-HBC. SWOT is an analytic strategy used for decision making in earlier stages of programmes to inform future planning. Since paediatric TB programmes cannot be evaluated against performance parameters at this preliminary stage, we have applied available information to the SWOT analysis to suggest future courses of action for paediatric TB programme development. SWOT has been applied to healthcare and nursing programmes49 and has also been applied to DOTS implementation by Bangladesh NTP.50 We present a wider-scope analysis of programme scale-up capacity to encompass paediatric TB control components.
The strengths and weaknesses of the NTPs were further assessed in light of present opportunities and threats in a threats, opportunities, weaknesses and strengths (TOWS) matrix (figure 3). The TOWS matrix puts together the SWOT analysis to generate feasible courses of action based on matching strengths with opportunities and weaknesses with threats in a two-by-two matrix.51
Based on the TOWS matrix analysis, we suggest a need for operational research in paediatric TB. That the results be used for generating future funding and also for developing informed policies on strengthening programmes enabling scale-up and creating occasions for joint ventures facilitating multidisciplinary programmes in primary healthcare. Despite imminent threats, primary care-focused healthcare can be used to educate the public and create horizontal collaborations across different vertical programmes to overcome wasted resources in isolated efforts to contain epidemics.
Unfortunately, the several built-in weaknesses when faced with acute threats do not offer ways to overcome built-in deficiencies. If faced with such threats, systems are likely to deteriorate with the only likely salvage situation being a shift from public–private mixes to an all-private contract to non-governmental organisations that may still be able to operate in dire circumstances. However, such a shift will not allow a scale-up of current services but will only be a strategy to continue healthcare services in the face of deteriorating government services. Furthermore, such a shift would be detrimental to the public health infrastructure and therefore, other strategies may be suggested by public health professionals in each operant environment based on local circumstances.
It is imperative that such analyses are performed at intervals to re-evaluate changing healthcare, epidemiological, political and economic local and international landscapes. Our suggestions for paediatric TB control in SA-HBC are presented in box 4.
Suggestions for improvement in paediatric tuberculosis (TB) control in high-burden countries in South Asia based on threats, opportunities, weaknesses and strengths matrix analysis
Create horizontal integrated programmes or lateral linkages between child healthcare programmes such as IMNCI, Expanded Program for Immunisation (EPI) and paediatric TB national TB control programme or private practitioner care
Introduce and implement routine household contact tracing for all childhood contacts of adult cases
Introduce and implement routine latent TB infection treatment of at-risk children
Create a multidisciplinary taskforce of paediatricians, microbiologists, information technology experts and epidemiologists to inform programme policy, develop indicators and evaluate strategies
Invest in measles supplementary immunisation activities
Fortify staple diet such as rice and flour with recommended daily allowance of nutrients to control malnutrition
Participate in international research and fund domestic operational research to develop practical models for all of the above suggestions
The current situation in South Asia shows a rapidly expanding, although underreported and underdetected, epidemic of childhood TB. Current health systems are weak and would benefit from integration of IMCI with NTPs. The status of public health and laboratory research shows that these countries have the capacity to scale-up efforts for TB informatics and paediatric TB research. Public health messages through mass media communications to spread awareness about childhood TB and TB in vulnerable populations can also be expected to improve health-seeking behaviour, therefore increasing detection and treatment rates. All of this, however, is dependent on a well-trained healthcare workforce. Researchers and public health practitioners should evaluate and present practical programmatic interventions to stakeholders to motivate buy-in for improvement of NTPs.
This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.
Files in this Data Supplement:
- Data supplement 1 - Online supplement
Contributors SS collected data and wrote the manuscript. AZ conceived the idea and edited the manuscript. RH supervised the study at all stages, wrote the manuscript and edited the manuscript. FM wrote the manuscript and edited graphs and tables. FNQ assisted with write-up and edited the manuscript.
Competing interests None.
Training support Drs Farah Naz Qamar and Fatima Mir received research training support from the National Institute of Health’s Fogarty International Center (1 D43 TW007585-01). The sponsors did not have a role in study design, data analysis or report writing.
Provenance and peer review Commissioned; externally peer reviewed.
If you wish to reuse any or all of this article please use the link below which will take you to the Copyright Clearance Center’s RightsLink service. You will be able to get a quick price and instant permission to reuse the content in many different ways.