This study assessed the barriers to childhood TB case detection and management from the perspective of healthcare providers and caregivers of children with TB. The studies depicted multiple barriers in childhood TB case detection and management. Lack of human resources for TB services, including either staff shortage or limited staff capacity to screen, diagnose, and treat childhood TB, were identified. These findings are similar to those from several studies in other countries 16–20.
Poor collaboration among providers from different services within health facilities, mainly at triage, to screen children for TB was identified in this study. This situation is a context-specific barrier in Cambodia. Through the joint program review of the national TB program in 2012 and 2019, internal referral linkages to facilitate early detection of TB cases were identified as a weak point and needed to be strengthened, such as hospital engagement to screen TB within each hospital department and unit, especially diabetes, pediatrics, and HIV clinics and wards 21,22. This finding suggested that more engagement in TB screening, awareness-raising, and staff capacity building must be strengthened among TB providers and other providers involved in TB detection within the same health facilities. Screening for childhood TB should be done for all children who come to seek healthcare in different services within the health facilities. Based on WHO, in settings where the TB prevalence in the general population is 100/100,000 population or higher, systematic screening for active TB should be considered among people seeking health care 22.
The hospital engagement model has been proved to increase TB case notification. In Pakistan, systematic engagement of hospital administration and all specialist doctors, staff training, and regular facility-based review meetings were associated with a 35% increase in childhood TB case detection during the same period 23. In Cambodia, from 2015 to 2017, FHI-360, through the Challenge TB project, piloted a project called Hospital Linkage in five provinces by identifying 7816 TB cases 24. In 2018, this model was expanded to 10 hospitals under the support of the Global Fund to Fight AIDS, Tuberculosis, and Malaria 25. A joint TB program review in 2019 also recommended strengthening TB management in public hospitals through internal coordination to detect and notify TB early and improve TB case management 21. In 2022, this model was implemented in referral hospitals in 70 operational districts under the Global Fund’s support and in 10 operational districts under the support of the United States Agency for International Development (USAID). The model should be adapted and expanded to other health facilities to strengthen TB screening and management.
All providers reported the lack of quality TB diagnostic tools and supplies of relevant consumables as a limitation to childhood TB detection. This challenge is common, especially in resource-limited settings. In Peru, a lack of adequately functioning radiograph machines was identified as a barrier to childhood TB case detection, and this problem was solved by referring patients to private facilities 16. A previous study in Cambodia also depicted the low availability of proper childhood TB diagnostic tools 12. The joint TB program review in 2019 identified limited access to chest X-ray machines and routine specimen collection for TB diagnosis TB in children 21. These could delay the diagnosis of childhood TB, and caregivers might bring their children to other services in the private sector.
In Cambodia, childhood TB was high, representing 22.5% of the total 29,136 notified TB cases in 2020 7, and almost all notified childhood TB cases in 2020 were clinically diagnosed 26. This situation may lead to empirical and inappropriate treatment and a low treatment success rate 27. Improving the quality of childhood TB diagnosis through investment in diagnostic tools such as GeneXpert® MTB/RIF and digital X-ray machines should be prioritized. Since early February 2021, the national TB program in Cambodia has deployed GeneXpert® Ultra as an initial test for diagnosing TB among the general population, including children in 30 operational districts. The program will be further expanded to other locations in the following years. This intervention is in line with a rapid recommendation recently released by WHO aiming to inform national TB programs and other stakeholders about the critical implications of the latest evidence on the use of specific molecular assays as initial diagnostic tests of pulmonary and extrapulmonary TB and rifampicin-resistant TB in adults and children 28.
Low community involvement was perceived as a barrier to childhood TB case detection and management. These challenges may be specific to the Cambodian context where children are looked after by their grandparents, who would hesitate to accept TB treatment for their grandchildren or decide on behalf of their parents on their grandchildren’s health. Patients' movement and the busyness of caregivers were also perceived as barriers to providing childhood TB services. In addition, caregivers’ ignorance of the seriousness of TB and doctors' advice by the community may result in poor management of childhood TB. In Peru, parental ignorance about TB was the reason for late or undiagnosed TB in children 16. Poor understanding of TB among the community was also perceived as a barrier. This finding is consistent with studies in Indonesia and Bangladesh 29–31. In a recent study, caregivers who were male and ≥ 45 years old and those who had no formal education and poor knowledge of the importance of adherence to TB treatment were the predictors significantly associated with non-adherence to the TB treatment 32.
The availability and quality of TB medicines are essential to ensure optimal TB treatment outcomes. In this study, healthcare providers and caregivers reported the unavailability of childhood TB medicines and the availability of medicines with short shelf-life as barriers to providing TB treatment. In Papua New Guinea, interruption of supplies was reported to cause people with TB to be given a partial supply of medicines, and interruptions in TB treatment could occur when TB medicines were not available 33. The shortage of medicines was identified as a factor associated with poor adherence to anti-TB treatment in India 34. In Cambodia, free anti-TB medicines were provided to patients nationwide. The central medical store is responsible for distributing TB medicines to operational districts, further distributing to health facilities where TB patients come to collect TB medicines. TB medicine unavailability could be due to maldistribution or poor TB medicine management. Ensuring uninterrupted supplies such as appropriate drug forecasting or strengthening the coordination between staff at TB program and pharmacies at each level is needed.
A healthcare provider reported transportation costs as barriers to accessing TB services. The transportation costs may interrupt access to TB services and delay childhood TB diagnosis and management, resulting in poor TB treatment outcomes and a financial burden to the families. In central and western Nepal, lack of transportation was a barrier to TB service utilization 35. In Ethiopia, transportation costs resulted in TB treatment interruptions 36 and posed a significant challenge in seeking TB treatment in India 37.
While TB services have been provided free of charge at public health facilities in Cambodia 38, a caregiver reported that her daughter spent some money while seeking TB care at public health facilities. Out-of-pocket expenditures have been reported while seeking care at public health facilities in Cambodia, but not specifically for TB services 39,40. This finding is similar to studies in other countries where TB diagnosis and treatment were provided for free, but patients still experienced out-of-pocket expenditures 41,42. This may impose a significant financial burden on the family and lead to catastrophic costs.
It was time-consuming to access TB service. This could be due to staff shortage and could lead to a substantial TB diagnosis and treatment delay and increase the opportunity of disease transmission. A similar challenge was identified in other studies. Due to the nature of health infrastructures in sub-Saharan Africa, over 90% of patients spent an average of four visits before their TB diseases were diagnosed 43. In Botswana, repeated visits to health facilities were done by caregivers due to the delay in TB test results, and this led to a delay in the initiation of TB treatment for children 44. To address this challenge, decentralizing childhood TB diagnosis and management, such as further allocating human resources and diagnostic tools for childhood TB, may be needed.
Two of the three grandparents who were the caregivers of children with TB reported physical difficulty and memory loss. Generally, grandparents are the older adults who usually have poor physical and mental health and may even face financial constraints 45. This group of caregivers should receive special attention and support to improve childhood TB case detection and management and other health outcomes. For instance, in this study setting, a grandfather, who was too old to bring his grandchild to the health center, received support from the village chief to facilitate TB medicine collection from the health center.
Study limitations. This study has some limitations. First, since data were collected through face-to-face interviews, reporting bias may occur. Second, this study collected the personal perspectives of healthcare providers and caregivers in Cambodia. Some identified barriers are context-specific for Cambodia or the selected study sites; hence they may not be directly generalized to other settings. Third, there was a gender imbalance among the respondents. The majority of caregiver participants (75%) were female who may experience fewer barriers to accessing childhood TB services than male caregivers. In Cambodia, men are usually the family’s breadwinners and may work far from home or health facilities resulting in difficulty accessing TB services during operating hours. Finally, the recruitment of caregivers by local healthcare providers may lead to selection bias. To reduce reporting bias, the interviewers reiterated the study’s objectives and the implications of the findings and reassured the participants regarding privacy and that whatever they said would not have any negative repercussions on them.