Background
Globally there have been considerable declines in malaria mortality rates during the past decade, but progress has been slowest in countries where the burden of malaria is highest and where access to primary healthcare is most limited [
1]. In Uganda, where malaria accounts for approximately 18% of all deaths in children under-5 years, approximately 65% of the population lived more than 5 km from the nearest government health centre [
2,
3]. To address the disease burden and increase access to healthcare, community health worker (CHW) programmes such as integrated community case management (iCCM), have been extensively supported by WHO, UNICEF and The Global Fund since 2012 [
4]. Studies suggest that when CHW are appropriately trained, supplied and supported, they can increase access to healthcare and reduce under-5 mortality by providing primary healthcare closer to homes of children at risk of malaria [
5‐
7].
A CHW is typically a member of the community with little or no previous professional medical experience, but are trained to diagnose and treat a small number of specific diseases, often including malaria [
8]. A crucial component of CHW training programmes is to identify and refer children who require the attention of higher-level healthcare professionals who are better equipped and trained to manage a wider range of clinical conditions [
9]. For a community based referral system to function optimally, the CHW should first be able to identify children requiring referral based on signs and symptoms and to advise caregivers to take the child to a referral centre; second the caregivers should comply with CHWs referral advice and seek care from health centres; and third health centres should be equipped and ready to manage appropriately the referred children [
10]. Progression through each of these stages is essential to help avoid treatment delays and possibly death.
iCCM has become national healthcare policy in 33 sub-Saharan African (SSA) countries, informed by an ever growing evidence base on how to implement and scale-up this approach. In comparison, data on the effectiveness of referral systems remains limited, despite being an integral component of primary healthcare [
11,
12]. Prior studies have usually reported low compliance with referral advice for example, studies of CHW using mRDTs for only malaria case management in Sierra Leone and Zambia found that 98% and 70% of caregivers respectively, did not comply with referral advice [
13,
14]. Poor compliance has also been reported in recent iCCM programmes, with less than 46% of all caregivers complying with referral [
15,
16]. Yet relatively few studies have examined the barriers that hinder caregivers’ compliance with referral advice. The limited evidence base on referral has been highlighted as a priority research area by the international task force on iCCM [
17]. In this analysis, we explored caregivers’ compliance to CHW referral advice in relation to the demographic, geographical and temporal barriers that might affect compliance, using data collected during two cluster randomised trials to introduce malaria rapid diagnostic tests (mRDT) in community case management in rural Uganda.
Discussion
In these studies, less than 10% of caregivers in rural Uganda adhered to the referral advice given by CHW trained to identify referral signs and symptoms in children under-5 in two different malaria transmission settings. There was a trend suggesting that testing for malaria with mRDTs in the moderate-to-high transmission setting increased caregivers compliance to referral advice compared with a presumptive diagnosis. However, there was no association between compliance and the mRDT result or ACT treatment in the multivariable analyses. The study also found compliance was greater when children presented with severe referral signs and symptoms compared with non-severe signs and symptoms in the moderate-to-transmission setting. Whilst there was some evidence of an association between mRDT testing and compliance in the moderate-to-high transmission setting, there was no association in the low transmission setting. Also, there was evidence that caregivers of children who were not treated with an ACT were more likely to comply with referral advice compared to caregivers of children treated by the CHW. The difference in compliance according to the severity of signs or symptoms might suggest that caregivers also applied their own judgement in deciding which symptoms required higher level management at health centres. Despite the poor overall compliance in both settings, there was evidence to suggest that amongst caregivers who complied with referral advice, many did so within 1 day of being referred.
CHWs in the study were also trained to give pre-referral rectal artesunate to children presenting with signs and symptoms of severe malaria. However, nearly all children treated with rectal artesunate failed to comply with the referral advice. This might be explained by an immediate improvement of signs and symptoms after administering pre-referral treatment and caregivers perceiving there is no longer a necessity to seek treatment. This is particularly concerning, because the failure to seek further curative treatment after pre-referral artesunate may lead to severe disease or a recrudescence of malaria because approximately one-third of children can still be parasitemic after receiving rectal-artesunate [
29,
30]. To improve compliance to referral advice amongst this high-risk group, training materials of CHW should emphasise more strongly that rectal artesunate is not a full curative treatment for malaria and that further care should be sought from health centres.
In both transmission settings, caregivers were less likely to comply when referred during the weekend compared to on weekdays. In the moderate-to-high transmission setting children living in villages further away from health centres were less likely to comply with referral advice, whilst in the low transmission setting caregivers living further away from a health facility were more likely to comply. This counterintuitive finding in the low transmission setting may partly be explained by a health insurance scheme run by a private hospital in the low-transmission setting, this may have facilitated timely use of healthcare services compared to the moderate to high transmission setting that lacked an insurance scheme. There may also have been differences in caregivers’ perceptions of the seriousness of a malaria diagnosis, in this high-altitude epidemic-prone setting where acquire immunity to malaria can be lower and malaria can be deadlier compared to an endemic setting.
In the moderate-to-high setting caregivers who visited CHWs within 24 h of symptoms starting were less likely to comply with referral advice compared to children who visited CHW more than 24 h and children referred during the wet season were less likely to comply compared with children referred during the dry season. By contrast, in the low-transmission setting, there was no association between compliance and the time of fever symptom onset or season. There was a trend that female children were more likely to comply with referral compared to males and compliance was unlikely when children were prescribed ACT compared to when an ACT was not prescribed. This suggests that having received a malaria treatment from the CHW, caregivers decided not to seek further care from health centres, despite being referred by CHW for other symptoms. This may also be a concern because ACTs are intended to treat uncomplicated cases of malaria and management should be sought for children who had other referral signs and symptoms.
Reviewing and linking referral forms completed by CHW and health centre workers, was advantageous as it enabled an assessment of referral compliance on a large sample of referred children and allowed an exploration of several geographical and temporal factors likely to be associated with compliance, such as age, sex, distance and seasonality. However, there are some disadvantages to this method of record linkage. For example, the CHWs reported that caregivers sometimes refused to accept referral forms upon being referred by CHW, indicating that the CHW may not always have issued a referral form. It is also possible that caregivers might leave the forms at home, or that health workers misplaced the forms of children taken to a health centre. In any of these situations, the absence of referral forms at the health centre would be interpreted as the caregiver failing to comply with the referral advice, which may underestimate actual compliance, for example if caregivers had visited without a form. Secondly, routinely available data from the treatment recording forms were used to examine factors likely to be associated with referral. However, these forms did not capture data on several other potentially relevant factors such as socio-economic and educational status of caregivers that may also be associated with compliance. Due to logistical constraints it was not possible to conduct follow-up household visits with all referrals which could have provided more information related to referral compliance, such as education, socio-economic status and attitudes and perceptions towards medicines [
16]. A related cost-effectiveness study reported the household costs for caregivers complying with the referral, which might suggest increased household costs for referral may be a consideration when deciding to comply with referral [
31]. Finally, this study did not follow-up caregivers who did not comply with the referral advice and therefore the health outcomes of these children were not assessed. Further research is required to understand the reasons for poor compliance and the health outcomes of children who do not comply with referral. Finally, this study did not follow-up caregivers who did not comply with the referral advice and therefore the health outcomes of these children were not assessed. Neither did it seek to examine whether CHW’s decision to refer caregivers was correct. It is possible that CHWs referred children who did not require referral and the caregivers’ non-compliance to referral advice had no negative consequence in terms of health outcomes. Further research is required to understand the reasons for poor compliance and the health outcomes of children who do not comply with referral. A qualitative investigation of attitudes towards referral from the perspectives of the caregiver and CHW may help to further understand referral and care seeking behaviours and inform future intervention strategies.
Despite the challenges of tracking referrals in this analysis, the results are consistent with other previous studies investigating referral compliance from community settings which also report low compliance. Studies in Sierra Leone and Zambia with CHW-managed malaria with mRDTs and ACTs found caregivers’ compliance ranged from 2% to 46% respectively [
13,
32]. More recent iCCM referral studies also found suboptimal compliance ranging from 30% to 46% with both iCCM studies also identifying distance to the health centre and household costs of referral to be barriers to access [
15,
16].
The findings from these studies in Uganda and elsewhere show that community based referral systems operate less than optimally at each stage of the referral process. In the first stage, CHW often do not refer children with referral signs and symptoms to the nearest health centre [
23,
33,
34]. In the second stage, caregivers often fail to comply with CHW referral advice and do not seek care from health centres [
13‐
16]. The combined effect of both the failure of CHWs to refer eligible children and the poor compliance to referral advice by caregivers risks undermining the full effectiveness of community based treatment programmes that aim to reduce child mortality by providing primary healthcare services closer to populations with poor access to health centres.
A functional and appropriately managed referral system is an essential component of primary healthcare yet remains poorly understood. In acknowledgement of the current evidence gaps regarding referral the international task force on iCCM has highlighted this as a global research priority [
17,
35]. The evidence presented here provides some evidence that CHWs can make appropriate referrals and caregivers comply with referral advice. It also raises additional research questions requiring further investigation to better inform recommendations and guidelines for countries implementing community programmes. First, our findings indicate that referral compliance may differ depending on the sign or symptom, and referral guidelines and communication with caregivers may thus need to address both clinical priorities and local caregivers’ perceptions of the severity of symptoms. Second, better coordination and monitoring of referrals from the CHW to health centres is required to track caregivers’ compliance and the health outcomes of children. Second, CHWs play an important role in advising caregivers on further treatment options. CHW training could include counselling caregivers about the importance of complying with referral and discussing alternative solutions to overcome barriers to seeking further care. This is particularly important for caregivers who fail to comply with referral advice after their child receives pre-referral rectal artesunate. Third, further research is needed on barriers and enablers of caregiver’s compliance with referral advice. Fourth, better coordination and monitoring of referrals from the CHW to health centres is required to track caregivers’ compliance and the health outcomes of children. Finally, health centres should be equipped and managed to receive referred cases effectively. For example, priority could be given to referral cases upon arrival allowing them to bypass waiting in outpatient departments. Finally, health centres should be equipped and managed to receive referred cases effectively. For example, priority could be given to referral cases upon arrival allowing them to bypass waiting in outpatient departments.
The referral challenges faced by community based programmes may be similar to the challenges to access and utilisation of health services faced by other health programmes. Interventions developed to improve attendance at health centres for pregnant women and utilisation of antenatal care and new-born health, could also be relevant to iCCM programmes to improve health seeking behaviour amongst referred caregivers [
36]. Findings from this field may also be adapted to iCCM programmes to improve health seeking behaviour amongst referred caregivers. For example, interventions that involve regular home visits by CHWs to prepare pregnant women for birth and immediate new-born care could also be adapted to iCCM programmes where CHWs regularly follow-up referred caregivers to encourage compliance and offer further support and counselling on the importance of referral. An important barrier to accessing public health centres are the household costs associated with seeking care [
37]. Financial incentives such as conditional cash transfers (CCTs) aim to offset some of the household financial burden associated with health seeking and CCT interventions have shown to increase the use of health centres for ANC services in Latin American and South East Asian countries [
38]. Further research could explore whether particular models of CCTs within iCCM programmes could also improve caregiver’s compliance with referral advice.
Conclusion
In two randomised controlled trials that evaluated the effectiveness of training CHWs to diagnose malaria using mRDT in Uganda, the majority of caregivers of children with a febrile illness did not comply with the referral advice given by CHW. This is particularly concerning for children with signs of severe disease, including children with severe malaria who received pre-referral treatment with rectal artesunate. Such children are beyond the capacity of CHW and lack of follow up treatment increases the risk of recrudescence, health complications and possible death. The findings also identified multiple geographical and temporal treatment seeking barriers associated with poor compliance. As countries in sub-Saharan Africa continue the scale-up of community based programmes, interventions to diminished barriers to accessing first level referral services are needed to ensure the continuum of care from the community to the health centre.
Over the past decade Uganda and 33 SSA countries have implemented community case management programmes as part of national healthcare strategies and despite the considerable literature on addressing the bottlenecks to scaling-up programmes there has been relatively limited evidence on strengthening referral systems as part of community programmes. The referral system is an important part of primary healthcare to improve access to appropriate care for children with conditions that cannot be managed by CHW. However, unless the referral barriers to comply with referral advice are overcome the full potential of community based programmes may not be achieved.