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Understanding the context of delays in seeking appropriate care for children with symptoms of severe malaria in Uganda

Understanding the context of delays in seeking appropriate care for children with symptoms of... Introduction OPENACCESS A large proportion of children with uncomplicated malaria receive appropriate treatment Citation: Mpimbaza A, Nayiga S, Ndeezi G, late, contributing to progression of illness to severe disease. We explored contexts of care- Rosenthal PJ, Karamagi C, Katahoire A (2019) giver delays in seeking appropriate care for children with severe malaria. Understanding the context of delays in seeking appropriate care for children with symptoms of severe malaria in Uganda. PLoS ONE 14(6): Methods e0217262. https://doi.org/10.1371/journal. This qualitative study was conducted at the Children’s Ward of Jinja Hospital, where children pone.0217262 with severe malaria were hospitalized. A total of 22in-depth interviews were conducted with Editor: Julie Gutman, Centers for Disease Control caregivers of children hospitalized with severe malaria. Issues explored were formulated and Prevention, UNITED STATES based on the Partners for Applied Social Sciences (PASS) model, focusing on facilitators Received: May 18, 2018 and barriersto caregivers’promptseeking and accessing ofappropriate care. The data were Accepted: May 8, 2019 coded deductively using ATLAS.ti (version 7.5). Codes were then grouped into families Published: June 5, 2019 based on emerging themes. Copyright: This is an open access article, free of all copyright, and may be freely reproduced, Results distributed, transmitted, modified, built upon, or Caregivers’ rating of initial symptoms as mild illness lead to delays in response. Use of otherwise used by anyone for any lawful purpose. home initiated interventions with presumably ineffective herbs or medicines was common, The work is made available under the Creative Commons CC0 public domain dedication. leading to further delay. When care was sought outside the home, drug shops were pre- ferred over public health facilities for reasons of convenience. Drug shops often provided Data Availability Statement: Because transcripts of interviews contain potentially identifiable sub-optimal care, and thus contributed to delays in access to appropriate care. Public facili- information, such as names of health facilities, ties were often a last resort when illness was perceived to be progressing to severe disease. health workers, and respondents, data will only be Further delays occurred at health facilities due to inadequate referral systems. available upon request as recommended by the respective institutional review boards that approved this study. Ms Deborah Ekusai Conclusion (dekusai@idrc-uganda.org); Training coordinator Communities living in endemic areas need to be sensitized about the significance of fever, FIC malaria-training program in Uganda, should be contacted for future data requests. even if mild, as an indicator of malaria. Additionally, amidst ongoing efforts at bringing PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 1 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda Funding: This research was supported by two antimalarial treatment services closer to communities, the value of drug shops as providers training awards from the NIH Fogarty International ofrationalantimalarialtreatment needs to be reviewed. Center, the University of California Global Health Institute GloCal Health Fellowship (TW009343) and the Training in Malaria Research in Uganda program (TW007375). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared Introduction that no competing interests exist. For African children with uncomplicated malaria, the World Health Organization (WHO) recommends prompt treatment with artemisinin-based combination therapies (ACTs) within 24 hours of illness onset as a key strategy for preventing progression to severe malaria [1]. Unlike in the past, when ACTs were scarce and expensive [2], efforts by governments, interna- tional organizations, and partner institutions have resulted in increased availability of high quality and affordable ACTs in both the private and public health sectors [3]. This achievement has likely contributed greatly to reductions in malaria morbidity and mortality in Africa [4, 5]. However, despite increases in ACT coverage rates, the proportion of eligible children receiving ACTs within 24 hours of illness onset remains low [6], partly explaining why hundreds of thousands of children continue to die of malaria each year [7]. If malaria control and elimination programs are to succeed, there is a need to ensure maxi- mum treatment effectiveness, characterized by high quality case management and appropriate health seeking behavior by patients or caregivers [8]. Studies in sub-Saharan Africa have shown that the delivery of antimalarials may fail at different stages, including at the initiation of treatment at home, or due to health care providers offering ineffective medicines [9]. For children, caregivers’ response to illness is the first and probably the most important step in determining if treatment is received promptly [10]. Circumstances surrounding caregivers’ delays in seeking appropriate care are complex [11]. Knowledge, perception, and beliefs of ill- ness are known to influence the time taken to appraise symptoms, thus influencing response time and potentially leading to delays in seeking care. Categorization of fever as a minor ailment by caregivers has been shown to delay response to illness among children with malaria in Tanzania [12]. Treatment of illness episodes with local remedies and herbs contributes to further delays in seeking appropriate care [13, 14]. Furthermore, if care is sought at drug shops, where the quality of care is often sub-optimal [15], delay in receiving appropriate treatment is a likely outcome [16, 17]. Social networks, including caregiver partners, parents, in-laws, and neighbors involved in negotiating response to illness can also be associated with delays in care [18]. Understanding caregivers’ health seeking behavior while taking into consideration contex- tual factors that govern behavior is a prerequisite for formulating policies targeted at optimiz- ing response to illness [19]. However, policy efforts continue to focus on provider factors such as increasing availability of ACTs to communities at risk, while neglecting demand side factors such as how caregivers interpret and respond to symptoms of illness. Sensitizing communities to availability of services and providing classical biomedical descriptions of symptoms of malaria have had little impact on caregivers seeking care promptly [20]. This situation is likely explained by consideration of care seeking as a linear pathway, neglecting social and environ- mental contexts that govern individual behavior and response types which shape pathways to care[20–22]. Utilizing interviews with caregivers of children who presented with severe malaria in Jinja, Uganda, we explored the social and environmental constraints that shape when and how caregivers respond to illness, and sought to explain delays in accessing appro- priate treatment for malaria. PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 2 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda Research team A social scientist with undergraduate and postgraduate training in social science, and epidemi- ology, respectively led all interviews. The lead interviewer is female and has experience span- ning a period of 10 years, working as a coordinator on several qualitative studies [23–25]. A member of the local hospital staff, who was well accustomed with local language, culture, and social norms of the locals recruited patients, explaining to respondents reasons for conducting the study, introducing the interviewer and when applicable translating and responses. At the time of conducting interviews, the interview team was aware of the main findings of the pri- mary study. Prior to conducting the interview, the interview team introduced themselves to the study participants highlighting, who they were, and where they came from. Additionally, they explained the purpose of the interview to study participants. Methods Study design This was a qualitative study, linked to a study of determinants of severe malaria in children, in which delay in seeking appropriate care was found to be a strong risk factor for severe malaria [16]. Caregivers of children hospitalized with severe malaria were interviewed to explore how their social and environmental contexts influenced when and how they responded to illness. We explored motivations for caregivers’ actions in response to illness, explaining delays in seeking and accessing appropriate treatment for their children. Our approach was mainly deductive in nature, driven by the hypothesis that delay in seeking appropriate care was a risk factor for severe malaria. Theoretical framework To explore contextual factors, this study drew on the Partners for Applied Social Sciences (PASS) model [26]. The model is built on the backbone ofa pathway model, focusing on factors involved ineach step of the pathway to care that hinder or facilitate prompt seeking or access to appropriate care. Factors in the model are grouped into four main categories: 1) illnessper- ception and explanatory models; 2) social values; 3) access tocare and resource seeking; and 4) medicalpluralism [26]. Considering social and environmental contexts, we explored how these factors contributed to caregiver delays in seeking appropriate care for children with malaria. Study setting The study was conducted in the catchment area of the Children’s Ward of Jinja Regional Referral Hospital, which includes 10 districts located in the Busoga sub-region, with a few patients also coming from two districts located in the Buganda region [16]. Malaria transmis- sion in the sub-region is considered hypo to hyper endemic [27]. In 2016, the malaria parasite prevalence rate among children in the Busoga sub-region was 53.1% based on an HRP2-base- drapid diagnostic test [28]. The economic base for 53% of the local people is subsistence-ori- ented farming [29], with some villagers engaging in small-scale business such as operating small roadside shops. The Busoga region has 42.0% of the population living in poverty and is known to suffer from famine [29], malnutrition, very high infant mortality rates, and rampant jigger epidemics [30, 31]. Literacy levels are low, with 56.1% and 43.8% of male and female heads of households being literate. The Early Childhood Development Index, a composite measure of the developmental status of children, was reported to be 55.5% in the region, the lowest value reported in Uganda [28]. PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 3 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda The local health arena in Busoga is pluralistic, with access to traditional medicine and bio- medicines at both public and private facilities [32]. The region has public health facilities rang- ing from level II to level IV health centers, district hospitals and a regional referral hospital. The average distance between level III (and above) health facilities and households is < 5 km [16]. Services rendered at public facilities are plagued by staff absenteeism and frequent stock outs of essential medicines [33]. Drug shops, though popular, often offer substandard services [15, 34, 35]. Initiatives at improving quality of services at drug shops have been implemented in the region, with reported success [36]. Sampling Sampling was purposive and research participants were selected based on gender, relation to the child, age, time taken to seek care, and form of severe malaria. Maximum variation in the selection of respondents ensured that different social groups were represented, including con- sideration of employment and socio-economic status. The study team approached eligible respondents during hospitalization at Jinja Children’s Hospital. Respondents were purposively included in the sampling frame. Sample size The final sample size for the study was 22 caregivers and was not pre-determined, but reached based on the principle of data saturation, where gathering fresh data from additional respon- dents did not reveal new insights or findings based on our theoretical model. All eligible study participants agreed to participate when approached. Setting of data collection Interviews with caregivers were conducted privately during the recovery period of the child’s hospitalization either in the hospital gardens or in one of the study offices, depending on the respondent’s choice. Both venues offered privacy, with minimum interruption. For all 22-interview sessions, no one other than the child’s primary caregiver and interviewers were present. Data collection An interview guide was developed (S1 Appendix) based on key themes agreed upon by the study team based on observations noted during the primary study. The interview guide was pilot tested and modified by the lead interviewer, improving on sequencing of questions. Inter- views lasted less than 2 hours and were conducted in the local language. The interviews were audio recorded and transcribed in the language in which they were conducted before transla- tion into English by an experienced interviewer. The interviewer did not repeat any of the interviews, nor were transcribed interviews returned to study participants for comment and correction. Additionally, upon completion of each interview, the interviewer noted a summary of key observations during the interview. Patient responses were categorized into three phases: 1) illness recognition, 2) response to illness and 3) actions. Definition of terms Delay was defined as a prolonged interval (typically >24 hours) between illness onset and commencement of appropriate treatment. Illness recognition was defined as the caregivers’ appraisal of symptoms as a sign of illness. Response was defined as the caregiver acknowledg- ing the need to intervene upon the child’s illness. Caregivers’ actions were defined as the PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 4 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda measures taken in response to illness. Individuals who provided advice to the caregiver in terms of how to respond to the child’s illness were referred to as the therapeutic management group[26]. The primary caregiver was the person who was with the child right from onset to presentation to hospital. Data analysis Analysis of data was deductive in nature, informed by preliminary findings of the primary study that identified delayed seeking of care and seeking care at drug shops as potent risk fac- tors for severe malaria [16]. Upon completion of the primary study, findings were presented to a panel of experts, including pediatricians, social scientists, and medical anthropologists, dur- ing which themes worthy exploration were formulated. Individual transcripts were entered into ATLAS.ti. Version 7.5.18 (Atlas.ti. GmbH, Berlin Parts), and coded (a code was a word or short phrase that symbolically assigned meaning to a portion of language in the data) by the lead investigator of the study under the supervision of a medical anthropologist using a mixed approach of both open and closed coding based on pre–defined criteria. Related codes were categorized into families’ representative of different themes informed by the findings of the quantitative study [16]. These themes formed the basis of the write-up and discussion. Partici- pants were not involved nor consulted for opinion on themes. The design and findings of this study are reported following the consolidated criteria for reporting qualitative research (COREQ; S2 Appendix;) [37] Ethics approval Institutional approval was obtained from the Uganda National Council of Science and Tech- nology, and the Institutional Review Boards from the College of Health Sciences, Makerere University, and the University of California San Francisco. Written informed consent was obtained from each caregiver. In addition to obtaining consent, the interviews were conducted in accordance with good clinical practice, applicable patient privacy requirements, and the guiding principles of the Declaration of Helsinki. Results Characteristics of the study sample We interviewed 22 caregivers, each with a child hospitalized with severe malaria at the Chil- dren’s Ward of Jinja Regional Referral Hospital during the months of February and March 2016.The majority of the caregivers were mothers (15, 68.2%), with grandmothers (3, 13.6%), fathers (2, 9.1%), aunts (2, 4.5%), and stepmothers (1, 4.5%) accounting for the others. The average age of caregivers’ was 31 years (range 18 to 48years). Most (68%) caregivers were pri- marily engaged in subsistence farming, with occasional selling of excess food (Table 1). Different kinds of fevers Caregivers reported that their children experienced different kinds of fevers, characterized as mild or severe, sometimes contributing to delays in seeking care outside of the home as some of the fevers were ranked as low grade, not deserving serious attention (Quotes A317, A324). A317: “If a child has a temperature. . . you get a damp cloth and sponge them. . ..for the simple one you give panadol, they sweat and the fever goes down” A324:“The body may be hot but not very hot. The child may be playing and eating. We can say that let us give them some coartem. They will get better.” PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 5 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda Table 1. Demographic and clinical characteristics of caregivers and their enrolled children. Characteristics of caregivers of enrolled children Average age in years 31.6 Age range in years 18 to 48 Relation with child Mother 114 (63.6%) Grandmother 1 (4.5%) Stepmother 2 (9.0%) Father 2 (9.0%) Grandmother 3 (13.6%) Occupation Peasant 15 (68.1%) Business 5 (22.7%) Tailor 1 (4.5%) Waitress 1 (4.5%) Characteristics of enrolled children Age in years 2.6 Age range in years 0.5 to 7.5 Gender Female 9 (40.9%) Type of severe malaria Unconsciousness 5 (22.7%) Severe anemia 10 (45.4%) Respiratory distress 3 (13.6%) Unconsciousness & Severe anemia 1 (4.5%) Respiratory distress & Severe anemia 1 (4.5%) Respiratory distress & Unconsciousness 1 (4.5%) Respiratory distress & Unconsciousness& Severe anemia 1 (4.5%) https://doi.org/10.1371/journal.pone.0217262.t001 Fever described as “hot "or “high “in isolation or with other symptoms such as loss of appe- tite or extreme body weakness was considered a sign of serious illness, triggering rapid response (Quotes A316, A308). A316:“The very high fever can cause me to run. If I delay, the child weakens. If I delay, the child gets dehydrated. If I delay it makes him anemic." A308: “When he is all hot? No, at least you put a cloth in water, squeeze the water out and wipe him from head to toe. . .then proceed. Because at that point it is excessive to the extent that both the hands and the legs are hot. It is excessive and you have to head straight to the hospital.” Caregivers understanding of malaria Caregivers also talked about mild and severe malaria, with some equating the occurrence of fever with malaria. They mentioned symptoms of severe malaria such as anemia that they con- sidered could result in death and indeed, when children had these symptoms caregivers responded promptly. A311: “. . ...he can get malaria, gets weak, blood gets low, water in his body gets drained. So if you stay home and ignore the situation and say I was given this let me just wait the child can die in that way.” Furthermore, caregivers explained that severe malaria was a result of delayed seeking of appropriate care (Quotes A319, A325, A326). PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 6 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda A319:“. . .. The only problem is that if you delay, the illness gets severe.” A326:“. . .. If (malaria) gets the child and you delay to go to hospital it has to kill the child because you have delayed.” These delays however were not necessarily deliberate or within the control of the caregivers. Therapeutic management groups as a source of delay Caregivers explained that the interpretation of the child’s illness sometimes involved other members of the family. Caregivers living with parents or mothers-in-law for example explained that they felt obliged to seek advice from them. Others consulted included fathers, grandparents, neighbors, and friends. The process of consultation itself caused delays. In some cases the symptoms were perceived to be because of witchcraft or other ailments and so herbal medicines were prescribed in place of conventional medicines, thus contributing to delays (Quote A309). A309:“They stopped me from giving her the drug. . .. . ..the old people including my mother in law.” Some mothers expressed independence to make decisions without consultation or approval of the fathers (Quote A315). A315: “Recently it happened. He told me to go to Nalufenya and I refused and decided to go � � � to another place because the people at hospital delay patients. My child will die from there. They toss you up and down before offering any treatment. In that way we did not agree. I went on my own and he did not give me money. When I got there I called him on phone and informed him of where I was and he came.” Delays due to home treatment At home, caregivers often initiated treatment with a combination of herbs and conventional medicines. This was often followed by a waiting period in anticipation of recovery following use of these medicines. This contributed to delays in seeking appropriate care. Conventional medicines provided included panadol, oral antibiotics, and antimalarials, often purchased from drug shops, or left over from treatment of a previous illness episode (Quotes A307). A307: "On Saturday I had some coartem so I picked one coartem and panadol and I gave him in the morning. Then in the evening, I gave him more. I then added him more on Sunday morning and also on Sunday evening. When it came to midnight in the night, he started con- vulsing. I tried to wipe him a bit. I feared to give him more medicine. I picked a car and brought him to hospital and they treated him from here.” Use of herbal medicines was common, with ’mululuza,’ bombo, ‘and ’lubirizi’ being the most frequently mentioned. These were given concurrently with conventional medicines. Herbs were primarily given to reduce fever, rarely with the intention to cure illness (Quote A328). A328: “When I am at home, I use a rag to wipe the body so that the temperature goes down. I also get lubirizi and bombo and give the child . . ... Now, I first crush them in a cup and give PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 7 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda the child to drink then I pour the rest in the child’s basin for the child to bathe. . .. . .. . .. . .. They relieve the child.” Mashed onions and garlic smeared on the child’s body were used to prevent and cure con- vulsions; however this intervention did not prevent caregivers from seeking care at public health facilities. A312:“I think that when a child convulses it is malaria. We were told that when he convulses we smear him with onions and it stops.” Delays due to drug shops Caregivers also reported going to drug shops and clinics because of their close proximity, low cost, and availability of medicines. A309:"The government hospital is very far from our home so we first go to the drug shop and then when the condition does not change then we go to the government hospital.” A325:"We take them to the nearby clinic where we can get some drugs. They tell us that when you go there sometimes they find him some drugs. They give us some drugs and I also explain the problems the child has, for this number of days and the illness is like this and they try to mix for me some drugs.” However, despite being convenient, drug shops often provide sub-optimal care. The inade- quacies of drug shops reported by caregivers included the staff’s lack of knowledge and equip- ment to diagnose malaria. There were delays described in the referral process even when the child was not getting better (Quotes A312, A308). A308:”the private clinic where we started, they ‘ate’ a lot of money. Because whatever they told us, we would do. They would tell you buy this, you would go and buy. They would tell you buy a syrup, you would go and buy. Even others I just left them behind. Because initially they gave us syrup but when I went with them to Lulyambuzi, they sorted them, we went with 7 syrups. New ones. They sorted them and we threw away 5 of them. They left us with 2 and said those are the ones we should use for this illness. Because all the person was chasing back there was money. Just wanting to get money. But we didn’t know what was wrong with the child. But when we gave him those two syrups and threw the 5, he started getting back in line. But when we combined with the others, it would be as if you are increasing the sickness. But he has ‘eaten’ money; I don’t even know the amount. For a long time, this child has not been well.” A metaphor used to suggest fraud, which in this context implied that providers were extorting money from caregivers for unwarranted services. A312:"I feel like when you go to the drug shop, the treatment is expensive.” . . . If you do not rush them to hospital and they check what the problem is, you may go to the drug shop and they give him treatment that does not relate with malaria and as a result they may die” Caregivers explained that they sought care at drug shops for illnesses that they considered mild. Only when symptoms persisted or the child deteriorated, did they opt to seek care at a public health facility, which they deemed more appropriate for treating severe malaria (Quotes A312, A324). PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 8 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda A312: “It seems what causes them is the same thing but I think the severe one will have grown and would no longer be managed by drug shops and the like but it requires a blood sample to be taken and they see the actual disease and the drugs they will use..” A324: "Where I stay there is a clinic nearby. That is where I usually get first aid. When it gets worse then we come here. . . . . .We only get first aid from there. When it gets worse and they cannot manage at the clinic then we go there.” Delays at public health facilities Caregivers explained that public health facilities often lacked medicines, and had rude health workers who were often absent from work (Quote A315).Caregivers expressed frustration regarding spending money on transport to public health facilities that did not have medicines. They further explained that often they were asked to buy medicines at public health facilities, which was a problem for caregivers that did not have money. A315: There is another place but they never have medicine. When you go there they tell you that there are no drugs Interviewer: What place is that? � � � A315: It is called health center. Interviewer: It is a government hospital. A315: Yes Interviewer: Health center three or two. A315: Three but when you get there they tell you that they do not have drugs. You may get there and there are no health workers. A317: “Yes, you need transport of 1500 plus it is painful. . .. . .. . .. . ...You find that there are no drugs, even panadol they don’t give you that is why we don’t go. So you would use that money and go to the clinic.” While public health facilities were reported to promptly refer patients, caregivers had to arrange for transport to the next level. This contributed to delays in accessing appropriate care (S3 Appendix). Overall, multiple processes contributed to delays in access to appropriate care for children that were eventually diagnosed with severe malaria. Discussion We studied contexts that contributed to delays in appropriate care for children who eventually developed severe malaria. Consistent with previous reports[20], mild fevers led to delays in response. Caregivers responded to what they perceived as mild illness with ineffective home interventions. When care was sought outside the home, drug shops were preferred over public facilities, but because the care was often sub-optimal, there was delay in accessing appropriate treatment. Caregivers ably explained the cause of malaria and were aware of the common manifesta- tions of severe malaria; appreciating the fact, that malaria could cause death. However, their understanding did not appear to have a bearing on how they responded to illness and on the time to seek appropriate care, suggesting that response were influenced by other factors, such PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 9 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda as the contexts within which they lived [20]. Caregivers’ perceptions of illness as mild based on low fever has been reported in other countries in sub-Saharan Africa [38], possibly explained by the subtle, non-specific and irregular nature of initial symptoms of most malaria episodes [39, 40]. In such circumstances, caregivers may feel that a child’s illness is benign, thus opting to observe or provide simple, ineffective home remedies [12, 41], contributing to delay in seek- ing appropriate care for malaria. Home remedies may suffice for common childhood viral infections, which are often self-limiting [42], but slow response to malaria is dangerous, as established infection can rapidly progress to severe disease [43]. Consultations with family members and neighbors were also a common cause of delay. Advice given was often using of herbs, contributing to delays in seeking appropriate care [18]. Culturally, grandmothers and mothers-in-law, particularly if paternal, hold a dominant posi- tion, to the extent that caregivers are obliged to follow advice, even if they disagree [18, 41]. Fathers were consulted, often times for financial support. However, in contrast to previous reports [44], involvement of fathers did not notably contribute to delays in care. Some caregiv- ers reported having autonomy to make decisions in the absence of fathers or when dealing with an uncooperative father, demonstrating empowerment of some mothers [45]. Outside homes, drug shops were the preferred choice of care, a finding consistent with results of other studies in the region [46, 47]. Drug shops have proliferated in both rural and urban areas [3, 47]. As reported previously, short distance from home, lower cost of obtaining care compared to health centers, short waiting times, and ease of accessing medicines were rea- sons for preference of drug shops [15, 48]. Interestingly, caregivers sought care at drug shops for symptoms deemed mild and not serious, suggesting that they were aware of the shortcom- ings of these shops. The popularity of drug shops offers an opportunity for promoting timely access to appropriate antimalarial treatment [46, 49]. However, limitations of drug shops, including lack of provider knowledge on management of malaria [36, 50, 51], poor referral practices [52], lack of diagnostic capacity [53, 54], and profit driven behaviors [55], remain major hurdles. Programs directed at improving services at drug shops have yielded mixed results [56]. Publications from the ACT Watch group, a multi-country research project designed to fill evidence gaps in malaria treatment [57], suggest that despite efforts to improve care, appropriateness of antimalarial treatment at drug shops remains sub-optimal [49, 58– 66]. In Tanzania, the Accredited Drug Dispensing Outlet program for regulating and training drug shops to provide affordable and quality medicines was successful in promoting appropri- ate antimalarial treatment [67, 68]. However, sustaining gains has proven to be a problem [69], with reports indicating providers returning to poor dispensing practices [70, 71]. Rapid Diag- nostic Tests have been introduced at drugs shops to rationalize use of antimalarials, but amidst resistance from providers given the desire to profit through the sale of anti-malarial treat- ments, and from caregivers due to high costs [72, 73]. What is the best approach for improving delivery of health services amidst constraints of the public health system and the popular private sector? One approach is to strengthen the public health system which, despite its challenges [74], has the infrastructure and human resources for effective delivery of health services [75]. Beyond focusing on patient care, efforts should to be directed at improving hospitality services at public facilities. Studies in Uganda and Malawi have shown that abusive and disrespectful health workers were barriers to access- ing care at public facilities [76, 77]. This may partly explain why caregivers initially seek care at drug shops, whose hospitability services are likely far better due to the need to maintain cus- tomers [78, 79]. Strengthening the quality of services at drug shops is an alternative option. However, achieving quality services at drug shops is limited by multiple challenges including sub-optimal drug dosing, use of medicines not in national treatment guidelines [80], limited diagnostic capacity and inconsistent referral practices [55, 81], and the desire for profits [82]. PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 10 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda Additionally, despite laws that provide for standards of operations, many drug shops operate illegally [83], with poor quality of health services [46, 84, 85], including inappropriate provi- sion of parenteral artesunate [86]. This situation calls for policymakers to embark on programs of action to empower and strengthen regulatory frameworks and instruments in relation to drug shops [75]. Regardless of limitations, policy makers must acknowledge that drug shops are a popular point of care and can be mobilized to treat acute febrile illnesses among rural populations. In Tanzania [67] and Kenya [87, 88] interventions including provision of subsidized packs of pedi- atric ACT to retail outlets, training of retail outlet staff, and community awareness activities resulted in significant increases in ACT coverage for reported fevers. In-appropriate use of anti- malarials by drug shops remains a concern. However, provision of rapid diagnostic tests for malaria in the private sector could minimize this problem as was demonstrated in a study in Ghana [89], where introduction of RDTs resulted in reduced dispensing of antimalarial to patients without malaria, and did not reduce prescribing of antimalarials to true malaria cases. Additionally, by applying principles of commercial marketing to social health problems, drug shops have the potential to serve as an effective mechanism for promoting socially beneficial behavior change [75]. Also banning drug shops because of poor quality of care concerns may run them underground, causing more harm than good. Key is finding the right balance, support- ing drug shops to provide much needed services, but maintaining acceptable standards of care. In conclusion, we report on delays in seeking appropriate care by caregivers of children eventually diagnosed with severe malaria. Lack of action for perceived mild fever contributed to delays in care. Social networks including grandmothers and mothers-in-law, whose influ- ence often resulted in inappropriate treatment options, led to further delays. Despite the opportunity, drug shops have been shown to contribute to delay in seeking appropriate care [16], possibly explained by providing inappropriate care. Unfortunately, caregivers often sought care at public health facilities only when interventions at home or at drug shops had failed and illness had progressed from mild to severe. To address these gaps, there is need for a multipronged approach, starting with prioritization of health education programs sensitizing communities living in endemic areas, not only on recognition of symptoms of malaria, but emphasizing the significance of fever, irrespective of grade as an indicator of malaria [20]. For drug shops, there is need to define the role ofdrug shops in providing care to sick children in sub-Saharan Africa. Once defined, shop attendants should be trained and regulated to operate appropriately. For the public health sector, governments and partners need to direct efforts towards improving quality of hospitality services, a neglected area deserving attention. Supporting information S1 Appendix. In-depth interview guide. (PDF) S2 Appendix. Checklist for fulfillment of consolidated criteria for reporting qualitative studies (COREQ). (XLSX) S3 Appendix. Transcript for interview A325. (PDF) Acknowledgments We thank the study team of Yasin Kisambira, Jessica Tagobera, AnnetNabweteme, ProssyEwi- nyo, AzizzKiwanuka, Rose Nabirye, Peter Wambi, Ronald Bayisuka, William Ambayo, Juliet PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 11 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda Nabunjje, Fiona Kassana, David Katikati, Sally Opus, and Benjamin Buyi. We also thank health workers in Jinja Hospital and other participating health facilities for supporting the study team. We thank the staff of the Infectious Diseases Research Collaboration for providing administrative support. Finally, we are grateful to the parents, guardians, and caretakers who agreed to take part in this study. Author Contributions Conceptualization: Arthur Mpimbaza, Grace Ndeezi, Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. Data curation: Arthur Mpimbaza, Susan Nayiga, Charles Karamagi, Anne Katahoire. Formal analysis: Arthur Mpimbaza, Susan Nayiga, Anne Katahoire. Funding acquisition: Arthur Mpimbaza, Philip J. Rosenthal. Investigation: Arthur Mpimbaza, Grace Ndeezi, Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. Methodology: Arthur Mpimbaza, Susan Nayiga, Grace Ndeezi, Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. Project administration: Arthur Mpimbaza, Philip J. Rosenthal, Anne Katahoire. Resources: Arthur Mpimbaza, Susan Nayiga, Philip J. Rosenthal. Software: Arthur Mpimbaza. Supervision: Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. Validation: Arthur Mpimbaza, Anne Katahoire. Writing – original draft: Arthur Mpimbaza, Susan Nayiga, Grace Ndeezi, Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. Writing – review & editing: Arthur Mpimbaza, Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. References 1. World Health Organization. WHO Global Technical Strategy for Malaria 2016–2030. 2016. 2. Nosten F, White NJ. Artemisinin-based combination treatment of falciparum malaria. American journal of tropical medicine and hygiene. 2007; 77(6 Suppl):181–92. 3. Opiyo N, Yamey G, Garner P. Subsidising artemisinin-based combination therapy in the private retail sector. The Cochrane database of systematic reviews. 2016; 3:CD009926. https://doi.org/10.1002/ 14651858.CD009926.pub2 PMID: 26954551 4. Camponovo F, Bever CA, Galactionova K, Smith T, Penny MA. Incidence and admission rates for severe malaria and their impact on mortality in Africa. Malar J. 2017; 16(1):1. https://doi.org/10.1186/ s12936-016-1650-6 PMID: 28049519 5. Korenromp E, Mahiane G, Hamilton M, Pretorius C, Cibulskis R, Lauer J, et al. Malaria intervention scale-up in Africa: effectiveness predictions for health programme planning tools, based on dynamic transmission modelling. Malar J. 2016; 15(1):417. https://doi.org/10.1186/s12936-016-1461-9 PMID: 6. Bennett A, Bisanzio D, Yukich JO, Mappin B, Fergus CA, Lynch M, et al. Population coverage of artemi- sinin-based combination treatment in children younger than 5 years with fever and Plasmodium falcipa- rum infection in Africa, 2003–2015: a modelling study using data from national surveys. Lancet Glob Health. 2017; 5(4):e418–e27. https://doi.org/10.1016/S2214-109X(17)30076-1 PMID: 28288746 7. World Health Orgnaization.World Malaria Report. 2017 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 12 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda 8. Zurovac D, Rowe AK. Quality of treatment for febrile illness among children at outpatient facilities in sub-Saharan Africa. Ann Trop Med Parasitol. 2006; 100(4):283–96. https://doi.org/10.1179/ 136485906X105633 PMID: 16762109 9. Whitty CJ, Chandler C, Ansah E, Leslie T, Staedke SG. Deployment of ACT antimalarials for treatment of malaria: challenges and opportunities. Malar J. 2008; 7 Suppl 1:S7. 10. Tanner M, Vlassoff C. Treatment-seeking behaviour for malaria: a typology based on endemicity and gender. Social science & medicine. 1998; 46(4–5):523–32. 11. Kassam R, Collins JB, Liow E, Rasool N. Narrative review of current context of malaria and manage- ment strategies in Uganda (Part I). Acta tropica. 2015; 152:252–68. https://doi.org/10.1016/j. actatropica.2015.07.028 PMID: 26257070 12. Kamat VR. "I thought it was only ordinary fever!" cultural knowledge and the micropolitics of therapy seeking for childhood febrile illness in Tanzania. Social science & medicine. 2006; 62(12):2945–59. 13. Tabuti JR. Herbal medicines used in the treatment of malaria in Budiope county, Uganda. J Ethnophar- macol. 2008; 116(1):33–42. https://doi.org/10.1016/j.jep.2007.10.036 PMID: 18054454 14. O’Neill S, Gryseels C, Dierickx S, Mwesigwa J, Okebe J, d’Alessandro U, et al. Foul wind, spirits and witchcraft: illness conceptions and health-seeking behaviour for malaria in the Gambia. Malar J. 2015; 14:167. https://doi.org/10.1186/s12936-015-0687-2 PMID: 25908392 15. Rutebemberwa E, Pariyo G, Peterson S, Tomson G, Kallander K. Utilization of public or private health care providers by febrile children after user fee removal in Uganda. Malar J. 2009; 8:45. https://doi.org/ 10.1186/1475-2875-8-45 PMID: 19284673 16. Mpimbaza A, Ndeezi G, Katahoire A, Rosenthal PJ, Karamagi C. Demographic, Socioeconomic, and Geographic Factors Leading to Severe Malaria and Delayed Care Seeking in Ugandan Children: A Case-Control Study. The American journal of tropical medicine and hygiene. 2017; 97(5):1513–23. https://doi.org/10.4269/ajtmh.17-0056 PMID: 29016322 17. Kassam R, Sekiwunga R, MacLeod D, Tembe J, Liow E. Patterns of treatment-seeking behaviors among caregivers of febrile young children: a Ugandan multiple case study. BMC public health. 2016; 16:160. https://doi.org/10.1186/s12889-016-2813-7 PMID: 26883506 18. Colvin CJ, Smith HJ, Swartz A, Ahs JW, de Heer J, Opiyo N, et al. Understanding careseeking for child illness in sub-Saharan Africa: a systematic review and conceptual framework based on qualitative research of household recognition and response to child diarrhoea, pneumonia and malaria. Social sci- ence & medicine. 2013; 86:66–78. 19. Mangham-Jefferies L, Hanson K, Mbacham W, Onwujekwe O, Wiseman V. What determines providers’ stated preference for the treatment of uncomplicated malaria? Social science & medicine. 2014; 104:98–106. 20. Williams HA, Jones CO. A critical review of behavioral issues related to malaria control in sub-Saharan Africa: what contributions have social scientists made? Social science & medicine. 2004; 59(3):501–23. 21. Glass TA, McAtee MJ. Behavioral science at the crossroads in public health: extending horizons, envi- sioning the future. Social science & medicine. 2006; 62(7):1650–71. 22. Bloom G, Standing H. Future health systems: Why future? Why now? Social science & medicine. 2008; 66(10):2067–75. 23. Bukirwa H, Nayiga S, Lubanga R, Mwebaza N, Chandler C, Hopkins H, et al. Pharmacovigilance of anti- malarial treatment in Uganda: community perceptions and suggestions for reporting adverse events. Tropical medicine & international health: TM & IH. 2008; 13(9):1143–52. 24. Nayiga S, DiLiberto D, Taaka L, Nabirye C, Haaland A, Staedke SG, et al. Strengthening patient-cen- tred communication in rural Ugandan health centres: A theory-driven evaluation within a cluster ran- domized trial. Evaluation. 2014; 20(4):471–91. https://doi.org/10.1177/1356389014551484 PMID: 25. Hutchinson E, Nayiga S, Nabirye C, Taaka L, Staedke SG. Data value and care value in the practice of health systems: A case study in Uganda. Social science & medicine. 2018; 211:123–30. 26. Muela Ribera J. The PASS-model: a model for guiding health-seeking behavior and access.Malaria Reports 2012; volume 2:e3s 27. Talisuna AO, Noor AM, Mundia CW, Otieno V, Mitto B, Amratia P, et al. An epidemiological profile of malaria and its control inUganda. Analysis and report funded by Roll Back Malaria and Department for InternationalDevelopment-UK, Sept 2013 28. Uganda Bureau of Statistics (UBOS) and ICF International Inc. (2016). Uganda Demographic and Health Survey 2011. Kampala, Uganda: UBOS and Calverton, Maryland: ICF International Inc. 2011 29. Uganda Bureau of Statistics (UBOS). Uganda National Household Survey 2012/2013. Kampala Uganda; UBOS. 2016 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 13 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda 30. Mutebi F, Krucken J, von Samson-Himmelstjerna G, Waiswa C, Mencke N, Eneku W, et al. Animal and human tungiasis-related knowledge and treatment practices among animal keeping households in Bugiri District, South-Eastern Uganda. Acta tropica. 2018; 177:81–8. https://doi.org/10.1016/j. actatropica.2017.10.003 PMID: 29017876 31. Wafula ST, Ssemugabo C, Namuhani N, Musoke D, Ssempebwa J, Halage AA. Prevalence and risk factors associated with tungiasis in Mayuge district, Eastern Uganda. The Pan African medical journal. 2016; 24:77. https://doi.org/10.11604/pamj.2016.24.77.8916 PMID: 27642416 32. Konde-Lule J, Gitta SN, Lindfors A, Okuonzi S, Onama VO, Forsberg BC. Private and public health care in rural areas of Uganda. BMC international health and human rights. 2010; 10:29. https://doi.org/ 10.1186/1472-698X-10-29 PMID: 21106099 33. Ministry of Health, Uganda. Uganda Hospital and Health Centre IV Census Survey 2014.Availablefrom: https://www.who.int/healthinfo/systems/SARA_H_UGA_Results_2014.pdf 34. Awor P, Wamani H, Bwire G, Jagoe G, Peterson S. Private sector drug shops in integrated community case management of malaria, pneumonia, and diarrhea in children in Uganda. The American journal of tropical medicine and hygiene. 2012; 87(5 Suppl):92–6. 35. Rutebemberwa E, Kallander K, Tomson G, Peterson S, Pariyo G. Determinants of delay in care-seek- ing for febrile children in eastern Uganda. Tropical medicine & international health: TM & IH. 2009; 14 (4):472–9. 36. Awor P, Wamani H, Tylleskar T, Peterson S. Drug seller adherence to clinical protocols with integrated management of malaria, pneumonia and diarrhoea at drug shops in Uganda. Malar J. 2015; 14:277. https://doi.org/10.1186/s12936-015-0798-9 PMID: 26178532 37. Tong A, Sainsbury P, Craig J. Consolidated criteria for reporting qualitative research (COREQ): a 32- item checklist for interviews and focus groups. Int J Qual Health Care. 2007; 19(6):349–57. https://doi. org/10.1093/intqhc/mzm042 PMID: 17872937 38. Wiseman V, Scott A, Conteh L, McElroy B, Stevens W. Determinants of provider choice for malaria treatment: experiences from The Gambia. Social science & medicine. 2008; 67(4):487–96. 39. Bartoloni A, Zammarchi L. Clinical aspects of uncomplicated and severe malaria. Mediterranean journal of hematology and infectious diseases. 2012; 4(1):e2012026. https://doi.org/10.4084/MJHID.2012.026 PMID: 22708041 40. Stauffer W, Fischer PR. Diagnosis and treatment of malaria in children. Clin Infect Dis. 2003; 37 (10):1340–8. https://doi.org/10.1086/379074 PMID: 14583868 41. Pierce H, Gibby AL, Forste R. Caregiver Decision-Making: Household Response to Child Illness in sub- Saharan Africa. Population research and policy review. 2016; 35(5):581–97. https://doi.org/10.1007/ s11113-016-9396-y PMID: 28794575 42. Mwandama D, Mwale C, Bauleni A, Phiri T, Chisaka J, Nsona H, et al. Clinical outcomes among febrile children aged 2 to 59 months with negative malaria rapid diagnostic test results in Mchinji District, Malawi. Malawi Med J. 2016; 28(4):150–3. PMID: 28321277 43. White NJ, Pukrittayakamee S, Hien TT, Faiz MA, Mokuolu OA, Dondorp AM. Malaria. Lancet. 2014; 383(9918):723–35. https://doi.org/10.1016/S0140-6736(13)60024-0 PMID: 23953767 44. Bedford KJ, Sharkey AB. Local barriers and solutions to improve care-seeking for childhood pneumo- nia, diarrhoea and malaria in Kenya, Nigeria and Niger: a qualitative study. PloS one. 2014; 9(6): e100038. https://doi.org/10.1371/journal.pone.0100038 PMID: 24971642 45. Ewing VL, Tolhurst R, Kapinda A, Richards E, Terlouw DJ, Lalloo DG. Increasing understanding of the relationship between geographic access and gendered decision-making power for treatment-seeking for febrile children in the Chikwawa district of Malawi. Malar J. 2016; 15(1):521. https://doi.org/10.1186/ s12936-016-1559-0 PMID: 27776549 46. Liu J, Prach LM, Treleaven E, Hansen M, Anyanti J, Jagha T, et al. The role of drug vendors in improv- ing basic health-care services in Nigeria. Bulletin of the World Health Organization. 2016; 94(4):267– 75. https://doi.org/10.2471/BLT.15.154666 PMID: 27034520 47. Mackintosh M, Channon A, Karan A, Selvaraj S, Cavagnero E, Zhao H. What is the private sector? Understanding private provision in the health systems of low-income and middle-income countries. Lan- cet. 2016; 388(10044):596–605. https://doi.org/10.1016/S0140-6736(16)00342-1 PMID: 27358253 48. Sudhinaraset M, Ingram M, Lofthouse HK, Montagu D. What is the role of informal healthcare providers in developing countries? A systematic review. PloS one. 2013; 8(2):e54978. https://doi.org/10.1371/ journal.pone.0054978 PMID: 23405101 49. Group AC, Phok S, Phanalasy S, Thein ST, Likhitsup A. Private sector opportunities and threats to achieving malaria elimination in the Greater Mekong Subregion: results from malaria outlet surveys in Cambodia, the Lao PDR, Myanmar, and Thailand. Malar J. 2017; 16(1):180. https://doi.org/10.1186/ s12936-017-1800-5 PMID: 28464945 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 14 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda 50. Rutebemberwa E, Buregyeya E, Lal S, Clarke SE, Hansen KS, Magnussen P, et al. Assessing the potential of rural and urban private facilities in implementing child health interventions in Mukono district, central Uganda-a cross sectional study. BMC health services research. 2016; 16:268. https://doi.org/ 10.1186/s12913-016-1529-9 PMID: 27421644 51. Buchner DL, Kitutu FE, Cross DE, Nakamoga E, Awor P. A cross-sectional study to identify the distribu- tion and characteristics of licensed and unlicensed private drug shops in rural Eastern Uganda to inform an iCCM intervention to improve health outcomes for children under five years. PloS one. 2019; 14(1): e0209641. https://doi.org/10.1371/journal.pone.0209641 PMID: 30625187 52. Mbonye AK, Buregyeya E, Rutebemberwa E, Clarke SE, Lal S, Hansen KS, et al. Referral of children seeking care at private health facilities in Uganda. Malar J. 2017; 16(1):76. https://doi.org/10.1186/ s12936-017-1723-1 PMID: 28196532 53. Hutchinson E, Hutchison C, Lal S, Hansen K, Kayendeke M, Nabirye C, et al. Introducing rapid tests for malaria into the retail sector: what are the unintended consequences? BMJ global health. 2017; 2(1): e000067. https://doi.org/10.1136/bmjgh-2016-000067 PMID: 28588992 54. Poyer S, Shewchuk T, Tougher S, Ye Y, Group AC, Mann AG, et al. Availability and price of malaria rapid diagnostic tests in the public and private health sectors in 2011: results from 10 nationally repre- sentative cross-sectional retail surveys. Tropical medicine & international health: TM & IH. 2015; 20 (6):744–56. 55. Webster P. Drug shops as primary point of care-the case of Nigeria. Lancet. 2017; 390(10089):15–7. https://doi.org/10.1016/S0140-6736(17)31722-1 PMID: 28677546 56. Wafula FN, Goodman CA. Are interventions for improving the quality of services provided by special- ized drug shops effective in sub-Saharan Africa? A systematic review of the literature. Int J Qual Health Care. 2010; 22(4):316–23. https://doi.org/10.1093/intqhc/mzq022 PMID: 20430823 57. Shewchuk T, O’Connell KA, Goodman C, Hanson K, Chapman S, Chavasse D. The ACTwatch project: methods to describe anti-malarial markets in seven countries. Malar J. 2011; 10:325. https://doi.org/10. 1186/1475-2875-10-325 PMID: 22039780 58. Group AC, Musuva A, Ejersa W, Kiptui R, Memusi D, Abwao E. The malaria testing and treatment land- scape in Kenya: results from a nationally representative survey among the public and private sector in 2016. Malar J. 2017; 16(1):494. https://doi.org/10.1186/s12936-017-2089-0 PMID: 29268789 59. Group AC, Kaula H, Buyungo P, Opigo J. Private sector role, readiness and performance for malaria case management in Uganda, 2015. Malar J. 2017; 16(1):219. https://doi.org/10.1186/s12936-017- 1824-x PMID: 28545583 60. Group AC, Newton PN, Hanson K, Goodman C. Do anti-malarials in Africa meet quality standards? The market penetration of non quality-assured artemisinin combination therapy in eight African countries. Malar J. 2017; 16(1):204. https://doi.org/10.1186/s12936-017-1818-8 PMID: 28539125 61. Group AC, Hanson K, Goodman C. Testing times: trends in availability, price, and market share of malaria diagnostics in the public and private healthcare sector across eight sub-Saharan African coun- tries from 2009 to 2015. Malar J. 2017; 16(1):205. https://doi.org/10.1186/s12936-017-1829-5 PMID: 62. Group AC, Michael D, Mkunde SP. The malaria testing and treatment landscape in mainland Tanzania, 2016. Malar J. 2017; 16(1):202. https://doi.org/10.1186/s12936-017-1819-7 PMID: 28521811 63. Group AC, Zinsou C, Cherifath AB. The malaria testing and treatment landscape in Benin. Malar J. 2017; 16(1):174. https://doi.org/10.1186/s12936-017-1808-x PMID: 28446236 64. Group AC, Tougher S, Hanson K, Goodman C. What happened to anti-malarial markets after the Affordable Medicines Facility-malaria pilot? Trends in ACT availability, price and market share from five African countries under continuation of the private sector co-payment mechanism. Malar J. 2017; 16 (1):173. https://doi.org/10.1186/s12936-017-1814-z PMID: 28441956 65. Group AC, Phanalasy S. The malaria testing and treatment landscape in the southern Lao People’s Democratic Republic (PDR). Malar J. 2017; 16(1):169. https://doi.org/10.1186/s12936-017-1769-0 PMID: 28438155 66. Group AC, Mpanya G, Tshefu A, Likwela JL. The malaria testing and treatment market in Kinshasa, Democratic Republic of the Congo, 2013. Malar J. 2017; 16(1):94. https://doi.org/10.1186/s12936-016- 1659-x PMID: 28241832 67. Rutta E, Kibassa B, McKinnon B, Liana J, Mbwasi R, Mlaki W, et al. Increasing Access to Subsidized Artemisinin-based Combination Therapy through Accredited Drug Dispensing Outlets in Tanzania. Health research policy and systems. 2011; 9:22. https://doi.org/10.1186/1478-4505-9-22 PMID: 68. Rutta E, Liana J, Embrey M, Johnson K, Kimatta S, Valimba R, et al. Accrediting retail drug shops to strengthen Tanzania’s public health system: an ADDO case study. Journal of pharmaceutical policy and practice. 2015; 8:23. https://doi.org/10.1186/s40545-015-0044-4 PMID: 26413304 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 15 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda 69. S. Benavides, H. Hong, A. Mantzavinou, E. Nikolopoulos, & B. Russell. Analysis of Tanzania’s ADDO Program.Global Health Markets. 2013. Available from: http://www.brandon-russell.com/addo.shtml 70. Embrey M, Vialle-Valentin C, Dillip A, Kihiyo B, Mbwasi R, Semali IA, et al. Understanding the Role of Accredited Drug Dispensing Outlets in Tanzania’s Health System. PloS one. 2016; 11(11):e0164332. https://doi.org/10.1371/journal.pone.0164332 PMID: 27824876 71. Bruxvoort K, Kalolella A, Cairns M, Festo C, Kenani M, Lyaruu P, et al. Are Tanzanian patients attending public facilities or private retailers more likely to adhere to artemisinin-based combination therapy? Malar J. 2015; 14:87. https://doi.org/10.1186/s12936-015-0602-x PMID: 25889767 72. Visser T, Bruxvoort K, Maloney K, Leslie T, Barat LM, Allan R, et al. Introducing malaria rapid diagnostic tests in private medicine retail outlets: A systematic literature review. PloS one. 2017; 12(3):e0173093. https://doi.org/10.1371/journal.pone.0173093 PMID: 28253315 73. Tawiah T, Malam K, Kwarteng A, Bart-Plange C, Febir L, Aubyn V, et al. Improving the first-line treat- ment of febrile illnesses in Ghana: willingness to pay for malaria rapid diagnostic tests at licensed chem- ical shops in the Kintampo area. Cost effectiveness and resource allocation: C/E. 2018; 16:4. https:// doi.org/10.1186/s12962-018-0090-2 PMID: 29434526 74. Kabaghe AN, Phiri MD, Phiri KS, van Vugt M. Challenges in implementing uncomplicated malaria treat- ment in children: a health facility survey in rural Malawi. Malar J. 2017; 16(1):419. https://doi.org/10. 1186/s12936-017-2066-7 PMID: 29047388 75. Awor P, Peterson S, Gautham M. Delivering child health interventions through the private sector in low and middle income countries: challenges, opportunities, and potential next steps. BMJ. 2018; 362: k2950. https://doi.org/10.1136/bmj.k2950 PMID: 30061154 76. Katahoire AR, Henriksson DK, Ssegujja E, Waiswa P, Ayebare F, Bagenda D, et al. Improving child sur- vival through a district management strengthening and community empowerment intervention: early implementation experiences from Uganda. BMC public health. 2015; 15:797. https://doi.org/10.1186/ s12889-015-2129-z PMID: 26286146 77. Lungu EA, Guda Obse A, Darker C, Biesma R. What influences where they seek care? Caregivers’ preferences for under-five child healthcare services in urban slums of Malawi: A discrete choice experi- ment. PloS one. 2018; 13(1):e0189940. https://doi.org/10.1371/journal.pone.0189940 PMID: 29351299 78. Rosapep L, Sanders E, Banke K. The influence of customer-medicine seller transactional dynamics on childhood diarrhoea management: a qualitative study in Ghana. Health Policy Plan. 2017; 32(4):527– 37. https://doi.org/10.1093/heapol/czw155 PMID: 28073934 79. Basu S, Andrews J, Kishore S, Panjabi R, Stuckler D. Comparative performance of private and public healthcare systems in low- and middle-income countries: a systematic review. PLoS medicine. 2012; 9 (6):e1001244. https://doi.org/10.1371/journal.pmed.1001244 PMID: 22723748 80. Goodman C, Kachur SP, Abdulla S, Bloland P, Mills A. Drug shop regulation and malaria treatment in Tanzania—why do shops break the rules, and does it matter? Health Policy Plan. 2007; 22(6):393–403. https://doi.org/10.1093/heapol/czm033 PMID: 17921151 81. Maloney K, Ward A, Krenz B, Petty N, Bryson L, Dolkart C, et al. Expanding access to parasite-based malaria diagnosis through retail drug shops in Tanzania: evidence from a randomized trial and implica- tions for treatment. Malar J. 2017; 16(1):6. https://doi.org/10.1186/s12936-016-1658-y PMID: 82. Kitutu FE, Mayora C, Johansson EW, Peterson S, Wamani H, Bigdeli M, et al. Health system effects of implementing integrated community case management (iCCM) intervention in private retail drug shops in South Western Uganda: a qualitative study. BMJ global health. 2017; 2(Suppl 3):e000334. https:// doi.org/10.1136/bmjgh-2017-000334 PMID: 29259824 83. National Drug Authority. PUBLIC NOTICE ON LICENSING OF PHARMACIES AND DRUG SHOPS. (2017).Available from: http://www.nda.or.ug/ug/dnews/60/Public-Notice-on-Licensing-Of-Pharmacies- And-Drug-Shops.html. 84. Wafula FN, Miriti EM, Goodman CA. Examining characteristics, knowledge and regulatory practices of specialized drug shops in Sub-Saharan Africa: a systematic review of the literature. BMC health ser- vices research. 2012; 12:223. https://doi.org/10.1186/1472-6963-12-223 PMID: 22838649 85. Doherty JE. Regulating the for-profit private health sector: lessons from East and Southern Africa. Health Policy Plan. 2015; 30 Suppl 1:i93–102. 86. Wang LT, Bwambale R, Keeler C, Reyes R, Muhindo R, Matte M, et al. Private sector drug shops fre- quently dispense parenteral anti-malarials in a rural region of Western Uganda. Malar J. 2018; 17 (1):305. https://doi.org/10.1186/s12936-018-2454-7 PMID: 30134987 87. Kedenge SV, Kangwana BP, Waweru EW, Nyandigisi AJ, Pandit J, Brooker SJ, et al. Understanding the impact of subsidizing artemisinin-based combination therapies (ACTs) in the retail sector—results from focus group discussions in rural Kenya. PloS one. 2013; 8(1):e54371. https://doi.org/10.1371/ journal.pone.0054371 PMID: 23342143 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 16 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda 88. Kangwana BP, Kedenge SV, Noor AM, Alegana VA, Nyandigisi AJ, Pandit J, et al. The impact of retail- sector delivery of artemether-lumefantrine on malaria treatment of children under five in Kenya: a clus- ter randomized controlled trial. PLoS medicine. 2011; 8(5):e1000437. https://doi.org/10.1371/journal. pmed.1000437 PMID: 21655317 89. Ansah EK, Narh-Bana S, Affran-Bonful H, Bart-Plange C, Cundill B, Gyapong M, et al. The impact of providing rapid diagnostic malaria tests on fever management in the private retail sector in Ghana: a cluster randomized trial. BMJ. 2015; 350:h1019. https://doi.org/10.1136/bmj.h1019 PMID: 25739769 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 17 / 17 http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png PLoS ONE Public Library of Science (PLoS) Journal

Understanding the context of delays in seeking appropriate care for children with symptoms of severe malaria in Uganda

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Introduction OPENACCESS A large proportion of children with uncomplicated malaria receive appropriate treatment Citation: Mpimbaza A, Nayiga S, Ndeezi G, late, contributing to progression of illness to severe disease. We explored contexts of care- Rosenthal PJ, Karamagi C, Katahoire A (2019) giver delays in seeking appropriate care for children with severe malaria. Understanding the context of delays in seeking appropriate care for children with symptoms of severe malaria in Uganda. PLoS ONE 14(6): Methods e0217262. https://doi.org/10.1371/journal. This qualitative study was conducted at the Children’s Ward of Jinja Hospital, where children pone.0217262 with severe malaria were hospitalized. A total of 22in-depth interviews were conducted with Editor: Julie Gutman, Centers for Disease Control caregivers of children hospitalized with severe malaria. Issues explored were formulated and Prevention, UNITED STATES based on the Partners for Applied Social Sciences (PASS) model, focusing on facilitators Received: May 18, 2018 and barriersto caregivers’promptseeking and accessing ofappropriate care. The data were Accepted: May 8, 2019 coded deductively using ATLAS.ti (version 7.5). Codes were then grouped into families Published: June 5, 2019 based on emerging themes. Copyright: This is an open access article, free of all copyright, and may be freely reproduced, Results distributed, transmitted, modified, built upon, or Caregivers’ rating of initial symptoms as mild illness lead to delays in response. Use of otherwise used by anyone for any lawful purpose. home initiated interventions with presumably ineffective herbs or medicines was common, The work is made available under the Creative Commons CC0 public domain dedication. leading to further delay. When care was sought outside the home, drug shops were pre- ferred over public health facilities for reasons of convenience. Drug shops often provided Data Availability Statement: Because transcripts of interviews contain potentially identifiable sub-optimal care, and thus contributed to delays in access to appropriate care. Public facili- information, such as names of health facilities, ties were often a last resort when illness was perceived to be progressing to severe disease. health workers, and respondents, data will only be Further delays occurred at health facilities due to inadequate referral systems. available upon request as recommended by the respective institutional review boards that approved this study. Ms Deborah Ekusai Conclusion (dekusai@idrc-uganda.org); Training coordinator Communities living in endemic areas need to be sensitized about the significance of fever, FIC malaria-training program in Uganda, should be contacted for future data requests. even if mild, as an indicator of malaria. Additionally, amidst ongoing efforts at bringing PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 1 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda Funding: This research was supported by two antimalarial treatment services closer to communities, the value of drug shops as providers training awards from the NIH Fogarty International ofrationalantimalarialtreatment needs to be reviewed. Center, the University of California Global Health Institute GloCal Health Fellowship (TW009343) and the Training in Malaria Research in Uganda program (TW007375). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared Introduction that no competing interests exist. For African children with uncomplicated malaria, the World Health Organization (WHO) recommends prompt treatment with artemisinin-based combination therapies (ACTs) within 24 hours of illness onset as a key strategy for preventing progression to severe malaria [1]. Unlike in the past, when ACTs were scarce and expensive [2], efforts by governments, interna- tional organizations, and partner institutions have resulted in increased availability of high quality and affordable ACTs in both the private and public health sectors [3]. This achievement has likely contributed greatly to reductions in malaria morbidity and mortality in Africa [4, 5]. However, despite increases in ACT coverage rates, the proportion of eligible children receiving ACTs within 24 hours of illness onset remains low [6], partly explaining why hundreds of thousands of children continue to die of malaria each year [7]. If malaria control and elimination programs are to succeed, there is a need to ensure maxi- mum treatment effectiveness, characterized by high quality case management and appropriate health seeking behavior by patients or caregivers [8]. Studies in sub-Saharan Africa have shown that the delivery of antimalarials may fail at different stages, including at the initiation of treatment at home, or due to health care providers offering ineffective medicines [9]. For children, caregivers’ response to illness is the first and probably the most important step in determining if treatment is received promptly [10]. Circumstances surrounding caregivers’ delays in seeking appropriate care are complex [11]. Knowledge, perception, and beliefs of ill- ness are known to influence the time taken to appraise symptoms, thus influencing response time and potentially leading to delays in seeking care. Categorization of fever as a minor ailment by caregivers has been shown to delay response to illness among children with malaria in Tanzania [12]. Treatment of illness episodes with local remedies and herbs contributes to further delays in seeking appropriate care [13, 14]. Furthermore, if care is sought at drug shops, where the quality of care is often sub-optimal [15], delay in receiving appropriate treatment is a likely outcome [16, 17]. Social networks, including caregiver partners, parents, in-laws, and neighbors involved in negotiating response to illness can also be associated with delays in care [18]. Understanding caregivers’ health seeking behavior while taking into consideration contex- tual factors that govern behavior is a prerequisite for formulating policies targeted at optimiz- ing response to illness [19]. However, policy efforts continue to focus on provider factors such as increasing availability of ACTs to communities at risk, while neglecting demand side factors such as how caregivers interpret and respond to symptoms of illness. Sensitizing communities to availability of services and providing classical biomedical descriptions of symptoms of malaria have had little impact on caregivers seeking care promptly [20]. This situation is likely explained by consideration of care seeking as a linear pathway, neglecting social and environ- mental contexts that govern individual behavior and response types which shape pathways to care[20–22]. Utilizing interviews with caregivers of children who presented with severe malaria in Jinja, Uganda, we explored the social and environmental constraints that shape when and how caregivers respond to illness, and sought to explain delays in accessing appro- priate treatment for malaria. PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 2 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda Research team A social scientist with undergraduate and postgraduate training in social science, and epidemi- ology, respectively led all interviews. The lead interviewer is female and has experience span- ning a period of 10 years, working as a coordinator on several qualitative studies [23–25]. A member of the local hospital staff, who was well accustomed with local language, culture, and social norms of the locals recruited patients, explaining to respondents reasons for conducting the study, introducing the interviewer and when applicable translating and responses. At the time of conducting interviews, the interview team was aware of the main findings of the pri- mary study. Prior to conducting the interview, the interview team introduced themselves to the study participants highlighting, who they were, and where they came from. Additionally, they explained the purpose of the interview to study participants. Methods Study design This was a qualitative study, linked to a study of determinants of severe malaria in children, in which delay in seeking appropriate care was found to be a strong risk factor for severe malaria [16]. Caregivers of children hospitalized with severe malaria were interviewed to explore how their social and environmental contexts influenced when and how they responded to illness. We explored motivations for caregivers’ actions in response to illness, explaining delays in seeking and accessing appropriate treatment for their children. Our approach was mainly deductive in nature, driven by the hypothesis that delay in seeking appropriate care was a risk factor for severe malaria. Theoretical framework To explore contextual factors, this study drew on the Partners for Applied Social Sciences (PASS) model [26]. The model is built on the backbone ofa pathway model, focusing on factors involved ineach step of the pathway to care that hinder or facilitate prompt seeking or access to appropriate care. Factors in the model are grouped into four main categories: 1) illnessper- ception and explanatory models; 2) social values; 3) access tocare and resource seeking; and 4) medicalpluralism [26]. Considering social and environmental contexts, we explored how these factors contributed to caregiver delays in seeking appropriate care for children with malaria. Study setting The study was conducted in the catchment area of the Children’s Ward of Jinja Regional Referral Hospital, which includes 10 districts located in the Busoga sub-region, with a few patients also coming from two districts located in the Buganda region [16]. Malaria transmis- sion in the sub-region is considered hypo to hyper endemic [27]. In 2016, the malaria parasite prevalence rate among children in the Busoga sub-region was 53.1% based on an HRP2-base- drapid diagnostic test [28]. The economic base for 53% of the local people is subsistence-ori- ented farming [29], with some villagers engaging in small-scale business such as operating small roadside shops. The Busoga region has 42.0% of the population living in poverty and is known to suffer from famine [29], malnutrition, very high infant mortality rates, and rampant jigger epidemics [30, 31]. Literacy levels are low, with 56.1% and 43.8% of male and female heads of households being literate. The Early Childhood Development Index, a composite measure of the developmental status of children, was reported to be 55.5% in the region, the lowest value reported in Uganda [28]. PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 3 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda The local health arena in Busoga is pluralistic, with access to traditional medicine and bio- medicines at both public and private facilities [32]. The region has public health facilities rang- ing from level II to level IV health centers, district hospitals and a regional referral hospital. The average distance between level III (and above) health facilities and households is < 5 km [16]. Services rendered at public facilities are plagued by staff absenteeism and frequent stock outs of essential medicines [33]. Drug shops, though popular, often offer substandard services [15, 34, 35]. Initiatives at improving quality of services at drug shops have been implemented in the region, with reported success [36]. Sampling Sampling was purposive and research participants were selected based on gender, relation to the child, age, time taken to seek care, and form of severe malaria. Maximum variation in the selection of respondents ensured that different social groups were represented, including con- sideration of employment and socio-economic status. The study team approached eligible respondents during hospitalization at Jinja Children’s Hospital. Respondents were purposively included in the sampling frame. Sample size The final sample size for the study was 22 caregivers and was not pre-determined, but reached based on the principle of data saturation, where gathering fresh data from additional respon- dents did not reveal new insights or findings based on our theoretical model. All eligible study participants agreed to participate when approached. Setting of data collection Interviews with caregivers were conducted privately during the recovery period of the child’s hospitalization either in the hospital gardens or in one of the study offices, depending on the respondent’s choice. Both venues offered privacy, with minimum interruption. For all 22-interview sessions, no one other than the child’s primary caregiver and interviewers were present. Data collection An interview guide was developed (S1 Appendix) based on key themes agreed upon by the study team based on observations noted during the primary study. The interview guide was pilot tested and modified by the lead interviewer, improving on sequencing of questions. Inter- views lasted less than 2 hours and were conducted in the local language. The interviews were audio recorded and transcribed in the language in which they were conducted before transla- tion into English by an experienced interviewer. The interviewer did not repeat any of the interviews, nor were transcribed interviews returned to study participants for comment and correction. Additionally, upon completion of each interview, the interviewer noted a summary of key observations during the interview. Patient responses were categorized into three phases: 1) illness recognition, 2) response to illness and 3) actions. Definition of terms Delay was defined as a prolonged interval (typically >24 hours) between illness onset and commencement of appropriate treatment. Illness recognition was defined as the caregivers’ appraisal of symptoms as a sign of illness. Response was defined as the caregiver acknowledg- ing the need to intervene upon the child’s illness. Caregivers’ actions were defined as the PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 4 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda measures taken in response to illness. Individuals who provided advice to the caregiver in terms of how to respond to the child’s illness were referred to as the therapeutic management group[26]. The primary caregiver was the person who was with the child right from onset to presentation to hospital. Data analysis Analysis of data was deductive in nature, informed by preliminary findings of the primary study that identified delayed seeking of care and seeking care at drug shops as potent risk fac- tors for severe malaria [16]. Upon completion of the primary study, findings were presented to a panel of experts, including pediatricians, social scientists, and medical anthropologists, dur- ing which themes worthy exploration were formulated. Individual transcripts were entered into ATLAS.ti. Version 7.5.18 (Atlas.ti. GmbH, Berlin Parts), and coded (a code was a word or short phrase that symbolically assigned meaning to a portion of language in the data) by the lead investigator of the study under the supervision of a medical anthropologist using a mixed approach of both open and closed coding based on pre–defined criteria. Related codes were categorized into families’ representative of different themes informed by the findings of the quantitative study [16]. These themes formed the basis of the write-up and discussion. Partici- pants were not involved nor consulted for opinion on themes. The design and findings of this study are reported following the consolidated criteria for reporting qualitative research (COREQ; S2 Appendix;) [37] Ethics approval Institutional approval was obtained from the Uganda National Council of Science and Tech- nology, and the Institutional Review Boards from the College of Health Sciences, Makerere University, and the University of California San Francisco. Written informed consent was obtained from each caregiver. In addition to obtaining consent, the interviews were conducted in accordance with good clinical practice, applicable patient privacy requirements, and the guiding principles of the Declaration of Helsinki. Results Characteristics of the study sample We interviewed 22 caregivers, each with a child hospitalized with severe malaria at the Chil- dren’s Ward of Jinja Regional Referral Hospital during the months of February and March 2016.The majority of the caregivers were mothers (15, 68.2%), with grandmothers (3, 13.6%), fathers (2, 9.1%), aunts (2, 4.5%), and stepmothers (1, 4.5%) accounting for the others. The average age of caregivers’ was 31 years (range 18 to 48years). Most (68%) caregivers were pri- marily engaged in subsistence farming, with occasional selling of excess food (Table 1). Different kinds of fevers Caregivers reported that their children experienced different kinds of fevers, characterized as mild or severe, sometimes contributing to delays in seeking care outside of the home as some of the fevers were ranked as low grade, not deserving serious attention (Quotes A317, A324). A317: “If a child has a temperature. . . you get a damp cloth and sponge them. . ..for the simple one you give panadol, they sweat and the fever goes down” A324:“The body may be hot but not very hot. The child may be playing and eating. We can say that let us give them some coartem. They will get better.” PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 5 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda Table 1. Demographic and clinical characteristics of caregivers and their enrolled children. Characteristics of caregivers of enrolled children Average age in years 31.6 Age range in years 18 to 48 Relation with child Mother 114 (63.6%) Grandmother 1 (4.5%) Stepmother 2 (9.0%) Father 2 (9.0%) Grandmother 3 (13.6%) Occupation Peasant 15 (68.1%) Business 5 (22.7%) Tailor 1 (4.5%) Waitress 1 (4.5%) Characteristics of enrolled children Age in years 2.6 Age range in years 0.5 to 7.5 Gender Female 9 (40.9%) Type of severe malaria Unconsciousness 5 (22.7%) Severe anemia 10 (45.4%) Respiratory distress 3 (13.6%) Unconsciousness & Severe anemia 1 (4.5%) Respiratory distress & Severe anemia 1 (4.5%) Respiratory distress & Unconsciousness 1 (4.5%) Respiratory distress & Unconsciousness& Severe anemia 1 (4.5%) https://doi.org/10.1371/journal.pone.0217262.t001 Fever described as “hot "or “high “in isolation or with other symptoms such as loss of appe- tite or extreme body weakness was considered a sign of serious illness, triggering rapid response (Quotes A316, A308). A316:“The very high fever can cause me to run. If I delay, the child weakens. If I delay, the child gets dehydrated. If I delay it makes him anemic." A308: “When he is all hot? No, at least you put a cloth in water, squeeze the water out and wipe him from head to toe. . .then proceed. Because at that point it is excessive to the extent that both the hands and the legs are hot. It is excessive and you have to head straight to the hospital.” Caregivers understanding of malaria Caregivers also talked about mild and severe malaria, with some equating the occurrence of fever with malaria. They mentioned symptoms of severe malaria such as anemia that they con- sidered could result in death and indeed, when children had these symptoms caregivers responded promptly. A311: “. . ...he can get malaria, gets weak, blood gets low, water in his body gets drained. So if you stay home and ignore the situation and say I was given this let me just wait the child can die in that way.” Furthermore, caregivers explained that severe malaria was a result of delayed seeking of appropriate care (Quotes A319, A325, A326). PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 6 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda A319:“. . .. The only problem is that if you delay, the illness gets severe.” A326:“. . .. If (malaria) gets the child and you delay to go to hospital it has to kill the child because you have delayed.” These delays however were not necessarily deliberate or within the control of the caregivers. Therapeutic management groups as a source of delay Caregivers explained that the interpretation of the child’s illness sometimes involved other members of the family. Caregivers living with parents or mothers-in-law for example explained that they felt obliged to seek advice from them. Others consulted included fathers, grandparents, neighbors, and friends. The process of consultation itself caused delays. In some cases the symptoms were perceived to be because of witchcraft or other ailments and so herbal medicines were prescribed in place of conventional medicines, thus contributing to delays (Quote A309). A309:“They stopped me from giving her the drug. . .. . ..the old people including my mother in law.” Some mothers expressed independence to make decisions without consultation or approval of the fathers (Quote A315). A315: “Recently it happened. He told me to go to Nalufenya and I refused and decided to go � � � to another place because the people at hospital delay patients. My child will die from there. They toss you up and down before offering any treatment. In that way we did not agree. I went on my own and he did not give me money. When I got there I called him on phone and informed him of where I was and he came.” Delays due to home treatment At home, caregivers often initiated treatment with a combination of herbs and conventional medicines. This was often followed by a waiting period in anticipation of recovery following use of these medicines. This contributed to delays in seeking appropriate care. Conventional medicines provided included panadol, oral antibiotics, and antimalarials, often purchased from drug shops, or left over from treatment of a previous illness episode (Quotes A307). A307: "On Saturday I had some coartem so I picked one coartem and panadol and I gave him in the morning. Then in the evening, I gave him more. I then added him more on Sunday morning and also on Sunday evening. When it came to midnight in the night, he started con- vulsing. I tried to wipe him a bit. I feared to give him more medicine. I picked a car and brought him to hospital and they treated him from here.” Use of herbal medicines was common, with ’mululuza,’ bombo, ‘and ’lubirizi’ being the most frequently mentioned. These were given concurrently with conventional medicines. Herbs were primarily given to reduce fever, rarely with the intention to cure illness (Quote A328). A328: “When I am at home, I use a rag to wipe the body so that the temperature goes down. I also get lubirizi and bombo and give the child . . ... Now, I first crush them in a cup and give PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 7 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda the child to drink then I pour the rest in the child’s basin for the child to bathe. . .. . .. . .. . .. They relieve the child.” Mashed onions and garlic smeared on the child’s body were used to prevent and cure con- vulsions; however this intervention did not prevent caregivers from seeking care at public health facilities. A312:“I think that when a child convulses it is malaria. We were told that when he convulses we smear him with onions and it stops.” Delays due to drug shops Caregivers also reported going to drug shops and clinics because of their close proximity, low cost, and availability of medicines. A309:"The government hospital is very far from our home so we first go to the drug shop and then when the condition does not change then we go to the government hospital.” A325:"We take them to the nearby clinic where we can get some drugs. They tell us that when you go there sometimes they find him some drugs. They give us some drugs and I also explain the problems the child has, for this number of days and the illness is like this and they try to mix for me some drugs.” However, despite being convenient, drug shops often provide sub-optimal care. The inade- quacies of drug shops reported by caregivers included the staff’s lack of knowledge and equip- ment to diagnose malaria. There were delays described in the referral process even when the child was not getting better (Quotes A312, A308). A308:”the private clinic where we started, they ‘ate’ a lot of money. Because whatever they told us, we would do. They would tell you buy this, you would go and buy. They would tell you buy a syrup, you would go and buy. Even others I just left them behind. Because initially they gave us syrup but when I went with them to Lulyambuzi, they sorted them, we went with 7 syrups. New ones. They sorted them and we threw away 5 of them. They left us with 2 and said those are the ones we should use for this illness. Because all the person was chasing back there was money. Just wanting to get money. But we didn’t know what was wrong with the child. But when we gave him those two syrups and threw the 5, he started getting back in line. But when we combined with the others, it would be as if you are increasing the sickness. But he has ‘eaten’ money; I don’t even know the amount. For a long time, this child has not been well.” A metaphor used to suggest fraud, which in this context implied that providers were extorting money from caregivers for unwarranted services. A312:"I feel like when you go to the drug shop, the treatment is expensive.” . . . If you do not rush them to hospital and they check what the problem is, you may go to the drug shop and they give him treatment that does not relate with malaria and as a result they may die” Caregivers explained that they sought care at drug shops for illnesses that they considered mild. Only when symptoms persisted or the child deteriorated, did they opt to seek care at a public health facility, which they deemed more appropriate for treating severe malaria (Quotes A312, A324). PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 8 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda A312: “It seems what causes them is the same thing but I think the severe one will have grown and would no longer be managed by drug shops and the like but it requires a blood sample to be taken and they see the actual disease and the drugs they will use..” A324: "Where I stay there is a clinic nearby. That is where I usually get first aid. When it gets worse then we come here. . . . . .We only get first aid from there. When it gets worse and they cannot manage at the clinic then we go there.” Delays at public health facilities Caregivers explained that public health facilities often lacked medicines, and had rude health workers who were often absent from work (Quote A315).Caregivers expressed frustration regarding spending money on transport to public health facilities that did not have medicines. They further explained that often they were asked to buy medicines at public health facilities, which was a problem for caregivers that did not have money. A315: There is another place but they never have medicine. When you go there they tell you that there are no drugs Interviewer: What place is that? � � � A315: It is called health center. Interviewer: It is a government hospital. A315: Yes Interviewer: Health center three or two. A315: Three but when you get there they tell you that they do not have drugs. You may get there and there are no health workers. A317: “Yes, you need transport of 1500 plus it is painful. . .. . .. . .. . ...You find that there are no drugs, even panadol they don’t give you that is why we don’t go. So you would use that money and go to the clinic.” While public health facilities were reported to promptly refer patients, caregivers had to arrange for transport to the next level. This contributed to delays in accessing appropriate care (S3 Appendix). Overall, multiple processes contributed to delays in access to appropriate care for children that were eventually diagnosed with severe malaria. Discussion We studied contexts that contributed to delays in appropriate care for children who eventually developed severe malaria. Consistent with previous reports[20], mild fevers led to delays in response. Caregivers responded to what they perceived as mild illness with ineffective home interventions. When care was sought outside the home, drug shops were preferred over public facilities, but because the care was often sub-optimal, there was delay in accessing appropriate treatment. Caregivers ably explained the cause of malaria and were aware of the common manifesta- tions of severe malaria; appreciating the fact, that malaria could cause death. However, their understanding did not appear to have a bearing on how they responded to illness and on the time to seek appropriate care, suggesting that response were influenced by other factors, such PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 9 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda as the contexts within which they lived [20]. Caregivers’ perceptions of illness as mild based on low fever has been reported in other countries in sub-Saharan Africa [38], possibly explained by the subtle, non-specific and irregular nature of initial symptoms of most malaria episodes [39, 40]. In such circumstances, caregivers may feel that a child’s illness is benign, thus opting to observe or provide simple, ineffective home remedies [12, 41], contributing to delay in seek- ing appropriate care for malaria. Home remedies may suffice for common childhood viral infections, which are often self-limiting [42], but slow response to malaria is dangerous, as established infection can rapidly progress to severe disease [43]. Consultations with family members and neighbors were also a common cause of delay. Advice given was often using of herbs, contributing to delays in seeking appropriate care [18]. Culturally, grandmothers and mothers-in-law, particularly if paternal, hold a dominant posi- tion, to the extent that caregivers are obliged to follow advice, even if they disagree [18, 41]. Fathers were consulted, often times for financial support. However, in contrast to previous reports [44], involvement of fathers did not notably contribute to delays in care. Some caregiv- ers reported having autonomy to make decisions in the absence of fathers or when dealing with an uncooperative father, demonstrating empowerment of some mothers [45]. Outside homes, drug shops were the preferred choice of care, a finding consistent with results of other studies in the region [46, 47]. Drug shops have proliferated in both rural and urban areas [3, 47]. As reported previously, short distance from home, lower cost of obtaining care compared to health centers, short waiting times, and ease of accessing medicines were rea- sons for preference of drug shops [15, 48]. Interestingly, caregivers sought care at drug shops for symptoms deemed mild and not serious, suggesting that they were aware of the shortcom- ings of these shops. The popularity of drug shops offers an opportunity for promoting timely access to appropriate antimalarial treatment [46, 49]. However, limitations of drug shops, including lack of provider knowledge on management of malaria [36, 50, 51], poor referral practices [52], lack of diagnostic capacity [53, 54], and profit driven behaviors [55], remain major hurdles. Programs directed at improving services at drug shops have yielded mixed results [56]. Publications from the ACT Watch group, a multi-country research project designed to fill evidence gaps in malaria treatment [57], suggest that despite efforts to improve care, appropriateness of antimalarial treatment at drug shops remains sub-optimal [49, 58– 66]. In Tanzania, the Accredited Drug Dispensing Outlet program for regulating and training drug shops to provide affordable and quality medicines was successful in promoting appropri- ate antimalarial treatment [67, 68]. However, sustaining gains has proven to be a problem [69], with reports indicating providers returning to poor dispensing practices [70, 71]. Rapid Diag- nostic Tests have been introduced at drugs shops to rationalize use of antimalarials, but amidst resistance from providers given the desire to profit through the sale of anti-malarial treat- ments, and from caregivers due to high costs [72, 73]. What is the best approach for improving delivery of health services amidst constraints of the public health system and the popular private sector? One approach is to strengthen the public health system which, despite its challenges [74], has the infrastructure and human resources for effective delivery of health services [75]. Beyond focusing on patient care, efforts should to be directed at improving hospitality services at public facilities. Studies in Uganda and Malawi have shown that abusive and disrespectful health workers were barriers to access- ing care at public facilities [76, 77]. This may partly explain why caregivers initially seek care at drug shops, whose hospitability services are likely far better due to the need to maintain cus- tomers [78, 79]. Strengthening the quality of services at drug shops is an alternative option. However, achieving quality services at drug shops is limited by multiple challenges including sub-optimal drug dosing, use of medicines not in national treatment guidelines [80], limited diagnostic capacity and inconsistent referral practices [55, 81], and the desire for profits [82]. PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 10 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda Additionally, despite laws that provide for standards of operations, many drug shops operate illegally [83], with poor quality of health services [46, 84, 85], including inappropriate provi- sion of parenteral artesunate [86]. This situation calls for policymakers to embark on programs of action to empower and strengthen regulatory frameworks and instruments in relation to drug shops [75]. Regardless of limitations, policy makers must acknowledge that drug shops are a popular point of care and can be mobilized to treat acute febrile illnesses among rural populations. In Tanzania [67] and Kenya [87, 88] interventions including provision of subsidized packs of pedi- atric ACT to retail outlets, training of retail outlet staff, and community awareness activities resulted in significant increases in ACT coverage for reported fevers. In-appropriate use of anti- malarials by drug shops remains a concern. However, provision of rapid diagnostic tests for malaria in the private sector could minimize this problem as was demonstrated in a study in Ghana [89], where introduction of RDTs resulted in reduced dispensing of antimalarial to patients without malaria, and did not reduce prescribing of antimalarials to true malaria cases. Additionally, by applying principles of commercial marketing to social health problems, drug shops have the potential to serve as an effective mechanism for promoting socially beneficial behavior change [75]. Also banning drug shops because of poor quality of care concerns may run them underground, causing more harm than good. Key is finding the right balance, support- ing drug shops to provide much needed services, but maintaining acceptable standards of care. In conclusion, we report on delays in seeking appropriate care by caregivers of children eventually diagnosed with severe malaria. Lack of action for perceived mild fever contributed to delays in care. Social networks including grandmothers and mothers-in-law, whose influ- ence often resulted in inappropriate treatment options, led to further delays. Despite the opportunity, drug shops have been shown to contribute to delay in seeking appropriate care [16], possibly explained by providing inappropriate care. Unfortunately, caregivers often sought care at public health facilities only when interventions at home or at drug shops had failed and illness had progressed from mild to severe. To address these gaps, there is need for a multipronged approach, starting with prioritization of health education programs sensitizing communities living in endemic areas, not only on recognition of symptoms of malaria, but emphasizing the significance of fever, irrespective of grade as an indicator of malaria [20]. For drug shops, there is need to define the role ofdrug shops in providing care to sick children in sub-Saharan Africa. Once defined, shop attendants should be trained and regulated to operate appropriately. For the public health sector, governments and partners need to direct efforts towards improving quality of hospitality services, a neglected area deserving attention. Supporting information S1 Appendix. In-depth interview guide. (PDF) S2 Appendix. Checklist for fulfillment of consolidated criteria for reporting qualitative studies (COREQ). (XLSX) S3 Appendix. Transcript for interview A325. (PDF) Acknowledgments We thank the study team of Yasin Kisambira, Jessica Tagobera, AnnetNabweteme, ProssyEwi- nyo, AzizzKiwanuka, Rose Nabirye, Peter Wambi, Ronald Bayisuka, William Ambayo, Juliet PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 11 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda Nabunjje, Fiona Kassana, David Katikati, Sally Opus, and Benjamin Buyi. We also thank health workers in Jinja Hospital and other participating health facilities for supporting the study team. We thank the staff of the Infectious Diseases Research Collaboration for providing administrative support. Finally, we are grateful to the parents, guardians, and caretakers who agreed to take part in this study. Author Contributions Conceptualization: Arthur Mpimbaza, Grace Ndeezi, Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. Data curation: Arthur Mpimbaza, Susan Nayiga, Charles Karamagi, Anne Katahoire. Formal analysis: Arthur Mpimbaza, Susan Nayiga, Anne Katahoire. Funding acquisition: Arthur Mpimbaza, Philip J. Rosenthal. Investigation: Arthur Mpimbaza, Grace Ndeezi, Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. Methodology: Arthur Mpimbaza, Susan Nayiga, Grace Ndeezi, Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. Project administration: Arthur Mpimbaza, Philip J. Rosenthal, Anne Katahoire. Resources: Arthur Mpimbaza, Susan Nayiga, Philip J. Rosenthal. Software: Arthur Mpimbaza. Supervision: Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. Validation: Arthur Mpimbaza, Anne Katahoire. Writing – original draft: Arthur Mpimbaza, Susan Nayiga, Grace Ndeezi, Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. Writing – review & editing: Arthur Mpimbaza, Philip J. Rosenthal, Charles Karamagi, Anne Katahoire. References 1. World Health Organization. WHO Global Technical Strategy for Malaria 2016–2030. 2016. 2. Nosten F, White NJ. Artemisinin-based combination treatment of falciparum malaria. American journal of tropical medicine and hygiene. 2007; 77(6 Suppl):181–92. 3. Opiyo N, Yamey G, Garner P. Subsidising artemisinin-based combination therapy in the private retail sector. The Cochrane database of systematic reviews. 2016; 3:CD009926. https://doi.org/10.1002/ 14651858.CD009926.pub2 PMID: 26954551 4. Camponovo F, Bever CA, Galactionova K, Smith T, Penny MA. Incidence and admission rates for severe malaria and their impact on mortality in Africa. Malar J. 2017; 16(1):1. https://doi.org/10.1186/ s12936-016-1650-6 PMID: 28049519 5. Korenromp E, Mahiane G, Hamilton M, Pretorius C, Cibulskis R, Lauer J, et al. Malaria intervention scale-up in Africa: effectiveness predictions for health programme planning tools, based on dynamic transmission modelling. Malar J. 2016; 15(1):417. https://doi.org/10.1186/s12936-016-1461-9 PMID: 6. Bennett A, Bisanzio D, Yukich JO, Mappin B, Fergus CA, Lynch M, et al. Population coverage of artemi- sinin-based combination treatment in children younger than 5 years with fever and Plasmodium falcipa- rum infection in Africa, 2003–2015: a modelling study using data from national surveys. Lancet Glob Health. 2017; 5(4):e418–e27. https://doi.org/10.1016/S2214-109X(17)30076-1 PMID: 28288746 7. World Health Orgnaization.World Malaria Report. 2017 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 12 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda 8. Zurovac D, Rowe AK. Quality of treatment for febrile illness among children at outpatient facilities in sub-Saharan Africa. Ann Trop Med Parasitol. 2006; 100(4):283–96. https://doi.org/10.1179/ 136485906X105633 PMID: 16762109 9. Whitty CJ, Chandler C, Ansah E, Leslie T, Staedke SG. Deployment of ACT antimalarials for treatment of malaria: challenges and opportunities. Malar J. 2008; 7 Suppl 1:S7. 10. Tanner M, Vlassoff C. Treatment-seeking behaviour for malaria: a typology based on endemicity and gender. Social science & medicine. 1998; 46(4–5):523–32. 11. Kassam R, Collins JB, Liow E, Rasool N. Narrative review of current context of malaria and manage- ment strategies in Uganda (Part I). Acta tropica. 2015; 152:252–68. https://doi.org/10.1016/j. actatropica.2015.07.028 PMID: 26257070 12. Kamat VR. "I thought it was only ordinary fever!" cultural knowledge and the micropolitics of therapy seeking for childhood febrile illness in Tanzania. Social science & medicine. 2006; 62(12):2945–59. 13. Tabuti JR. Herbal medicines used in the treatment of malaria in Budiope county, Uganda. J Ethnophar- macol. 2008; 116(1):33–42. https://doi.org/10.1016/j.jep.2007.10.036 PMID: 18054454 14. O’Neill S, Gryseels C, Dierickx S, Mwesigwa J, Okebe J, d’Alessandro U, et al. Foul wind, spirits and witchcraft: illness conceptions and health-seeking behaviour for malaria in the Gambia. Malar J. 2015; 14:167. https://doi.org/10.1186/s12936-015-0687-2 PMID: 25908392 15. Rutebemberwa E, Pariyo G, Peterson S, Tomson G, Kallander K. Utilization of public or private health care providers by febrile children after user fee removal in Uganda. Malar J. 2009; 8:45. https://doi.org/ 10.1186/1475-2875-8-45 PMID: 19284673 16. Mpimbaza A, Ndeezi G, Katahoire A, Rosenthal PJ, Karamagi C. Demographic, Socioeconomic, and Geographic Factors Leading to Severe Malaria and Delayed Care Seeking in Ugandan Children: A Case-Control Study. The American journal of tropical medicine and hygiene. 2017; 97(5):1513–23. https://doi.org/10.4269/ajtmh.17-0056 PMID: 29016322 17. Kassam R, Sekiwunga R, MacLeod D, Tembe J, Liow E. Patterns of treatment-seeking behaviors among caregivers of febrile young children: a Ugandan multiple case study. BMC public health. 2016; 16:160. https://doi.org/10.1186/s12889-016-2813-7 PMID: 26883506 18. Colvin CJ, Smith HJ, Swartz A, Ahs JW, de Heer J, Opiyo N, et al. Understanding careseeking for child illness in sub-Saharan Africa: a systematic review and conceptual framework based on qualitative research of household recognition and response to child diarrhoea, pneumonia and malaria. Social sci- ence & medicine. 2013; 86:66–78. 19. Mangham-Jefferies L, Hanson K, Mbacham W, Onwujekwe O, Wiseman V. What determines providers’ stated preference for the treatment of uncomplicated malaria? Social science & medicine. 2014; 104:98–106. 20. Williams HA, Jones CO. A critical review of behavioral issues related to malaria control in sub-Saharan Africa: what contributions have social scientists made? Social science & medicine. 2004; 59(3):501–23. 21. Glass TA, McAtee MJ. Behavioral science at the crossroads in public health: extending horizons, envi- sioning the future. Social science & medicine. 2006; 62(7):1650–71. 22. Bloom G, Standing H. Future health systems: Why future? Why now? Social science & medicine. 2008; 66(10):2067–75. 23. Bukirwa H, Nayiga S, Lubanga R, Mwebaza N, Chandler C, Hopkins H, et al. Pharmacovigilance of anti- malarial treatment in Uganda: community perceptions and suggestions for reporting adverse events. Tropical medicine & international health: TM & IH. 2008; 13(9):1143–52. 24. Nayiga S, DiLiberto D, Taaka L, Nabirye C, Haaland A, Staedke SG, et al. Strengthening patient-cen- tred communication in rural Ugandan health centres: A theory-driven evaluation within a cluster ran- domized trial. Evaluation. 2014; 20(4):471–91. https://doi.org/10.1177/1356389014551484 PMID: 25. Hutchinson E, Nayiga S, Nabirye C, Taaka L, Staedke SG. Data value and care value in the practice of health systems: A case study in Uganda. Social science & medicine. 2018; 211:123–30. 26. Muela Ribera J. The PASS-model: a model for guiding health-seeking behavior and access.Malaria Reports 2012; volume 2:e3s 27. Talisuna AO, Noor AM, Mundia CW, Otieno V, Mitto B, Amratia P, et al. An epidemiological profile of malaria and its control inUganda. Analysis and report funded by Roll Back Malaria and Department for InternationalDevelopment-UK, Sept 2013 28. Uganda Bureau of Statistics (UBOS) and ICF International Inc. (2016). Uganda Demographic and Health Survey 2011. Kampala, Uganda: UBOS and Calverton, Maryland: ICF International Inc. 2011 29. Uganda Bureau of Statistics (UBOS). Uganda National Household Survey 2012/2013. Kampala Uganda; UBOS. 2016 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 13 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda 30. Mutebi F, Krucken J, von Samson-Himmelstjerna G, Waiswa C, Mencke N, Eneku W, et al. Animal and human tungiasis-related knowledge and treatment practices among animal keeping households in Bugiri District, South-Eastern Uganda. Acta tropica. 2018; 177:81–8. https://doi.org/10.1016/j. actatropica.2017.10.003 PMID: 29017876 31. Wafula ST, Ssemugabo C, Namuhani N, Musoke D, Ssempebwa J, Halage AA. Prevalence and risk factors associated with tungiasis in Mayuge district, Eastern Uganda. The Pan African medical journal. 2016; 24:77. https://doi.org/10.11604/pamj.2016.24.77.8916 PMID: 27642416 32. Konde-Lule J, Gitta SN, Lindfors A, Okuonzi S, Onama VO, Forsberg BC. Private and public health care in rural areas of Uganda. BMC international health and human rights. 2010; 10:29. https://doi.org/ 10.1186/1472-698X-10-29 PMID: 21106099 33. Ministry of Health, Uganda. Uganda Hospital and Health Centre IV Census Survey 2014.Availablefrom: https://www.who.int/healthinfo/systems/SARA_H_UGA_Results_2014.pdf 34. Awor P, Wamani H, Bwire G, Jagoe G, Peterson S. Private sector drug shops in integrated community case management of malaria, pneumonia, and diarrhea in children in Uganda. The American journal of tropical medicine and hygiene. 2012; 87(5 Suppl):92–6. 35. Rutebemberwa E, Kallander K, Tomson G, Peterson S, Pariyo G. Determinants of delay in care-seek- ing for febrile children in eastern Uganda. Tropical medicine & international health: TM & IH. 2009; 14 (4):472–9. 36. Awor P, Wamani H, Tylleskar T, Peterson S. Drug seller adherence to clinical protocols with integrated management of malaria, pneumonia and diarrhoea at drug shops in Uganda. Malar J. 2015; 14:277. https://doi.org/10.1186/s12936-015-0798-9 PMID: 26178532 37. Tong A, Sainsbury P, Craig J. Consolidated criteria for reporting qualitative research (COREQ): a 32- item checklist for interviews and focus groups. Int J Qual Health Care. 2007; 19(6):349–57. https://doi. org/10.1093/intqhc/mzm042 PMID: 17872937 38. Wiseman V, Scott A, Conteh L, McElroy B, Stevens W. Determinants of provider choice for malaria treatment: experiences from The Gambia. Social science & medicine. 2008; 67(4):487–96. 39. Bartoloni A, Zammarchi L. Clinical aspects of uncomplicated and severe malaria. Mediterranean journal of hematology and infectious diseases. 2012; 4(1):e2012026. https://doi.org/10.4084/MJHID.2012.026 PMID: 22708041 40. Stauffer W, Fischer PR. Diagnosis and treatment of malaria in children. Clin Infect Dis. 2003; 37 (10):1340–8. https://doi.org/10.1086/379074 PMID: 14583868 41. Pierce H, Gibby AL, Forste R. Caregiver Decision-Making: Household Response to Child Illness in sub- Saharan Africa. Population research and policy review. 2016; 35(5):581–97. https://doi.org/10.1007/ s11113-016-9396-y PMID: 28794575 42. Mwandama D, Mwale C, Bauleni A, Phiri T, Chisaka J, Nsona H, et al. Clinical outcomes among febrile children aged 2 to 59 months with negative malaria rapid diagnostic test results in Mchinji District, Malawi. Malawi Med J. 2016; 28(4):150–3. PMID: 28321277 43. White NJ, Pukrittayakamee S, Hien TT, Faiz MA, Mokuolu OA, Dondorp AM. Malaria. Lancet. 2014; 383(9918):723–35. https://doi.org/10.1016/S0140-6736(13)60024-0 PMID: 23953767 44. Bedford KJ, Sharkey AB. Local barriers and solutions to improve care-seeking for childhood pneumo- nia, diarrhoea and malaria in Kenya, Nigeria and Niger: a qualitative study. PloS one. 2014; 9(6): e100038. https://doi.org/10.1371/journal.pone.0100038 PMID: 24971642 45. Ewing VL, Tolhurst R, Kapinda A, Richards E, Terlouw DJ, Lalloo DG. Increasing understanding of the relationship between geographic access and gendered decision-making power for treatment-seeking for febrile children in the Chikwawa district of Malawi. Malar J. 2016; 15(1):521. https://doi.org/10.1186/ s12936-016-1559-0 PMID: 27776549 46. Liu J, Prach LM, Treleaven E, Hansen M, Anyanti J, Jagha T, et al. The role of drug vendors in improv- ing basic health-care services in Nigeria. Bulletin of the World Health Organization. 2016; 94(4):267– 75. https://doi.org/10.2471/BLT.15.154666 PMID: 27034520 47. Mackintosh M, Channon A, Karan A, Selvaraj S, Cavagnero E, Zhao H. What is the private sector? Understanding private provision in the health systems of low-income and middle-income countries. Lan- cet. 2016; 388(10044):596–605. https://doi.org/10.1016/S0140-6736(16)00342-1 PMID: 27358253 48. Sudhinaraset M, Ingram M, Lofthouse HK, Montagu D. What is the role of informal healthcare providers in developing countries? A systematic review. PloS one. 2013; 8(2):e54978. https://doi.org/10.1371/ journal.pone.0054978 PMID: 23405101 49. Group AC, Phok S, Phanalasy S, Thein ST, Likhitsup A. Private sector opportunities and threats to achieving malaria elimination in the Greater Mekong Subregion: results from malaria outlet surveys in Cambodia, the Lao PDR, Myanmar, and Thailand. Malar J. 2017; 16(1):180. https://doi.org/10.1186/ s12936-017-1800-5 PMID: 28464945 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 14 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda 50. Rutebemberwa E, Buregyeya E, Lal S, Clarke SE, Hansen KS, Magnussen P, et al. Assessing the potential of rural and urban private facilities in implementing child health interventions in Mukono district, central Uganda-a cross sectional study. BMC health services research. 2016; 16:268. https://doi.org/ 10.1186/s12913-016-1529-9 PMID: 27421644 51. Buchner DL, Kitutu FE, Cross DE, Nakamoga E, Awor P. A cross-sectional study to identify the distribu- tion and characteristics of licensed and unlicensed private drug shops in rural Eastern Uganda to inform an iCCM intervention to improve health outcomes for children under five years. PloS one. 2019; 14(1): e0209641. https://doi.org/10.1371/journal.pone.0209641 PMID: 30625187 52. Mbonye AK, Buregyeya E, Rutebemberwa E, Clarke SE, Lal S, Hansen KS, et al. Referral of children seeking care at private health facilities in Uganda. Malar J. 2017; 16(1):76. https://doi.org/10.1186/ s12936-017-1723-1 PMID: 28196532 53. Hutchinson E, Hutchison C, Lal S, Hansen K, Kayendeke M, Nabirye C, et al. Introducing rapid tests for malaria into the retail sector: what are the unintended consequences? BMJ global health. 2017; 2(1): e000067. https://doi.org/10.1136/bmjgh-2016-000067 PMID: 28588992 54. Poyer S, Shewchuk T, Tougher S, Ye Y, Group AC, Mann AG, et al. Availability and price of malaria rapid diagnostic tests in the public and private health sectors in 2011: results from 10 nationally repre- sentative cross-sectional retail surveys. Tropical medicine & international health: TM & IH. 2015; 20 (6):744–56. 55. Webster P. Drug shops as primary point of care-the case of Nigeria. Lancet. 2017; 390(10089):15–7. https://doi.org/10.1016/S0140-6736(17)31722-1 PMID: 28677546 56. Wafula FN, Goodman CA. Are interventions for improving the quality of services provided by special- ized drug shops effective in sub-Saharan Africa? A systematic review of the literature. Int J Qual Health Care. 2010; 22(4):316–23. https://doi.org/10.1093/intqhc/mzq022 PMID: 20430823 57. Shewchuk T, O’Connell KA, Goodman C, Hanson K, Chapman S, Chavasse D. The ACTwatch project: methods to describe anti-malarial markets in seven countries. Malar J. 2011; 10:325. https://doi.org/10. 1186/1475-2875-10-325 PMID: 22039780 58. Group AC, Musuva A, Ejersa W, Kiptui R, Memusi D, Abwao E. The malaria testing and treatment land- scape in Kenya: results from a nationally representative survey among the public and private sector in 2016. Malar J. 2017; 16(1):494. https://doi.org/10.1186/s12936-017-2089-0 PMID: 29268789 59. Group AC, Kaula H, Buyungo P, Opigo J. Private sector role, readiness and performance for malaria case management in Uganda, 2015. Malar J. 2017; 16(1):219. https://doi.org/10.1186/s12936-017- 1824-x PMID: 28545583 60. Group AC, Newton PN, Hanson K, Goodman C. Do anti-malarials in Africa meet quality standards? The market penetration of non quality-assured artemisinin combination therapy in eight African countries. Malar J. 2017; 16(1):204. https://doi.org/10.1186/s12936-017-1818-8 PMID: 28539125 61. Group AC, Hanson K, Goodman C. Testing times: trends in availability, price, and market share of malaria diagnostics in the public and private healthcare sector across eight sub-Saharan African coun- tries from 2009 to 2015. Malar J. 2017; 16(1):205. https://doi.org/10.1186/s12936-017-1829-5 PMID: 62. Group AC, Michael D, Mkunde SP. The malaria testing and treatment landscape in mainland Tanzania, 2016. Malar J. 2017; 16(1):202. https://doi.org/10.1186/s12936-017-1819-7 PMID: 28521811 63. Group AC, Zinsou C, Cherifath AB. The malaria testing and treatment landscape in Benin. Malar J. 2017; 16(1):174. https://doi.org/10.1186/s12936-017-1808-x PMID: 28446236 64. Group AC, Tougher S, Hanson K, Goodman C. What happened to anti-malarial markets after the Affordable Medicines Facility-malaria pilot? Trends in ACT availability, price and market share from five African countries under continuation of the private sector co-payment mechanism. Malar J. 2017; 16 (1):173. https://doi.org/10.1186/s12936-017-1814-z PMID: 28441956 65. Group AC, Phanalasy S. The malaria testing and treatment landscape in the southern Lao People’s Democratic Republic (PDR). Malar J. 2017; 16(1):169. https://doi.org/10.1186/s12936-017-1769-0 PMID: 28438155 66. Group AC, Mpanya G, Tshefu A, Likwela JL. The malaria testing and treatment market in Kinshasa, Democratic Republic of the Congo, 2013. Malar J. 2017; 16(1):94. https://doi.org/10.1186/s12936-016- 1659-x PMID: 28241832 67. Rutta E, Kibassa B, McKinnon B, Liana J, Mbwasi R, Mlaki W, et al. Increasing Access to Subsidized Artemisinin-based Combination Therapy through Accredited Drug Dispensing Outlets in Tanzania. Health research policy and systems. 2011; 9:22. https://doi.org/10.1186/1478-4505-9-22 PMID: 68. Rutta E, Liana J, Embrey M, Johnson K, Kimatta S, Valimba R, et al. Accrediting retail drug shops to strengthen Tanzania’s public health system: an ADDO case study. Journal of pharmaceutical policy and practice. 2015; 8:23. https://doi.org/10.1186/s40545-015-0044-4 PMID: 26413304 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 15 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda 69. S. Benavides, H. Hong, A. Mantzavinou, E. Nikolopoulos, & B. Russell. Analysis of Tanzania’s ADDO Program.Global Health Markets. 2013. Available from: http://www.brandon-russell.com/addo.shtml 70. Embrey M, Vialle-Valentin C, Dillip A, Kihiyo B, Mbwasi R, Semali IA, et al. Understanding the Role of Accredited Drug Dispensing Outlets in Tanzania’s Health System. PloS one. 2016; 11(11):e0164332. https://doi.org/10.1371/journal.pone.0164332 PMID: 27824876 71. Bruxvoort K, Kalolella A, Cairns M, Festo C, Kenani M, Lyaruu P, et al. Are Tanzanian patients attending public facilities or private retailers more likely to adhere to artemisinin-based combination therapy? Malar J. 2015; 14:87. https://doi.org/10.1186/s12936-015-0602-x PMID: 25889767 72. Visser T, Bruxvoort K, Maloney K, Leslie T, Barat LM, Allan R, et al. Introducing malaria rapid diagnostic tests in private medicine retail outlets: A systematic literature review. PloS one. 2017; 12(3):e0173093. https://doi.org/10.1371/journal.pone.0173093 PMID: 28253315 73. Tawiah T, Malam K, Kwarteng A, Bart-Plange C, Febir L, Aubyn V, et al. Improving the first-line treat- ment of febrile illnesses in Ghana: willingness to pay for malaria rapid diagnostic tests at licensed chem- ical shops in the Kintampo area. Cost effectiveness and resource allocation: C/E. 2018; 16:4. https:// doi.org/10.1186/s12962-018-0090-2 PMID: 29434526 74. Kabaghe AN, Phiri MD, Phiri KS, van Vugt M. Challenges in implementing uncomplicated malaria treat- ment in children: a health facility survey in rural Malawi. Malar J. 2017; 16(1):419. https://doi.org/10. 1186/s12936-017-2066-7 PMID: 29047388 75. Awor P, Peterson S, Gautham M. Delivering child health interventions through the private sector in low and middle income countries: challenges, opportunities, and potential next steps. BMJ. 2018; 362: k2950. https://doi.org/10.1136/bmj.k2950 PMID: 30061154 76. Katahoire AR, Henriksson DK, Ssegujja E, Waiswa P, Ayebare F, Bagenda D, et al. Improving child sur- vival through a district management strengthening and community empowerment intervention: early implementation experiences from Uganda. BMC public health. 2015; 15:797. https://doi.org/10.1186/ s12889-015-2129-z PMID: 26286146 77. Lungu EA, Guda Obse A, Darker C, Biesma R. What influences where they seek care? Caregivers’ preferences for under-five child healthcare services in urban slums of Malawi: A discrete choice experi- ment. PloS one. 2018; 13(1):e0189940. https://doi.org/10.1371/journal.pone.0189940 PMID: 29351299 78. Rosapep L, Sanders E, Banke K. The influence of customer-medicine seller transactional dynamics on childhood diarrhoea management: a qualitative study in Ghana. Health Policy Plan. 2017; 32(4):527– 37. https://doi.org/10.1093/heapol/czw155 PMID: 28073934 79. Basu S, Andrews J, Kishore S, Panjabi R, Stuckler D. Comparative performance of private and public healthcare systems in low- and middle-income countries: a systematic review. PLoS medicine. 2012; 9 (6):e1001244. https://doi.org/10.1371/journal.pmed.1001244 PMID: 22723748 80. Goodman C, Kachur SP, Abdulla S, Bloland P, Mills A. Drug shop regulation and malaria treatment in Tanzania—why do shops break the rules, and does it matter? Health Policy Plan. 2007; 22(6):393–403. https://doi.org/10.1093/heapol/czm033 PMID: 17921151 81. Maloney K, Ward A, Krenz B, Petty N, Bryson L, Dolkart C, et al. Expanding access to parasite-based malaria diagnosis through retail drug shops in Tanzania: evidence from a randomized trial and implica- tions for treatment. Malar J. 2017; 16(1):6. https://doi.org/10.1186/s12936-016-1658-y PMID: 82. Kitutu FE, Mayora C, Johansson EW, Peterson S, Wamani H, Bigdeli M, et al. Health system effects of implementing integrated community case management (iCCM) intervention in private retail drug shops in South Western Uganda: a qualitative study. BMJ global health. 2017; 2(Suppl 3):e000334. https:// doi.org/10.1136/bmjgh-2017-000334 PMID: 29259824 83. National Drug Authority. PUBLIC NOTICE ON LICENSING OF PHARMACIES AND DRUG SHOPS. (2017).Available from: http://www.nda.or.ug/ug/dnews/60/Public-Notice-on-Licensing-Of-Pharmacies- And-Drug-Shops.html. 84. Wafula FN, Miriti EM, Goodman CA. Examining characteristics, knowledge and regulatory practices of specialized drug shops in Sub-Saharan Africa: a systematic review of the literature. BMC health ser- vices research. 2012; 12:223. https://doi.org/10.1186/1472-6963-12-223 PMID: 22838649 85. Doherty JE. Regulating the for-profit private health sector: lessons from East and Southern Africa. Health Policy Plan. 2015; 30 Suppl 1:i93–102. 86. Wang LT, Bwambale R, Keeler C, Reyes R, Muhindo R, Matte M, et al. Private sector drug shops fre- quently dispense parenteral anti-malarials in a rural region of Western Uganda. Malar J. 2018; 17 (1):305. https://doi.org/10.1186/s12936-018-2454-7 PMID: 30134987 87. Kedenge SV, Kangwana BP, Waweru EW, Nyandigisi AJ, Pandit J, Brooker SJ, et al. Understanding the impact of subsidizing artemisinin-based combination therapies (ACTs) in the retail sector—results from focus group discussions in rural Kenya. PloS one. 2013; 8(1):e54371. https://doi.org/10.1371/ journal.pone.0054371 PMID: 23342143 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 16 / 17 Delay in seeking appropriate care for children with severe malaria in Uganda 88. Kangwana BP, Kedenge SV, Noor AM, Alegana VA, Nyandigisi AJ, Pandit J, et al. The impact of retail- sector delivery of artemether-lumefantrine on malaria treatment of children under five in Kenya: a clus- ter randomized controlled trial. PLoS medicine. 2011; 8(5):e1000437. https://doi.org/10.1371/journal. pmed.1000437 PMID: 21655317 89. Ansah EK, Narh-Bana S, Affran-Bonful H, Bart-Plange C, Cundill B, Gyapong M, et al. The impact of providing rapid diagnostic malaria tests on fever management in the private retail sector in Ghana: a cluster randomized trial. BMJ. 2015; 350:h1019. https://doi.org/10.1136/bmj.h1019 PMID: 25739769 PLOS ONE | https://doi.org/10.1371/journal.pone.0217262 June 5, 2019 17 / 17

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