Population.

The study was carried out in the Cambodian province of Ratanakiri, which in 2008 had a population of 150,000 inhabitants (1% of the total Cambodian population) [16]. The study villages were home to 10 indigenous ethnic groups [17], the Jarai, the Tompuon and the Kreung being the largest of them. Most ethnic minorities practice slash and burn agriculture at forest fields and collect various forest products (hunting and gathering). They often live where they are working, and as such may have several residences spread over the village, rice field or forest farm. Animistic beliefs require agricultural activities to be performed in cooperation with the spirits and ancestors that pervade the trees, rocks and rivers of the village territory [18–20].

Malaria transmission.

Malaria transmission is perennial with two peaks, June-July and October-November, the rainy season lasting from May to October. The main malaria vector is Anopheles dirus, an anthropophylic, outdoor and sylvatic species [10,11]. P. falciparum and P. vivax prevalence is similar and in 2010 the overall incidence of clinical malaria was 49/1000 population [21]. Given the high number of Long Lasting Insecticidal Nets (LLINs) distributed by the National Malaria Control Program (1 net per 2 persons since 2008 and 1 net per person since 2011), malaria transmission is assumed to occur mostly outdoors, and before or after sleeping time, when people are not protected by bed nets [11,22].

Malaria treatment guidelines.

In the public sector, malaria control measures are implemented through VMWs at community level, health posts at commune level, health centres at district level and referral hospitals usually in the provincial capital. At the time of this study, the first-line treatment was prepackaged (blister pack) mefloquine-artesunate for P. falciparum and chloroquine for P. vivax - both taken over three days. Mefloquine-artesunate, provided under the brand name A+M, is officially available free of charge at the commune health posts, district health centers and the provincial hospital. For severe malaria, the recommended treatment was either artemether or quinine injections, available at the provincial referral hospital and certain district health centers.

In remote villages, VMWs, after confirmation by an RDT, can administer A+M free of charge [15,23,24]. They are supposed to keep detailed records of both RDT results and treatments given and are supervised by the district health centre staff that check the records and replenish their stock.

The private sector in Cambodia is officially organized in four levels of recognized practitioners: (i) private clinics run by medical doctors, (ii) pharmacies with a registered pharmacist, (iii) ‘Depot A’ pharmacies run by assistant pharmacists and (iii) ‘Depot B’ pharmacies operated by nurses or midwifes [25]. In terms of antimalarial treatment, Population Services International (PSI) provides Malarine™ blisterpacks (mefloquine-artesunate) to the private sector, which is sold at highly subsidized prizes. Nevertheless, in addition, private practitioners or pharmacists can assemble “cocktails” for their clients [13,15]. One cocktail consists of a one-day treatment dose combining pills cut off from a blister pack strip or taken from a jar, and provided in a little plastic bag (see Figure 1).

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Figure 1. Local “anti-malaria cocktail”.

https://doi.org/10.1371/journal.pone.0080343.g001

In addition, the ethnic minority groups in Ratanakiri consult diviners, i.e. traditional healers able to spiritually divine the cause of an illness. Research on home treatment such as coin massages and the use of herbs is outside the scope of this study and was not further explored.

Data collection.

Fieldwork was conducted between April and July in 2010 in Oyadao district, mostly in the border villages of Lom and Phi. For participant observation, the research team participated actively in and observed the daily life of the study population. Continuous informal conversations and interviews with respondents built up confidence for the discussions on more sensitive issues such as adherence to treatment obtained from public facilities. Frequent overnight stays in the two study villages, multiple visits to 11 private sector establishments (including pharmacies and private practitioners) along the main road in Oyadao district, and observation sessions at the health center and health post during consultation hours and monthly VMW meetings, were used to collect information on people’s behavior and to compare it with the information given by interviewees. This was an essential step to uncover response bias.

A total of 126 interviews were carried out with various respondents from different social, ethnic, professional and economic categories. These interviews were recorded and transcribed. When a conversation was of a more informal nature, or when the interviewer decided it was inappropriate to record the interview or the interviewee refused recording, notes were taken immediately after the interview. An additional 32 unrecorded informal conversations were included in the analysis.

Sampling.

Respondents were theoretically selected, referring to the purposive, gradual and continuous inclusion of respondents based on emerging results during the research process. Access to respondents was usually granted through snowball-sampling techniques, where certain key-informants introduce the researcher to selected participants. Many informants were visited several times as an additional way of building confidence between researcher and respondent, hence reducing bias.

Data collection.

After the qualitative strand of the study, two surveys were carried out. In the household survey a structured questionnaire was administered to all household leaders of the two villages involved in the qualitative study. Questions focused on the different providers of antimalarial treatment and on the choice for their last malaria episode (health centre, private practitioners, VMWs, traditional healers, etc.), including the reason for the choice. The other survey, a large scale cross-sectional survey, focused exclusively on treatment choice.

Sampling.

For the household survey, all households in the two study villages for the qualitative study (Phi and Lom) were sampled. For the cross-sectional survey, 900 individuals were randomly selected from the census of the villages included in the research project “Repellents as an Added Control Measure to Long-lasting Insecticidal Nets in Southeast Asia”, a community-based trial implemented in 113 villages of Ratanakiri province. The sample size was calculated based on the expected difference between study arms in the main outcome variable of the overall study, which was repellent use in villages and at farms. In total, 824 people from 109 different villages answered the structured questionnaire. An additional non-response form was used to measure possible systematic self-selection bias.

Qualitative data.

Thematic analysis was continuously carried out, after which emerging results and hypotheses were tested in the field until saturation was reached. For the preparation of the study and for analytical purposes, the PASS Health Seeking Behaviour Model was used [26]. Briefly, this model presents various elements that guide health seeking behaviour and access to care and, as such, can be adapted to different research contexts. The final analysis of all qualitative data was carried out in NVivo 9 Qualitative Analysis Software.

Quantitative data.

Preliminary analysis of the qualitative data was used to build the standardized questionnaires for the two quantitative surveys. Quantitative data were entered in Excel and analysed in SPSS (IBM SPSS Statistics 19). Frequency tables for the main outcome variables were produced, i.e. perceived VMW treatment availability, availability during last visit to VMW, treatment taken during last malaria episode, provider visited during last malaria episode. Data on the perceived performance of the VMWs were elicited only in the household survey (real life, non-trial setting).

Village Malaria Workers.

More than half (55.7%) of all household survey participants reported having ever visited their VMW, and 54.0% of those who had had malaria in the past reported having received treatment from the VMW for their last malaria episode (Table 1). However, qualitative interviews with villagers and VMWs revealed the general perception that the VMW’s ran out of stock (RDTs/treatments) rapidly during the rainy season, either due to the difficulty to replenish their stock (heavy workload in the fields, inaccessibility) or due to a higher demand. Indeed, in the household survey, 50.8% of all survey respondents perceived the VMW did not always have medication, 60.6% did not think the VMW would have the required test available, and 48% reported that the VMW was not always available when visited by patients. When asked about their last visit to the VMW, 30.7% of the respondents answered that the VMW did not have a test available, and 36.5% that there was treatment stock out. (Table 1).

Health centres, health posts and hospitals.

Only 9.3% of respondents in the household survey had attended the health centre during their last suspected malaria episode, and 1.2% had attended the provincial referral hospital (Table 1). Qualitative data consistently showed that only severe cases attended or were referred to the hospital by health centre staff or VMWs.

Private sector.

The following categories of private health providers were identified through observation and in-depth interviews with villagers, health staff and private practitioners: (i) medical cabinets, referring to private practitioners, not necessarily with any official medical training, working in a medical cabinet; (ii) pharmacies: practitioners (sometimes nurses from the health center, sometimes people without any medical training or untrained pharmacists) owning pharmacies and providing treatment; (iii) mobile private practitioners: practitioners visiting villages when called upon by patients; (iv) informal drug selling (grocery shops or individuals). In the household survey, 34.2% of respondents reported having attended one of private sector options during their last malaria episode (private practitioners, pharmacies, market) (Table 1).

Public-private overlap.

Despite the general distinction between public and private sectors, qualitative data clearly showed that this distinction is not so clear-cut. Indeed, each of the health center staff interviewed or observed owned his/her own private pharmacy at home, which was usually located near the health center. During informal conversations at health centers, informants reported that the medical staff often ‘advised’ people to buy the medication at their private pharmacy before being treated at the health centre, particularly when the type of medication desired was not available at the health center (e.g. artemether injections).

Blister packs.

Observations and interviews indicate that blister packs were common in both public and private sectors. In both the household and cross-sectional surveys, more than 75% of the respondents claimed to have bought pills in blister packs during the last malaria episode (Table 1 and 2).

Cocktails.

Following repeated observations at private facilities as well as respondents’ homes, a cocktail to treat malaria contained one or several antipyretic/analgesics (paracetamol), one antibiotic, vitamins, and one kind of antimalarial monotherapy (either chloroquine or artesunate) (Figure 1). Informants reported to buy one cocktail for around zero point two fiveUS$, and usually bought as many as they could afford. 13.7% of respondents in the household survey reported having bought cocktails for their last malaria episode, while this percentage was 26.0% in the cross-sectional survey (Table 1 and 2).

Injections.

Observations in pharmacies and interviews with informants indicate that artemether injections (intra-muscular), both European and Asian brands, were for sale in most of the private sector establishments, and were usually administered by the private practitioner or, in order to reduce the cost, were bought as ‘take-away’ for self-administration. Private practitioners reported the latter option to be the most popular since patients could often not afford to buy a full-dose 5-day injection treatment. In the household survey, 6.2% of household leaders reported having bought injections during their last malaria infection (Table 1), while this was 32.2% in the cross-sectional survey (Table 2).

Infusions.

Although generally not perceived as a malaria treatment, respondents in the qualitative study often reported intravenous infusions (glucose/vitamins) to be necessary to relieve symptoms and ‘strengthen’ the patient during a malaria episode. According to the cross-sectional survey, 26.4% of the respondents stated to have bought infusions during the last malaria episode for one of their household members.

Diviners.

In the qualitative study area, we identified two diviners (specialized villagers that can divine the causes of illness and discomforts for a small fee). Informants from those villages stated that it was common for each village to have at least one diviner. Interviews with both villagers and diviners showed that illness etiologies pointed out by diviners referred to the transgression of social norms by the patient, and sacrificial actions to restore health. The diagnosed transgressions usually involved a social disruption (familial disputes, failure to perform ceremonies). Treatments of patients mostly consisted of a ceremony (a social event involving the drinking of rice wine) and sacrifice of a costly buffalo, pig or chicken to the involved spirit, ancestor or witch, depending on the nature of the transgression and the financial situation of the family. In the cross-sectional survey, 37.3% of respondents claimed to have performed a ceremonial animal sacrifice during the last malaria episode of one of the household’s members, although most of them combined this treatment with “modern medicine” (blister pack, injections or cocktails).

Availability of treatment.

According to interviews and informal conversations with villagers, the VMW is usually the first option for suspected malaria but if he is not available or does not have treatment or diagnostic tests, people are reluctant to travel to the health centre.

Perceived side effects.

Both A+M and Malarine™ were perceived to cause strong side effects, i.e. dizziness and vomiting, and were therefore avoided whenever possible, as illustrated by the following quote: “My husband also got medication from the VMW. He took it for three days, but it had very strong side effects. He almost committed suicide!” (Jarai farmer, Phi). The mentioned side effects were one of the factors leading people to seek treatment in the private sector, either to buy antimalarial cocktails or injections, or to reduce the adverse effects of the public sector treatment with infusions, cocktails or injections. Some patients report to ‘preventively’ get an infusion at the private practitioner to counteract the expected side effects of the first-line ACT they would get from the VMW or HC staff. Although most pharmacies advertised for Malarine™, private health providers often reported that patients able to afford artemether injections chose for this more expensive but better tolerated option.

Perceived efficacy of the drug.

Despite the official indication for hospital use only, qualitative research showed that artemether injections were available in pharmacies without medical prescription. Reasons for their popularity were the quick relief provided which, together with the absence of side effects, allowed patients to rapidly return to their fields, where the workload is the highest during the malaria (rainy) season. Injections were also preferred because they would avoid swallowing of pills by an already weak patient, an often disliked act.

Expected costs.

Villagers reported prices ranging from 0.35 to 5 US$ for a consultation at the HC. Prices were similar for private practitioners but without the long waiting period, an appealing option that reduced the loss of productivity. Given the affordable price of cocktails compared to injections (0.25$ versus 2.5$), the former were quite popular and patients were usually able to buy 2-3 single-dose bags.

Health provider - patient encounter.

Patients’ reluctance to consult the local HC was not only related to the long waiting hours, but also by the fact that HC staff did not have the time to attend the numerous patients waiting for treatment. Informants often reported on the ‘unfriendly’ reception by the HC personnel, stressing the inherent hierarchy between doctor and patient, and sometimes between Khmer and ethnic minority. Conversely, private practitioners were reported to ‘take better care’ of their patients, taking more time, and delivering instant care with rapid tests and the client’s choice of medication.

Perceived etiology.

Despite the overall good knowledge of the “cause-symptoms-treatment” relations of malaria in the study area, the same symptoms could also be perceived as having a “supernatural” etiology, as illustrated by the following quote: “My children took malaria medication and recovered. But for me it was necessary to make an offer. I took the medication for only one day, and almost died. [So] I have a different problem: with the spirits. After one day of medication I offered a pig to the spirits. Before we go to the VMW, we go to meet the diviner and we follow the diviner” (Jarai farmer, Phi village). Thus, it was not uncommon that villagers experiencing symptoms such as fever, chills and headaches, consulted immediately the local diviner before considering biomedical treatment options.

Moreover, although illnesses of natural origin and those of supernatural origin were not seen as directly related, they could interact and aggravate the patient’s situation as illustrated hereafter: “The witch makes sure you don’t get hungry, you become skinny, or she makes you have pain all over your body. If this is combined with malaria, you die even sooner” (Jarai farmer, Phi village).