Engaging the private sector in malaria surveillance: a review of strategies and recommendations for elimination settings

Ethical approval was sought from the University of California, San Francisco Institutional Review Board (IRB). The IRB determined that this study posed minimal risk and was exempt from a full review.

In sending invitations to key informants as well as at the start of each interview, the researchers explicitly articulated the aims of the study and the data collection methodology. The key informants were free to decline the invitation or withdraw at any point during the interview. All transcribed responses were de-identified to uphold respondents’ confidentiality.

1890 titles and abstracts were found through database searches. After removing 829 duplicates, 484 full-text articles were retrieved and reviewed, and 119 were included in this paper. 139 additional documents, reports and websites cited throughout this paper were identified through online searches or provided by key informants. It was found through the literature reviews that only very few articles were on malaria elimination specifically, thus this paper drew from the malaria control literature or from the experiences of other disease programmes where relevant.

Of the 36 domain experts invited as key informants, 29 responded and were interviewed. Interviews in person, over the phone or through video teleconferencing were 46 min on average (range 33–60). Three interviews were done over several e-mail exchanges when the interviewers and key informants could not agree on a common time and date and method of communication. Key informants included researchers from North America, Europe, Africa and Asia (7 out of 29) whose work focused on private sector healthcare delivery systems and financing, programme managers of nongovernmental organizations (NGOs) and implementers working in malaria-endemic countries (17 out of 29), and representatives from the World Health Organization (WHO; 5 out of 29).

The private health sector includes any outlet, facility or person that provides clinical or diagnostic services and is not managed by a national or local government [3, 17, 45]. As almost all key informants emphasized, the composition of the private health sector varies greatly across countries, but private providers can generally be organized into four groups based on their commercial orientation or business model (for-profit vs nonprofit) and regulation status and/or level of training (formal vs informal) [46, 47]. Based on the literature review and key informant interviews, a private sector matrix was developed (Fig. 1).

Formal private providers have some formal training, accreditation or licensure [48]. The formal for-profit private sector consists of private hospitals and clinics, pharmacies, registered or accredited drug dispensaries and large corporations and companies that provide their own medical services and private diagnostic facilities. Formal nonprofit providers include health facilities owned and operated by NGOs and faith-based groups.

The informal private sector consists of a vast array of outlets run by individuals with little or no formal training [48]. The informal for-profit sector includes unregistered drug vendors and retailers, private and public practitioners who work from home, village doctors and traditional healers, smaller unregulated companies that provide health services, untrained providers and itinerant drug vendors. Volunteer workers fall in the final category of the informal nonprofit sector. Informal providers are responsible for widely varying levels of healthcare interactions in different settings, from 9% in Kenya to 77% in Bangladesh, and are more likely to serve poorer populations and rural areas [49, 50].

Formal providers are often easier to include in national malaria surveillance systems because they are regulated by the government and are typically required to submit records of their services. As all key informants stressed, the informal sector may be more difficult to include because of a lack of regulation or enforcement, making it hard to obtain records in a timely and coordinated manner. Potential legal consequences for operating outside the law may also make such providers hesitant to participate.

The size, contribution and makeup of the private sector in the 35 malaria-eliminating countries varies widely (Additional file 1: Table S1) [51]. In some regions, such as Southeast Asia and some parts of East and West Africa, the private sector is a major, if not the primary, source of healthcare for people across socioeconomic strata. In other regions, such as Southern Africa and some countries in Latin America, the public sector dominates the health system and provides most preventive and curative care.

The types of private providers that are most visited for malaria diagnostic and curative services differ widely by country. In Uganda, private health facilities such as clinics and hospitals are a more popular source of fever treatment than pharmacies, drug stores or general retailers [52]. In contrast, Nigerians are more likely to approach proprietary patent medicine vendors (PPMVs)—a specific type of drug retail outlet in Nigeria that is popular among the poor—for fever treatment compared to any other type of private health facility [53‐56]. Similarly, in Benin, Madagascar and Zambia, more people seek fever treatment from general retailers, pharmacies and drug shops than at private health facilities [57‐59], whereas in Cambodia, pharmacies and mobile providers are the most common sources of private sector diagnosis and artemisinin-based combination therapy (ACT) [60].

There are many challenges that national malaria programmes must address to ensure proper and timely diagnosis, management and reporting of malaria cases in the private sector. A number of these challenges exist in the public sector as well [23, 61‐66], but the mechanisms for resolving them may differ given the accountability public providers have to the government. The following primary challenges with private sector malaria surveillance were identified, focusing specifically on case management and reporting, based on the review of the literature and discussions with key informants.

Developing strategies to engage the private health sector, either through incentive schemes, greater communication, training or policy, is critical for ensuring high quality diagnosis and case management for malaria. However, only limited operational and implementation research has been conducted to guide how to effectively engage the private sector, especially informal providers, across a variety of conditions [97, 112]. Several experts have documented the primary available strategies for incorporating private sector providers to achieve positive child health outcomes across a range of conditions, which include (1) contracting private providers for specific services, (2) social marketing, (3) regulation and standard setting and (4) information dissemination or training [5, 10]. Here, these strategies are discussed, as well as social franchising, as they apply to malaria diagnosis and case management.

Contracting private providers includes utilizing public funds to engage private entities to deliver specific types, qualities and quantities of services which may improve the transparency and efficiency of publicly funded services [113, 114]. However, there is limited evidence on the effectiveness of contracting for malaria services. Contracting of health services to NGOs in Senegal and Madagascar increased coverage of nutritional services and decreased malnutrition rates, notably in areas where public care was less available [97, 115, 116]. In Cambodia, contracting replaced existing public services and resulted in improved access by the poor and lower rates of childhood diarrhea [117]. In Suriname, an NGO called the Medical Mission was funded directly by the Global Fund to Fight AIDS, Tuberculosis and Malaria to provide case management, among other malaria interventions, targeted specifically to high-risk areas with limited access to health services, such as remote gold mining areas. This included training local malaria service providers in delivering free diagnosis and treatment. This programme coincided with a dramatic decline in incidence [118].

Difficulties with contracting include its limited ability to scale, its lower cost-effectiveness compared with government services, increased inequity in service delivery at times, and government’s limited capacity to manage contracts and financial sustainability [114, 119, 120]. However, a review of ten health contracting experiences found that these challenges can be mitigated [119, 121]. A subsequent review found that contracting can improve health system access, though its potential for improving equity, quality and efficiency of health service delivery depended on how well-targeted the programmes were and if quality was adequately monitored and directly linked to payment [122]. Contract management by government agencies is a potential challenge and can be costly, but must be balanced against potential improvements in service delivery. In the case of Cambodia, contracted childhood health services ultimately achieved better outcomes with similar amounts of financial inputs [122]. Financial sustainability is a remaining concern subject to government and donor financing, but in these examples initial contracts were either continued or expanded.

Social marketing or commercialization of health products is used to expand delivery of key interventions to target populations and requires that interventions or services become more profitable and therefore appealing to private providers [5, 97]. This frequently involves a substantial subsidy on the marketed product so that they are affordable for consumers and also profitable for private providers and are therefore more likely to be sold [123]. A prominent example for malaria case management is the subsidization of ACT medicines in the private and public sectors through the Affordable Medicines Facility-malaria (AMFm) programme [124‐127] which has shown varying success in improving access to and affordability of frontline anti-malarials and crowding out of AMTs [128‐138]. Similar programmes, including randomized trials in Kenya and Tanzania and a pilot study in Uganda whose results informed the AMFm, have also shown that distribution of subsidized ACT medicines paired with training and community education can improve stocking and availability of ACT and the likelihood of being treated with ACT [23, 123, 138‐146]. Detailed understanding of the complex distribution chains for anti-malarials is crucial to achieving success of subsidized ACT, as is understanding the role of consumer demand in determining supply [89]. Social marketing strategies have also been used extensively to increase demand and use of insecticide-treated bed nets (ITNs) and to promote hand washing practices [5]. However, the effectiveness of these strategies varies [123]. Social marketing was not able to achieve equity consistently and reach those most at-risk populations in selected projects involving ITNs [147, 148] and anti-malarials through the AMFm in some study sites [149, 150].

Evidence around the ability of social marketing to generate demand for and improve access to RDTs is growing but remains limited to a number of settings [48, 92, 151‐158], leaving overtreatment a persistent challenge for many countries that may have successfully expanded access to anti-malarials [16, 79, 127, 128]. Combining training with financial incentives may be an optimal approach to improving diagnosis and appropriate treatment. A recent evaluation of incentives schemes for the use of RDTs by informal private providers in Myanmar compared combinations of price subsidies, financial incentives, and intensified information, education and communication (IEC), and found that a price subsidy combined with intensified IEC resulted in the highest uptake in use and quality of care [154]. Indeed, several reviews suggest subsidization schemes for RDTs would be wise to learn from the experience of ACT and ensure complementary activities such as community awareness, behaviour change communication (BCC) campaigns and training and supervision of providers are integrated with financial mechanisms [137, 157].

Social franchising is a related mechanism for linking private providers to provide and market socially desirable goods [159]. Social franchising has been successfully employed in a number of settings whereby networks of private sector providers are connected through formal agreements, the end result of which is social in addition to financial gain [97, 159, 160]. In this mechanism individual providers are incentivized to join a network of franchises through the creation of brand identity, mass marketing campaigns, access to commodities below market rates and trainings. Throughout their engagement, franchised providers are trained and supported to provide specific services and given access to data and feedback to improve their practices [160]. In Myanmar, providers who joined the Sun Quality Health (SQH) network cited social responsibility for serving the poor as a primary motivation [161, 162]. Social franchising through this network has resulted in more clients because of the perception that these SQH providers provide higher quality care and effective and affordable drugs [161]. However, a systematic review found that while social franchising globally has been shown to increase client volume and client satisfaction, it has had mixed results in terms of healthcare utilization and impact [163].

Regulation through the establishment of laws, policies and standards is a potential means to ensure appropriate case management and reporting in the private health sector, but requires ongoing monitoring to verify that standards are followed [97, 164]. Regulation includes creating specific diagnosis and treatment protocols, creating price controls for health services, regulating pharmaceuticals and essential drug lists, regulating private insurance, executing drug quality standards and involving private providers in establishing standards [10, 63, 164‐166]. Licensing and accreditation of private providers is another form of private sector regulation that has shown to successfully improve the supply of ACT medicines among drug sellers and drug shops in Tanzania [166‐170]. However, developing countries often allocate insufficient resources to enforce regulations. Often there are gaps in regulatory frameworks, such as infrequent inspections, lack of effective sanctions and lack of enforcement on the part of local regulatory staff, despite awareness of regulation infractions [77, 171, 172]. As Additional file 2: Table S2 shows, regulation over malaria surveillance in elimination settings is largely present, with a few exceptions.

Training of private sector providers may be one of the more operationally feasible and cost-effective approaches to improving private sector case management and has been shown to improve adherence to national guidelines for anti-malarial prescription and improved prescription behaviors by private practitioners in integrated management of childhood illnesses [5, 15, 173‐175]. In limited examples, training among drug sellers in Kenya and Tanzania has been associated with improved stocking and selling of recommended anti-malarials and giving the right advice to patients [144, 176, 177]. In Myanmar, IEC was found to be the most cost-effective approach for improving uptake of RDTs by informal providers [178]. Training and provision of subsidized commodities, such as ACT medicines and RDTs, is also commonly reported by providers as a means to improve the stature of their business and empower them to provide better care [179, 180]. Private health providers can also be included in the design and implementation of training, encouraging engagement and ensuring that the trainings address the needs of the intended audience. However, reviews of training interventions reveal that training alone may be insufficient if market-based strategies aligned with a provider’s incentives are not employed at the same time [181]. Combinations of interventions that reinforce each other are likely the most effective approach [182], and effectiveness is likely greatest when training is ongoing and integrated with social marketing approaches, referral systems and increased local regulatory oversight [181].

Several mechanisms have been employed in different settings to integrate private providers to disease reporting systems. In most countries, formal healthcare providers and facilities such as clinics, hospitals and laboratories that are registered, accredited or monitored by a country’s MOH are required to submit routine statistical reports on specified indicators to a local or national authority [183].

In some countries, certain private for-profit and nonprofit providers are seamlessly integrated into the national HMIS. For example, in Zambia health facilities run by the Churches Health Association of Zambia (CHAZ)—a group of Christian organizations that provides over 35% of healthcare in the country and implements malaria control activities in 22 districts—and other large hospitals submit monthly morbidity and mortality data to the national HMIS [184, 185]. Angola, Kenya, South Africa, Tanzania, Uganda, Zimbabwe and other countries also receive some HMIS data from the private sector, but reporting completeness among private health facilities is variable [186‐191]. Limited evidence from elimination settings suggests that reporting may be low. In South Africa, studies have shown that only 26% of malaria cases diagnosed in the private sector are being reported [186, 192]. In Swaziland, while the majority of private providers reported to the HMIS, only half reported to the immediate disease notification system (IDNS) [193].

Disease-specific surveillance systems are a model for integrating the private sector into reporting [187, 188, 190, 194, 195]. Many of these surveillance systems were established through donor funding and are now run by MOHs. For example in Kenya, the National AIDS/STD Control Programme has successfully engaged the private sector in reporting by tying the release of key commodities to case reporting [188]. At the same time the Division of Malaria Control at the Kenyan MOH runs a separate surveillance system with five facilities in epidemic-prone areas reporting regularly on disease burden [188]. However, in some cases these parallel surveillance systems cause fragmentation due to different reporting formats and timeframes and strain limited human resources available to manage these reporting systems [190].

While standalone tuberculosis (TB) surveillance systems still exist, most countries have included TB surveillance in their national HMISs where the private sector is an active participant [196]. This was primarily driven by the adoption of the Stop TB Strategy in 2006 which clearly specified that countries must engage all providers that provide TB care, including those in the private sector [197]. Several public–private mixes (PPMs) were established between national TB programmes and private providers that not only addressed appropriate treatment of TB but also integrated case reporting. As part of a PPM project in Cambodia, a short message service (SMS) malaria reporting and referral system has been implemented among private sector healthcare providers in Pailin Province, with early results suggesting a high proportion of referrals reached the public sector.

Another common method of capturing private sector surveillance is to establish a list of notifiable diseases. A notifiable or reportable disease is any disease or medical condition that medical providers and laboratories are required by law to report to local or national authorities [198]. Most notifiable diseases are rare or vaccine-preventable communicable diseases, such as polio, measles and malaria in elimination settings, but a number of non-communicable diseases such as cancer are reportable to cancer registries. The list of notifiable diseases varies from country to country, and in countries with decentralized health systems, different states or provinces may establish their own list of notifiable diseases while still adhering to national guidelines [199‐201].

Making a disease notifiable can improve surveillance, but it is not a perfect system. Many countries have documented varying levels of reporting completeness (with completeness rates ranging from 2 to 95% in different studies) and timeliness among public and private providers, both of which are critical for disease control and elimination [198, 202‐208]. Several barriers have been identified in reporting notifiable diseases, including poor physician knowledge about which diseases are notifiable, poor understanding of the proper procedures when reporting a disease and the significant amount of time required to fill out the forms for disease reporting [110, 111, 209‐219].

To address these barriers, a number of interventions have been implemented, including posting a condensed list of notifiable diseases in health facilities, making reporting forms widely available, conducting disease reporting trainings and providing regular feedback to providers about how their data is used [201, 213, 214]. The use of electronic or Internet-based reporting systems has been shown to improve completeness and timeliness of reporting in many settings [201, 220]. Appropriate incentives can promote consistent and timely reporting, such as in Taiwan where notifiable disease reporting is linked to national health insurance reimbursements and a small remuneration and has significantly improved reporting completeness and timeliness [221, 222]. In Swaziland, providers reported willingness to report into the malaria surveillance system without additional incentives, but requested improved training on how to use reporting forms and frequent follow up and interaction with malaria programme officers [193]. However, research on improving reporting for informal private providers remains an important gap across all settings.