Barriers against and strategies for malaria control during the COVID-19 pandemic in low- and middle-income countries: a systematic review

Following the PRISMA guidelines, a systematic literature review (Fig. 1) was conducted to identify studies on barriers against and strategies for malaria control during the COVID-19 pandemic in LMICs. The self-reported PRISMA checklist can be seen in Additional file 3, 4. Electronic databases including PubMed, Cochrane Library, Embase, CINAHL, Web of Science, PsycInfo, Global Health as well as Google Scholar were used to identify relevant literature. The search focused on studies published in the last two years from January 2020 to December 2021. Variants of the following search terms were used: malaria, COVID-19, and LMICs. The complete search terms are annexed [see Additional file 1]. Additionally, relevant grey literature (e.g., reports) were also obtained through additional searches. Lastly, the reference lists of selected literature were examined to identify any additional articles that fit the inclusion criteria.

Original research conducted in English that examine barriers to and strategies for control of malaria in LMICs in the era of the COVID–19 pandemic were included. The category of the countries was based on the World Bank List of Economies as of the 2022 fiscal year. In addition to peer-reviewed publications, limited types of grey literature (i.e., reports from the major malaria-related actors and preprints of journal articles) were included in the analysis as there was a limited number of published literature on hoarding during the COVID-19 pandemic. Similar search strategies were used to identify such grey literature. If the preprints were published prior to journal publication, the latest updates were reflected. According to the inclusion criteria, only literature released by December 2021 should have been included in the analyses. However, some articles that were published in 2022 (after their original inclusion into this review as preprints in 2021) were exceptionally included. Literature was excluded if the authors did not address either barriers or strategies in their own analysis or actual outcomes related to malaria control as in the cases of modelling studies or study protocols. In addition, case reports, inability to access full text, and grey literature (other than reports and preprints) were criteria by which literature was excluded from the analysis.

The results of the final search were collated using EndNote 20. The selection of literature was conducted in two stages after removing duplicates. At the first stage, the title and abstracts of the retrieved literature were screened. In the next stage, the literature that was considered potentially relevant to this study’s topic was assessed for eligibility and fully read. All processes were conducted independently by two randomly assigned reviewers, and any conflicts of inclusion were resolved through a team consensus.

The Mixed Methods Quality Appraisal Tool (MMAT) and the Authority, Accuracy, Coverage, Objectivity, Date and Significance (AACODS) checklist were used to explore the risk of bias at the individual study level. The articles, whether published in peer-reviewed journals or in progress as preprints, were assessed using the MMAT version 2018. The MMAT is a methodological quality appraisal tool designed for systematic reviews encompassing studies with various types of study designs [14]. One point was given for each of the criteria met and the maximum possible score for each article was seven. The AACODS checklist was used for grey literature as the MMAT methodology is not fit for grey literature [15]. A point was given for each of the six criteria and an overall score was calculated for each literature. Similarly, two researchers independently identified the study designs and scored the literature. Any conflicts were discussed and adjusted.

Key information from eligible literature was extracted and summarized into a predetermined template, consisting of categories such as: literature type, study design, study setting, study population, interventions, outcomes, barriers to malaria control, and strategies. In this study, “barriers to malaria control” were defined as obstacles that restrain interventions for malaria prevention, diagnosis, and treatment that are planned or implemented during the COVID-19 pandemic in LMICs. Researchers extracted barriers from selected studies only when the barriers were identified by the literature under review, were explicitly mentioned and identified by the authors, all the while considering the context, analysis, and results of each study. The barrier extraction process excluded indirectly induced barriers that referred to other literature. The extracted barriers were thoroughly cross-checked and categorized by two independent reviewers. Disagreements were resolved through team discussion.

The study categorized the identified barriers to malaria control based on the analytical framework developed by Jacobs et al. [13] for assessing barriers to health services. The framework was built upon the study by Ensor & Cooper, which assessed barriers while taking into account the supply and demand sides as well as the four dimensions of Peters et al. [16, 17]: accessibility, affordability, availability, and acceptability. The descriptions of the four dimensions by Peters et al. [17] were modified for this study to better fit the context of malaria control during the pandemic. The strategies identified from the previous literature were also categorized using the same framework. The categorized barriers and strategies were divided into two subcategories: supply and demand sides. In addition, the strategies were further stratified into short-term, mid-term, and long-term based on the time by which the goals are likely to be achieved. In the subsequent analysis, short-term strategies are defined as “immediate responses which take place within days to weeks after disruptions.” Long-term responses are defined as “those that go on for years after disruptions.” Mid-term strategies are defined as “responses that take place at any timeframe between short- term and long-term.”

The first dimension, geographical accessibility, was a significant factor. Inability to physically move from one place to another greatly affected malaria control. Travel restriction served as a critical barrier for both supply and demand sides (Table 2). In order to stop the spread of the coronavirus, many governments-imposed lockdown measures, which led to health services disruptions. A total of 14 studies reported travel restrictions as part of lockdown measures as a barrier of malaria service provision or uptake (A1, A3, A4, A5, A8, A10, A11, A12, A13, A16, A19, A20, A24, A28).

Lack of transportation was another challenge to malaria control for both supply and demand sides (A9, A10, A19, A22, A25). For example, in Rwanda, measures to curb the impact of the COVID-19 pandemic limited the availability of transportation, resulting in delays in delivery and utilization of malaria service (A9).

For improvements in geographic accessibility, strategies for supply side encompassed technical innovation in malaria interventions and approaches (A19, A25), allowing healthcare workers to travel during lockdown (A14), non-contact monitoring and management methods for distribution of insecticide-treated nets (ITNs) (A2, A15, A18, A19), and malaria diagnosis linked with COVID-19 screening (A1, A12). Strategies for demand side included mobilizing community health workers for malaria intervention (A1, A7, A9, A20, A21, A22), door-to-door distribution of ITNs (A2, A15, A19, A20, A22), and enhancements in community-based malaria control (A5, A9, A25).

COVID-19 affected the affordability dimension as well. Economic damage was the main barrier for people on the demand side as opportunities to earn money were taken away due to COVID-19 (A4, A24). Lockdown measures to curb coronavirus affected people’s socioeconomic statuses, creating financial barriers that discouraged them to seek health services (A9, A24). Financial barriers prevented patients from getting timely treatment. For example, transportation fees and visit fees for malaria services were a substantial burden to people in rural areas of Sierra Leone (A4).

Additionally, increased costs for malaria control made it difficult for healthcare professionals to provide care (A25, A27). Challenges in the global supply chain contributed to the increased price of raw materials for malaria commodities and freight (A25, A27).

Also, during the pandemic, funding for malaria control became inconsistent, and the healthcare workforce and resources initially allocated to malaria prevention efforts were re-allocated to COVID-19 (A13, A25). In Zimbabwe, malaria cases increased exponentially in 2020. Experts concluded that the increase was primarily due to the lack and inconsistency of funding allocated towards malaria control (A13). The strategies to improve affordability dimension are crucial to ensure more long-term approaches for pandemic preparedness. For both supply and demand sides, expanding investments in malaria intervention (A16) and continuous financial support from external partners (A2, A3, A18, A22) are suggested as strategies for the affordability dimension.

The COVID-19 pandemic most heavily affected availability. For this, many factors were considered. From the supply side, essential health services and malaria control interventions were disrupted (A8, A9, A11, A13, A17, A20, A22, A24, A26, A28). The World Health Organization (WHO)’s survey assessing the impact of the pandemic on essential health services in 2020 showed that almost half of the responses reported disruptions in malaria diagnosis and treatment during the pandemic (A24). A follow-up survey conducted in 2021 detailed the features of the disruptions. Disruptions were identified in providing diagnosis and treatment, distributing ITNs, indoor residual spraying (IRS), and seasonal malaria chemoprevention (SMC), making up between 30 and 40% of disruptions to the implementation of those services in malaria endemic countries (A26). Especially the widely implemented vector control activities, such as ITN campaign or long-lasting insecticidal nets (LLINs) and IRS distribution, were hindered (A9, A11, A13, A17, A20, A26, A28). Additionally, the COVID-19 lockdowns and travel restrictions are noted as reason of delays in many different countries, including but not limited to IRS and LLINs distribution in Rwanda (A9), ITN distribution during delivery of antenatal care (ANC) in Ghana (A11), IRS activities in Zimbabwe (A13), and canceled LLINs distribution campaign in Western Kenya (A17). The aforementioned cases indicate that the delay in malaria control is closely interlinked with the onset of the pandemic. Limited access to and delivery of antenatal care interrupted the routine provision of IPTp (Intermittent preventive treatment of pregnancy) to the women in the Northern region of Ghana, resulting in the decline of malaria patients in March and April 2020 (A11). The trend bounced back after lifting movement restrictions. The delay in hiring and training the workforce (A13) and closure of health facilities (A12, A16, A24) are other barriers that negatively affected malaria control efforts.

Specifically, supply chain issues were reported. Procuring commodities for malaria control and equipment such as mosquito nets, sprays, medicines were difficult (A6, A8, A9, A10, A11, A12, A13, A14, A15, A17, A19, A22, A24, A25, A27). The pandemic challenges the logistics of delivering malaria products between and within countries, resulting in delayed procurement of items for vector control such as ITN, LLIN, and IRS (A25). For example, in Uganda and the Democratic Republic of the Congo (DRC), the decrease in the number of patients who tested for malaria in 2020 is attributed to the disrupted global supply chain of malaria commodities that resulted in lack of local stock of malaria test kits (A10, A14). While Nigeria reported that limited procurement of malaria tests to healthcare providers was a barrier against visiting health facilities (A12), the Global Fund Results Report highlights the increased demand for COVID-19 tests and vector control products in the market disrupted the supply chain of malaria products (A22).

Amidst the pandemic, both resources and the healthcare workforce initially dedicated to malaria control was re-allocated to COVID-19 prevention measures (A2, A5, A6, A11, A16, A20, A25). Allocation of resources for COVID-19 control were prioritized, resulting in neglect in malaria control and its preventive measures such as essential tools (A6, A11, A16). Additionally, the delivery of health service was weakened due to limited personnel available. Many studies report unavailability of healthcare workers because many had fallen ill, died, were subject to quarantine, and/or engaged in COVID-19 strikes (A17, A18, A20, A22, A25).

Insufficient resources for healthcare workers became a barrier as well. The most notable barrier was a lack of personal protective equipment (PPE). PPEs such as masks were unavailable and insufficient and their delivery was delayed to healthcare workers at the frontline of the responses (A2, A9, A22, A25). The shortage of PPE sometimes resulted in healthcare professionals refusing to physically take care of patients (A9).

Among the general population, it was reported that the lack of information and knowledge regarding the two diseases, malaria and COVID-19, was a barrier to utilizing health services. Because patients were unaware of the serious symptoms and signs of infection, consultations were delayed (A6). One study noted how because of the shift in focus to the COVID-19 pandemic, people were less likely to get the information they needed on malaria (A9). In Gombe, DRC, for example, even though hospitals and health clinics remained open and functional, a lack of clear information on the lockdown transportation and activity policies hindered people from using health services (A10). Furthermore, lack of trustworthy health messages was a barrier when looking for health advisement (A1, A11, A13, A25). At the beginning of the COVID-19 pandemic, the media propagated “stay home” messages to help curb the spread of the coronavirus. This, however, worsened health conditions of people with malaria (A1, A11). COVID-19 and malaria share many similar symptoms like having a fever. And because the large bulk of the general population was unable to distinguish between the two, many were told to stay home (A11, A13, A25), negatively affecting malaria control and prevention efforts.

On the supply side, case management was heavily disrupted by the pandemic. Lack of management in medical records to keep track of patients and changes in medical practices and case management further negatively affected the already fragile health systems (A6, A8, A15). Also, as mentioned before, similar onset of symptoms between malaria and COVID-19 made it harder for the healthcare providers to distinguish between the two and make a correct prompt diagnosis (A14, A23, A29). In Uganda, the overlapping symptoms such as fever led to an increase of suspected cases and supply demand for malaria, resulting in overdiagnosis and overtreatment (A14). The literature indicates that the impact of COVID-19 on preventative measures. It is widely known that public campaigns to raise awareness of malaria play an important role. However, during the pandemic, campaigns, program promotion, awareness and marketing strategies were affected (A13).

As shown in Table 3, there are 17 strategies for the availability dimension that were either actually implemented or suggested from the selected documents. Notably, a majority of strategies for the availability dimension are recommended for the supply side and they include the following: maintaining essential healthcare services during a pandemic situation like the COVID-19 pandemic (A2, A6, A7, A8, A10, A14, A16, A24, A26), strengthening data and surveillance systems (A14, A21, A22, A25, A29), using PPE when conducting malaria intervention (A2, A7, A18, A20, A22), integrating malaria interventions with existing regular healthcare activities (A5, A23), implementing technical innovation in malaria interventions and approaches (A19, A25), and enhancing health workforce and malaria experts (A25). Further, some studies (A1, A5, A12, A23) suggested combining healthcare services (e.g., COVID-19 prevention measures) and malaria control. Another study (A4) recommended providing not only health services but also social services.

The three strategies recommended for the demand side are: mobilizing community health workers or malaria intervention (A1, A7, A9, A20, A21, A22), enhancing community-based health systems and building systematic resilience (A5, A9, A17, A20, A21, A22, A25), and conducting door-to-door distribution of ITNs (A2, A15, A19, A20, A22).

Acceptability refers to how people react to COVID-19 and malaria control measures. Fear of contracting COVID-19 was seen on both sides. While healthcare providers feared getting infected at the workplace, the general population feared getting infected upon their visit to healthcare facilities (A1, A5, A7, A8, A9, A10, A11, A12, A15, A16, A18, A20, A21, A23, A25, A28). In Sierra Leone and Myanmar, people were afraid of contracting the virus at health centers (A5, A18, A21). In Ghana, pregnant women were hesitant to utilize health facilities because they feared exposure to COVID-19 (A11). In Kinshasa, the use of treatment centers declined, and many studies attribute such a reduction to the fear of contracting COVID-19. The literature is prolific in documenting the stigmatization of health centers (A10). Consequently, many healthcare providers feared getting attacked due to COVID-19 stigmatization (A22).

Malaria campaigns are important when it comes to malaria prevention measures, but the community's engagement was low (A13, A23). In Nigeria, Burkina Faso, Chad and Zimbabwe, the community’s engagement in malaria campaigns was restricted due to COVID-19. For example, Ward et al. (2021), reported difficulty implementing door-to-door delivery of SMC (A23). Furthermore, lack of political will was one of the challenges of malaria elimination strategies (A13).

Adhering to COVID-19 hygiene measures seemed to be another challenge because community health workers hardly followed hygiene rules like thirty-second hand washing, safe distancing and thermal screening. According to a study conducted in three African countries—Nigeria, Burkina Faso and Chad—community distributors rarely followed the recommended thirty-second hand washing rule in Nigeria and Burkina Faso. Safe distancing and thermal screening were not explicitly practiced as recommended for infection prevention (A23).

Strategies for resolving the acceptability problems focused on increasing awareness and transmission of appropriate communication. For the supply side, the following strategies were identified: establishing guidelines for malaria intervention during COVID-19 (A3, A7, A9, A15, A18, A23, A27), applying trust, relevance, and connection management strategies for malaria control (A7) and continuing communication and monitoring (A3). For the demand side, disseminating correct information about COVID-19 and malaria (A5, A7, A9, A23), delivering information on malaria intervention using mobile technology and/or ICT (A2, A13) and utilizing social media for health education and promotion for community (A15, A23) are appropriate strategies. As acceptability issues are accounted for both supply and demand sides, the strategies, likewise, are evenly reported.

Additionally, there are six cross-cutting strategies reported throughout the studies that are worth noting for addressing barriers in all the dimensions (Table 3). All of them are applicable for both supply and demand sides: (1) continuous technical support from external partners and international cooperation (A2, A3, A18, A22, A28), (2) strong political commitment and interest from the government to support building resilient society from the pandemic (A2, A5, A28), (3) improved ownership, leadership and management at all governmental levels and sectors for active engagement (A12, A19, A25), (4) strategic partnerships across various sectors and effective coordination (A2, A7), (5) cross-border collaboration (A19), and (6) rapid problem-solving culture for efficient decision-making process (A2).

Moreover, the strategies are divided into three phases (i.e., short-term, mid-term, and long-term) based on the time it takes for the goals to be achieved (Fig. 2). Among the four dimensions, geographic availability and acceptability are more geared towards short-term, focusing on instant response to COVID-19. Availability dimension requires both long-term and short-term strategies simultaneously. Short-term strategies alone could help overcome current barriers; however, they are ultimately helpful for health system strengthening. As for the affordability dimension, strategies appear to be lacking and inconclusive.

In order for the strategies to work effectively, financial resources and long-term planning are necessary. As there are many barriers reported for the availability dimension, there are many suggested strategies as well compared to other dimensions. Several dimensions in blue are helpful for both geographic accessibility and availability and they can be interchangeably used.