key: cord-0846201-e4lrr1d3
authors: Heuschen, A.-K.; Lu, G.; Razum, O.; Abdul-Mumin, A.; Sankoh, O.; Von Seidlein, L.; D'Alessandro, U.
title: Public health relevant consequences of the COVID-19 pandemic on malaria in sub-Saharan Africa: A scoping review
date: 2021-06-21
journal: nan
DOI: 10.1101/2021.06.17.21258914
sha: 72254f86f0f95efa920eac5ed1466fb96dbe49e6
doc_id: 846201
cord_uid: e4lrr1d3

Background: The COVID-19 pandemic has resulted in unprecedented challenges to health systems worldwide, including the control of non-COVID-19 diseases. Malaria cases and deaths may increase due to the direct and indirect effects of the pandemic in malaria endemic countries, particularly in sub-Saharan Africa (SSA). Objectives: This scoping review aims to summarize information on public health relevant effects of the COVID-19 pandemic on the malaria situation in SSA. Methods: Review of publications and manuscripts on preprint servers, in peer-reviewed journals and in grey literature documents from December 1, 2019, to June 9, 2021. A structured search was conducted on different databases using predefined eligibility criteria for the selection of articles. Results: A total of 51 papers have been included in the analysis. Modeling papers have predicted a significant increase in malaria cases and malaria deaths in SSA due to the effects of the COVID-19 pandemic. Many papers provided potential explanations for expected COVID-19 effects on the malaria burden; these ranged from relevant diagnostic and clinical aspects, to reduced access to health care services, impaired availability of curative and preventive commodities and medications, and effects on malaria prevention campaigns. Compared to previous years, fewer country reports provided data on the actual number of malaria cases and deaths in 2020, with mixed results. While highly endemic countries reported evidence of decreased malaria cases in health facilities, low endemic countries reported an overall higher numbers of malaria cases and deaths in 2020. Conclusions: The findings from this review provide evidence for a significant but diverse impact of the COVID-19 pandemic on malaria in SSA. There is the need to further investigate the public health consequences of the Covid-19 pandemic on the malaria burden.

Grey literature was included using WHO database and Google Scholar. Three broad blocks of search terms were used: (1) COVID-19, (2) malaria, (3) sub-Saharan Africa. The detailed search strategy is available in appendix 1.

For the extracted findings two researcher (OM and AH) conducted independently the title screening, then the abstract screening and finally the full text review. The papers selected for full-text reading were assessed for eligibility; ineligible papers did not include information on public health relevant consequences of the COVID-19 pandemic on malaria in SSA. Inclusion decisions depended on whether the paper agreed to the PICo-framework and the formal eligibility criteria. Results were compared after each step for discussion and for reaching a consensus. For the analysis of the finally included papers, a data extraction table was constructed (appendix 2).

The following information was extracted from the papers: Authors, title, study place, study population, study design and outcome. Moreover, the papers were categorized by study type: modeling study, report (country report, general report, case report), review, opinion paper, and policy guideline. The information content was structured and analyzed around the following themes:

• Modeled impact of COVID-19 on malaria • Diagnostic and clinical aspects • Access to health care services • Availability of curative and preventive malaria commodities • Impact on malaria programs

• Epidemiologic data from countries . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted June 21, 2021. ; https://doi.org/10.1101/2021.06.17.21258914 doi: medRxiv preprint Based on these findings, a conceptual framework was created, with input from all co-authors (figure 1). Figure 2 visualizes the study selection process. The initial search produced 851 documents.

After removal of 203 duplicates, 648 documents underwent title and abstract screening. After exclusion of 535 documents which did not meet the inclusion criteria, 113 papers were included for full-text review. 9 papers were added from reference screening; 71 were excluded as they also did not meet the inclusion criteria. Thus, a total of 51 papers were reviewed (6 modeling studies, 10 country reports, 6 general reports, 1 case report, 9 review papers, 18 opinion papers, and 1 policy guideline). 

Five papers predicted the evolution of the malaria burden in SSA based on different potential scenarios. Considering primarily a reduced access to effective antimalarial treatment and reduced insecticide-treated mosquito net (ITN) distribution, Weiss et al. predicted is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review)

The copyright holder for this preprint this version posted June 21, 2021. ; https://doi.org/10.1101/2021.06.17.21258914 doi: medRxiv preprint deaths by 99% (from 386,000 to 769,000); the lower access to antimalarial treatment had a larger effect than reduced ITN distribution (21) . These estimates mirror those by the WHO, but the authors described the effects of nine different scenarios compared to the effects of three scenarios by Weiss et al. (22) . Comparable estimates were published by Sherrard-Smith et al.; for the scenario of complete interruption of ITN distribution and 50% decreased access to antimalarials they predicted malaria deaths would increase in SSA to 779,000 for the year 2020 (23) . A further analysis by WHO predicted up to 100,000 additional deaths in 2020 with a 50% lower access to antimalarials (17) . However, all these authors emphasized that the projected effects on malaria services and mortality are highly uncertain because these estimates are heavily dependent on how countries respond to the COVID-19 pandemic.

Regarding the relative burden of COVID-19 in Africa, one study concluded that the excess Disability-Adjusted Life Years (DALYs) lost by malaria due to COVID-19 may exceed those directly lost due to COVID-19 (24).

The clinical manifestations of COVID-19 and malaria largely overlap; fever, headache, joint pain, respiratory symptoms, and general weakness are frequently seen with both diseases (25-27). Thus, diagnosis based on symptoms alone can result in inadequate treatment, with potentially harmful consequences. Untreated malaria can be rapidly fatal and COVID-19 patients must be quarantined to interrupt community transmission (14, 28) . Despite increasing availability of rapid diagnostic tests (RDTs) for malaria in all endemic areas, presumptive diagnosis of malaria is still common in SSA, and the WHO Malaria Technical Guidelines adapted to COVID-19 confirm this situation (29, 30) . Initial information available for 2020 suggests major disruptions in malaria diagnosis and treatment due to COVID-19 (31, 32) .

. CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review)

The copyright holder for this preprint this version posted June 21, 2021. ; https://doi.org/10.1101/2021.06.17.21258914 doi: medRxiv preprint Human travel history is important for SARS-CoV-2 and malaria, as for both of them asymptomatic persons can spread and/or maintain transmission of the infectious agent (26) .

Moreover, malaria and SARS-CoV-2 co-infections may be associated with clinical disease modification, although data on this are limited (27, (33) (34) (35) .

While symptomatic malaria affects mainly children and younger age groups in endemic areas, COVID-19 affects all age groups but is more frequently symptomatic and severe with increasing age (33) . However, in areas of low malaria transmission, the age groups affected by the two diseases largely overlap (36) . RDTs are essential for malaria diagnosis in rural SSA and may also become important for COVID-19, as the PCR test capacity is very limited (32). However, the impact of rather low sensitivity and specificity of COVID-19 RDTs is still under intense discussion (27, 37) . Additional challenges for differential diagnosis is the increasing frequency of gene-mutated Plasmodium parasites, especially in the Horn of Africa, that escape detection by standard RDTs (36) .

The role of the artemisinin derivate and chloroquine (CQ) antimalarials in the COVID-19 pandemic is complex. Various artemisinin derivates, artemisinin-based combination therapies (ACTs) as well as CQ have been shown to be effective against SARS-CoV-1 and SARS-CoV-2 in vitro (38) (39) (40) (41) . However, such beneficial effect has not been confirmed by several clinical trials (42) (43) (44) (45) . The wide use of these treatments in highly malaria endemic countries has been suggested to be responsible for the reported low COVID-19 burden in SSA (35, 46) .

On the other hand, the increased usage of these drugs for COVID-19 prevention and treatment in some malaria endemic countries might have reduced malaria (25). A frequent off-label use of artemisinin-based drugs may also increase the likelihood of emerging drug resistance and thus threatens the most important of the remaining effective antimalarials (47) (48) (49) (50) .

. CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) (34, 49) . Stay-at-home advices for febrile diseases, especially at the beginning of the pandemic, enhanced such a behavior (17, 48) .

Indirect factors include reduced income during lockdowns due to inability to perform informal work, and subsequently reduced purchasing power (52) . The resulting increase in poverty leads to challenges for paying the costs for routine care, drugs, or transportation fees (51) . Lockdowns and movement restrictions further complicate access to health facilities and have also threatened the functioning of malaria surveillance systems (28, 48, 51) . Institutional mistrust and lack of valid information further reduced visits to health care facilities and reduced uptake of preventive measures; as an example, myths about the spread of COVID-19

via ITNs led to a reduced usage of this essential intervention in Sierra Leone (25).

. CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review) 1 1

Increased material costs, reluctance of producers to invest, travel restrictions, border closures, and lockdowns resulted in a lower availability of medical malaria products (26, 28, 47) . Lowand middle-income countries (LMICs) are disproportionately affected as they essentially rely on importation of these commodities (52) . Excessive use of antimalarials for COVID-19

prevention and treatment in some regions has led to shortages for their original purpose (17, 30) . Some international companies switched from the production of malaria products to COVID-19 products (47, 49, 51) . Difficult access to health facilities lowered the availability of essential drugs and increased their price, with subsequent increases in purchase and usage of sub-standard drugs and alternative medicines (28, (51) (52) (53) . In addition, PPE needed for the implementation of different malaria services (e.g. indoor residual spraying of insecticides, IRS) have become scarce and expensive on global markets (17, 54) .

The extent of the pandemic's impacts on malaria depends on the timing of its waves. The largest effects may occur if the COVID-19 transmission peaks and the planned malaria campaigns overlap (21, 23, 53, 55) . About three quarters of malaria-affected countries reported disruptions of malaria services and programs (17, 32, 48, 50, 53, (56) (57) (58) . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted June 21, 2021. ; https://doi.org/10.1101/2021.06.17.21258914 doi: medRxiv preprint Nevertheless, these challenges led to new approaches: Benin digitalized its ITN mass distribution campaign using a 'no touch' payment for campaign workers. The national strategy was changed from a fixed-point to a door-to-door-distribution procedure, which enabled health workers to provide additional community health education on COVID-19 and other aspects; other countries followed the Benin model and by the end of 2020, 90% of all globally planned malaria prevention campaigns had been implemented (17, 28, 54, 57, 59) .

Compared to previous years, fewer papers provided data from African countries on the actual number of malaria cases and deaths in 2020. A small study from Sierra Leone reported a significant lower number of malaria outpatient visits in one health facility during the March/April 2020 lockdown period as compared to the same period in 2019 (29) . In addition, preliminary national data from Uganda point to a reduction of malaria cases seen in health facilities during the first quarter of 2020 compared to the same period in 2019 (61) . Another study from Uganda reported a 54% decrease in visits for malaria treatment of febrile children;

visits for antenatal care declined by 26%, restricting the delivery of intermittent preventive malaria treatment in pregnancy (IPTp) (62) . In the Democratic Republic of the Congo (DRC), lower attendance to health facilities for malaria treatment ranged from 20% to 90%, depending on local lockdown measures (63) . In contrast, a study from one rural district in Zimbabwe reported a large increase in malaria cases in 2020 compared to previous years, which was associated with delayed IRS in 2020 (50) . These findings were confirmed by national data from Zimbabwe, which compared the number of malaria cases and deaths in 2020 with those in previous years; in 2020, there was a large excess of reported malaria cases and deaths (27, 64) . Moreover, national data from Zambia showed an increase of malaria . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted June 21, 2021. ; https://doi.org/10.1101/2021.06.17.21258914 doi: medRxiv preprint cases between August 2019, and June 2020; however, no data from control periods were provided (65) .

The COVID-19 pandemic has a massive impact on nearly all countries across the world.

While the initial spread of SARS-CoV-2 to Africa has been slow and the COVID-19 burden appears to be much lower than in other continents, the pandemic carries a high potential to negatively affect the control of other diseases such as malaria (7). Both malaria and COVID-19 affect disproportionally the low socio-economic classes (28, 32, 66) . It is possible that the COVID-19 pandemic and its indirect effects, including the measures to contain it, may produce collateral damages similar to those seen six years ago during the West African Ebola epidemic, i.e. sharp increase of malaria deaths which finally exceeded the direct Ebola mortality (17, 35, 67) . Thus, understanding how the COVID-19 pandemic affects malaria control measures is of extreme importance for SSA (17, 59) .

Accelerated malaria control efforts since the early 21 st century have significantly reduced the malaria burden in Africa and worldwide (17) . Control strategies include ITN and IRS interventions, early diagnosis and rapid treatment with ACT, and intermittent preventive treatment for infants, children and pregnant women (14) . However, the rate of reduction in malaria morbidity and mortality in SSA has recently stalled, and the initial overall positive trend could be seriously reversed due to the effects of the COVID-19 pandemic as shown in several modelling studies (17, (21) (22) (23) .

In accordance with our conceptual framework, four major themes likely play a major role for the effects of the COVID-19 pandemic on malaria in SSA: (1) Diagnostic and clinical aspects;

(2) Access to health care services; (3) Availability of curative and preventive malaria . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted June 21, 2021. ; https://doi.org/10.1101/2021.06.17.21258914 doi: medRxiv preprint commodities; and (4) Impact on malaria prevention programs. While diagnostic and clinical aspects will play an obvious role due to the overlapping symptoms of both diseases (27, 68, 69) , therapeutic aspects related to initial misperceptions regarding the efficacy of certain antimalarials against COVID-19 may have been overemphasized (25, 35) . Co-infection with malaria may complicate COVID-19, while immunomodulation caused by previous malaria exposure may result in less severe COVID-19, as previously also shown in other respiratory diseases (70) (71) (72) (73) . Reduced access to health care services due to direct and indirect effects of the pandemic has a negative impact on access to antimalarial treatment, thus it would likely have a major effect on the malaria burden in endemic countries (17, 49, 53) . This will be compounded by the clear negative impact of the pandemic on global supply chains for curative and preventive malaria commodities (47, 52) . The consequences of the pandemic for preventive malaria control programs have been much emphasized by many of the reviewed papers and particularly in modeling papers. However, as an effect of such early warnings, country programs and funding for malaria have probably adapted rapidly to the pandemic as early as 2020, which may have reduced the modeled impact (28, 59) .

Until June 2021, only a few reports provided actual epidemiological data on malaria in SSA during the first wave of the pandemic in 2020. These reports showed that the number of reported malaria cases in highly endemic countries (e.g. Sierra Leone, Uganda, DRC) was much lower than expected (29, (61) (62) (63) , while the number of reported malaria cases in countries of low endemicity (e.g. Zimbabwe, Zambia) was higher than in previous years (27, 29, 64, 65) . Possibly lower access to health care services in combination with impaired malaria surveillance systems may have led to a lower number of reported malaria cases and deaths in these selected highly endemic countries, while in the two low endemic southern SSA countries disruption of malaria control activities within relatively well-functioning health systems, including surveillance activities, may have resulted in a higher number of reported . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted June 21, 2021. ; https://doi.org/10.1101/2021.06.17.21258914 doi: medRxiv preprint malaria cases and deaths. More information from other African endemic countries is needed to fully assess such developments (59, 74) . As the COVID-19 pandemic is far from being under control in most LMICs as new and more infectious SARS-CoV-2 variants are emerging, and as SSA countries have limited access to COVID-19 vaccines, dramatic increases of the malaria burden may occur (59, 75, 76) . Although the findings of existing modeling studies are already alarming, the final impact of the pandemic on the malaria burden could be even more devasting (21, 51) . Better education, sensitization and de-stigmatization of both diseases is essential, including emphasis on early care seeking behaviour, which needs also more community participation (25, 29) . Community health workers should be encouraged to treat all uncomplicated malaria cases in the community and to refer to health facilities only severe cases (51, 77) . As 2020 was a year with many planned malaria prevention campaigns, the negative effects of disrupted programs would probably last for some years (21, 23) . Fortunately, the international community, including the WHO, acted fast to counteract such developments (17) . However, there is the need for more support for SSA countries from the international community and from high income countries (32). Malaria, one of Africa's deadliest diseases which disproportionally affects the most vulnerable population groups, must be kept under control (16, 34, 59) .

The findings from this review provide evidence for a significant but diverse impact of the COVID-19 pandemic on the malaria burden in SSA. Only results of further studies will enable a full understanding of these developments and its public health consequences. In the meantime, SSA countries need more support from the international community including the urgent delivery of COVID-19 vaccines for high-risk groups.

. CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted June 21, 2021. 

The datasets used and/or analysed during the current study are available from the corresponding author on reasonable request.

The authors declare that they have no competing interests. 

AH and OM performed the systematic search and screening. AH wrote the first draft, GL did the methodological foundation, OR drafted the conceptual framework; all authors read, reviewed and approved the final manuscript.

Appendix . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted June 21, 2021. . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted June 21, 2021. Chanda-COVID- 19 and Africa General Opinion Health system . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.

The copyright holder for this preprint this version posted June 21, 2021. is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. . CC-BY 4.0 International license It is made available under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity. (which was not certified by peer review)

The copyright holder for this preprint this version posted June 21, 2021. ; https://doi.org/10.1101/2021.06.17.21258914 doi: medRxiv preprint

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