Impact of the COVID-19 pandemic on the malaria burden in northern Ghana: Analysis of routine surveillance data

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The COVID-19 pandemic and its collateral damage severely impact 19 health systems globally and risk to worsen the malaria situation in endemic countries. Malaria 20 is a leading cause of morbidity and mortality in Ghana. This study aims to analyze routine 21 surveillance data to assess possible effects on the malaria burden in the first year of the 22 COVID-19 pandemic in the Northern Region of Ghana. 23 . CC-BY 4.0 International licenseIt 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under a is the author/funder, who has granted medRxiv a license to display the preprint in perpetuity.(which was not certified by peer review)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint NOTE: This preprint reports new research that has not been certified by peer review and should not be used to guide clinical practice. 2

Monthly routine data from the District Health Information Management 24 System II (DHIMS2) of the Northern Region of Ghana were analyzed. Overall outpatient 25 department visits and malaria incidence rates from the years 2015 to 2019 were compared to 26 the corresponding data of the year 2020. 27

Compared to the corresponding periods of the years 2015 to 2019, overall 28 visits and malaria incidence in pediatric and adult outpatient departments in northern Ghana 29 decreased in March and April 2020, when major movement and social restrictions were 30 implemented in response to the pandemic. Incidence slightly rebounded afterwards in 2020 31 but stayed below the average of the previous years. Data from inpatient departments showed 32 a similar but more pronounced trend when compared to outpatient departments. In pregnant 33 women, however, malaria incidence in outpatient departments increased after the first 34 COVID-19 wave. 35

The findings from this study show that the COVID-19 pandemic affects 36 the malaria burden in health facilities of Ghana, with declines in in- and outpatient rates. 37 Pregnant women may experience reduced access to intermittent preventive malaria treatment 38 and insecticide treated nets, resulting in subsequent higher malaria morbidity. Further data 39 from other African countries, particularly on community-based studies, are needed to fully 40 determine the impact of the pandemic on the malaria situation. 41 42

43 COVID-19, pandemic, malaria, sub-Saharan Africa, Ghana, Northern Region, health 44 information system, surveillance, morbidity, routine data 45 46

47 . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 3 Malaria remains one of the leading causes of morbidity and mortality in sub-Saharan 48 Africa (SSA). It is responsible for nearly one quarter of all under five childhood deaths in this 49 region (1, 2). 50 The global spread of the coronavirus disease 2019 (COVID-19) was declared a Public 51 Health Emergency of International Concern, which is the highest level of alarm, at the end of 52 January 2020 (3). Many African governments responded rapidly to this threat by 53 implementing control measures even before first cases were detected in their countries, 54 comprising border closures, movement restrictions, social distancing and school closures (4). 55 By November 2021, there were nearly 6.2 million COVID-19 cases reported from the WHO 56 African Region, with about 152,000 deaths, mostly from the southern and northern rims of 57 the continent (5). In the global context, SSA accounts for only about 2.5% and 3% of the 58 overall reported COVID-19 morbidity and mortality, respectively, while it is home to 17% of 59 the global population (6-8). This may be explained by factors such as a younger population, 60 hotter climate, interferences with other infectious diseases, and especially lack of diagnostics 61 and underreporting (9, 10). Ghana is among the countries with the highest reported COVID-62 19 cases (130,920) and deaths (1,209) in western and central SSA, as of November 2021 (8). 63 COVID-19 vaccinations started in February 2021 but coverage in Ghana is still low with only 64 2.7% of the population fully vaccinated by November 2021 (11). 65 The socio-economic disruptions associated with the disease and the preventive 66 measures present huge challenges for health systems and whole societies, especially in low- 67 and middle income countries (12). In the highly malaria-endemic African countries, the 68 progress made in malaria control during the last two decades is feared to be reversed by the 69 side effects of the COVID-19 pandemic (13, 14). 70 This study aims to compare the malaria burden in the Northern Region of Ghana in 71 the first year of the pandemic to previous years to assess whether a reversal indeed occurred. 72 . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 4 73

74 Study area 75 Ghana, with its population of about 31 million, lies in western SSA and has a 76 relatively well functioning health care system (15, 16). Ghana is divided into 16 77 administrative regions. The Northern Region, with its capital city Tamale, had a population of 78 1.9 million in 2020. The socio-economic situation of the Northern Region is below the 79 national average of the country and the region has the highest rate of mortality under the age 80 of five years (17). The rainy season in northern Ghana, which is usually associated with an 81 increase in the malaria incidence, lasts from May to October (18). 82 Malaria is highly endemic in Ghana; the country accounts for 2% of the global 83 malaria morbidity and 3% of the malaria mortality (19, 20). In 2020, malaria was the cause of 84 34% of all outpatient attendances (21). Treatment expenditures for common diseases like 85 malaria are covered by a health insurance (22). 86 The first two confirmed COVID-19 cases in Ghana were seen on March 12, 2020; two 87 days later, all public gatherings were banned. Travel restrictions and border closures were 88 implemented on March 22, 2020 and the country’s major cities were placed under partial 89 lockdown soon after. Schools were partially reopened on June 21, 2020 and borders were 90 reopened to international airlines on September 21, 2020 (23). In Ghana, effects of the 91 COVID-19 pandemic on malaria control interventions concerned the country’s stock of 92 artemisinin-based combination therapies (ACT), the functioning of its insecticide-treated 93 mosquito net (ITN) routine distribution, and the overall access to primary health care services 94 and facilities (24). 95 96 Study design and data 97 . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 5 This retrospective observational study uses monthly malaria morbidity data on the 98 overall number of outpatients (interpreted as less severe cases) and inpatients (more severe 99 cases). Additionally, all outpatient visits (including non-malaria related visits) are analyzed. 100 Cases were extracted from the district health information management system II (DHIMS2) 101 on demographic and health parameters of northern Ghana from January 1, 2015, to December 102 31, 2020. This system was implemented in 2007 with an update in 2012 and has improved the 103 data quality and completeness since (25). 104 Malaria diagnosis was based either on the results of rapid diagnostic tests or microscopy. 105 Mid-year population estimates of the Northern Region of Ghana were also provided through 106 the DHIMS2. 107 108 Analysis 109 The data have been processed with Microsoft Excel Version 16.52 and analyzed with 110 Stata IC Version 16 (Statacorp, College Station, TX, USA). We have calculated and plotted 111 monthly incidence rates of all outpatient visits and confirmed malaria cases for the year 2020 112 and as a comparison for the years 2015 to 2019 separately and combined using population 113 figures of the Northern Region of Ghana. Additionally, we calculated incidence rate ratios 114 with 95% confidence intervals (95% CI) comparing quarterly incidence rates of 2020 versus 115 the combined rates of 2015 to 2019. The data allowed analyzing children under five years and 116 pregnant women separately using the fraction of the under-five population (14% of the 117 population) and the fraction of women between 15 and 45 years (23% of the population) as 118 estimates of the respective population denominators (26). 119 120

121 Number Percentage (%) outpatient department visits . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 6 All 5,804,910 100 Malaria confirmed 2,278,296 39 Malaria confirmed among children <5 years 454,779 20 Malaria confirmed among pregnant women 46,693 2 hospital-admitted patients Malaria confirmed 295,465 100 Malaria confirmed among children <5 years 165,313 56 mean mid-year population Total population 1,842,701 100 Children <5 years* 257,978 14 Women aged 15 to 45* 423,821 23 Table 1: Description of the dataset 122 123 Table 1 presents a brief description of the dataset. Altogether 5.8 million outpatient 124 department visits were reported between 2015 and 2020; 39% of those included a malaria 125 diagnosis. Of all confirmed malaria cases, 20% were children under the age of five years and 126 2% were pregnant women. 295,465 patients were hospitalized with diagnosed malaria, 56% 127 of those were children under the age of five years. The mean population of the years from 128 2015 to 2020 was 1,842,701 with 14% of children under the age of five years and 23% of 129 women between the age of 15 and 45 considered as of possible childbearing age. 130 . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 7 131 Figure 1: Reported monthly incidence rates per 100,000 of the Northern Region, Ghana for 132 the years 2015 to 2020 133 134 Figure 1 presents the incidence rates of the different outcomes reported in the 135 Northern Region of Ghana for the years between 2015 and 2020 separately as well as a 136 combined rate for the period 2015 to 2019. All visits of the outpatient department (OPD) (see 137 Figure 1a), including also non-malaria patients, have experienced a major decline in 138 . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 8 March/April 2020, the months where COVID-19 control measures were implemented in the 139 country, and stayed low during the following months. After a further decrease in September 140 2020, the numbers increased again in October 2020 to the levels observed in previous years. 141 This trend is similar but not as pronounced in the general malaria OPD visits (Figure 1b). In 142 children under the age of five years, the decline in accessing OPD malaria health care is 143 stronger, especially from June to September 2020 (Figure 1 c). In pregnant women, however, 144 a different trend with an earlier increase, starting in June and exceeding previous year’s 145 levels, can be observed (Figure 1d). The 2020 numbers of the hospitally admitted malaria 146 patients stayed below the previous standards from March to October 2020 (Figure 1e); and in 147 accordance with the OPD figures, this trend is more pronounced in the children under five 148 years population (Figure 1f). 149 150 Incidence rate ratios (IRR) depicting quarterly measures comparing the rates of 2020 151 to the combined rate of the years 2015 to 2019 are presented in table 2. General OPD visits 152 were reduced in the 2 nd and 3 rd quarters of 2020 compared to the previous years (IRR 3 rd 153 quarter 0.736) with a return to previous standards at the end of the year. The same applies to 154 the overall malaria cases (IRR 0.742 in the 3 rd quarter) but with increases in the 4 th quarter 155 (IRR 1.265). Ambulatory malaria cases in children under five experienced stronger 156 reductions compared to previous years with an IRR 0.566 in the 3 rd quarter of 2020. These 157 evolutions are not mirrored by the population of pregnant women with malaria infections, 158 where no major reductions were observed during the first quarters of 2020 compared to 159 previous years but with an earlier increase (IRR 1.481 in the 4 th quarter). The situation is 160 slightly different in malaria infected patients admitted to the hospital. The reductions in the 161 2nd and 3 rd quarters of 2020 are more pronounced (IRR 0.548 for all ages in the 2 nd quarter) 162 and the numbers do not fully recover at the end of the year. Again, as for the outpatient 163 . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 9 population, this trend is more pronounced in children under five years of age (IRR 0.465 in 164 the 2nd quarter). 165 166 Outcome IRR (95% CI) 1st Quarter IRR (95% CI) 2nd Quarter IRR (95% CI) 3rd Quarter IRR (95% CI) 4th Quarter outpatient department visits All 0.930 (0.925-0.934) 0.800 (0.796-0.804) 0.736 (0.732-0.739) 1.026 (1.022-1.030) Malaria 1.035 (1.026-1.044) 0.899 (0.892-0.907) 0.742 (0.737-0.746) 1.265 (1.258-1.272) Malaria children <5 years 0.956 (0.937-0.974) 0.806 (0.790-0.823) 0.566 (0.557-0.575) 1.190 (1.176-1.206) Malaria pregnant women 0.865 (0.815-0.918) 0.957 (0.905-1.011) 1.136 (1.091-1.182) 1.481 (1.424-1.540) hospital-admitted patients Malaria 0.799 (0.780-0.817) 0.548 (0.531-0.565) 0.574 (0.563-0.586) 0.946 (0.930-0.962) Malaria children <5 years 0.749 (0.726-0.773) 0.465 (0.445-0.486) 0.435 (0.422-0.448) 0.820 (0.800-0.839) Table 2: Quarterly incidence rate ratios (IRR) with 95% confidence intervals (95% CI) 167 comparing the incidence rates of 2020 with the combined incidence rates of the years 2015 to 168 2019 169 170

171 Since the beginning of the COVID-19 pandemic, several modelling studies have predicted 172 negative collateral effects on the malaria burden in SSA, considering especially disrupted 173 ITN campaigns and a limited access to antimalarial drugs. The study team of Weiss et al. 174 created nine scenarios for different reductions of ITN coverage and access to antimalarial 175 medication as well as regarding effects on malaria morbidity and mortality. As no ITN mass 176 campaigns were scheduled for 2020 in Ghana, the worst-case scenario would have been a 177 decline in access to antimalarials by 75% resulting in an increase of malaria morbidity and 178 mortality by 12.6% and 54.6%, respectively (13). Overall, the predicted public health 179 relevant effects of the COVID-19 pandemic on malaria include shared clinical disease 180 manifestations leading to diagnostical challenges, disruptions of the availability of curative 181 and preventive malaria commodities, significant effects on malaria programs, and in 182 particular reduced access to malaria health services and health facilities in general (27). 183 . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 10 In this study, we observed a slight but significant decline in malaria incidence during 184 the 2nd and 3rd quarter of 2020 (April to September), and only a rebound to the average levels 185 of previous years at the end of 2020. This pattern was visible in both, outpatient and inpatient 186 settings, but more pronounced in the hospitalized population. The same applies to children 187 and adults, where the reductions were also observed in both groups, but were more marked in 188 children under five years of age. The marked decline in March/April 2020 can be explained 189 by the extensive restrictions of movement and gathering and early stay-at-home advices for 190 COVID-19-like symptoms unless these get severe. Such measures have likely supported the 191 hesitancy to visit health facilities during the pandemic, which in turn poses a major risk for 192 developing severe malaria (12, 28). The decline observed in March/April 2020 was even 193 more remarkable in inpatients. This does not support our initial hypothesis, that in cases of 194 more severe malaria manifestation, patients were still brought to health facilities and 195 hospitalized, despite the pandemic. The findings from this analysis support the hypothesis, 196 that the reported malaria burden in health facilities will shrink due to the effects of the 197 COVID-19 pandemic in highly malaria-endemic countries (Heuschen et al. 2021). They also 198 support results of the WHO World Malaria Report (12), and they agree with results of similar 199 studies from other SSA countries classified as highly endemic for malaria, such as Sierra 200 Leone, Uganda and the Democratic Republic of the Congo (29-32). 201 The distinct decrease of OPD visits in the health facilities of northern Ghana in 202 September 2020 may also be explained by unusual heavy floods that started mid-August and 203 could have further complicated the access to health services. Flooded land is a favorable 204 habitat for Anopheles mosquitos, the malaria vector, what could have led to the observed 205 increases of malaria incidence in October 2020. 206 Malaria incidence among pregnant women shows a different trend in northern Ghana. 207 After a decline in reported malaria cases in April 2020, malaria figures have rebounded 208 . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 11 rapidly in this population and reached even higher levels compared to previous years. The 209 most likely explanation of such an opposite trend would be the hesitancy of pregnant women 210 to visit health facilities. This is probably due to the fear of getting infected with COVID-19, 211 combined with initial disruptions of the provision of intermittent preventive treatment in 212 pregnancy (IPTp) to women in antenatal care (ANC) services as well as the disruption of 213 routine distribution of ITNs (33). The disrupted access to and delivery of ANC services is 214 likely to explain the malaria case trend in April. However, without IPTp and ITNs, more 215 women were at risk for malaria thereafter, which can explain the subsequent rise in malaria 216 cases over the following months. Also, many pregnant women probably have sought the 217 missed ANC after the initial movement restrictions were lifted with subsequent malaria 218 diagnosis. 219 Ghana had already achieved high levels of ITN coverage, and no ITN mass campaign 220 was planned for 2020 (12). However, the routine distribution of ITNs, which is usually done 221 in health facilities during ANC sessions and in primary schools, needed to be adapted to the 222 COVID-19 measures, which included school closure from March 2020 until January 2021 223 (34, 35). Also the seasonal malaria chemoprevention intervention for children and the annual 224 indoor residual spraying of insecticides, which both require physical contact between the 225 health workers and the community, needed to be modified (36, 37). As another consequence 226 of the COVID-19 pandemic, the provision of rapid diagnostic tests for malaria is fragile, 227 which may have led to under-diagnosis of cases (38). Finally, reports of hesitancy to visit 228 health facilities due to fear of getting infected with COVID-19 are still common (33, 38). 229 Last but not least, the malaria health care workers capacities were limited due to frequent 230 reassignments to the control of COVID-19, to stigmatization or absence following 231 quarantine, or to the development of COVID-19 disease or even death (13, 35, 39). 232 . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 12 This study has strengths and limitations. A strength of the study is that the data 233 represent a whole year of follow-up into the pandemic, which provides a more 234 comprehensive picture of the effects compared to the previous studies with much shorter 235 study periods. Limitations are that the surveillance system itself may have been affected by 236 the pandemic, with a bias in the reported numbers. Moreover, it is not clear if the quality of 237 surveillance data is fully comparable during the five years observed. Finally, much more 238 people with malaria symptoms may have switched to self-medication during the pandemic, 239 which may also have an albeit unknown effect on the malaria figures. 240 241 In conclusion, this study shows that the COVID-19 pandemic has been accompanied 242 by a reduced malaria incidence in northern Ghana’s health facilities. Further data from other 243 African countries and in particular data from community-based studies are needed to fully 244 judge the impact of the pandemic on the global malaria situation. 245 246 Declarations 247 Ethics approval and consent to participate 248 No ethical approval and consent to participate was required as only secondary data 249 have been used. 250 251 Consent for publication 252 No consent for publication was required (only secondary data used). 253 254 Availability of data and material 255 The datasets used and/or analyzed in this study are available from the corresponding 256 author on reasonable request. 257 . CC-BY 4.0 International licenseIt 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)preprint The copyright holder for thisthis version posted November 29, 2021. ; https://doi.org/10.1101/2021.11.29.21266976doi: medRxiv preprint 13 258 Competing interests 259 The authors declare that they have no competing interests. 260 261 Funding 262 Anna-Katharina Heuschen acknowledges the support by the Else Kröner-Fresenius-263 Stiftung within the Heidelberg Graduate School of Global Health. 264 265 Authors' contributions 266 AAM and MNA were responsible for the data collection. AH, VW and OR performed 267 the data analysis. AH wrote the first draft under the supervision of OM, AAM and MNA 268 supported the data interpretation. All authors read, reviewed and approved the final 269 manuscript. 270 271

272 We acknowledge financial support by the Else Kröner-Fresenius-Stiftung within the 273 Heidelberg Graduate School of Global Health, by Deutsche Forschungsgemeinschaft within 274 the funding programme Open Access Publishing, by the Baden-Württemberg Ministry of 275 Science, Research and the Arts and by Ruprecht-Karls-Universität Heidelberg. 276 277

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