A Protracted Malaria Outbreak in Upper Muzarabani, Centenary District, Zimbabwe, 2023

Chiboyiwa Nathan^1,&, Kavenga Fungai Nyarai², Shambira Gerald¹, Gombe Notion Tafara³, Mandozana Gibson¹, Tshimanga Mufuta¹

 

¹University of Zimbabwe, Department of Global Public Health and Family Medicine, Harare, Zimbabwe, ²National TB and Leprosy Control Unit, Ministry of Health and Child Care, Harare, Zimbabwe, ³African Field Epidemiology Network, Harare, Zimbabwe

 

 

^&Corresponding author
Chiboyiwa Nathan, University of Zimbabwe, Department of Global Public Health and Family Medicine, Harare, Zimbabwe.

 

 

 

 

Globally, there were an estimated 247 million malaria cases in 2021 in 84 malaria endemic countries, an increase from 245 million cases in 2020, with the increase coming from countries in the WHO African Region [1]. Malaria case incidence (i.e. cases per 1000 population at risk) although significantly decreasing over the past two decades from 82 in 2000 to 57 in 2019, still remains high with the estimate incidence at 59/1000 as at 2021 [1]. Although malaria mortality has steadily declined over the past 20 years, it still remains high with an estimate of 625 000 malaria deaths recorded in 2021. The African region bears the greatest burden of malaria, with an estimated 234 million cases recorded in 2021, accounting for about 95% of global cases [1-2].

 

Zimbabwe has significantly progressed towards malaria elimination, with 30 districts transitioning from control to pre-elimination phase. Zimbabwe National Malaria Control Programme and Roll Back Malaria Programme have achieved major successes in combating the diseases over the last 13 years, leading to the focus reorientation from malaria control to elimination [3-4].The National Malaria Control Program data indicate that the malaria incidence has significantly decreased from 58 cases per 1000 population in 2009 to 32/1000 population in 2020 and further down to 9/1000 as at 2022 [5].

 

Centenary District, one of the seven districts in Mashonaland Central is among the high and perennial malaria risk districts in Zimbabwe with a malaria annual parasite incidence (API) still above the 5/1000 target national control goal [5-6]. Upper Muzarabani wards in Centenary District however have had relatively low malaria API over the past 5 years compared to lower Muzarabani. Upper Muzarabani has been implementing specific control strategies for areas with a malaria API between 2- 4/1000 population which include distribution and use of Long Lasting Insecticide treated nets (LLINS), intensified surveillance, health education and health promotion.

 

During week one of 2023, David Nelson Clinic (DNC), serving upper Muzarabani attended to a total of 84 patients presenting with symptoms consistent with malaria mainly fever, joint pains and general body weakness. Diagnosis of malaria was made for the 84 cases using malaria antibody Rapid Diagnostic Test. The facility notified the District rapid response team of the surge in confirmed malaria cases which had surpassed week one threshold of 26 cases. The district rapid response was instituted leading to a facility visit for confirmation, situation analysis and response planning. Despite implementation of outbreak containment activities such as LLINs distribution, larviciding, intensified case surveillance and management as well as community engagement, the surge in malaria cases persisted pointing out to a protracted malaria outbreak.

 

We sought to determine human host, malaria vector and climate related factors associated with the protracted malaria outbreak in Upper Muzarabani, Centenary District, 2023. Specifically, we described the malaria outbreak in Upper Muzarabani in terms of person, place and time, determined patient related factors associated with the outbreak, described five-year annual rainfall trends and malaria cases from 2018 - 2022 and described malaria vector entomology in Upper Muzarabani.

 

 

Study setting

 

The study was conducted in David Nelson Clinic catchment area wards 14, 15, 22 and 26 in Upper Muzarabani, Centenary District. Centenary is one of the 7 districts in Mashonaland Central Province [7]. The district has an estimated population of 134 076 and has 14 health facilities, 29 wards and about 27,000 households, averaging 4.5 persons per household (6) (8).The district´s yearly average temperature is 23.24°C (73.83°F) and it is 0.51% higher than Zimbabwe´s averages [8]. The district has a longitude of -30.6976298 and a latitude of -16.0893164. About 97% of the Muzarabani population live in rural areas mainly depending economically on small-holder rain-fed agriculture, growing maize, small grains, cotton and tobacco which also expose them to late night outdoor exposure to vector mosquito bites. It has two main distinct geographical regions upper and lower Muzarabani with the latter more prone to disasters due to low resilience to economic, physical and social vulnerabilities mainly because of the low lying geographical location [9].

 

David Nelson Clinic serves the majority of the population in upper Muzarabani with an estimate catchment population of 26,591. The clinic is manned by four nurses who provide facility level diagnosis and clinical care for malaria patients. A microscopist is available at the clinic to provide further parasitological investigations at diagnosis and for patient follow up. Three environmental health technicians conduct ecological and entomological investigations and oversee malaria outbreak preparedness and response activities. Furthermore, the clinic has 32 community health workers who provide LLINs distribution and monitoring, malaria diagnosis, management of uncomplicated malaria and referral of severe malaria to the health facilities. Overall, the district hospital, St Alberts Mission serves as a referral facility for the clinic for management of severe malaria cases and has a doctor to patient ratio of 1:26,815.

 

Study Design

 

We conducted a 1:1 unmatched case control study of 156 respondents (78 cases and 78 controls) calculated using Fleiss formula and sampled using cluster sampling. We also conducted a trend analysis of available 5-year rainfall data and malaria case incidence data as a proxy to assess climatic variations and effect on malaria incidence in Upper Muzarabani. Furthermore, a desk review of 5-year entomological investigation data was conducted as part of the outbreak investigation to ascertain the prevailing vector bionomics in Upper Muzarabani.

 

Sample size

 

The sample size was calculated using the Stat Calc function of Epi Info™7, Fleiss formula with continuity correction based on a previous local study, assuming that sleeping under a net is a significant factor for malaria transmission with an odds ratio of 0,3 with 87,4% of controls having been exposed [10, 11]. A case-control study, with 95% Confidence interval, and 80% power was conducted. The calculated minimum sample size was 70 cases and 70 controls. Accounting for non-response rate of 10% a minimum of 78 cases and 78 controls was calculated. Using the facility malaria line list as the sampling frame, we conducted stratified sampling, classifying the cases into the 4 catchment population enumeration wards in Upper Muzarabani, David Nelson Clinic catchment (ward 14- Nyamanetsa, ward 15-Gatu, ward 22-Chaona and ward 26-Mutute) and randomly sampling 20 cases per each ward. Controls were sampled conveniently from neighbors of the cases.

 

We defined a case as a resident of Upper Muzarabani who presented with symptoms consistent with malaria and tested malaria positive on malaria rapid diagnostic test between week 1 and week 18 of 2023 whereas a control was a resident of Upper Muzarabani who did not experience symptoms of malaria during the same period.

 

Data collection and analysis

 

We collected data using interviewer administered questionnaires and retrospective review of entomology and rainfall data using questions and themes based on Zimbabwe Malaria Indicator Survey, 2016 (4).We described the outbreak in time, place and person using proportions, median and range for age distribution and outbreak attack rates defined as cases among 1000 persons at risk (# of cases/total population at risk), case fatality defined as proportion of malaria deaths among total malaria cases. We used Zimbabwe 2022 National Census data as reference population size to calculate malaria case incidence [7].We reviewed rainfall data captured in the local district Agricultural Research Extension paper-based register and the facility malaria case incidence captured in the District Health Information System 2 (DHIS2) to determine 5-year rainfall and malaria case trends represented by correlation coefficient R², with a correlation ≥0.7indicating high correlation. We further analysed entomological data based on the desk review of available 5-year entomological investigation reports to determine the prevailing vector bionomics.

 

Knowledge of malaria was based on standard questions on malaria transmission, signs and symptoms, complications and treatment adopted from the Malaria Indicator survey. Questions were scored to a total of 14 points. A score of 7-14 points was rated good whilst a score <7 was rated as poor knowledge. Vector bionomics data reviewed had the following indicators: predominant malaria vector species in the area, phenotypic and genotypic resistance profile of vector to vector control based on presence of single cytochrome P450 allele (CYP6P9a_R) of the cis-regulatory polymorphism that drives the overexpression of the gene in An. Funestus which in turn reduces the efficacy of pyrethroid insecticides especially on nets.

 

ArcGIS version 10.8.2 was used to describe the spatial distribution of the outbreak. Chi-square and Fishers test for equality of cases and controls was conducted using Epi Info™7.2.5.0. We conducted univariate, bivariate and backward stepwise multivariate logistic regression analysis with the outcome of interest being malaria case (yes/no) to determine human host related factors associated with contracting malaria expressed as adjusted odds ratios with 95% confidence intervals and 5% level of significance.

 

Mashonaland Central Provincial Ethics Committee approved the study (MC/IEC/06/2023). We obtained permission from Ministry of Health and Child Care Health Studies Office, Provincial Medical Director Mashonaland Central Province and District Medical Officer Centenary. We obtained written informed consent from study participants prior to data collection. Privacy and confidentiality were duly observed during the conduct of the study.

 

 

Outbreak description by time

 

The malaria outbreak in David Nelson clinic catchment wards persisted from week 1 to week 28 of 2023, peak cases being recorded in week 19 despite implementation of outbreak control strategies which include intensified community surveillance, community dialogues, and provision of LLINs through continuous net distribution. Cases gradually increased from week 1, by week 8 the clinic had reported 941 cases indicating a 10-fold increase in malaria cases from 82 cases in week 1. During week 9, targeted indoor residual spraying using Fludora Fusion (insecticide containing a pyrethroid-deltamethrin and a neonicotinoid -clothianidin) was conducted, however malaria cases remained above weekly thresholds until week 20 when a progressive decline in cases was noted. The progressive decline in cases was sustained till week 29 when the outbreak receded. The epicurve pattern resembled a continuous common source pattern (Figure 1).

 

Outbreak description by place

 

All the 4 catchment population enumeration wards in Upper Muzarabani, David Nelson Clinic catchment (ward 14- Nyamanetsa, ward 15-Gatu, ward 22-Chaona and ward 26-Mutute) recorded malaria case incidences above 20/1000 population during the outbreak period. Ward 14 (Nyamanetsa ward) was the most affected ward recording a case incidence of 361/1000 population, nearly 1 case per every household. Nyamanetsa ward is characterized by major farming activities and presence of many water bodies (upto 23 dams and rivers compared to 10 main water bodies in Chaona ward 22 and 1 waterbody in ward 15 Gatu (Figure 2).

 

Outbreak description by Person

 

A total of 2763 malaria case patients were recorded in Upper Muzarabani, David Nelson Clinic catchment wards between week 1 and week 26, an overall attack rate of 13.2% (2763/20 886 at risk population). The case fatality rate was 0.14% (4 deaths/2763 case patients). The majority of case patients (75.6%) were managed by community health workers with a quarter of patients managed at the health facility.

 

Case control study findings

 

A 1:1 unmatched case control study was conducted to determine individual factors associated with the malaria outbreak. A total of 78 cases and 78 controls of comparable sociodemographic characteristics were interviewed for the case control study. The majority of study respondents were females among them 44 (56.4%) cases and 36 (46.2%) controls (p=0.20). A total of 36 (50%) cases and 31 (43%) controls (p=0.4) were in the 21-30 years´ age group. The median age for cases was 35 years (Q1=23 Q3=44) whilst median age of controls was 34 years (Q1=21; Q3=45 Table 1).

 

Factors associated with contracting malaria in Upper Muzarabani, DNC 2023

 

Engaging in late night outdoor activities (aOR=3.86; 95% C.I 1.64-9.06; p<0.001), engaging in early morning outdoor activities (aOR=4.18; 95% C.I 1.61-10.83; p=0.003) and staying near a water body (aOR= 4.69; 95% CI 1.99-11.07; p<0.001) were independent individual risk factors associated with contracting malaria in Upper Muzarabani, David Nelson Clinic catchment. Availability of LLIN in all sleeping areas at household (aOR= 0.20; 95%CI 0.09-0.49; p <0.001) and wearing protective clothing when engaging in outdoor activities during peak mosquito biting times (AOR= 0.30; 95% CI 0.10-0.86; p = 0.020) were independent protective factors (Table 2).

 

Trend analysis of rainfall and malaria cases

 

A records review of rainfall trends available at Agritex (Agricultural Technical and Extension Services) over the past 5 years in Centenary district Upper Muzarabani indicated a positive trend in amount of rainfall received during the peak rainfall months November - January from 2018 -2023 season. The positive rainfall trends coincided with an increase in the number of malaria cases from 2018 - 2023 for the period week 1 - week 26 (R²= 0.78, Figure 3).

 

Entomological investigation findings

 

Review of records for Entomological investigation carried out in 2023 June noted the abundant presence of known vector mosquitoes with 51 out of 75 total mosquitoes (68%) collected being known malaria vector mosquitoes. The predominant malaria vector (primary vector) was noted to be Anopheles funestus ss (senso stricto) at 30 out of 51 vector mosquitoes and the presence of a secondary vector Anopheles polypalpis was also a key finding.

 

Furthermore, genetic insecticide resistance testing for the presence of cytochrome P450 allele CYP6P9a_R that drives overexpression of the gene associated with pyrethroids resistance was conducted. Out of the 30 malaria vectors samples tested, 8 mosquitoes (27%) had homozygous resistant (RR) gene, 16 (53%) had heterozygous gene while 6 mosquitoes (20%) expressed a pyrethroid susceptible gene.

 

 

The study sought to describe the protracted malaria outbreak in Upper Muzarabani and determine factors associated with the outbreak. Exposure to malaria vectors through engagement in early and late outdoor activities, increased rainfall providing optimal malaria vector breeding conditions and emerging vector adaptation to current vector control measures led to a protracted outbreak in Upper Muzarabani.

 

The timing of the outbreak coincided with peak tobacco farming season when most people involved in tobacco farming spend extended periods outdoors predisposing them to malaria vector mosquito bites. This was also highlighted with considerably more case patients being farmers compared to the controls. Typical of agro communities like Upper Muzarabani, particularly Nyamanetsa with many water bodies to sustain farming activities, malaria transmission is prevalent. This was evident in our study with Nyamanetsa ward reporting the highest case incidence. The findings concur with previous studies that indicated the increased risk of malaria epidemics in agro - communities [11-13] .

 

The increased rainfall patterns provided optimum breeding conditions for malaria vectors leading to a protracted outbreak. The surge in cases indicated presence of sufficient viable malaria vectors to result in increased malaria transmission. These findings highlight the increasingly realised impact of climate change on malaria epidemics [14]. The cases progressively declined from week 20 which coincided with the inception of winter season further indicating the seasonality of malaria transmission. Increase in breeding sites due to high rainfalls could have provided viable malaria vectors that led to the protracted outbreak. Persistent surge in malaria cases post increase in rainfall was also described in a study by Nsereko et al in Uganda 2020 [15].

 

Vector adaptation to current malaria control measures could have contributed to the protracted outbreak in Upper Muzarabani. Genetic pyrethroids resistance was high among sampled malaria vectors and yet the affected wards mainly implemented LLINs use as the key vector control measure. This might explain why malaria cases remained high above weekly thresholds even after implementing targeted indoor residual spraying since a pyrethroid containing insecticide was used. Vector adaptation to local malaria vector control measures has been described in other settings were a predominantly indoor feeding vector adapted to outdoor feeding following scale up of indoor vector control measures [16]. Relatedly in this study, wearing protective clothing whilst engaging in outdoor activities was protective against contracting malaria. This finding was also described in a previous local study. This justifies implementation of vector control strategies which target outdoor biting to complement the well implemented indoor vector control strategies [17].

 

The LLINs available in use in Upper Muzarabani were pyrethroid based and the insecticide used during targeted IRS contained a pyrethroid. Given that the entomological investigation report noted emerging pyrethroid resistant anopheles funestus vector, a possibility of a pyrethroid resistant vector driven outbreak cannot be ruled out. This provides additional evidence of the growing concern of pyrethroid resistant anopheles funestus driving persistent malaria outbreaks [17, 18]. The choice of other efficacious insecticides in the face of pyrethroid resistant vectors in farming communities like Upper Muzarabani is a challenge. The other common insecticide used in IRS in the country DDT (dichlorodiphenyltrichloroethane) could not be used to control the outbreak due to its regulated use in farming areas in this protracted outbreak [18].

 

The occurrence of an outbreak in a setting of high LLIN coverage may indicate that most bites could have been outdoors, out of reach of the current indoor focused vector control measures [19]. Alternatively the occurrence of an outbreak in a high LLIN coverage community could also signal that LLIN might not be utilized even though available at households. This finding was consistent with a previous local study [20]. Needless to say, availability of LLIN in all sleeping areas still showed significant protective effect highlighting the importance of LLINs as a vector control strategy for malaria prevention.

 

The majority of cases were managed in the community by community health workers. The surge in cases could have emanated from improved reporting and surveillance by CHWs. This could have contributed to the protracted outbreak picture as the previously set malaria thresholds were based on historical data which mainly comprised of facility reported cases and incomplete community health worker data. This highlights importance of strengthening community-based surveillance in program control of infectious diseases. However, concerns over poor quality of data collected by community health care workers have been highlighted in previous studies [21]. This could have also contributed to consistently high malaria cases reported during the outbreak period.

 

Limitations

 

Entomological investigation reports were not readily available hence no baseline data and past data to carry out a trend analysis over the past 5 years. We conducted a case-control study which is prone to recall bias. Adherence to control measures i.e proper and consistent use of LLINs among cases and controls could not be objectively assessed.

 

 

The protracted outbreak in Upper Muzarabani DNC was multifactorial. Engagement in extended outdoor activities during peak vector biting times, vector adaptation to current control measures and optimal vector breeding conditions from increased rainfall patterns were key factors associated with the outbreak. We recommended to the District Medical Officer setting up of a district One Health committee which can provide a platform for multi-sectoral engagement to effectively address climate change-related malaria risk factors as well as spearhead insecticide resistance surveillance in the district. Targetted risk communication and community engagement among at-risk populations like agro communities is key to ensuring communities remain aware of the continued malaria transmission risk and the importance of adhering to available vector control strategies.

 

Public Health Actions

 

We conducted targeted community risk sensitization meetings in Nyamanetsa agro- community highlighting the continued high risk of malaria transmission in such areas. We also sensitized the District Medical Officer on One Health Committees, a key step towards operationalisation of such a committee at the subnational level.

 

 

The authors declare no competing interests.

 

Funding

 

The study was conducted with support from the Zimbabwe Field Epidemiology Training Programme (ZimFETP)

 

 

Conceptualization: Nathan Chiboyiwa, Fungai Kavenga, Gerald Shambira, Gibson Mandozana, Notion Tafara Gombe, Mufuta Tshimanga.nFormal analysis: Nathan Chiboyiwa, Fungai Kavenga, Gerald Shambira, Gibson Mandozana, Notion Tafara Gombe, Mufuta Tshimanga. Methodology: Nathan Chiboyiwa, Notion Tafara Gombe, Gibson Mandozana, Gerald Shambira. Supervision: Fungai Kavenga, Manners Ncube, Gerald Shambira, Gibson Mandozana, Notion Tafara Gombe, Mufuta Tshimanga. Validation: Mufuta Tshimanga. Resources: Mufuta Tshimanga. Writing – original draft: Nathan Chiboyiwa, Fungai Kavenga, Gerald Shambira. Writing – review & editing: Nathan Chiboyiwa, Gerald Shambira, Notion Tafara Gombe, Gibson Mandozana, Fungai Kavenga, Mufuta Tshimanga. All the authors read and approved the final version of the manuscript.

 

 

We would like to acknowledge the following for making this study a success: The Ministry of Health and Child Care, Provincial Medical Directorate, Mashonaland Central Province. The Ministry of Health and Child Care, District Medical Officer, Centenary District, Mashonaland Central Province. The Ministry of Health and Child Care, David Nelson Clinic, Centenary District Rapid Response team. We acknowledge the contributions of Chadambuka Addmore and Juru Tsitsi P, both of the Zimbabwe Field Epidemiology Training Programme.

 

 

Table 1: Sociodemographic characteristics of study respondents in David Nelson Clinic catchment area, Upper Muzarabani in Centenary District, Zimbabwe 2023

Table 2: Factors associated with contracting malaria in David Nelson clinic catchment, Upper Muzarabani, Centenary District, Zimbabwe 2023

Figure 1: Epi-curve of a protracted malaria outbreak in Upper Muzarabani, Zimbabwe, Week 1-29, 2023

Figure 2: Spot map of malaria case in a protracted malaria outbreak in Upper Muzarabani, Zimbabwe, Week 1-26, 2023

Figure 3: Trends in rainfall and malaria cases in upper Muzarabani, Centenary, Zimbabwe 2018-2023

 

 

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