Correction: Plague in Zimbabwe from 1974 to 2018: A review article.

[This corrects the article DOI: 10.1371/journal.pntd.0007761.].

Plague in Zimbabwe from 1974 to 2018: A review article.

Plague is a zoonotic disease caused by the bacterium Yersinia pestis and is transmitted through the bites of infected rodent fleas. Plague is well known for causing 3 major human pandemics that have killed millions of people since 541 A.D. The aim of this Review is to provide an overview of the epidemiology and ecology of plague in Zimbabwe with special emphasis on its introduction, its potential reservoirs and vectors, and possible causes of its persistence and cyclic outbreaks. To achieve this, we carried out a search and document reported plague outbreaks in Zimbabwe. In the country, human plague cases have been reported in Hwange, Nkayi, and Lupane since 1974. The highest number of cases occurred in 1994 in the Nkayi district of Matabeleland North Province with a total of 329 confirmed human cases and 28 deaths. Plague is encountered in 2 different foci in the country, sylvatic and rural. Risk factors for contracting plague in the country include man-to-rodent contact, cultivation, hunting, cattle herding, handling of infected materials, camping in forests, and anthropic invasion of new areas. Plague is now enzootic in Zimbabwe, and the most recent case was reported in 2012, hence its effective control requires up-to-date information on the epidemiology and ecology of the disease. This can be achieved through continuous monitoring and awareness programs in plague-prone areas.

Getting ready for integrated vector management for improved disease prevention in Zimbabwe: a focus on key policy issues to consider.

BACKGROUND: This paper outlines Zimbabwe's potential readiness in harnessing integrated vector management (IVM) strategy for enhanced control of vector-borne diseases. The objective is to provide guidance for the country in the implementation of the national IVM strategy in order to make improvements required in thematic areas of need. The paper also assesses the existing opportunities and gaps to promote and adopt the approach as a national policy. MAIN TEXT: Despite recent gains in combating vector-borne diseases, especially malaria, management of vector control programmes still remains insecticide-based and vertical in nature. Therefore, concerns have been raised on whether the current long-standing conventional vector control strategy still remains with sufficient action to continue to break the transmission cycle to the levels of elimination. This is so, given the continuous dwindling resources for vector control, changes in vector behaviour, the emergence of resistance to medicines and insecticides, climate change, environmental degradation, as well as diversity in ecology, breeding habitats, and community habits. Cognizant of all that, elements of a surveillance-driven IVM approach are rapidly needed to move vector control interventions a step further. These include advocacy, policy formulation, capacity building, public and private partnerships, community engagement, and increasingly basing decisions on local evidence. Understanding the existing opportunities and gaps, and the recognition that some elements of IVM are already imbedded in the current health programmes is important to encourage stakeholders to promptly support its implementation. Leveraging on the existing opportunities, combined with sufficient advocacy, IVM could easily be accepted by the Zimbabwe government as part of a wider integrated disease management strategy. The strategy could represent an excellent breakthrough to establish much needed intra and inter-sectoral dialogue, and coordination for improved vector-borne disease prevention. CONCLUSIONS: After synthesis of the opportunities and challenges clearly presented, it was concluded that it is imperative for Zimbabwe to adopt and implement IVM strategy that is informed by work already done, while addressing the bottlenecks. The significance of refocusing for improved disease prevention that has the potential to accomplish elimination of not only malaria but all vector borne diseases much earlier than anticipated under the existing vector control system is underscored.

Progress towards malaria elimination in Zimbabwe with special reference to the period 2003-2015.

BACKGROUND: An intensive effort to control malaria in Zimbabwe has produced dramatic reductions in the burden of the disease over the past 13 years. The successes have prompted the Zimbabwe's National Malaria Control Programme to commit to elimination of malaria. It is critical to analyse the changes in the morbidity trends based on surveillance data, and scrutinize reorientation to strategies for elimination. METHODS: This is a retrospective study of available Ministry of Health surveillance data and programme reports, mostly from 2003 to 2015. Malaria epidemiological data were drawn from the National Health Information System database. Data on available resources, malaria control strategies, morbidity and mortality trends were analysed, and opportunities for Zimbabwe malaria elimination agenda was perused. RESULTS: With strong government commitment and partner support, the financial gap for malaria programming shrank by 91.4% from about US$13 million in 2012 to US$1 million in 2015. Vector control comprises indoor residual house spraying (IRS) and long-lasting insecticidal nets, and spray coverage increased from 28% in 2003 to 95% in 2015. Population protected by IRS increased also from 20 to 96% for the same period. In 2009, diagnostics improved from clinical to parasitological confirmation either by rapid diagnostic tests or microscopy. Artemisinin-based combination therapy was used to treat malaria following chloroquine resistance in 2000, and sulfadoxine-pyrimethamine in 2004. In 2003, there were 155 malaria cases per 1000 populations reported from all health facilities throughout the country. The following decade witnessed a substantial decline in cases to only 22 per 1000 populations in 2012. A resurgence was reported in 2013 (29/1000) and 2014 (39/1000), thereafter morbidity declined to 29 cases per 1000 populations, only to the same level as in 2013. Overall, morbidity declined by 81% from 2003 to 2015. Inpatient malaria deaths per 100,000 populations doubled in 4 years, from 2/100,000 to 4/100,000 populations in 2012-2015 respectively. Twenty of the 47 moderate to high burdened districts were upgraded from control to malaria pre-elimination between 2012 and 2015. CONCLUSIONS: A significant progress to reduce malaria transmission in Zimbabwe has been made. While a great potential and opportunities to eliminate malaria in the country exist, elimination is not a business as usual approach. Instead, it needs an improved, systematic and new programmatic strategy supported strongly by political will, sustained funding, good leadership, community engagement, and a strong monitoring and evaluation system all year round until the cessation of local transmission.

A pilot study to delimit tsetse target populations in Zimbabwe.

BACKGROUND: Tsetse (Glossina sensu stricto) are cyclical vectors of human and animal trypanosomoses, that are presently targeted by the Pan African Tsetse and Trypanosomiasis Eradication Campaign (PATTEC) coordinated by the African Union. In order to achieve effective control of tsetse, there is need to produce elaborate plans to guide intervention programmes. A model intended to aid in the planning of intervention programmes and assist a fuller understanding of tsetse distribution was applied, in a pilot study in the Masoka area, Mid-Zambezi valley in Zimbabwe, and targeting two savannah species, Glossina morsitans morsitans and Glossina pallidipes. METHODOLOGY/PRINCIPAL FINDINGS: The field study was conducted between March and December 2015 in 105 sites following a standardized grid sampling frame. Presence data were used to study habitat suitability of both species based on climatic and environmental data derived from MODIS and SPOT 5 satellite images. Factors influencing distribution were studied using an Ecological Niche Factor Analysis (ENFA) whilst habitat suitability was predicted using a Maximum Entropy (MaxEnt) model at a spatial resolution of 250 m. Area Under the Curve (AUC), an indicator of model performance, was 0.89 for G. m. morsitans and 0.96 for G. pallidipes. We then used the predicted suitable areas to calculate the probability that flies were really absent from the grid cells where they were not captured during the study based on a probability model using a risk threshold of 0.05. Apart from grid cells where G. m. morsitans and G. pallidipes were captured, there was a high probability of presence in an additional 128 km2 and 144 km2 respectively. CONCLUSIONS/SIGNIFICANCE: The modelling process promised to be useful in optimizing the outputs of presence/absence surveys, allowing the definition of tsetse infested areas with improved accuracy. The methodology proposed here can be extended to all the tsetse infested parts of Zimbabwe and may also be useful for other PATTEC national initiatives in other African countries.

A review of new challenges and prospects for malaria elimination in Mutare and Mutasa Districts, Zimbabwe.

This review outlines and discusses the new challenges in malaria control and prospects for its elimination in Mutare and Mutasa Districts, Zimbabwe. The burden of malaria has declined significantly over the past 5 years in most regions in Zimbabwe, including Mutare and Mutasa Districts. The nationwide malaria reduction has been primarily linked to scaled-up vector control interventions and early diagnosis and treatment with effective anti-malarial medicines. The successes recorded have prompted Zimbabwe's National Malaria Control Programme to commit to a global health agenda of eliminating malaria in all districts in the country. However, despite the decline in malaria burden in Mutare and Mutasa Districts, there is clear evidence of new challenges, including changes in vector behaviour, resistance to insecticides and anti-malarial medicines, invasion of new areas by vectors, vectors in various combination of sympatry, changes in vector proportions, outdoor malaria transmission, climate change and lack of meticulousness of spray operators. These new challenges are likely to retard the shift from malaria control to elimination in Mutare and Mutasa Districts.

Biting behaviour of Anopheles funestus populations in Mutare and Mutasa districts, Manicaland province, Zimbabwe: Implications for the malaria control programme.

BACKGROUND & OBJECTIVES: Biting behaviour of Anopheles funestus in Mutare and Mutasa districts, Zimbabwe, is little understood. An investigation was conducted to primarily compare indoor and outdoor biting behaviour of the mosquito, as well as blood meal sources and sporozoite rates. METHODS: Monthly adult anopheline sampling was conducted from October 2013 to September 2014 using Centers for Disease Control light-traps, pyrethrum spray catch and artificial pit shelter methods. Mosquitoes sampled by light-traps were divided into two cohorts. In one cohort, traps were left overnight and mosquitoes were collected the following morning, while in the other set, mosquitoes were collected hourly from 1800-0600 hrs . Collected females were identified using morphological characters and categorised according to their abdominal status. Polymerase chain reaction was used to identify An. funestus sibling species and blood meal sources. Infection rate was tested by enzyme-linked immunosorbent assay. RESULTS: Morphological identification showed that indoor and outdoor catches comprised Anopheles funestus (98.3%) and Anopheles gambiae s.l. (1.7%). Of the 2268 mosquitoes collected, 66.2% were caught by light-traps, and 33.8% were caught resting indoors and outdoors. Anopheles funestus and An. gambiae s.l. were trapped more abundantly indoors (68%) than outdoors (32%). Both indoor and outdoor An. funestus densities were higher in wet (4.3) than dry season (1.8). In Burma Valley and Zindi areas, An. funestus demonstrated variable nocturnal indoor and outdoor flight activity rhythms, with two peaks during the night; between 2200-2300 hrs and 0200- 0400 hrs. Human blood index in An. funestus was 0.64, with Plasmodium falciparum infection rate of 1.8%. INTERPRETATION & CONCLUSION: The present work highlighted important information on the host-seeking behaviour, blood meal sources and infection rates in An. funestus. The information would be helpful in improving the vector control strategies.

The emergence of insecticide resistance in the major malaria vector Anopheles funestus (Diptera: Culicidae) from sentinel sites in Mutare and Mutasa Districts, Zimbabwe.

BACKGROUND: Insecticide resistance in major malaria vectors poses severe challenges for stakeholders responsible for controlling the disease. During the 2013/14 season, malaria vector sentinel sites in Mutare and Mutasa Districts, Zimbabwe, experienced high presence of gravid malaria vector mosquitoes resting indoors in recently pyrethroid-sprayed structures. Subsequently, an evaluation of insecticide resistance in Anopheles funestus populations, the major malaria vector, was conducted to better inform the Zimbabwe National Malaria Control Programme. METHODS: Indoor-resting mosquitoes were collected in randomly selected pyrethroid-sprayed houses around Burma Valley and Zindi sentinel sites in Mutare and Mutasa Districts, respectively, using prokopac aspirator in February 2014. A. funestus mosquitoes were identified in the field using morphological keys and divided into two cohorts. One cohort was used immediately for WHO susceptibility tests and the other batch was transferred to the National Institute of Health Research insectary in Harare for oviposition. Susceptibility and intensity resistance assays were carried out on polymerase chain reaction-assayed, 3-5 days old, A. funestus s.s. F1 progeny females. RESULTS: Eight-hundred and thirty-six A. funestus and seven Anopheles gambiae complex mosquitoes were collected resting inside living structures. Wild caught females showed resistance to lambda-cyhalothrin (3.3% mortality), deltamethrin (12.9% mortality), etofenprox (9.2% mortality), and bendiocarb (11.7% mortality). F1 A. funestus female progeny indicated resistance to deltamethrin (14.5% mortality), lambda-cyhalothrin (6.9% mortality), etofenprox (8.3% mortality), and bendiocarb (16.8% mortality). Wild caught and female progeny were susceptible to DDT and pirimiphos-methyl (100% mortality). Intensity resistance assay to bendiocarb was 100% mortality, while deltamethrin, lambda-cyhalothrin, and etofenprox had increased knockdown times with mortalities ranging between 66.7 and 92.7% after 24-h exposures. CONCLUSION: This study is the first report of pyrethroid and carbamate resistance in A. funestus populations from Burma Valley and Zindi areas and indicates a major threat to the gains made in malaria vector control in Zimbabwe. In view of the current extension and intensity of such resistance, there is urgent need to set up a periodic and systematic insecticide resistance-monitoring programme which will form the basis for guiding the selection of insecticides for indoor residual spraying and distribution of pyrethroid-treated mosquito nets.

Seasonal abundance and epidemiological indices of potential plague vectors Dinopsyllus lypusus (Siphonaptera: Hystrichopsyllidae) and Ctenophthalmus calceatus (Siphonaptera: Ctenophthalmidae) on rodents captured from three habitat types of Hatcliffe and Dzivarasekwa suburbs of Harare, Zimbabwe.

The seasonal abundance of Dinopsyllus lypusus Jordan and Rothschild and Ctenophthalmus calceatus Waterson (potential vectors of plague in southern Africa) were studied on rodent hosts captured in selected habitat types of two periurban suburbs of Harare, Zimbabwe. Removal trapping was used to capture the rodents, from which fleas were collected and identified. Prevalence (proportion of animals infested) and specific flea index (SFI = number of fleas per animal) were calculated for each species of rodent host. Cohabitation of the two flea species on the host and its implications were also assessed. In total, 1,083 rodents belonging to nine species were trapped and over 97% of the total captures comprised of four species; Mastomys natalensis Smith, Rattus rattus L., Tatera leucogaster Peters, and Rhabdomys pumilio Sparrman. In total, 735 D. lypusus and 335 C. calceatus were recorded on these four common rodent species. Population density of D. lypusus as measured by prevalence and SFI varied from 13.4 to 53.3% and 0.2-1.5, respectively, while that of C. calceatus varied from 8.2 to 26.7% and 0.2-0.6, respectively. For all rodent species captured, both prevalence and SFI of D. lypusus and C. calceatus were highest during the cold-dry season, followed by the hot dry season, with the hot-wet season recording the lowest indices. Overall cohabitation was highest during the cold-dry season and nonexistent during the hot-wet season. Our findings on the abundance and ecology of D. lypusus and C. calceatus suggest that their roles in the transmission of plague in Zimbabwe need further investigation.

Seasonal abundance of plague vector Xenopsylla brasiliensis from rodents captured in three habitat types of periurban suburbs of Harare, Zimbabwe.

The study was aimed at determining the seasonal abundance of Xenopsylla brasiliensis, an important vector of plague in Zimbabwe, from rodent hosts captured in selected habitat types of two periurban suburbs of Harare, Zimbabwe. The removal-trapping method was used to capture the rodents, from which fleas were collected and identified. Percentage incidence index (PII) and specific flea index (SFI) were calculated for X. brasiliensis in relation to rodent species host. Mastomys natalensis, Rattus rattus, Tatera leucogaster, and Rhabdomys pumilio were the rodent species present in the study areas and all species were infested with X. brasiliensis. PII for T. leucogaster in relation to X. brasiliensis was significantly higher (p < 0.05) compared with that of the other rodent species and T. leucogaster also recorded the highest SFI, whereas R. pumilio recorded the lowest indices. In both formal and informal settlements, the highest PII of X. brasiliensis was attained for M. natalensis, followed by R. rattus. In the cultivated habitat, T. leucogaster recorded the highest indices and R. pumilio the lowest. X. brasiliensis was found to cohabitat with Dinopsyllus lypusus and Ctenophthalmus calceatus on M. natalensis, R. rattus, and T. leucogaster. No cohabitation was recorded for R. pumilio. For all the rodent species captured, both the PII and SFI of X. brasiliensis were highest during the hot-dry season, followed by the hot-wet season, with the cold-dry season recording the lowest indices. The overall cohabitation was highest during the hot-dry season and lowest during the hot-wet season. The findings of the present study fit the reported occurrence of plague outbreaks during the hot-dry season in periurban Zimbabwe.