Home Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
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Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe

  • Annabel Banda EMAIL logo , Edson Gandiwa , Never Muboko and Victor K. Muposhi
Published/Copyright: September 3, 2022

Abstract

This study assessed the prevalence of plague bacterium (Yersinia pestis) among rodents captured in Umzingwane and Nkayi districts, south-western Zimbabwe. A total of 44 rodents were captured on three consecutive days per trapping session in the study sites using a removal trapping method in April 2018. Captured rodents were euthanized, and blood samples were collected. The Giemsa stain method was used to detect plague bacteria. The trapping success was not significantly different (χ² = 1.50, df = 1, P = 0.221), 8.5% for the Nkayi district, while in the Umzingwane district, it was 8%. Overall, only one rodent species, i.e., Mastomys natalensis, tested positive for Y. pestis in the Umzingwane district, thus yielding a prevalence rate of 2.3% for the entire study area. This was the most important finding of a Y. pestis-positive rodent in a non-endemic wild area in the Umzingwane district. These results point to a low prevalence of Y. pestis in the study area and the importance of an active plague disease surveillance and monitoring system.

1 Introduction

Plague, a disease caused by the bacilli bacterium, Yersinia pestis, primarily affects rodents, mainly transmitted from one host to another through bites of infective fleas [1]. However, there are alternative transmission routes, such as inhalation and direct contact, which do not normally play a role in the maintenance of plague bacterium in the animal reservoirs [2]. Fleas are generalists in their feeding behavior; thus, in the absence of rodents, they seek alternative hosts, such as wild and domestic animals, as well as people [3]. Thus, some flea species, for instance, Xenopsylla brasiliensis, are implicated as effective plague transmitters [4]. Alternatively, humans can acquire plague by handling infected rodents or by droplet infection, although humans do not play a role in the long-term survival of the plague bacterium [2]. In most cases, a plague outbreak causes a great population decrease in rodents of some species within their local and established ranges (Barnes, 1993, cited in Thiagarajan et al. [5]). However, some rodent hosts act as reservoirs of the disease in the enzootic environment allowing low levels of the pathogen circulation [3].

The first cases of human plague in Zimbabwe were recorded in 1974. The cases showed a complicated combination of plagues [6]. From then up to 1985, there were 89 cases noted, of which 23 deaths occurred [7]. Subsequent plague human cases were recorded in 1994 and 1997, where the highest cases of plague were noted, with about 400 cases and 30 deaths confirmed in Nkayi and Lupane districts, Matabeleland North [7,8]. In 2012 (latest information), plague was detected in Zimbabwe, but there was no full report of the disease [6]. Unavailability of active plague surveillance may have adverse repercussions, as an epidemic can occur undetected [9]. Plague foci are dynamic and keep on emerging and re-emerging [10], hence the importance of research to establish any potential new plague foci.

Plague bacterium can be hosted by a number of rodents. It was detected in multimammate mouse (Mastomys natalensis) and Gerbilliscus species in Tanzania [11]. Furthermore, small mammals, such as rabbits (Sylvilagus floridanus), marmots (Marmota), and chipmunks (Eutamias spp.), were shown to maintain plague in the wilderness [3]. Surveying diseases among free ranging wild animal populations may provide an early warning system for the presence of a disease. There is generally less active plague surveillance in Zimbabwe [4], except the few publications on rodents and fleas which largely focus on rodent and flea species diversity [12,13]. Therefore, this study aims to fill the gap in knowledge on plague prevalence in Zimbabwe by assessing the prevalence of plague bacteria among rodent species in Nkayi and Umzingwane districts. These two districts are in the same agro-ecological zone but differ in their plague occurrence: one is plague endemic (Nkayi district) while the other is plague non-endemic (Umzingwane district) [6,7].

2 Materials and methods

The study was conducted in south-western Zimbabwe in Nkayi and Umzingwane districts’ located in natural region IV (Figure 1). Nkayi district has deep Kalahari sands occupying 60% of the area whereas Umzingwane district’s soils are derived from granite rocks being coarse, sandy, and low in fertility [14]. The most common type of vegetation in Nkayi district is broad leafed woodlands, teak (Baikiaea plurijuga), and Brachystegia spp. [15]. Umzingwane district is characterized by three types of vegetation, which are bushveld, mainly covered with Acacia ranging between 1 and 5 m high, wooded grassland, and woodland covered by Terminalia and Combretum genus trees. The grasslands are the main source of grazing land [14].

Figure 1 
               Location of Nkayi and Umzingwane Districts in south-western Zimbabwe. Notes: 15, 27, 3, and 17 represent Monki, Mathoba, Nhlekiyane, and Crocodile wards, respectively.
Figure 1

Location of Nkayi and Umzingwane Districts in south-western Zimbabwe. Notes: 15, 27, 3, and 17 represent Monki, Mathoba, Nhlekiyane, and Crocodile wards, respectively.

In the Nkayi district, most of the local rural community members are engaged in extensive livestock production and cultivation of some drought-tolerant crops, such as sorghum (Sorghum vulgare), finger millet (Eleusine coracana) and pearl millet (Pennisetum glaucum). However, farmers do sometimes grow some short-season maize (Zea mays) varieties. Nkayi district’s population was reported to be 109,135 people, while the Umzingwane district had 62,990 people in 2012 [16].

This study followed a quasi-experimental design comprising two strata, i.e., districts and then two villages in each district. In the Nkayi district, the two villages studied were Mathoba and Monki villages while in the Umzingwane district were Crocodile and Nhlekiyane villages. All the trapping procedures and further processing of rodents were carried out following Dennis et al. [7], except that traps were placed 10 m apart.

Rodent trapping was conducted in April 2018 by first observing rodent activity, such as maize cob consumption and/or clearly constructed tracks and warrens. Rodents were captured in villages, i.e., bushes habitats using 15 Sherman live traps placed about 10 m apart in transects [17]. Three transects were placed in uncultivated places near fields in each study village. On the first day of sampling, traps were set late afternoon and inspected the following morning between 6 am and 7 am before it was too hot to reduce stress in captured rodents. Traps were left open for three consecutive days per village, i.e., 45 traps.

Productive traps were replaced in the morning following Kimaro et al. [17]. Traps with captures were taken to a central processing point in each study village, in an open area, for euthanization of rodents using chloroform, species identification and blood sample collection. Rodents were identified according to the illustrations and descriptions by du Plessis et al. [18]. Rodents identified were confirmed with the Natural History Museum, Bulawayo, Zimbabwe. Rodents’ cadavers were buried in a pit of about 50 cm deep.

After about 2–3 min after introducing the rodent to chloroform, blood was collected from the euthanized rodent using a hypodermic needle with a connected syringe. Blood was collected from the heart blood on which blood smears were made. Slides with Giemsa stain were examined at ×1,000 for 5–10 min, searching for bipolar coccobacilli [19] in the Wildlife Laboratory at Chinhoyi University of Technology, Chinhoyi, Zimbabwe.

2.1 Data analysis

Trapping success was calculated as the number of animals caught divided by the trapping period divided by the number of traps set per period multiplied by 100 (7). The Chi-square (χ²) test of independence or cross-tabulation was used to determine if there were differences among the trapping success in STATISTICA version 10 for Windows [20]. Diversity of rodents in each district was calculated following the Shannon–Wiener (H′) index measure of diversity [21]. The prevalence of Y. pestis in rodents’ blood samples was calculated as the number of Y. pestis-positive rodent individuals divided by the total number of rodents examined multiplied by 100.

3 Results

A total of 44 rodents were captured in the two study districts, i.e., Nkayi (H′ = 0.89) and Umzingwane (H′ = 0.62). There was no significant difference in the trapping success between the study districts, i.e., Nkayi (8.5%) and Umzingwane (8%) (Table 1) (χ² = 1.50, df = 1, P = 0.221). Twenty-three (23) rodents were caught in the Nkayi district and 21 in the Umzingwane district, i.e., 17 M. natalensis (Smith, 1834), 6 Gerbilliscus brantsi (Smith, 1836), 4 Gerbilliscus leucogaster (Peters, 1852), and 17 Saccostomys campestris (Peters, 1846). Only one rodent, i.e., M. natalensis, caught in the Umzingwane district tested positive for the plague bacterial, indicating an overall prevalence of plague of 2.4% in the study area (Table 2).

Table 1

Rodents trapping success in the study area

Variable Nkayi district Umzingwane district
Mathoba Monki Crocodile Nhlekiyane
No. rodents per site 10 13 13 8
Trapping success (%) 7 10 10 6
Mean trapping success (%) 8.50 8.00
Table 2

Rodents captured species diversity and prevalence of bacterial plague in the study area

Rodent species Nkayi district Umzingwane district Overall prevalence (%)
# of rodents captured # of rodents that are positive for Y. pestis Prevalence (%) # of rodents captured # of rodents that positive for Y. pestis Prevalence (%)
M. natalensis 0 0 17 1 5.9 5.9
S. campestris 4 0 0 2 0 0 0
G. brantsi 4 0 0 2 0 0 0
G. leucogaster 15 0 0 0 0 0 0
Species diversity (H′) 0.89 0.62
Total/average (%) 23 0 0 21 1 4.8 2.4

Note: – denotes not applicable; # – denotes number.

4 Discussion

This study is the first to report the presence of plague bacteria among rodents in Umzingwane district, even though a low prevalence of plague disease exists in the study area. Elsewhere, plague bacteria were reported as being difficult to detect in rodents and fleas associated with prairie dog colonies (Cynomys) at Thunder Basin National Grassland in Wyoming, USA [5]. Thus, it was suggested that where possible plague determination investigations could be conducted in places where there are noticeable rodent die-offs [5]. Since time immemorial M. natalensis was observed not to easily succumb to plague bacteria, thus termed an enzootic host [11,22]. Thus, some of the caught species may not be ideal host for Y. pestis, for instance T. leucogaster was observed to easily succumb to Y. pestis closely related bacilli Y. pestis tuberculosis subspecies pestis [23].

Since no die-offs were observed during the sampling time, it may imply that an inter-epizootic period could have existed during which Y. pestis cannot be recovered from fleas, rodents, or any other host [1]. Instead, it was proposed in Iran and Madagascar that the bacteria could remain in existence in the soil. However, one study recommended that the transmission route by exposure of susceptible mice to Y. pestis-contaminated soil seems doubtful under natural conditions because the infectious period was short-lived and the transmission efficiency was low [24]. Thus, during plague quiescent times, it is likely that detecting Y. pestis is by mere chance.

In northern Tanzania, 517 wild, peri-domestic, and small commensal mammals, including rodents and wild carnivores, were captured, but only three tested positive for Y. pestis. This is an indication for the need for large samples to fully get a good picture of the infection status of a rodent population [11]. There can, however, be possibilities that Y. pestis is concentrated on certain rodent body organs as was reported in a study in Mongolia, where Y. pestis was detected in spleen samples, while liver samples from rodents tested negative using Polymerase Chain Reaction [25]. This therefore points to the importance of a large sample associated with diversified samples from the rodent body parts to enhance the chances of detection of the representative infection status of populations.

5 Conclusion

The study provides the first evidence of plague bacteria infection in a rodent species in Umzingwane district, a non-endemic region for the plague disease. It is recommended that future studies on plague bacteria assessment should involve a larger sample both for rodent populations and areas covering endemic and non-endemic regions, cover a longer sampling timeframe, and take samples from other body parts of rodents (liver and spleen) for testing beyond the blood.


# Present address: Scientific Services, Zimbabwe Parks and Wildlife Management Authority, P.O. Box CY 140, Causeway, Harare, Zimbabwe.


Acknowledgments

Our sincere gratitude goes to the following village heads, Mr. R. Ncube and Mr. R. Tshuma (Umzingwane district) and Mr. A Mlotshwa and Mr. J. M. Gwayi (Nkayi district) for permission to conduct the study in their areas of jurisdiction. We are also indebted to Nkayi Principal Environmental Health Technician, Mr. J. Sibanda, and the Health Technicians, Mr. G. Mabhena and Mr. N. Ncube, for providing us with plague historical information.

  1. Funding information: Authors state no funding involved.

  2. Author contributions: Annabel Banda conceived and designed the experiments, performed the experiments, analyzed the data, contributed reagents/materials/analysis tools, prepared figures and/or tables, authored or reviewed drafts of the manuscript, and approved the final draft. Edson Gandiwa conceived and designed the experiments, analyzed the data, contributed analysis tools, authored or reviewed drafts of the manuscript, and approved the final draft. Never Muboko and Victor K. Muposhi authored or reviewed drafts of the manuscript, and approved the final draft.

  3. Conflict of interest: Authors state no conflict of interest.

  4. Data availability statement: The datasets generated during and/or analyzed during the current study are available from the corresponding author on reasonable request.

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Received: 2021-07-13
Revised: 2021-12-11
Accepted: 2022-01-03
Published Online: 2022-09-03

© 2022 Annabel Banda et al., published by De Gruyter

This work is licensed under the Creative Commons Attribution 4.0 International License.

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  112. Abnormal methylation caused by folic acid deficiency in neural tube defects
  113. Silencing TLR4 using an ultrasound-targeted microbubble destruction-based shRNA system reduces ischemia-induced seizures in hyperglycemic rats
  114. Plant Sciences
  115. Seasonal succession of bacterial communities in cultured Caulerpa lentillifera detected by high-throughput sequencing
  116. Cloning and prokaryotic expression of WRKY48 from Caragana intermedia
  117. Novel Brassica hybrids with different resistance to Leptosphaeria maculans reveal unbalanced rDNA signal patterns
  118. Application of exogenous auxin and gibberellin regulates the bolting of lettuce (Lactuca sativa L.)
  119. Phytoremediation of pollutants from wastewater: A concise review
  120. Genome-wide identification and characterization of NBS-encoding genes in the sweet potato wild ancestor Ipomoea trifida (H.B.K.)
  121. Alleviative effects of magnetic Fe3O4 nanoparticles on the physiological toxicity of 3-nitrophenol to rice (Oryza sativa L.) seedlings
  122. Selection and functional identification of Dof genes expressed in response to nitrogen in Populus simonii × Populus nigra
  123. Study on pecan seed germination influenced by seed endocarp
  124. Identification of active compounds in Ophiopogonis Radix from different geographical origins by UPLC-Q/TOF-MS combined with GC-MS approaches
  125. The entire chloroplast genome sequence of Asparagus cochinchinensis and genetic comparison to Asparagus species
  126. Genome-wide identification of MAPK family genes and their response to abiotic stresses in tea plant (Camellia sinensis)
  127. Selection and validation of reference genes for RT-qPCR analysis of different organs at various development stages in Caragana intermedia
  128. Cloning and expression analysis of SERK1 gene in Diospyros lotus
  129. Integrated metabolomic and transcriptomic profiling revealed coping mechanisms of the edible and medicinal homologous plant Plantago asiatica L. cadmium resistance
  130. A missense variant in NCF1 is associated with susceptibility to unexplained recurrent spontaneous abortion
  131. Assessment of drought tolerance indices in faba bean genotypes under different irrigation regimes
  132. The entire chloroplast genome sequence of Asparagus setaceus (Kunth) Jessop: Genome structure, gene composition, and phylogenetic analysis in Asparagaceae
  133. Food Science
  134. Dietary food additive monosodium glutamate with or without high-lipid diet induces spleen anomaly: A mechanistic approach on rat model
  135. Binge eating disorder during COVID-19
  136. Potential of honey against the onset of autoimmune diabetes and its associated nephropathy, pancreatitis, and retinopathy in type 1 diabetic animal model
  137. FTO gene expression in diet-induced obesity is downregulated by Solanum fruit supplementation
  138. Physical activity enhances fecal lactobacilli in rats chronically drinking sweetened cola beverage
  139. Supercritical CO2 extraction, chemical composition, and antioxidant effects of Coreopsis tinctoria Nutt. oleoresin
  140. Functional constituents of plant-based foods boost immunity against acute and chronic disorders
  141. Effect of selenium and methods of protein extraction on the proteomic profile of Saccharomyces yeast
  142. Microbial diversity of milk ghee in southern Gansu and its effect on the formation of ghee flavor compounds
  143. Ecology and Environmental Sciences
  144. Effects of heavy metals on bacterial community surrounding Bijiashan mining area located in northwest China
  145. Microorganism community composition analysis coupling with 15N tracer experiments reveals the nitrification rate and N2O emissions in low pH soils in Southern China
  146. Genetic diversity and population structure of Cinnamomum balansae Lecomte inferred by microsatellites
  147. Preliminary screening of microplastic contamination in different marine fish species of Taif market, Saudi Arabia
  148. Plant volatile organic compounds attractive to Lygus pratensis
  149. Effects of organic materials on soil bacterial community structure in long-term continuous cropping of tomato in greenhouse
  150. Effects of soil treated fungicide fluopimomide on tomato (Solanum lycopersicum L.) disease control and plant growth
  151. Prevalence of Yersinia pestis among rodents captured in a semi-arid tropical ecosystem of south-western Zimbabwe
  152. Effects of irrigation and nitrogen fertilization on mitigating salt-induced Na+ toxicity and sustaining sea rice growth
  153. Bioengineering and Biotechnology
  154. Poly-l-lysine-caused cell adhesion induces pyroptosis in THP-1 monocytes
  155. Development of alkaline phosphatase-scFv and its use for one-step enzyme-linked immunosorbent assay for His-tagged protein detection
  156. Development and validation of a predictive model for immune-related genes in patients with tongue squamous cell carcinoma
  157. Agriculture
  158. Effects of chemical-based fertilizer replacement with biochar-based fertilizer on albic soil nutrient content and maize yield
  159. Genome-wide identification and expression analysis of CPP-like gene family in Triticum aestivum L. under different hormone and stress conditions
  160. Agronomic and economic performance of mung bean (Vigna radiata L.) varieties in response to rates of blended NPS fertilizer in Kindo Koysha district, Southern Ethiopia
  161. Influence of furrow irrigation regime on the yield and water consumption indicators of winter wheat based on a multi-level fuzzy comprehensive evaluation
  162. Discovery of exercise-related genes and pathway analysis based on comparative genomes of Mongolian originated Abaga and Wushen horse
  163. Lessons from integrated seasonal forecast-crop modelling in Africa: A systematic review
  164. Evolution trend of soil fertility in tobacco-planting area of Chenzhou, Hunan Province, China
  165. Animal Sciences
  166. Morphological and molecular characterization of Tatera indica Hardwicke 1807 (Rodentia: Muridae) from Pothwar, Pakistan
  167. Research on meat quality of Qianhua Mutton Merino sheep and Small-tail Han sheep
  168. SI: A Scientific Memoir
  169. Suggestions on leading an academic research laboratory group
  170. My scientific genealogy and the Toronto ACDC Laboratory, 1988–2022
  171. Erratum
  172. Erratum to “Changes of immune cells in patients with hepatocellular carcinoma treated by radiofrequency ablation and hepatectomy, a pilot study”
  173. Erratum to “A two-microRNA signature predicts the progression of male thyroid cancer”
  174. Retraction
  175. Retraction of “Lidocaine has antitumor effect on hepatocellular carcinoma via the circ_DYNC1H1/miR-520a-3p/USP14 axis”
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