Skip to main content
PMC home page
The Onderstepoort Journal of Veterinary Research logoLink to The Onderstepoort Journal of Veterinary Research
. 2021 Aug 3;88(1):1911. doi: 10.4102/ojvr.v88i1.1911

Surveillance of the rabies-related lyssavirus, Mokola in non-volant small mammals in South Africa

William C McMahon 1, Jessica Coertse 1,2, Teresa Kearney 3,4, Mark Keith 3, Lourens H Swanepoel 5, Wanda Markotter 1,✉
PMCID: PMC8424720  PMID: 34342470

Abstract

The reservoir host of Mokola virus (MOKV), a rabies-related lyssavirus species endemic to Africa, remains unknown. Only sporadic cases of MOKV have been reported since its first discovery in the late 1960s, which subsequently gave rise to various reservoir host hypotheses. One particular hypothesis focusing on non-volant small mammals (e.g. shrews, sengis and rodents) is buttressed by previous MOKV isolations from shrews (Crocidura sp.) and a single rodent (Lophuromys sikapusi). Although these cases were only once-off detections, it provided evidence of the first known lyssavirus species has an association with non-volant small mammals. To investigate further, retrospective surveillance was conducted in 575 small mammals collected from South Africa. Nucleic acid surveillance using a pan-lyssavirus quantitative real-time reverse transcription polymerase chain reaction (qRT-PCR) assay of 329 brain samples did not detect any lyssavirus ribonucleic acid (RNA). Serological surveillance using a micro-neutralisation test of 246 serum samples identified 36 serum samples that were positive for the presence of MOKV neutralising antibodies (VNAs). These serum samples were all collected from Gerbilliscus leucogaster (Bushveld gerbils) rodents from Meletse in Limpopo province (South Africa). Mokola virus infections in Limpopo province have never been reported before, and the high MOKV seropositivity of 87.80% in these gerbils may indicate a potential rodent reservoir.

Keywords: Bushveld gerbil, lyssavirus, Mokola, non-volant small mammal, rabies-related, reservoir, rodent, surveillance

The Mokola virus (MOKV), a rabies-related lyssavirus, represents one of 17 recognised species within the Lyssavirus genus, all capable of causing a fatal encephalitic disease (Walker et al. 2018). The Mokola virus is exclusively endemic in Africa with only 30 sporadic cases reported since its discovery more than 50 years ago (Figure 1; Table 1) (Coertse et al. 2017; Kgaladi et al. 2013). The reservoir host of MOKV is still unknown, with spillover dead-end hosts such as domestic cats (Felis catus) and dogs (Canis familiaris), most commonly reported to be infected with MOKV. This has led to the hypothesis that the reservoir of MOKV might be a prey species that interacts with domesticated animals via a prey-to-predator pathway (Kgaladi et al. 2013). Non-volant small mammals (i.e. shrews, sengis and rodents) have been suggested as possible reservoir hosts considering that previous MOKV isolations were in shrews (Crocidura spp.), four in Nigeria and one in Cameroon (Causey et al. 1969; Kemp et al. 1972; Le Gonidec et al. 1978), and a single reported case in a rodent (Lophuromys sikapusi) in the Central African Republic (Saluzzo et al. 1984). To investigate further, nucleic acid and serological surveillance were retrospectively conducted, targeting non-volant small mammals from specific locations in South Africa.

FIGURE 1.

FIGURE 1

Open in a new tab

Geographical distribution of all reported Mokola virus cases (n = 30) in the African continent.

TABLE 1.

Summary of all reported Mokola virus cases in Africa.

Date Virus/Laboratory Reference Numbers Host Species Detection Material Geographical Location Reference‡
Nigeria (n = 6)
May 1968 IbAn 26801† Crocidura sp. (Shrew) Organ pool (heart, lung, liver, spleen & kidney) Ife Farm, Ibadan, Nigeria Causey and Kemp (1968); Kemp et al. (1972)
May 1968 IbAn 27157† Crocidura sp. (Shrew) Organ pool (heart, lung, liver, spleen & kidney) Private residence, University of Ibadan, Ibadan, Nigeria Causey and Kemp (1968); Kemp et al. (1972)
July 1968 IbAn 27377†
RV4		 Crocidura sp. (Shrew) Organ pool (heart, lung, liver, spleen & kidney) Mokola, Ibadan, Nigeria Causey and Kemp (1968); Kemp et al. (1972)
August 1968 IbAn 29777† Homo sapiens (Human) Cerebrospinal fluid (CSF) Inalende, Ibadan, Nigeria Familusi and Moore (1972); Kemp et al. (1972)
December 1969 IbAn 51715† Crocidura sp. (Shrew) Organ pool (liver & spleen) Virus Research Laboratory, Ibadan, Nigeria Causey and Kemp (1969); Kemp et al. (1972)
March 1971 IbAn 56909† Homo sapiens (Human) Brain Idikan, Ibadan, Nigeria Familusi and Moore (1972); Kemp et al. (1972)
Cameroon (n = 1)
January 1974 An Y1307†
RV39
86100CAM		 Crocidura sp. (Shrew) Organ pool (brain, liver & spleen) Nkol-Owona, Yaounde, Cameroon Le Gonidec et al. (1978)
Central African Republic (n = 1)
October 1981 AnRB3247†
RV40
86101RCA		 Lophuromys sikapusi (Rodent) Brain Botami, Bangui, Central African Republic Saluzzo et al. (1984)
Ethiopia (n = 1)
1989–1990 Eth-16†
RA 133/82
RV610		 Felis catus (Cat) Brain Addis Ababa, Ethiopia Mebatsion, Cox and Frost (1992)
Zimbabwe (n = 8)
April 1981 12017† Felis catus (Cat) Brain Bulawayo, Zimbabwe Foggin (1982); Foggin (1988)
May 1981 12245† Felis catus (Cat) Brain Bulawayo, Zimbabwe Foggin (1982); Foggin (1988)
June 1981 12341† Felis catus (Cat) Brain Bulawayo, Zimbabwe Foggin (1982); Foggin (1988)
August 1981 12574† Felis catus (Cat) Brain Bulawayo, Zimbabwe Foggin (1982); Foggin (1988)
October 1981 12800† Canis familiaris (Dog) Brain Bulawayo, Zimbabwe Foggin (1982); Foggin (1988)
March 1982 13270† Felis catus (Cat) Brain Bulawayo, Zimbabwe Foggin (1983); Foggin (1988)
April 1982 13371†
Zim82
RV1035		 Felis catus (Cat) Brain Bulawayo, Zimbabwe Foggin (1983); Foggin (1988)
November 1993 21846†
RV1017		 Felis catus (Cat) Brain Selous, Zimbabwe Bingham et al. (2001)
South Africa (n = 13)
December 1970 700/70†
V21.G3
V241		 Felis catus (Cat) Brain Umhlanga Rocks, KwaZulu-Natal, South Africa Meredith and Nel (1996); Nel et al. (2000)
July 1995 543/95† Felis catus (Cat) Brain Mdantsane, Eastern Cape, South Africa Meredith and Nel (1996); Nel et al. (2000)
February 1996 112/96†
RV1021		 Felis catus (Cat) Brain East London, Eastern Cape, South Africa Von Teichman et al. (1998); Nel et al. (2000)
May 1996 322/96† Felis catus (Cat) Brain Yellow Sands, Eastern Cape, South Africa Von Teichman et al. (1998); Nel et al. (2000)
May 1997 252/97†
V552.S3		 Felis catus (Cat) Brain Pinetown, KwaZulu-Natal, South Africa Von Teichman et al. (1998); Nel et al. (2000)
May 1997 229/97†
V550.S3		 Felis catus (Cat) Brain Pinetown, KwaZulu-Natal, South Africa Von Teichman et al. (1998); Nel et al. (2000)
March 1998 071/98†
V635.S3
RA361		 Felis catus (Cat) Brain Pietermaritzburg, KwaZulu-Natal, South Africa Von Teichman et al. (1998); Nel et al. (2000
June 2005 404/05† Canis familiaris (Dog) Brain Nkomazi, Mpumalanga, South Africa Sabeta et al. (2007)
March 2006 173/06† Felis catus (Cat) Brain Farm near East London, Eastern Cape, South Africa Sabeta et al. (2007)
2008 226/08† Felis catus (Cat) Brain Grahamstown, Eastern Cape, South Africa Sabeta et al. (2010)
June 2012 12/458† Felis catus (Cat) Brain Durban, KwaZulu-Natal, South Africa Coertse et al. (2017)
July 2012 12/604† Felis catus (Cat) Brain Durban, KwaZulu-Natal, South Africa Coertse et al. (2017)
January 2014 14/024† Felis catus (Cat) Brain Pietermaritzburg, KwaZulu-Natal, South Africa Coertse et al. (2017)
Open in a new tab

Sp., species; RV, rabies virus; IbAn, Ibadan.

†

, The original virus reference number as indicated in the reference article(s);

‡

, References form part of Appendix 2.

Non-volant small mammals were captured and sampled in accordance with the field procedure guidelines of Sikes and Gannon (2011) during the period of 2015–2017 from two different sites in South Africa: Meletse area in Limpopo province (24.5914° S, 27.6258° E) and Secunda area in Mpumalanga Province (26.5158° S, 29.1914° E). All the species investigated were designated as of Least Concern by The International Union for Conservation of Nature Red List of Threatened Species. Morphological species identification followed classifications by Meester et al. (1986), Newbery (1999), as well as Monadjem et al. (2015). Following morphological identification, animals were anesthetised with Isofor (Safeline Pharmaceuticals, South Africa), after which blood was collected by cardiac puncture (1% – 3% volume/body mass) in 0.8 mL MiniCollect serum separator tubes (Greiner Bio-One, Austria). Serum was separated from whole blood by centrifugation (Centrifuge 5418, Eppendorf, Germany) at 4300 g for 5 min and transferred to 2.0 mL Sarstedt tubes (Sarstedt Inc.). Animals that were not collected as voucher specimens were marked with a unique tattoo number near the base of their tail, and released back to their respective capture sites. Voucher specimens were euthanised with an overdose of Isofor, after which their organs were harvested (i.e. brain, tongue, salivary glands, heart, kidney, lungs, pectoral muscle, spleen, intestines, rectum and bladder) in 2.0 mL Sarstedt tubes for a broader pathogen surveillance study and immediately stored in liquid nitrogen until storage at –80 °C. Carcasses were placed in a 3 L PathoPak (Intelsius Solutions, United Kingdom [UK]) containing 80% ethanol and were submitted to Ditsong National Museum of Natural History and the Natural History Collection for Public Health and Economics for voucher-based morphological identification, and museum archiving.

Total ribonucleic acids (RNAs) were extracted from brain samples (n = 329) (nine shrews, four sengis and 316 rodents) using TRIzol™ reagent (Invitrogen, United States [US]), followed by nucleic acid surveillance using a pan-lyssavirus quantitative real-time reverse transcription polymerase chain reaction (qRT-PCR) assay as previously described (Coertse et al. 2019). Serum samples (n = 246) (three shrews, four sengis and 239 rodents) were subjected to serological surveillance using a micro-neutralisation test as previously described (Smith & Gilbert 2017), during which MOKV 12/458 (2012, Felis catus, Durban, KwaZulu-Natal, South Africa) (Coertse et al. 2017) was used as challenge virus. If a reduction or absence of fluorescence was observed at the 1:25 serum dilution during initial screening, the serum sample was subjected to follow-up screening (in duplicate) at 1:10, 1:50, 1:250 and 1:1250 serum dilutions. The 50% end-point (ED) neutralisation titre was calculated by the Reed and Muench method (1938) and considered positive for Mokola virus neutralising antibodies (MOKV VNAs) when they had a 50% ED neutralisation titre at a serum dilution of ≥ 25 (i.e. where ≤ 5 out of the 10 counted fields contain infected cells at the 1:25 serum dilution). If additional material was available, non-volant small mammals that tested positive for the presence of MOKV VNAs were subjected to genetic species identification with the Cytochrome B (CytB) barcoding PCR assay as previously described (Greenberg et al. 2012). Template deoxyribonucleic acid (DNA) required for the barcoding assay was extracted from various biological sample types (such as blood, kidney, heart and pectoral tissue) using the Quick-DNA™ Miniprep Plus Kit (Zymo Research, US).

All of the brain samples were negative for the presence of viral RNA with the pan-lyssavirus qRT-PCR assay (Appendix Table 1-A1). Negative results were expected as these animals were apparently healthy individuals and did not exhibit any visible signs of disease. An overall MOKV seropositivity of 87.80% (36 out of 41) was observed for the gerbils (Gerbilliscus leucogaster) tested from Meletse at the cut-off 1:25 serum dilution (Figure 2; Appendix Tables 1-A1, 2-A1, 3-A1 & 4-A1). The titre ranges for this rodent species were high when compared to another serological surveillance study conducted in Zimbabwe (Foggin 1988). Foggin identified MOKV VNAs in 5.63% (18 out of 320) of all rodents that were tested. An overall MOKV seropositivity of 17.57% (13 out of 74) was observed for gerbils which neutralised MOKV infection at various serum dilutions that ranged from 1:8, 1:16 to 1:32. None of the other MOKV serological surveillance studies have tested this rodent species for the presence of MOKV VNAs (Aghomo et al. 1990; Kemp et al. 1972; Nottidge, Omobowale & Oladiran 2007; Ogunkoya et al. 1990). Even though MOKV has been shown to cross-react in serological assays with other closely-related lyssaviruses (Kuzmin et al. 2008), cross-reactivity with other phylogroup II lyssaviruses was not investigated in this study.

FIGURE 2.

FIGURE 2

Open in a new tab

Graphical representation of the micro-neutralisation test results of the Gerbilliscus leucogaster serum samples from Meletse (n = 36).

Of the 36 gerbils showing MOKV seropositivity, only 28 were genetically identified with the CytB barcoding PCR assay (Table 2). The same identification was obtained from morphological examination of 24 voucher specimens (Table 2). Eight gerbils could not be identified to species level as they were released and no additional sample material was available. The Highveld gerbil, Gerbilliscus brantsii, is sympatric with G. leucogaster, however, based on known museum records, no G. brantsii has been caught at Meletse before (Rautenbach 1982) and these were, therefore, allocated to G. cf. leucogaster. The variability observed in the per cent identity (i.e. 83.78% – 100.00%) between the individual gerbils is expected since previous molecular characterisation assays performed on the Gerbilliscus genus have recorded intra-species genetic variation that range from 1% to 20% (Aghová et al. 2017; Colangelo et al. 2007).

TABLE 2.

Genetic and morphological species identification and voucher information for all Gerbilliscus leucogaster serum samples from Meletse, Limpopo province that were positive for the presence of Mokola virus neutralising antibodies.

UP reference number Sample information
 Museum information†
 Genetic identification information‡
Original morphological identification (Field) Museum number Morphological identification confirmation PCR assay DNA source Query cover (%) Per cent (%) identity GenBank accession number§ Genetic identification (BLAST result)
UP4962 Gerbilliscus sp. TM49197 Gerbilliscus leucogaster CytB Pectoral 99 97.78 AJ875295 Gerbilliscus leucogaster
UP12086 Gerbilliscus sp. TM49248 Gerbilliscus leucogaster CytB Kidney 100 99.79 AJ875294 Gerbilliscus leucogaster
UP12133 Gerbilliscus sp. TM49251 Gerbilliscus leucogaster CytB Kidney 66 84.33 AJ875295 Gerbilliscus leucogaster
UP12166 Gerbilliscus leucogaster TM49259 Gerbilliscus leucogaster CytB Heart 98 94.85 AJ875295 Gerbilliscus leucogaster
UP12183 Gerbilliscus leucogaster N/A Gerbilliscus leucogaster - - - - - -
UP12185 Gerbilliscus leucogaster TM50540 Gerbilliscus leucogaster CytB Rectum 86 98.31 AJ875294 Gerbilliscus leucogaster
UP12187 Gerbilliscus leucogaster TM50541 Gerbilliscus leucogaster CytB Pectoral 100 99.57 AJ875294 Gerbilliscus leucogaster
UP12193 Gerbilliscus leucogaster TM50542 Gerbilliscus leucogaster CytB Lung 97 93.33 AJ875295 Gerbilliscus leucogaster
UP12194 Gerbilliscus leucogaster NHCPHE_MAM-20 Gerbilliscus leucogaster CytB Kidney 100 99.60 KM454057 Gerbilliscus leucogaster
UP12195 Gerbilliscus leucogaster NHCPHE_MAM-21 Gerbilliscus leucogaster CytB Kidney 100 95.10 AJ875295 Gerbilliscus leucogaster
UP12196 Gerbilliscus leucogaster N/A Gerbilliscus leucogaster CytB Blood 100 89.29 AJ875295 Gerbilliscus leucogaster
UP12197 Gerbilliscus leucogaster NHCPHE_MAM-22 Gerbilliscus leucogaster CytB Kidney 100 96.59 KM454057 Gerbilliscus leucogaster
UP12202 Gerbilliscus leucogaster NHCPHE_MAM-23 Gerbilliscus leucogaster CytB Kidney 96 99.16 AJ875294 Gerbilliscus leucogaster
UP12207 Gerbilliscus leucogaster TM50543 Gerbilliscus leucogaster CytB Lung 100 93.40 KM453987 Gerbilliscus leucogaster
UP12208 Gerbilliscus sp. NHCPHE_MAM-3 Gerbilliscus leucogaster CytB Kidney 99 86.76 KM453992 Gerbilliscus leucogaster
UP12221 Gerbilliscus sp. N/A Gerbilliscus leucogaster CytB Blood 100 99.57 AJ875294 Gerbilliscus leucogaster
UP12223 Gerbilliscus sp. TM50544 Gerbilliscus leucogaster CytB Pectoral 100 97.23 AJ875295 Gerbilliscus leucogaster
UP12246 Gerbilliscus leucogaster TM50545 Gerbilliscus leucogaster CytB Pectoral 100 97.87 AJ875295 Gerbilliscus leucogaster
UP12259 Gerbilliscus sp. TM50546 Gerbilliscus leucogaster CytB Pectoral 100 100.00 AJ875294 Gerbilliscus leucogaster
UP12296 Gerbilliscus leucogaster NHCPHE_MAM-24 Gerbilliscus leucogaster CytB Heart 66 83.78 AJ865294 Gerbilliscus leucogaster
UP12297 Gerbilliscus sp. NHCPHE_MAM-5 Gerbilliscus leucogaster CytB Kidney 100 90.71 KM453986 Gerbilliscus leucogaster
UP12303 Gerbilliscus leucogaster TM50547 Gerbilliscus leucogaster CytB Pectoral 100 99.15 AJ875294 Gerbilliscus leucogaster
UP12307 Gerbilliscus leucogaster TM50548 Gerbilliscus leucogaster CytB Kidney 98 85.41 KM453992 Gerbilliscus leucogaster
UP12350 Gerbilliscus leucogaster N/A Gerbilliscus leucogaster - - - - - -
UP12354 Gerbilliscus leucogaster N/A Gerbilliscus leucogaster - - - - - -
UP12373 Gerbilliscus leucogaster N/A Gerbilliscus leucogaster CytB Blood 100 94.03 KM453987 Gerbilliscus leucogaster
UP12426 Gerbilliscus sp. N/A Gerbilliscus leucogaster CytB Blood 100 94.24 KM454060 Gerbilliscus leucogaster
UP12431 Gerbilliscus sp. N/A Gerbilliscus leucogaster - - - - - -
UP12457 Gerbilliscus sp. N/A Gerbilliscus leucogaster - - - - - -
UP12517 Gerbilliscus sp. NHCPHE_MAM-25 Gerbilliscus leucogaster CytB Pectoral 100 99.57 AJ875294 Gerbilliscus leucogaster
UP12518 Gerbilliscus sp. NHCPHE_MAM-26 Gerbilliscus leucogaster CytB Kidney 96 97.66 AJ875295 Gerbilliscus leucogaster
UP12524 Gerbilliscus sp. TM50549 Gerbilliscus leucogaster CytB Heart 81 97.10 AJ875294 Gerbilliscus leucogaster
UP12526 Gerbilliscus sp. TM50550 Gerbilliscus leucogaster CytB Kidney 97 97.45 AJ875295 Gerbilliscus leucogaster
UP12539 Gerbilliscus sp. N/A Gerbilliscus leucogaster - - - - - -
UP12543 Gerbilliscus sp. N/A Gerbilliscus leucogaster - - - - - -
UP12553 Gerbilliscus sp. N/A Gerbilliscus leucogaster - - - - - -
Open in a new tab

UP, University of Pretoria; DNA, deoxyribonucleic acid; N/A, not available; TM, Transvaal museum; NHCPHE_MAM, Natural History Collection of Public Health and Economics; CytB, Cytochrome B; PCR, polymerase chain reaction; BLAST, Basic Local Alignment Search tool.

†

, Museum information (i.e. museum number & morphological identification) for vouchers in Ditsong National Museum of Natural History (TM) and Natural History Collection of Public Health and Economics (NHCPHE_MAM), N/A refers to not available because no voucher was taken;

‡

, Genetic identification information: (1) PCR assay refers to the molecular barcoding assay that was used to determine the genetic identity of the rodent – Cytochrome B (CytB); (2) DNA source refers to the material that was used to extract DNA from for the PCR assay; (3) Query cover refers to how much the submitted sequence (i.e. the query sequence) is covered by the target sequence; (4) Per cent identity refers to the similarity of the query sequence to the target sequence; (5) GenBank accession number refers to GenBank’s reference for the target sequence; (6) BLAST results refer to the genetic identity (i.e. genus and species name) of the target sequence’s organism;

§

, The genus and species names associated with the listed GenBank accession numbers from the BLAST results refer to Tatera leucogaster. T. leucogaster underwent a taxonomic name change in 2005 and is currently referred to as Gerbilliscus leucogaster.

Members of the Gerbilliscus genus are nocturnal and terrestrial, exhibit no sexual dimorphism (Skinner & Chimimba 2005) and occupy simple to complex, deep burrows (i.e. warrens) (De Graaff 1981; Granjon & Dempster 2013). They are physiologically, morphologically and behaviourally adapted to live in arid climates (Granjon & Dempster 2013; Monadjem et al. 2015). Gerbilliscus leucogaster, however, is less arid adapted and can be found along rivers and drainage lines in open grasslands and wooded savannas (Dempster 2013; Monadjem et al. 2015). The breeding pattern and social organisation of G. leucogaster rodents are not well-understood, however, studies have reported a communal nature (De Graaff 1981; Smithers 1971) with burrows being occupied by a pair (Skinner & Chimimba 2005) and some warrens housing families or several adults (Choate 1972). The ecological nature of Bushveld gerbils may potentially be the reason why this specific rodent species are more likely to be MOKV seropositive compared to solitary rodent species belonging to the Steatomys and Rhabdomys genera occurring at Meletse.

More nucleic acid and serological surveillance studies in non-volant small mammal populations are required to obtain a better understanding of MOKV distribution, prevalence and its potential reservoir species. Brain and serum samples in this study were collected from seemingly healthy small mammals in areas that do not coincide with areas where previous MOKV cases have been reported in South Africa. Surveillance should be expanded to areas where MOKV spillover infections in cats and dogs have previously been reported. Furthermore, because lyssavirus distribution and dynamics might be influenced by seasonality, surveillance efforts should also include samples that were collected in different seasons and over multiple years. This expansion, together with representative sample sizes of certain non-volant small mammal species, will collectively increase the possibility of identifying more of these animals that are infected or that have previously been exposed to MOKV.

Acknowledgements

Competing interests

The authors declare that they have no financial or personal relationships that may have inappropriately influenced them in writing this article.

Authors’ contributions

W.C.M. performed all experiments associated with this study which forms part of his M.Sc. Medical Virology degree. J.C. and W.M. provided academic guidance and supervised the overall process and operations of this study. T.K., M.K. and L.H.S. assisted with non-volant small mammal sample collection and species identification in the field. T.K. provided museum information from the Ditsong National Museum of Natural History. All authors contributed equally to the construction of this research communication.

Ethical considerations

This study formed part of a larger surveillance programme of the Bio-surveillance and Ecology of Emerging Zoonoses Research Group in the Centre for Viral Zoonoses that focuses on zoonotic pathogens in bats and non-volant small mammals. The overall research had animal ethical clearance from the University of Pretoria’s Animal Ethics Committee (AEC) (principal investigator: W.M.; project reference number: EC071-15) and had permission to do research in terms of Section 20 of the Animal Diseases Act of 1984 (Act No. 35 of 1984) from the Department of Agriculture, Land Reform and Rural Development (DALRRD) (Project Name: Epidemiology of zoonotic pathogens in rodents, shrews and sengis in Southern Africa; project reference number: 12/11/1/1/8). Sampling permits were obtained from Limpopo’s Department of Economic Development, Environment and Tourism (ZA/LP/73972 [2016–2017] and ZA/LP/83642 [2017–2018]) and Mpumalanga’s Tourism and Parks Agency (MPB.5583 [2017]). The M.Sc. Committee from the University of Pretoria’s School of Medicine, Faculty of Health Sciences approved the protocol of this research project (Project Reference Number: 13057368). Individual animal ethical clearance (Principal Investigator: WM.; Project Reference Number: H008-18), as well as research ethical clearance was obtained from the University of Pretoria’s AEC and Research Ethics Committee (Project Reference Number: 426/2018).

Funding information

This study was funded by the South African Research Chair in Infectious Diseases of Animal (Zoonoses) from the National Research Foundation of the Department of Science and Innovation, W.M. (UID98339), as well as additional grants awarded to W.M. by the NRF (UID92524, UID85756 and UID91496). The National Research Foundation for funding the equipment based at the DNA Sanger Sequencing Facility in the Faculty of Natural of Agricultural Sciences, University of Pretoria (UID78566) and the Poliomyelitis Research Foundation.

Data availability

The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.

Disclaimer

The contents of this research communication are solely the responsibility of the authors. The opinions, findings and conclusions expressed do not necessarily reflect the official view of the National Research Foundation.

Appendix 1

TABLE 1-A1.

Non-volant small mammal species included in the surveillance of Mokola virus in South Africa.

Non-volant small mammal type Non-volant small mammal species Brain samples
 Serum samples
Amount tested Amount positive Amount tested Amount positive
Meletse, Limpopo, South Africa (n = 473)
Shrews (n = 9) Crocidura hirta 2 0 2 0
Crocidura maquassiensis 1 0 1 0
Suncus lixus 3 0 0 0
Sengis (n = 8) Elephantulus brachyrhynchus 4 0 4 0
Rodents (n = 457) Acomys selousi 2 0 3 0
Aethomys sp. 1 0 16 0
Aethomys ineptus 30 0 23 0
Aethomys chrysophilus 20 0 16 0
Gerbilliscus sp. 1 0 5 5
Gerbilliscus leucogaster 33 0 36 31
Graphiurus murinus 3 0 2 0
Lemniscomys rosalia 9 0 7 0
Mastomys coucha 45 0 23 0
Mastomys natalensis s.l. 13 0 12 0
Micaelamys sp. 0 0 3 0
Micaelamys namaquensis 11 0 10 0
Mus (Nannomys) minutoides 29 0 12 0
Rattus sp. 2 0 0 0
Saccostomus campestris 19 0 19 0
Steatomys sp. 13 0 1 0
Steatomys pratensis 21 0 16 0
Total amount of samples tested for Meletse 262 0 211 36
Secunda, Mpumalanga, South Africa (n = 102)
Shrews (n = 3) Crocidura sp. 2 0 0 0
Suncus sp. 1 0 0 0
Rodents (n = 101) Mastomys sp. 40 0 26 0
Mastomys natalensis 3 0 3 0
Rhabdomys sp. 21 0 6 0
Total amount of samples tested for Secunda 67 0 35 0
Open in a new tab

Note: Positive results are indicated in bold.

Sp., species.

TABLE 2-A1.

Sampling event details of collected Gerbilliscus leucogaster serum samples from Meletse, Limpopo province and their seropositivity.

Sampling (Month & year) Associated season† Number of serum samples collected Number of serum samples positive for MOKV VNAs Percentage Seropositivity
February 2015 Summer 1 1 100.00 1/1
January 2016 Summer 1 0 0.00 0/1
June 2016 Winter 1 1 100.00 1/1
September 2016 Spring 1 1 100.00 1/1
November 2016 Spring 1 1 100.00 1/1
March 2017 Autumn/Fall 17 15 88.24 15/17
May 2017 Autumn/Fall 9 7 77.78 7/9
August 2017 Winter 3 3 100.00 3/3
November 2017 Spring 7 7 100.00 100/100
Total 41 36 87.80% 36/41
Open in a new tab

MOKV VNAs, Mokola virus neutralising antibodies.

†

, Season delineation in South Africa: (1) Summer, 01 December to 28/29 February; (2) Autumn/Fall, 01 March to 31 May; (3) Winter, 01 June to 31 August; (4) Spring, 01 September to 30 November.

TABLE 3-A1.

The 50% end-point neutralisation titres of all Gerbilliscus leucogaster serum samples from Meletse, Limpopo province that were positive for the presence of Mokola virus neutralising antibodies.

Reference number Serum sample information
 Initial screening‡
 Follow-up screening‡
 MOKV VNA titre
Sample collection date Sex 1:10 (i) 1:25 (i) 1:10 (f) 1:25 (f) 1:10 (i) 1:50 (i) 1:250 (i) 1:1250 (i) Log ED50§ (i) 1:10 (f) 1:50 (f) 1:250 (f) 1:1250 (f) Log ED50§ (f) Average Log ED50 ± s.d.
UP4962† 26 Feb 2015 M 1 3 1 3 1 6 9 10 1.59 1 6 10 10 1.53 1.56 ± 0.03
UP12086† 08 June 2016 M 0 2 0 2 0 5 8 10 1.83 1 5 8 10 1.76 1.80 ± 0.04
UP12133† 06 Sept. 2016 M 2 4 2 4 2 6 9 10 1.53 2 6 10 10 1.48 1.51 ± 0.03
UP12166† 09 Nov. 2016 M 0 1 0 2 0 3 6 9 2.17 0 3 7 10 2.05 2.11 ± 0.06
UP12183 27 Mar. 2017 F 1 2 0 2 0 4 8 10 1.92 0 5 9 10 1.77 1.85 ± 0.08
UP12185† 27 Mar. 2017 F 0 3 1 3 0 4 8 9 1.97 0 4 8 10 1.92 1.95 ± 0.03
UP12187† 27 Mar. 2017 F 1 5 1 4 0 6 8 10 1.40 1 6 9 10 1.58 1.49 ± 0.09
UP12193† 28 Mar. 2017 M 0 1 0 1 0 3 7 9 2.10 0 4 8 10 1.92 2.01 ± 0.09
UP12194† 28 Mar. 2017 F 0 0 0 0 0 3 7 10 2.05 0 3 7 10 2.05 2.05
UP12195† 28 Mar. 2017 M 0 0 1 0 0 2 8 10 2.05 0 3 7 10 2.05 2.05
UP12196†† 28 Mar. 2017 F 1 0 0 0 - - - - - - - - - - -
UP12197† 28 Mar. 2017 M 0 0 0 0 0 5 8 10 1.83 0 4 9 10 1.87 1.85 ± 0.02
UP12202† 28 Mar. 2017 F 1 3 0 4 0 6 8 10 1.40 0 6 8 10 1.40 1.40
UP12207† 28 Mar. 2017 M 0 0 0 0 0 1 5 8 2.46 0 2 4 8 2.51 2.49 ± 0.02
UP12208† 28 Mar. 2017 F 0 2 0 1 0 7 10 10 1.50 0 8 10 10 1.44 1.47 ± 0.03
UP12221 29 Mar. 2017 F 0 2 0 1 0 6 9 10 1.64 0 7 10 10 1.50 1.57 ± 0.07
UP12223† 29 Mar. 2017 M 1 3 0 2 0 4 7 10 1.98 1 5 8 10 1.76 1.87 ± 0.11
UP12246† 30 Mar. 2017 M 0 5 1 6 0 8 10 10 1.44 0 8 10 10 1.44 1.44
UP12259† 31 Mar. 2017 F 0 5 0 4 0 8 10 10 1.44 0 8 10 10 1.44 1.44
UP12296† 16-May-2017 M 0 4 1 5 1 7 10 10 1.45 2 8 10 10 1.35 1.40 ± 0.05
UP12297† 16 May 2017 F 1 5 0 5 0 7 10 10 1.50 0 7 10 10 1.50 1.50
UP12303† 16 May 2017 F 2 4 2 5 1 7 10 10 1.45 2 8 10 10 1.35 1.40 ± 0.05
UP12307† 16 May 2017 F 0 0 0 0 0 3 6 9 2.17 0 4 6 10 2.05 2.11 ± 0.06
UP12350 18 May 2017 M 2 5 1 5 1 7 10 10 1.45 1 8 10 10 1.40 1.42 ± 0.03
UP12354 18 May 2017 F 0 3 0 2 0 5 8 10 1.83 0 5 9 10 1.77 1.80 ± 0.03
Open in a new tab

UP, University of Pretoria; MOKV VNA, Mokola virus neutralising antibodies ; ED50, effective dose; s.d., standard deviation; F, female; M, male.

†

, Small non-volant mammal individuals that were collected as voucher specimens and whose brains were negative for the presence of MOKV RNA. Animal ethics clearance was obtained from the University of Pretoria’s Animal Ethics Committee (Reference Numbers: EC071-15 & H008-18);

‡

, Results for the 1:10, 1:25, 1:50, 1:250 & 1:1250 serum dilutions are recorded as a number that represents the number of fields (out of a total of 10) that contain MOKV 12/458 infected cells for both initial (i) and duplicate (f) rounds of the micro-neutralisation test;

§

, The log10 50% end-point (ED) neutralisation titre for each serum sample as calculated by Reed and Muench (1938);

, The average log10 50% ED neutralisation titre, together with the standard deviation (s.d.) for each serum sample as calculated by Reed and Muench (1938);

††

, Follow-up screening could not be completed as the serum sample was depleted during initial screening.

TABLE 4-A1.

Micro-neutralisation test results of all non-volant small mammal serum samples that tested negative for the presence of Mokola virus neutralising antibodies.

Reference number Serum sample information
 Initial screening†
Sample collection date Non-volant small mammal type Non-volant small mammal species 1:10 (i) 1:25 (i) 1:10 (f) 1:25 (f)
Meletse, Limpopo, South Africa (n = 211)
4961 26 Feb. 2015 Rodent Aethomys chrysophilus 10 10 9 10
4963 26 Feb. 2015 Rodent Aethomys chrysophilus 10 10 10 10
4967 27 Feb. 2015 Rodent Aethomys chrysophilus 10 10 10 10
4968 27 Feb. 2015 Rodent Saccostomus campestris 7 10 8 10
4969 27 Feb. 2015 Rodent Aethomys chrysophilus 7 10 8 10
5011 03 Mar. 2015 Rodent Steatomys pratensis 10 10 10 10
5012 03 Mar. 2015 Rodent Aethomys chrysophilus 7 9 7 10
5015 04 Mar. 2015 Rodent Steatomys pratensis 9 10 10 10
5017 05 Mar. 2015 Rodent Steatomys pratensis 8 10 10 10
5352 12 May 2015 Rodent Aethomys ineptus 10 10 9 10
5353 12 May 2015 Sengi Elephantulus brachyrhynchus 10 10 10 10
5354 12 May 2015 Rodent Mastomys coucha 10 10 10 10
5355 12 May 2015 Sengi Elephantulus brachyrhynchus 9 10 10 10
5356 12 May 2015 Rodent Mastomys natalensis 10 9 10 10
5525 22 July 2015 Rodent Aethomys chrysophilus 8 10 9 10
5527 23 July 2015 Shrew Crocidura maquassiensis 10 10 10 10
5528 24 July 2015 Rodent Mastomys coucha 10 10 9 10
5529 24 July 2015 Rodent Mus (Nannomys) minutoides 9 10 10 10
5934 15 Sept. 2015 Rodent Mus (Nannomys) minutoides 9 9 10 10
5935 15 Sept. 2015 Rodent Micaelamys namaquensis 9 10 10 10
5936 15 Sept. 2015 Rodent Aethomys ineptus 10 10 9 10
5939 17 Sept. 2015 Rodent Mus (Nannomys) minutoides 9 10 8 10
12001 10 Nov. 2015 Rodent Mastomys coucha 10 10 10 10
12003 11 Nov. 2015 Rodent Aethomys chrysophilus 10 10 10 10
12004 11 Nov. 2015 Rodent Steatomys pratensis 10 10 10 10
12005 12 Nov. 2015 Rodent Aethomys ineptus 5 9 6 10
12006 13 Nov. 2015 Rodent Aethomys ineptus 10 10 10 10
12007 13 Nov. 2015 Rodent Steatomys pratensis 10 10 10 10
12010 19 Jan. 2016 Rodent Mastomys coucha 10 10 10 10
12011 19 Jan. 2016 Rodent Steatomys pratensis 10 10 10 10
12012 19 Jan. 2016 Rodent Gerbilliscus leucogaster 10 10 10 10
12018 20 Jan. 2016 Rodent Mastomys coucha 10 10 10 10
12019 20 Jan. 2016 Rodent Saccostomus campestris 9 10 10 10
12020 20 Jan. 2016 Rodent Mastomys coucha 9 10 10 10
12023 20 Jan. 2016 Rodent Saccostomus campestris 10 10 9 10
12062 05 Apr. 2016 Rodent Saccostomus campestris 10 9 10 10
12065 06 Apr. 2016 Rodent Saccostomus campestris 10 10 10 10
12066 06 Apr. 2016 Rodent Graphiurus murinus 10 10 10 10
12067 06 Apr. 2016 Rodent Aethomys ineptus 9 10 10 10
12075 07 June 2016 Rodent Mastomys natalensis 10 10 9 10
12081 07 June 2016 Rodent Aethomys ineptus 2 8 2 8
12082 07 June 2016 Rodent Aethomys ineptus 10 10 10 10
12083 07 June 2016 Rodent Acomys selousi 10 10 10 10
12084 08 June 2016 Rodent Saccostomus campestris 8 10 9 10
12085 08 June 2016 Rodent Micaelamys namaquensis 10 10 10 10
12087 08 June 2016 Rodent Aethomys ineptus 10 10 9 10
12088 09 June 2016 Rodent Aethomys chrysophilus 10 10 10 10
12132 06 Sept. 2016 Rodent Aethomys ineptus 9 9 10 10
12134 06 Sept. 2016 Rodent Micaelamys sp. 8 10 10 10
12140 07 Sept. 2016 Rodent Micaelamys sp. 9 9 10 10
12142 07 Sept. 2016 Sengi Elephantulus brachyrhynchus 9 9 10 10
12143 08 Sept. 2016 Rodent Micaelamys sp. 8 9 10 10
12145 09 Sept. 2016 Rodent Micaelamys namaquensis 9 10 9 10
12146 09 Sept. 2016 Rodent Acomys selousi 10 10 9 10
12147 09 Sept. 2016 Rodent Steatomys pratensis 10 10 9 10
12148 09 Sept. 2016 Rodent Saccostomus campestris 10 10 10 10
12149 09 Sept. 2016 Rodent Saccostomus campestris 10 10 10 10
12154 08 Nov. 2016 Rodent Micaelamys namaquensis 9 10 10 10
12157 08 Nov. 2016 Rodent Aethomys chrysophilus 9 10 10 10
12159 09 Nov. 2016 Rodent Saccostomus campestris 9 10 10 10
12167 09 Nov. 2016 Rodent Aethomys chrysophilus 9 9 10 10
12168 10 Nov. 2016 Rodent Micaelamys namaquensis 8 9 10 10
12169 10 Nov. 2016 Rodent Mus (Nannomys) minutoides 10 10 10 10
12170 10 Nov. 2016 Rodent Aethomys chrysophilus 8 10 7 10
12171 11 Nov. 2016 Rodent Acomys spp. 9 10 8 10
12176 07 Feb. 2017 Rodent Saccostomus campestris 3 9 3 10
12177 08 Feb. 2017 Rodent Aethomys chrysophilus 9 10 7 10
12178 08 Feb. 2017 Rodent Aethomys ineptus 6 9 7 9
12179 08 Feb. 2017 Rodent Aethomys ineptus 6 9 7 9
12180 09 Feb. 2017 Rodent Aethomys chrysophilus 10 10 9 10
12181 09 Feb. 2017 Rodent Aethomys chrysophilus 10 10 10 10
12184 27 Mar. 2017 Rodent Gerbilliscus leucogaster 3 6 2 6
12188 27 Mar. 2017 Rodent Saccostomus campestris 9 9 10 10
12189 27 Mar. 2017 Rodent Saccostomus campestris 7 10 6 9
12190 27 Mar. 2017 Rodent Steatomys pratensis 10 10 10 10
12191 27 Mar. 2017 Rodent Steatomys pratensis 10 10 10 10
12192 28 Mar. 2017 Rodent Steatomys pratensis 10 10 9 10
12200 28 Mar. 2017 Rodent Gerbilliscus leucogaster 4 7 5 7
12201 28 Mar. 2017 Rodent Steatomys pratensis 10 10 9 10
12203 28 Mar. 2017 Rodent Mastomys coucha 6 9 6 10
12204 28 Mar. 2017 Rodent Aethomys ineptus 7 10 8 10
12205 28 Mar. 2017 Rodent Mastomys coucha 9 10 10 10
12206 28 Mar. 2017 Rodent Mastomys coucha 5 9 8 9
12209 29 Mar. 2017 Rodent Aethomys chrysophilus 8 10 7 10
12210 29 Mar. 2017 Rodent Mastomys coucha 10 10 10 10
12211 29 Mar. 2017 Rodent Steatomys pratensis 9 10 8 10
12212 29 Mar. 2017 Rodent Aethomys chrysophilus 8 10 9 10
12213 29 Mar. 2017 Shrew Crocidura hirta 9 10 8 9
12215 29 Mar. 2017 Rodent Mus (Nannomys) minutoides 7 10 8 9
12216 29 Mar. 2017 Rodent Steatomys pratensis 10 10 10 10
12217 29 Mar. 2017 Rodent Mastomys coucha 8 10 7 10
12218 29 Mar. 2017 Rodent Saccostomus campestris 8 9 10 10
12219 29 Mar. 2017 Rodent Steatomys pratensis 8 10 8 10
12236 30 Mar. 2017 Rodent Saccostomus campestris 9 10 8 10
12237 30 Mar. 2017 Rodent Mus (Nannomys) minutoides 9 10 9 10
12238 30 Mar. 2017 Rodent Mastomys coucha 7 10 6 10
12240 30 Mar. 2017 Rodent Saccostomus campestris 10 10 10 10
12242 30 Mar. 2017 Rodent Aethomys ineptus 9 10 7 10
12244 30 Mar. 2017 Rodent Saccostomus campestris 10 10 10 10
12248 30 Mar. 2017 Rodent Saccostomus campestris 10 10 10 10
12256 31 Mar. 2017 Rodent Graphiurus murinus 8 10 10 10
12258 31 Mar. 2017 Rodent Steatomys pratensis 10 10 10 10
12260 31 Mar. 2017 Rodent Steatomys pratensis 10 10 10 10
12285 16 May 2017 Rodent Micaelamys namaquensis 8 9 9 10
12289 16 May 2017 Rodent Saccostomus campestris 10 10 10 10
12291 16 May 2017 Rodent Micaelamys namaquensis 9 10 10 10
12292 16 May 2017 Rodent Aethomys ineptus 9 10 10 10
12294 16 May 2017 Rodent Aethomys ineptus 8 10 8 10
12295 16 May 2017 Rodent Aethomys ineptus 10 10 10 10
12298 16 May 2017 Rodent Mastomys coucha 10 10 10 10
12299 16 May 2017 Rodent Mus (Nannomys) minutoides 10 10 10 10
12300 16 May 2017 Rodent Mastomys coucha 9 10 10 10
12301 16 May 2017 Rodent Mastomys coucha 10 10 10 10
12302 16 May 2017 Rodent Aethomys sp. 10 10 10 10
12304 16 May 2017 Rodent Aethomys sp. 10 10 10 10
12305 16 May 2017 Rodent Lemniscomys rosalia 9 10 10 10
12306 16 May 2017 Rodent Mastomys coucha 9 10 10 10
12311 17 May 2017 Rodent Mastomys natalensis 9 10 10 10
12319 17 May 2017 Rodent Micaelamys namaquensis 9 10 10 10
12320 17 May 2017 Rodent Gerbilliscus leucogaster 1 6 2 7
12321 17 May 2017 Rodent Aethomys ineptus 8 10 10 10
12324 17 May 2017 Rodent Gerbilliscus leucogaster 9 10 10 10
12329 17 May 2017 Rodent Mastomys coucha 10 10 10 10
12331 17 May 2017 Rodent Mastomys natalensis 10 10 10 10
12332 17 May 2017 Rodent Mastomys coucha 10 10 10 10
12348 18 May 2017 Rodent Mastomys coucha 10 10 10 10
12349 18 May 2017 Rodent Aethomys sp. 10 10 10 10
12356 18 May 2017 Rodent Aethomys sp. 10 10 10 10
12365 18 May 2017 Rodent Aethomys sp. 7 10 10 10
12366 18 May 2017 Rodent Mus (Nannomys) minutoides 10 10 10 10
12367 18 May 2017 Rodent Mastomys coucha 7 10 8 10
12374 18 May 2017 Rodent Aethomys ineptus 9 10 10 10
12375 18 May 2017 Rodent Mastomys natalensis 10 10 10 10
12376 18 May 2017 Rodent Mastomys coucha 9 10 10 10
12377 19 May 2017 Rodent Mus (Nannomys) minutoides 7 10 10 10
12378 18 May 2017 Rodent Steatomys sp. 10 10 10 10
12380 19 May 2017 Rodent Aethomys ineptus 10 10 10 10
12381 19 May 2017 Rodent Mastomys natalensis 10 10 10 10
12394 29 Aug. 2017 Rodent Mastomys natalensis 6 10 5 10
12395 29 Aug. 2017 Rodent Mastomys natalensis 10 10 10 10
12405 29 Aug. 2017 Rodent Aethomys sp. 10 10 10 10
12406 29 Aug. 2017 Rodent Aethomys sp. 10 10 10 10
12409 29 Aug. 2017 Rodent Aethomys sp. 10 10 9 10
12414 29 Aug. 2017 Sengi Elephantulus brachyrhynchus 10 10 10 10
12422 29 Aug. 2017 Rodent Aethomys sp. 9 10 10 10
12423 29 Aug. 2017 Rodent Aethomys sp. 9 10 9 10
12428 29 Aug. 2017 Rodent Lemniscomys rosalia 10 10 10 10
12434 29 Aug. 2017 Rodent Aethomys ineptus 10 10 10 10
12435 29 Aug. 2017 Rodent Aethomys ineptus 10 10 10 10
12438 29 Aug. 2017 Rodent Aethomys sp. 10 10 10 10
12442 29 Aug. 2017 Rodent Aethomys sp. 9 10 10 10
12443 29 Aug. 2017 Rodent Lemniscomys rosalia 9 10 10 10
12447 30 Aug. 2017 Rodent Micaelamys namaquensis 10 10 10 10
12449 30 Aug. 2017 Rodent Aethomys sp. 10 10 10 10
12452 30 Aug. 2017 Rodent Aethomys sp. 9 10 9 10
12453 30 Aug. 2017 Rodent Aethomys sp. 10 10 10 10
12458 30 Aug. 2017 Rodent Mastomys coucha 10 10 10 10
12468 30 Aug. 2017 Rodent Aethomys sp. 10 10 10 10
12474 31 Aug. 2017 Rodent Aethomys ineptus 10 10 10 10
12475 31 Aug. 2017 Rodent Lemniscomys rosalia 10 10 10 10
12515 21 Nov. 2017 Rodent Mastomys natalensis 10 10 10 10
12516 21 Nov. 2017 Rodent Lemniscomys rosalia 10 10 10 10
12519 21 Nov. 2017 Rodent Mastomys natalensis 10 10 10 10
12520 21 Nov. 2017 Rodent Lemniscomys rosalia 7 10 10 10
12521 21 Nov. 2017 Rodent Mastomys natalensis 10 10 10 10
12525 21 Nov. 2017 Rodent Mastomys natalensis 10 10 10 10
12538 21 Nov. 2017 Rodent Lemniscomys rosalia 8 10 7 10
12547 23 Nov. 2017 Shrew Crocidura hirta 10 10 10 10
12549 23 Nov. 2017 Rodent Mus (Nannomys) minutoides 9 10 10 10
12552 23 Nov. 2017 Rodent Aethomys ineptus 10 10 10 10
12556 23 Nov. 2017 Rodent Micaelamys namaquensis 10 10 10 10
12557 23 Nov. 2017 Rodent Mus (Nannomys) minutoides 7 10 6 10
12558 23 Nov. 2017 Rodent Saccostomus campestris 6 10 6 10
12562 24 Nov. 2017 Rodent Mus (Nannomys) minutoides 10 10 10 10
12563 24 Nov. 2017 Rodent Mastomys coucha 10 10 10 10
Secunda, Mpumalanga, South Africa (n = 35)
5532 30 June 2015 Rodent Mastomys sp. 9 9 9 10
5552 01 July 2015 Rodent Mastomys sp. 10 10 10 10
5553 01 July 2015 Rodent Mastomys sp. 4 6 5 6
5566 02 July 2015 Rodent Mastomys sp. 9 10 10 9
5567 02 July 2015 Rodent Mastomys sp. 9 10 10 10
5568 02 July 2015 Rodent Rhabdomys sp. 10 10 10 10
5569 02 July 2015 Rodent Rhabdomys sp. 10 10 10 10
5570 03 July 2015 Rodent Mastomys sp. 10 10 10 9
5571 03 July 2015 Rodent Mastomys sp. 10 9 10 10
5572 03 July 2015 Rodent Rhabdomys sp. 10 10 10 10
5573 03 July 2015 Rodent Mastomys sp. 10 10 10 10
5574 03 July 2015 Rodent Mastomys sp. 10 10 10 10
5575 03 July 2015 Rodent Rhabdomys sp. 9 10 10 9
5576 03 July 2015 Rodent Rhabdomys sp. 9 10 10 10
5577 03 July 2015 Rodent Mastomys sp. 9 10 10 10
5580 03 July 2015 Rodent Mastomys sp. 10 10 10 10
5581 03 July 2015 Rodent Mastomys sp. 9 10 9 9
5582 03 July 2015 Rodent Mastomys sp. 10 10 9 10
5584 03 July 2015 Rodent Mastomys sp. 10 10 10 10
5585 03 July 2015 Rodent Mastomys sp. 9 9 10 9
5586 03 July 2015 Rodent Mastomys sp. 9 10 10 10
12025 26 Jan. 2016 Rodent Mastomys natalensis 9 10 9 10
12026 26 Jan. 2016 Rodent Mastomys natalensis 10 10 10 10
12027 26 Jan. 2016 Rodent Mastomys natalensis 10 10 10 10
12028 27 Jan. 2016 Rodent Mastomys sp. 9 10 8 10
12029 27 Jan. 2016 Rodent Mastomys sp. 10 10 10 10
12030 27 Jan. 2016 Rodent Mastomys sp. 10 10 10 10
12031 27 Jan. 2016 Rodent Rhabdomys sp. 10 10 10 10
12032 27 Jan. 2016 Rodent Mastomys sp. 5 8 5 7
12034 27 Jan. 2016 Rodent Mastomys sp. 10 10 10 10
12035 28 Jan. 2016 Rodent Mastomys sp. 8 10 3 10
12036 28 Jan. 2016 Rodent Mastomys sp. 10 10 10 10
12037 28 Jan. 2016 Rodent Mastomys sp. 10 10 10 10
12038 28 Jan. 2016 Rodent Mastomys sp. 9 10 10 10
12050 29 Jan. 2016 Rodent Mastomys sp. 10 10 10 10
Open in a new tab

Sp., species.

†

, Results for the 1:10 and 1:25 serum dilutions are recorded as a number that represents the number of fields (out of a total of 10) that contain MOKV 12/458 infected cells for both initial (i) and duplicate (f) rounds of the micro-neutralisation test.

Appendix 2

Additional References

  1. Bingham, J., Javangwe, S., Sabeta, C.T., Wandeler, A.I. & Nel, L.H., 2001, ‘Report of isolations of unusual lyssaviruses (rabies and Mokola virus) identified retrospectively from Zimbabwe’, Journal of the South African Veterinary Association 72(2), 92–94. 10.4102/jsava.v72i2.624 [DOI] [PubMed] [Google Scholar]
  2. Causey, O.R. & Kemp, G.E., 1968, ‘Surveillance and study of viral infections of vertebrates in Nigeria’, Nigerian Journal of Science 2, 131–135. [Google Scholar]
  3. Familusi, J.B. & Moore, D.L., 1972, ‘Isolation of a rabies-related virus from the cerebrospinal fluid of a child with “aseptic meningitis”’, African Journal of Medical Sciences 3(1), 93–96. [PubMed] [Google Scholar]
  4. Foggin, C.M., 1982, ‘Atypical rabies virus in cats and a dog in Zimbabwe’, Veterinary Record 110(14), 338–338. 10.1136/vr.110.14.338 [DOI] [PubMed] [Google Scholar]
  5. Foggin, C.M., 1983, ‘Mokola virus infection in cats and a dog in Zimbabwe’, The Veterinary Record 113(5), 115. 10.1136/vr.113.5.115 [DOI] [PubMed] [Google Scholar]
  6. Mebatsion, T., Cox, J.H. & Frost, J.W., 1992, ‘Isolation and characterization of 115 street rabies virus isolates from Ethiopia by using monoclonal antibodies: Identification of 2 isolates as Mokola and Lagos bat viruses’, Journal of Infectious Diseases 166(5), 972–977. 10.1093/infdis/166.5.972 [DOI] [PubMed] [Google Scholar]
  7. Meredith, C.D. & Nel, L.H., 1996, ‘Further isolation of Mokola virus in South Africa’, The Veterinary Record 138(5), 119–120. [PubMed] [Google Scholar]
  8. Nel, L., Jacobs, J., Jaftha, J., Von Teichman, B. & Bingham, J., 2000, ‘New cases of Mokola virus infection in South Africa: A genotypic comparison of Southern African virus isolates’, Virus Genes 20(2), 103–106. 10.1023/A:1008120511752 [DOI] [PubMed] [Google Scholar]
  9. Sabeta, C.T., Blumberg, L., Miyen, J., Mohale, D., Shumba, W. & Wandeler, A., 2010, ‘Mokola virus involved in a human contact (South Africa)’, FEMS Immunology & Medical Microbiology 58(1), 85–90. 10.1111/j.1574-695X.2009.00609.x [DOI] [PubMed] [Google Scholar]
  10. Sabeta, C.T., Markotter, W., Mohale, D.K., Shumba, W., Wandeler, A.I. & Nel, L.H., 2007, ‘Mokola virus in domestic mammals, South Africa’, Emerging Infectious Diseases 13(9), 1371. 10.3201/eid1309.070466 [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Von Teichman, B.F., De Koker, W.C., Bosch, S.J.E., Bishop, G.C., Meredith, C.D. & Bingham, J., 1998, ‘Mokola virus infection: Description of recent South African cases and a review of the virus epidemiology: Case report’, Journal of the South African Veterinary Association 69(4), 169–171. 10.4102/jsava.v69i4.847 [DOI] [PubMed] [Google Scholar]

Footnotes

How to cite this article: McMahon, W.C., Coertse, J., Kearney, T., Keith, M., Swanepoel, L.H. & Markotter, W., 2021, ‘Surveillance of the rabies-related lyssavirus, Mokola in non-volant small mammals in South Africa’, Onderstepoort Journal of Veterinary Research 88(1), a1911. https://doi.org/10.4102/ojvr.v88i1.1911

References

  1. Aghomo, H.O., Tomori, O., Oduye, O.O. & Rupprecht, C.E., 1990, ‘Detection of Mokola virus neutralising antibodies in Nigerian dogs’, Research in Veterinary Science 48(2), 264. 10.1016/S0034-5288(18)31005-1 [DOI] [PubMed] [Google Scholar]
  2. Aghová, T., Šumbera, R., Piálek, L., Mikula, O., McDonough, M.M., Lavrenchenko, L.A. et al. , 2017, ‘Multilocus phylogeny of East African gerbils (Rodentia, Gerbilliscus) illuminates the history of the Somali-Masai savanna’, Journal of Biogeography 44(10), 2295–2307. 10.1111/jbi.13017 [DOI] [Google Scholar]
  3. Causey, O.R., Kemp, G.E., Madbouly, M.H. & Lee, V.H., 1969, ‘Arbovirus surveillance in Nigeria, 1964–1967’, Bulletin de la Société de Pathologie Exotique 62(2), 249–253. [PubMed] [Google Scholar]
  4. Choate, T.S., 1972, ‘Behavioural studies on some Rhodesian rodents’, African Zoology 7(1), 103–118. 10.1080/00445096.1972.11447433 [DOI] [Google Scholar]
  5. Coertse, J., Markotter, W., Le Roux, K., Stewart, D., Sabeta, C.T. & Nel, L.H., 2017, ‘New isolations of the rabies-related Mokola virus from South Africa’, BMC Veterinary Research 13(1), 37. 10.1186/s12917-017-0948-0 [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Coertse, J., Weyer, J., Nel, L.H. & Markotter, W., 2019, ‘Reverse transcription recombinase polymerase amplification assay for rapid detection of canine associated rabies virus in Africa’, PLoS One 14(7), e0219292. 10.1371/journal.pone.0219292 [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Colangelo, P., Granjon, L., Taylor, P.J. & Corti, M., 2007, ‘Evolutionary systematics in African gerbilline rodents of the genus Gerbilliscus: Inference from mitochondrial genes’, Molecular Phylogenetics and Evolution 42(3), 797–806. 10.1016/j.ympev.2006.10.001 [DOI] [PubMed] [Google Scholar]
  8. De Graaff, G., 1981, The rodents of southern Africa: Notes on their identification, distribution, ecology, and taxonomy, Butterworth-Heinemann, Oxford, United Kingdom. [Google Scholar]
  9. Dempster, E.R., 2013, ‘Gerbilliscus leucogaster’, Mammals of Africa 3, 279–281. [Google Scholar]
  10. Foggin, C.M., 1988, ‘Rabies and rabies-related viruses in Zimbabwe: Historical, virological and ecological aspects’, PhD thesis, University of Zimbabwe, Harare. [Google Scholar]
  11. Granjon, L. & Dempster, E.R., 2013, ‘Genus Gerbilliscus gerbils’, Mammals of Africa 3, 268–270. [Google Scholar]
  12. Greenberg, J.A., DiMenna, M.A., Hanelt, B. & Hofkin, B.V., 2012, ‘Analysis of post-blood meal flight distances in mosquitoes utilizing zoo animal blood meals’, Journal of Vector Ecology 37(1), 83–89. 10.1111/j.1948-7134.2012.00203.x [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kemp, G.E., Causey, O.R., Moore, D.L., Odelola, A. & Fabiyi, A., 1972, ‘Mokola virus’, The American Journal of Tropical Medicine and Hygiene 21(3), 356–359. 10.4269/ajtmh.1972.21.356 [DOI] [PubMed] [Google Scholar]
  14. Kgaladi, J., Wright, N., Coertse, J., Markotter, W., Marston, D., Fooks, A.R. et al. , 2013, ‘Diversity and epidemiology of Mokola virus’, PLoS Neglected Tropical Diseases 7(10), e2511. 10.1371/journal.pntd.0002511 [DOI] [PMC free article] [PubMed] [Google Scholar]
  15. Kuzmin, I.V., Niezgoda, M., Franka, R., Agwanda, B., Markotter, W., Beagley, J.C. et al. , 2008, ‘Lagos bat virus in Kenya’, Journal of Clinical Microbiology 46(4), 1451–1461. 10.1128/JCM.00016-08 [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Le Gonidec, G., Rickenbach, A., Robin, Y. & Heme, G., 1978, ‘Isolement d’une souche de virus Mokola au Cameroun’, Annales des Microbiologie (Institute Pasteur) 129(A), 245–249. [PubMed] [Google Scholar]
  17. Meester, J.A.J., Rautenbach, I.L., Dippenaar, N.J. & Baker, C.M., 1986, ‘Classification of Southern African mammals’, Transvaal Museum Monograph 5(1), 1–359. [Google Scholar]
  18. Monadjem, A., Taylor, P.J., Denys, C. & Cotterill, F.P., 2015, Rodents of sub-Saharan Africa: A biogeographic and taxonomic synthesis, Walter de Gruyter GmbH & Co. KG, Berlin, Germany [Google Scholar]
  19. Newbery, C.H., 1999, ‘A key to the Soricidae, Macroscelididae, Gliridae and Muridae of Gauteng, North West Province, Mpumalanga and the Northern province, South Africa’, Koedoe 42(1), 51–55. 10.4102/koedoe.v42i1.221 [DOI] [Google Scholar]
  20. Nottidge, H.O., Omobowale, T.O. & Oladiran, O.O., 2007, ‘Mokola virus antibodies in humans, dogs, cats, cattle, sheep, and goats in Nigeria’, International Journal of Applied Research in Veterinary Medicine 5(3), 105. [Google Scholar]
  21. Ogunkoya, A.B., Beran, G.W., Umoh, J.U., Gomwalk, N.E. & Abdulkadir, I.A., 1990, ‘Serological evidence of infection of dogs and man in Nigeria by lyssaviruses (family Rhabdoviridae)’, Transactions of the Royal Society of Tropical Medicine and Hygiene 84(6), 842–845. 10.1016/0035-9203(90)90103-L [DOI] [PubMed] [Google Scholar]
  22. Rautenbach, I.L., 1982, Mammals of the Transvaal, Ecoplan monograph no. 1:1–211, Transvaal Museum, Pretoria. [Google Scholar]
  23. Reed, L.J. & Muench, H., 1938, ‘A simple method of estimating fifty per cent endpoints’, American Journal of Epidemiology 27(3), 493–497. 10.1093/oxfordjournals.aje.a118408 [DOI] [Google Scholar]
  24. Saluzzo, J.F., Rollin, P.E., Dauguet, C., Digoutte, J.P., Georges, A.J. & Sureau, P., 1984, ‘Premier isolement du virus Mokola à partir d’un rongeur (Lophuromys sikapusi)’, Annales de l’Institut Pasteur/Virologie 135(1), 57–66. 10.1016/S0769-2617(84)80039-8 [DOI] [Google Scholar]
  25. Sikes, R.S. & Gannon, W.L., 2011, ‘Guidelines of the American society of mammalogists for the use of wild mammals in research’, Journal of Mammalogy 92(1), 235–253. 10.1644/10-MAMM-F-355.1 [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Skinner, J.D. & Chimimba, C.T., 2005, The mammals of the Southern African sub-region, Cambridge University Press, United Kingdom. [Google Scholar]
  27. Smithers, R.H.N., 1971, A checklist of the mammals of Botswana, Trustees of the National Museum of Rhodesia, Salisbury. [Google Scholar]
  28. Smith, T.G. & Gilbert, A.T., 2017, ‘Comparison of a micro-neutralization test with the rapid fluorescent focus inhibition test for measuring rabies virus neutralizing antibodies’, Tropical Medicine and Infectious Disease 2(3), 24. 10.3390/tropicalmed2030024 [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Walker, P.J., Breyta, R., Blasdell, K.R., Calisher, C.H., Dietzgen, R.G., Fooks, A.R. et al. , 2018, ‘Rhabdoviridaee’, in Kuhn J.H. & Siddel S.G. (eds.), ICTV Report Negative-sense RNA viruses, Journal of Gen eral Virology, 99, 447–448. viewed 24 May 2020, from https://talk.ictvonline.org/ictv-reports/ictv_online_report/negative-sense-rna-viruses/w/rhabdoviridae [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Availability Statement

The authors confirm that the data supporting the findings of this study are available within the article and its supplementary materials.

Articles from The Onderstepoort Journal of Veterinary Research are provided here courtesy of AOSIS

RESOURCES