Molecular detection of viruses in Kenyan bats and discovery of novel astroviruses, caliciviruses and rotaviruses
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This is the first country-wide surveillance of bat-borne viruses in Kenya spanning from 2012–2015 covering sites perceived to have medium to high level bat-human interaction. The objective of this surveillance study was to apply a non-invasive approach using fresh feces to detect viruses circulating within the diverse species of Kenyan bats. We screened for both DNA and RNA viruses; specifically, astroviruses (AstVs), adenoviruses (ADVs), caliciviruses (CalVs), coronaviruses (CoVs), flaviviruses, filoviruses, paramyxoviruses (PMVs), polyomaviruses (PYVs) and rotaviruses. We used family-specific primers, amplicon sequencing and further characterization by phylogenetic analysis. Except for filoviruses, eight virus families were detected with varying distributions and positive rates across the five regions (former provinces) studied. AstVs (12.83%), CoVs (3.97%), PMV (2.4%), ADV (2.26%), PYV (1.65%), CalVs (0.29%), rotavirus (0.19%) and flavivirus (0.19%). Novel CalVs were detected in Rousettus aegyptiacus and Mops condylurus while novel Rotavirus-A-related viruses were detected in Taphozous bats and R. aegyptiacus. The two Rotavirus A (RVA) strains detected were highly related to human strains with VP6 genotypes I2 and I16. Genotype I16 has previously been assigned to human RVA-strain B10 from Kenya only, which raises public health concern, particularly considering increased human-bat interaction. Additionally, 229E-like bat CoVs were detected in samples originating from Hipposideros bats roosting in sites with high human activity. Our findings confirm the presence of diverse viruses in Kenyan bats while providing extended knowledge on bat virus distribution. The detection of viruses highly related to human strains and hence of public health concern, underscores the importance of continuous surveillance.
Keywordsastroviruses (AstVs) calicivirus (CalVs) Rotavirus A 229-E-like bat coronavirus
We are grateful for the Government of Kenya who permitted this study, specifically the Directors of Kenya Wildlife Service and National Museums of Kenya. We also appreciate the field and laboratory teams in Kenya and China who assisted in many different ways towards the success of this work. This work was funded by Sino-Africa Joint Research Center (SAJC201313 and SAJC 201605).
Z-LS, SO and CW designed the study. Z-LS, SO, BA and VO coordinated the study. Z-LS, SO, VO, BA, FG, XYG, XLY, LJW and CW participated and supported in field sampling. CW and AZ carried out molecular studies under the supervision of HB. CW analyzed the data. CW and Z-LS drafted the manuscript. All authors read and approved the final manuscript
Compliance with Ethics and Guidelines
The authors declare they have no conflicts of interest. The study was approved by the Kenya Wildlife Service, research permit, KWS/BRM/5001. All institutional and National guidelines for care and handling use of animals were followed.
- Aljofan M. 2015. Henipaviruses are not yet history. Future Virol, 10: 507–515.Google Scholar
- Anthony SJ, Epstein JH, Murray KA, Navarrete-Macias I, Zambrana-Torrelio CM., Solovyov A. Ojeda-Flores R, Arrigo NC, Islam A, Ali-Khan S, Hosseini P, Bogich TL, Olival KJ, Sanchez-Leon MD, Karesh WB, Goldstein T, Luby SP, Morse SS, Mazet JAK, Daszak P, Lipkin WI 2013. A strategy to estimate unknown viral diversity in mammals. mBio, 4: e00598.PubMedPubMedCentralGoogle Scholar
- Asano KM, Gregori F, Hora AS, Scheffer KC, Fahl WO, Iamamoto K, Mori E, Silva FDF, Taniwaki SA, Brandão PE. 2016. Group A rotavirus in Brazilian bats: description of novel T15 and H15 genotypes. Arch of Virol, 161: 3225.Google Scholar
- Baker KS, Leggett RM, Bexfield NH, Alston M, Daly G, Todd S, Tachedjian M, Holmes CEG, Crameri S, Wang L-F, Heeney JL, Suu-Ire R, Kellam P, Cunningham AA, Wood JLN, Caccamo M, Murcia PR. 2013. Metagenomic study of the viruses of African straw-coloured fruit bats: Detection of a chiropteran poxvirus and isolation of a novel adenovirus. Virol J, 441: 95–106.Google Scholar
- Chua KB, Bellini WJ, Rota PA, Harcourt BH, Tamin A, Lam SK, Ksiazek TG, Rollin PE, Zaki SR, Shieh WJ, Goldsmith CS, Gubler DJ, Roehrig JT, Eaton B, Gould R, Olson J, Field H, Daniels P, Ling AE, Peters CJ, Anderson LJ, Mahy BW. 2000. Nipah virus: a recently emergent deadly paramyxovirus. Science, 288: 1432–1435.PubMedGoogle Scholar
- Corman VM, Baldwin HJ, Tateno AF, Zerbinati RM, Annan A, Owusu M, Nkrumah EE, Maganga GD, Oppong S, Adu-Sarkodie Y, Vallo P, Ribeiro LV, Filho F, Leroy EM, Thiel V, Hoek L, Poon LLM, Tschapka M, Drexler JF. 2015. Evidence for an ancestral association of human coronavirus 229E with bats. J Virol, 89: 11858–11870.PubMedPubMedCentralGoogle Scholar
- Esona MD, Banyai K, Foytich K, Freeman M, Mijatovic-Rustempasic S, Hull J, Kerin T, Steele AD, Armahd GE, Geyer A, Page N, Agbaya VA, Forbi JC, Aminui M, Gautama R, Seheri LM, Nyangao J, Glass R, Bowena MD, Gentsch JR. 2011. Genomic characterization of human rotavirus G10 strains from the African Rotavirus Network: Relationship to animal rotaviruses. Infect Genet Evol, 11: 237–241.PubMedGoogle Scholar
- Johnson E, Johnson B, Silverstein D, Tukei P, Geisbert T, Sanchez A, Jahrling P. 1996. Characterization of a new Marburg virus isolated from a 1987 fatal case in Kenya. Arch Virol, 11: 101–114.Google Scholar
- Kemenesi G, Dallos B, Gorfol T, Boldogh S, Estok P, Kurucz K, Kutas A, Foldes F, Oldal M, Nemeth V, Martella V, Banyai K, Jakab F. 2014. Molecular survey of RNA viruses in Hungarian bats: discovering novel astroviruses, coronaviruses, and caliciviruses. Vector-Borne Zoonot Dis, 14: 846–855.Google Scholar
- Kim HK, Yoon SW, Kim DJ, Koo BS, Noh JY, Kim JH, Choi YG, Na W, Chang KT, S Ong D, Jeong DG. 2016. Detection of Severe Acute Respi ratory Syndrome-Like, Middle East Respiratory Syndrome-Like bat coronaviruses and group H Rotavirus in faeces of Korean bats. Transbound Emerg Dis, 63: 365–372.PubMedGoogle Scholar
- Matthijnssens J, Ciarlet M, Heiman E, Arijs I, Delbeke T, McDonald SM, Palombo EA, Iturriza-Gomara M, Maes P, Patton JT, Rahman M, Van Ranst M. 2008a. Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains. J Virol, 82: 3204–3219.PubMedPubMedCentralGoogle Scholar
- Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Bányai K, Estes MK, Gentsch JR, Itturiza-Gomara M, Kirkwood C, Martella V, Merens PPC, Nakagomi O, Patton JT, Ruggeri FM, Saif LJ, Santos N, Steyer A, Taniguchi K, Desselberger U, Van Ranst M. 2008b. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch Virol, 153: 1621–1629.PubMedPubMedCentralGoogle Scholar
- Moratelli R, Calisher CH. 2015. Bats and zoonotic viruses: Can we confidently link bats with emerging deadly viruses? Mem. I. Oswaldo-Cruz, 110: 1–22.Google Scholar
- Patterson BD, Webala PW. 2012. Keys to the bats (Mammalia: Chiroptera) of East Africa. Fieldiana Life and Earth Sciences, 12: 6.Google Scholar
- Plowright RK, Eby P, Hudson PJ, Smith IL, Westcott D, Bryden WL, Martin G, Tabor GM, Skerratt LF, Anderson DL, Crameri G, Quammen D, Jordan D, Freeman P, Wand LF, Epstein JH, Marsh GA, Kung NY, McCallum H. 2015. Ecological dynamics of emerging bat virus spillover. Proc Biol Sci, 282: 2014–2124.Google Scholar
- Shi Z. 2013. Emerging infectious diseases associated with bat viruses. Sci China Ser C, 56: 678–682.Google Scholar
- Smith DH, Isaacson M, Johnson KM, Bagshawe A, Johnson BK, Swanapoel R, Johnson KM, Killey M, Bagshawe A, Siongok T, Keruga WK. 1982. Marburg-Virus Disease in Kenya. Lancet, 319: 816–820.Google Scholar
- Tao Y, Shi M, Conrardy C, Kuzmin IV, Recuenco S, Agwanda B, Alvares DA, Ellison JA, Gilbert AT, Moran D, Niezgoda M, Lindblade KA, Holmes EC, Brieman RF, Rupprecht CE, Tong S. 2013. Discovery of diverse polyomaviruses in bats and the evolutionary history of the Polyomaviridae. J Gen Virol, 94: 738–748.PubMedPubMedCentralGoogle Scholar
- Van Thiel PPAM, De Bie RMA, Eftimov F, Tepaske R, Zaaijer HL, Van Doornum GJJ, Schutten M, Osterhaus ADM, Majoie CBL, Aronica E, Fehlner-Gardiner C, Wandeler AI, Kager PA. 2009. Fatal human rabies due to duvenhage virus from a bat in Kenya: Failure of treatment with coma-induction, ketamine, and antiviral drugs. PLoS Neglect Trop. D, 3: 1–8.Google Scholar
- Wang M, Yan M, Xu H, Liang W, Kan B, Zheng B, Chen H, Zheng H, Xu Y, Zhang E, Wang H, Ye J, Li G, Li M, Cui Z, Liu YF, Guo RT, Liu XN, Zhan LH, Zhou DH, Zhao A, Hai R, Yu D, Guan Y, Xu J. 2005. SARS-CoV infection in a restaurant from palm civet. Emerg Infect Dis, 11: 1860–1865.PubMedPubMedCentralGoogle Scholar
- Woolhouse MEJ. 2002. Population biology of emerging and reemerging pathogens. Trends Microbiol, 10: 3–7.Google Scholar
- Zhong NS, Zheng BJ, Li YM, Poon LM, Xie ZH, Chan KH, Li PH, Tan SY, Chang Q, Xie JP, Liu XQ, XU J, Li DX, Yuen KY, Peiris JSM, Guan Y. 2003. Epidemiology and cause of severe acute respiratory syndrome (SARS) in Guangdong, People’s Republic of China, in February, 2003. Lancet, 362: 1353–1358.PubMedGoogle Scholar
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