A systematic review of evidence that enteroviruses may be zoonotic

Figures & data

Species within the Enterovirus genus

Current species name	Former species name	Number of unique viruses recognized
Enterovirus A	Human enterovirus A	25
Enterovirus B	Human enterovirus B	63
Enterovirus C	Human enterovirus C	23
Enterovirus D	Human enterovirus D	5
Enterovirus E	Bovine enterovirus (group A)	4
Enterovirus F	Bovine enterovirus (group B)	6
Enterovirus G	Porcine enterovirus B	20
Enterovirus H	Simian enterovirus A	1
Enterovirus I	–	1
Enterovirus J	Unclassified simian viruses	6
Enterovirus K	–	1
Enterovirus L	–	1
Rhinovirus A	Human rhinovirus A	80
Rhinovirus B	Human rhinovirus B	32
Rhinovirus C	Human rhinovirus C	56

Derived from: refs. ^51,52

Fig. 1 Flow chart of the literature search process. Based on the search strategy, 4592 articles were identified in total, which included 3906 English articles and 686 Chinese articles. Duplicates were removed

Publications found to be important in considering the zoonotic potential of enteroviruses

Publications	Country and year	Main summary	Strength of evidence
Gür et al.^Citation17	Turkey 2008	Bovine enterovirus type 1-specific antibodies were detected using a microneutralization test in sera from 74 out of 244 humans living in urban areas of Turkey (no report of clinical infection), as well as horses, dogs, goats, and sheep.	Serological study; humans sampled reportedly healthy
Oberste et al.^Citation30	USA 2008	Genome sequences of simian enteroviruses SV6, SV19, SV46, and enteroviruses EV92 and EV103 detected in captive primates demonstrated close phylogenetic relationships to HEV-A. The EV103-POo-1 amino acid sequences also shared 93 and 96% identity with the SV6 on the P2 and P3 regions.	RT-PCR and complete genome sequencing
Smura et al.^Citation34	Finland 2011	A review of enterovirus species evolution includes a description of possible zoonotic origin of EV-70.	Review article
Harvala et al.^Citation23	Cameroon 2011	Enteroviruses infecting wild chimpanzees were characterized and found to be related to human strains detected in patients in Central Africa, including LM1677 (clustered closely with EV79 in VP1 and VP4/VP2 regions) and KK2640 (grouped closely with the EV70 in the VP1 region and with the EV94 in the 5′UTR and 3Dpol).	RT-PCR and near-complete genome sequencing
Nielsen et al.^Citation31	Denmark 2012	A near-complete viral genome of a human strain of coxsackie B3 (CB3) virus was found to be the cause of severe respiratory symptoms and death in a chimpanzee at a zoo in Copenhagen.	RT-qPCR and near-complete genome sequencing
Oberste et al.^Citation32	Bangladesh 2013	Among non-human primates at a zoo in Dhaka, 12.5% of all enteroviruses detected (8/64) based on an analysis of the VP1 region were EVs previously detected in humans. The most common human enterovirus was echovirus 24 (E24). These results are surprising considering the authors’ findings among synanthropic NHP populations (Oberste et al.^Citation33).	RT-qPCR and partial genome sequencing
Oberste et al.^Citation33	Bangladesh 2013	Twenty human EVs were detected in synanthropic NHP in Bangladesh with four from HEV-A, 13 from HEV-B and three from HEV-C types determined by the partial VP1 sequencing.	RT-qPCR and partial genome sequencing
Sadeuh-Mba et al.^Citation24	Cameroon 2013	The strain C08-142 was isolated from a patient with AFP; this strain is related to EV-A76 strain LM1677 and was previously detected in a wild chimpanzee in Cameroon. Similarly, EV-D111 was isolated from healthy child; this strain is closely related to the KK2640, which was also isolated from chimpanzee in Cameroon.	Viral isolation, RT-PCR, and partial genome sequencing
Harvala et al.^Citation26	Cameroon, DRC 2014	Species A enteroviruses EV-A76, EV-A89 (based on the VP4 sequences), and A119 (based on the VP4 and VP1 sequences) were detected in apes in Cameroon. EV-A76 and EV-A89 were also isolated from human stool specimens from patients with AFP in a previous study (Oberste et al.^Citation29).	RT-PCR, viral isolation and partial genome sequencing
Sadeuh-Mba et al.^Citation25	Cameroon 2014	Coxsackievirus A13 and A24, Echovirus 15 and 29 and EV-B82 (VP1 region) were detected in stool samples of captive chimpanzees and gorillas. In addition, EV-A76 (wildly circulated in humans) was found in wild chimpanzees.	RT-snPCR, partial genome sequencing and viral isolation
Mombo et al.^Citation27	Congo 2015	First identification of a human EV-C (EV-C 99; targeting the capsid gene VP1) found to be associated with AFP in a chimpanzee.	RT-qPCR, and near-complete genome sequencing
Bruhn et al.^Citation36	USA 2015	Through recombination analysis and phylogenic analysis of 51 SVDV samples (27 from this study and 24 from a previous study) provide evidence that SVDV originates from a single recombinant origin of CV-B5 and CV-A9, supporting the hypothesis of a single anthroponotic transfer origin (human to pig).	RT-PCR and near-complete genome sequencing
Grützmacher et al.^Citation19	CAR 2016	A gorilla fecal sample tested positive for EV most similar to simian agent 5 B165; a human fecal sample tested positive for EV most similar to swine vesicular virus (89% identity, 5′UTR; Accession: AY875991.1) and human enterovirus 71 (90% identity, partial, gene for polyprotein, Accession: AB575924.1).	RT-qPCR and partial genome sequencing
Du et al.^Citation22	China 2016	Sequencing of EV from rodents in china detected 72% identity with human coxsackie virus A11 (nt sequence 295-632 of 5′UTR) and 73% identity with EV-D68 (179-628 of 5′UTR).	Sequence-independent PCR and next-generation sequencing
Lomakina et al.^Citation37	Russia 2016	Coxsackie B4 characterization demonstrated phylogenetic evidence that SVDV emerged from a human ancestor between 1945 and 1975 (T75 diverging from human CVB4 after 1945).	Viral isolation, Sanger sequencing using PCR
Mombo et al.^Citation28	Gabon 2017	Thirty-two out of 600 fecal samples from wild apes and monkeys were positive for EVs with HEV-A and HEV-B strains (targeting the VP1 and VP2 regions) detected in the chimpanzee samples and HEV-B and simian EV-J identified in mandrill samples.	RT-qPCR and partial genome sequencing

RT-PCR reverse transcription-polymerase chain reaction, RT-qPCR real-time reverse transcription-polymerase chain reaction, RT-snPCR semi-nested reverse transcription-polymerase chain reaction, HEV-A human enterovirus A, NHP non-human primate, AFP acute flaccid paralysis, SVDV swine vesicular disease virus

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