Journal of Clinical Virology 59 (2014) 74–76
Contents lists available at ScienceDirect
Journal of Clinical Virology journal homepage: www.elsevier.com/locate/jcv
Letter to the Editor Unexpected detection of bovine G10 rotavirus in a Brazilian child with diarrhea Keywords: Gastroenteritis Interspecies transmission Zoonotic transmission
Group A Rotavirus (RVA) has been reported as the major etiologic pathogen causing gastroenteritis in human and animal [1]. On January 2012, an unusual strain G10P[?] (IAL-R2803) was detected in a 3-year-old male child with acute gastroenteritis during the epidemiological survey in Presidente Prudente city, São Paulo, Brazil. RVA strains with G10 specificity are usually detected in calves, and rarely detected in humans [2–5]. Phylogenetic analysis based on VP7 gene showed that IAL-R2803 strain (accession number JX566991) had highest nucleotide identity to bovine strain DQ-75, isolated in China in 2008 (94.6% nt; 98.9% aa). IAL-R2803 strain also exhibited high nucleotide and amino acid identity to bovine strains RVL-Bov2 (93.6% nt; 98.3% aa), VICG10.01 (93.6% nt; 97.2% aa), RVL-Bov3 (93.4% nt; 98.3% aa), B11 (93.4% nt; 97.8% aa), XJX-07 (93.4% nt; 97.8% aa), and MX001 (92.9% nt; 97.2%); and to human strain 163 (93.4% nt; 96.7% aa). When compared with other human G10 strains, strain IAL-R2803 had only 84.8–89.9% nucleotide homology (90.2–96.1% aa), including the Brazilian strain R239 (86.1% nt; 94% aa) (Fig. 1). Although several attempts were made to obtain the VP4 genotype, they were unsuccessful. Genetic analysis of IAL-R2803 strain revealed that the VP7 gene displayed a possible bovine origin. Although human G10 strains
1386-6532/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jcv.2013.11.001
had already been described and sequenced in Brazil [2], this is the first strong evidence of an animal G10 strain interspecies transmission in the country. It is noteworthy that one or more of its other segments could be derived from human RVA strains making it a human–animal reassortant. Genetic characterization of additional genes is necessary to determine the full genetic profile of this strain [4]. Presidente Prudente city is located in a country site area of Brazil, and known for its large bovine herd. In addition, available data on circulating bovine RVA strains in Brazil have reported G6 and G10 as the most common G-types found in herds [6,7]. In country sites areas, domestic animals and humans live close together in rural villages, and often share the same source of water, increasing the chance of animal–human transmission and mixed infections [3]. Therefore it was not surprising that a G10 strain, known to circulate in bovine herds, could be detected in a Brazilian child living in the same region. Unfortunately, none of the animals from the sampling site were screened for the presence of RVA. Surveillance studies has shown that animal strains can contribute to generating diversity among the human RVA population [8], and could become an increasingly important contributor to diversity due to vaccine selective pressure [9]. There is an urgent need to include pet and domestic animals in the RVA surveillance programs because their close contact with humans (especially from rural areas); increased reports of the detection of strains unique to animals in human populations, and the increasing spread and isolation of strains with unusual VP7 and VP4 genotypes [3,5,8]. Sequencing of both animal and human RVA genes is need in order to comprehend better the extent to which reassortment and interspecies transmission contribute to diversity in both species.
Letter to the Editor / Journal of Clinical Virology 59 (2014) 74–76
75
AB714266 Human 163 VIE 2008
100 85
GQ352366 Bovine VICG10.01 AUS 2005 M64679 Bovine B11 AUS 1988
25
GQ433985 Bovine RVL-Bov2 IRL xxxx 30
100 GQ433986 Bovine RVL-Bov3 IRL xxxx
EU828784 Bovine XJX-07 CHN 2007 74 19
X57852 Bovine B223 USA xxxx FJ217204 Bovine MX001 MEX 2006
53 61
IAL-R2803 2012 GU144587 Bovine DQ-75 CHN 2008
47 62
HQ419066 Camel VRLCU EGY 2004 HQ315854 Bovine HUN-Z8 HUN 2002 AY644385 Bovine CIT10A/02 IRL 2002-2004
92
JN410618 Bovine DK11311C DEN 2007 83
100
AF386918 Bovine B75 IND xxxx
20 39
GU259585 Bovine DijonA037 FRA 2006 U35850 Porcine P343 THA xxxx
25
X53403 Bovine 61A THA xxxx
99
45
GU584051 Human SI-R241/07 SLO 2007 D14033 Human Mc35 THA xxxx
83 100
GQ240619 Human mani-265 IND 2007 DQ981476 Equine Erv2 IND 2003-2005 FJ598311 Bovine E29TR TUR 2006
90 74
JF681943 Human kol-679 IND 2005
99
AY843332 Human 402 GHA 2003-2004 80
57 EF218666 Human 6755 CIV 2002 97
AY816182 Human 3008CM CMR 1999
84
AY816181 Human 1784CI CIV 1999
41 EF218664 Human 6730 NGR 1999
HM800948 Lamb LLR CHN 1985 100
FJ031029 Lamb Lamb-NT CHN 2007
AY855063 Human R239 BRA 2000-2004 AB118023 Human DS1 G2 outgroup 0.05 Fig. 1. Nucleotide based phylogenetic relatedness of IAL-R2803 RVA G10 VP7 gene (indicated by the arrow) to other selected human and animal G10 strains. Neighbor-joining tree of the partial VP7 nucleotide sequence was generated with MEGA 4.0 software. Reference G10 strains were obtained from GenBank database. Accession number, species, isolates, countries and year of each strain are indicated. The scale indicates the number of divergent nucleotide residues. Percentages of bootstrap values are shown at the branch node.
Conflict of interest
humans beings – Conselho Nacional de Saúde (CNS)/Ministério da Saúde (MS), Brasília, 1996.
None. Funding None. Ethical approval Previous ethics committee approval was granted by Adolfo Lutz Institute – São Paulo – Brazil (Ref. 14/05; Ref. 53/05). This was an anonymous unlinked study and informed consent was not required according to the resolution 196/96 concerning research evolving
Acknowledgments We thank the Enteric Diseases Laboratory of Adolfo Lutz Institute staff: Rita de Cássia C. Carmona for laboratorial supervision; Adeline M. Fernandes, Audrey Cilli, Carolina J. Gill, Cibele D. Ribeiro and Simone G. Morillo for laboratorial assistance; Antonio Erculiani Junior and Sirlene Henrique Rodrigues Silva for technical assistance. We are grateful to Centers for Surveillance, São Paulo State Health Department (CVE) for assistance in sample collection and epidemiological data.
76
Letter to the Editor / Journal of Clinical Virology 59 (2014) 74–76
References [1] Estes MK, Kapikian AZ. Rotaviruses. In: Knipe DM, Howley PM, Griffin DD, Lamb RA, Martin MA, Roizman B, Straus SE, editors. Fields virology. Philadelphia: Wolters Kluwer Health/Lippincot. Williams and Wilkins; 2007. p. 1917–74. [2] Volotão EM, Soares CC, Maranhão AG, Rocha LN, Hoshino Y, Santos N. Rotavirus surveillance in the city of Rio de Janeiro-Brazil during 2000–2004: detection of unusual strains with G8P[4] or G10P[9] specificities. J Med Virol 2006;78(2):263–72. [3] Esona MD, Page NA, Akran VA, Armah GE, Steele AD. Characterization of 2 human genotype G10 rotavirus strains, 3008CM and 1784/CI/1999, isolated in Cameroon and Cote d’Ivoire during the 1999–2000 rotavirus season. J Infect Dis 2010;202(Suppl.):S212–9. [4] Esona MD, Banyai K, Foytich K, Freeman M, Mijatovic-Rustempasic S, Hull J, et al. Genomic characterization of human rotavirus G10 strains from the African Rotavirus Network: relationship to animal rotaviruses. Infect Genet Evol 2011;11(1):237–41. [5] Mukherjee A, Nayak MK, Roy T, Ghosh S, Naik TN, Kobayashi N, et al. Detection of human G10 rotavirus strains with similarity to bovine and bovinelike equine strains from untypable samples. Infect Genet Evol 2012;12(2): 467–70. [6] Alfieri AF, Alfieri AA, Barreiros MA, Leite JP, Richtzenhain LJ. G and P genotypes of group A rotavirus strains circulating in calves in Brazil, 1996–1999. Vet Microbiol 2004;99(3/4):167–73. [7] Caruzo TA, Brito WM, Munford V, Rácz ML. Molecular characterization of G and P-types bovine rotavirus strains from Goiás, Brazil: high frequency of mixed P-type infections. Mem Inst Oswaldo Cruz 2010;105(8):1040–3.
[8] Luchs A, Cilli A, Morillo SG, Carmona Rde C, Timenetsky Mdo C. Rare G3P[3] rotavirus strain detected in Brazil: possible human-canine interspecies transmission. J Clin Virol 2012;54(1):89–92. [9] Matthijnssens J, Bilcke J, Ciarlet M, Martella V, Bányai K, Rahman M, et al. Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol 2009;4(10):1303–16.
Adriana Luchs ∗ Maria do Carmo Sampaio Tavares Timenetsky ∗ Adolfo Lutz Institute, Virology Center, Enteric Diseases Laboratory, São Paulo, SP, Brazil ∗ Corresponding authors at: Instituto Adolfo Lutz, Centro de Virologia, Núcleo de Doenc¸as Entéricas, Av. Dr Arnaldo, No. 355, São Paulo, SP 01246-902, Brazil. Tel.: +55 11 3068 2909; fax: +55 11 3088 3753. E-mail addresses: [email protected] (A. Luchs), [email protected] (M.d.C.S.T. Timenetsky)
11 October 2013
Contents lists available at ScienceDirect
Journal of Clinical Virology journal homepage: www.elsevier.com/locate/jcv
Letter to the Editor Unexpected detection of bovine G10 rotavirus in a Brazilian child with diarrhea Keywords: Gastroenteritis Interspecies transmission Zoonotic transmission
Group A Rotavirus (RVA) has been reported as the major etiologic pathogen causing gastroenteritis in human and animal [1]. On January 2012, an unusual strain G10P[?] (IAL-R2803) was detected in a 3-year-old male child with acute gastroenteritis during the epidemiological survey in Presidente Prudente city, São Paulo, Brazil. RVA strains with G10 specificity are usually detected in calves, and rarely detected in humans [2–5]. Phylogenetic analysis based on VP7 gene showed that IAL-R2803 strain (accession number JX566991) had highest nucleotide identity to bovine strain DQ-75, isolated in China in 2008 (94.6% nt; 98.9% aa). IAL-R2803 strain also exhibited high nucleotide and amino acid identity to bovine strains RVL-Bov2 (93.6% nt; 98.3% aa), VICG10.01 (93.6% nt; 97.2% aa), RVL-Bov3 (93.4% nt; 98.3% aa), B11 (93.4% nt; 97.8% aa), XJX-07 (93.4% nt; 97.8% aa), and MX001 (92.9% nt; 97.2%); and to human strain 163 (93.4% nt; 96.7% aa). When compared with other human G10 strains, strain IAL-R2803 had only 84.8–89.9% nucleotide homology (90.2–96.1% aa), including the Brazilian strain R239 (86.1% nt; 94% aa) (Fig. 1). Although several attempts were made to obtain the VP4 genotype, they were unsuccessful. Genetic analysis of IAL-R2803 strain revealed that the VP7 gene displayed a possible bovine origin. Although human G10 strains
1386-6532/$ – see front matter © 2013 Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.jcv.2013.11.001
had already been described and sequenced in Brazil [2], this is the first strong evidence of an animal G10 strain interspecies transmission in the country. It is noteworthy that one or more of its other segments could be derived from human RVA strains making it a human–animal reassortant. Genetic characterization of additional genes is necessary to determine the full genetic profile of this strain [4]. Presidente Prudente city is located in a country site area of Brazil, and known for its large bovine herd. In addition, available data on circulating bovine RVA strains in Brazil have reported G6 and G10 as the most common G-types found in herds [6,7]. In country sites areas, domestic animals and humans live close together in rural villages, and often share the same source of water, increasing the chance of animal–human transmission and mixed infections [3]. Therefore it was not surprising that a G10 strain, known to circulate in bovine herds, could be detected in a Brazilian child living in the same region. Unfortunately, none of the animals from the sampling site were screened for the presence of RVA. Surveillance studies has shown that animal strains can contribute to generating diversity among the human RVA population [8], and could become an increasingly important contributor to diversity due to vaccine selective pressure [9]. There is an urgent need to include pet and domestic animals in the RVA surveillance programs because their close contact with humans (especially from rural areas); increased reports of the detection of strains unique to animals in human populations, and the increasing spread and isolation of strains with unusual VP7 and VP4 genotypes [3,5,8]. Sequencing of both animal and human RVA genes is need in order to comprehend better the extent to which reassortment and interspecies transmission contribute to diversity in both species.
Letter to the Editor / Journal of Clinical Virology 59 (2014) 74–76
75
AB714266 Human 163 VIE 2008
100 85
GQ352366 Bovine VICG10.01 AUS 2005 M64679 Bovine B11 AUS 1988
25
GQ433985 Bovine RVL-Bov2 IRL xxxx 30
100 GQ433986 Bovine RVL-Bov3 IRL xxxx
EU828784 Bovine XJX-07 CHN 2007 74 19
X57852 Bovine B223 USA xxxx FJ217204 Bovine MX001 MEX 2006
53 61
IAL-R2803 2012 GU144587 Bovine DQ-75 CHN 2008
47 62
HQ419066 Camel VRLCU EGY 2004 HQ315854 Bovine HUN-Z8 HUN 2002 AY644385 Bovine CIT10A/02 IRL 2002-2004
92
JN410618 Bovine DK11311C DEN 2007 83
100
AF386918 Bovine B75 IND xxxx
20 39
GU259585 Bovine DijonA037 FRA 2006 U35850 Porcine P343 THA xxxx
25
X53403 Bovine 61A THA xxxx
99
45
GU584051 Human SI-R241/07 SLO 2007 D14033 Human Mc35 THA xxxx
83 100
GQ240619 Human mani-265 IND 2007 DQ981476 Equine Erv2 IND 2003-2005 FJ598311 Bovine E29TR TUR 2006
90 74
JF681943 Human kol-679 IND 2005
99
AY843332 Human 402 GHA 2003-2004 80
57 EF218666 Human 6755 CIV 2002 97
AY816182 Human 3008CM CMR 1999
84
AY816181 Human 1784CI CIV 1999
41 EF218664 Human 6730 NGR 1999
HM800948 Lamb LLR CHN 1985 100
FJ031029 Lamb Lamb-NT CHN 2007
AY855063 Human R239 BRA 2000-2004 AB118023 Human DS1 G2 outgroup 0.05 Fig. 1. Nucleotide based phylogenetic relatedness of IAL-R2803 RVA G10 VP7 gene (indicated by the arrow) to other selected human and animal G10 strains. Neighbor-joining tree of the partial VP7 nucleotide sequence was generated with MEGA 4.0 software. Reference G10 strains were obtained from GenBank database. Accession number, species, isolates, countries and year of each strain are indicated. The scale indicates the number of divergent nucleotide residues. Percentages of bootstrap values are shown at the branch node.
Conflict of interest
humans beings – Conselho Nacional de Saúde (CNS)/Ministério da Saúde (MS), Brasília, 1996.
None. Funding None. Ethical approval Previous ethics committee approval was granted by Adolfo Lutz Institute – São Paulo – Brazil (Ref. 14/05; Ref. 53/05). This was an anonymous unlinked study and informed consent was not required according to the resolution 196/96 concerning research evolving
Acknowledgments We thank the Enteric Diseases Laboratory of Adolfo Lutz Institute staff: Rita de Cássia C. Carmona for laboratorial supervision; Adeline M. Fernandes, Audrey Cilli, Carolina J. Gill, Cibele D. Ribeiro and Simone G. Morillo for laboratorial assistance; Antonio Erculiani Junior and Sirlene Henrique Rodrigues Silva for technical assistance. We are grateful to Centers for Surveillance, São Paulo State Health Department (CVE) for assistance in sample collection and epidemiological data.
76
Letter to the Editor / Journal of Clinical Virology 59 (2014) 74–76
References [1] Estes MK, Kapikian AZ. Rotaviruses. In: Knipe DM, Howley PM, Griffin DD, Lamb RA, Martin MA, Roizman B, Straus SE, editors. Fields virology. Philadelphia: Wolters Kluwer Health/Lippincot. Williams and Wilkins; 2007. p. 1917–74. [2] Volotão EM, Soares CC, Maranhão AG, Rocha LN, Hoshino Y, Santos N. Rotavirus surveillance in the city of Rio de Janeiro-Brazil during 2000–2004: detection of unusual strains with G8P[4] or G10P[9] specificities. J Med Virol 2006;78(2):263–72. [3] Esona MD, Page NA, Akran VA, Armah GE, Steele AD. Characterization of 2 human genotype G10 rotavirus strains, 3008CM and 1784/CI/1999, isolated in Cameroon and Cote d’Ivoire during the 1999–2000 rotavirus season. J Infect Dis 2010;202(Suppl.):S212–9. [4] Esona MD, Banyai K, Foytich K, Freeman M, Mijatovic-Rustempasic S, Hull J, et al. Genomic characterization of human rotavirus G10 strains from the African Rotavirus Network: relationship to animal rotaviruses. Infect Genet Evol 2011;11(1):237–41. [5] Mukherjee A, Nayak MK, Roy T, Ghosh S, Naik TN, Kobayashi N, et al. Detection of human G10 rotavirus strains with similarity to bovine and bovinelike equine strains from untypable samples. Infect Genet Evol 2012;12(2): 467–70. [6] Alfieri AF, Alfieri AA, Barreiros MA, Leite JP, Richtzenhain LJ. G and P genotypes of group A rotavirus strains circulating in calves in Brazil, 1996–1999. Vet Microbiol 2004;99(3/4):167–73. [7] Caruzo TA, Brito WM, Munford V, Rácz ML. Molecular characterization of G and P-types bovine rotavirus strains from Goiás, Brazil: high frequency of mixed P-type infections. Mem Inst Oswaldo Cruz 2010;105(8):1040–3.
[8] Luchs A, Cilli A, Morillo SG, Carmona Rde C, Timenetsky Mdo C. Rare G3P[3] rotavirus strain detected in Brazil: possible human-canine interspecies transmission. J Clin Virol 2012;54(1):89–92. [9] Matthijnssens J, Bilcke J, Ciarlet M, Martella V, Bányai K, Rahman M, et al. Rotavirus disease and vaccination: impact on genotype diversity. Future Microbiol 2009;4(10):1303–16.
Adriana Luchs ∗ Maria do Carmo Sampaio Tavares Timenetsky ∗ Adolfo Lutz Institute, Virology Center, Enteric Diseases Laboratory, São Paulo, SP, Brazil ∗ Corresponding authors at: Instituto Adolfo Lutz, Centro de Virologia, Núcleo de Doenc¸as Entéricas, Av. Dr Arnaldo, No. 355, São Paulo, SP 01246-902, Brazil. Tel.: +55 11 3068 2909; fax: +55 11 3088 3753. E-mail addresses: [email protected] (A. Luchs), [email protected] (M.d.C.S.T. Timenetsky)
11 October 2013
