Abstract
During 2006-2011, 5035 fecal samples were tested by PCR for human adenovirus (HAdV) and sequenced. HAdV was detected in 198 cases (3.9%), with the highest rate in children ≤ 5 years. Enteric HAdVs were the most prevalent genotypes (78%; 146/187): HAdV-F41 (63.6%; 119/187), HAdV-F40 (12.3%; 23/187), HAdV-A12 (1.6%; 3/187) and HAdV-A31 (0.5%; 1/187). Non-enteric HAdVs were detected in 22% (41/187): HAdV-C1 (8.0%; 15/187), HAdV-C2 (6.9%; 13/187), HAdV-C5 (4.3%; 8/187), HAdV-D8 (1.3%; 2/187), HAdV-B21 (0.5%; 1/187), HAdV-B3 (0.5%; 1/187) and HAdV-C6 (0.5%; 1/187). This 6-year retrospective study points out a high diversity of HAdV types circulating in Brazil and highlights the need to carry out molecular epidemiological studies of HAdV among patients with acute diarrheal infection on a regular basis.
References
Echavarria M (2009) Adenoviruses. In: Zuckerman AJ, Banatvala JE, Schoub BD, Griffihs PD, Mortimer P, Wiley-Blackwell (editor) Principles and practice of clinical virology 6th ed. Wiley, Hoboken, p 463–488
Lynch JP 3rd, Kajon AE (2016) Adenovirus: Epidemiology, Global Spread Of Novel Serotypes, And Advances In Treatment And Prevention. Semin Respir Crit Care Med. 37(4):586–602. https://doi.org/10.1055/s-0036-1584923
Li L, Phan TG, Nguyen TA et al (2005) Molecular epidemiology of adenovirus infection among pediatric population with diarrhea in Asia. Microbiol Immunol. 49(2):121–128. https://doi.org/10.1111/j.1348-0421.2005.tb03711.x
Portes SA, Volotao Ede M, Rocha MS et al (2016) A non-enteric adenovírus A12 gastroenteritis outbreak in Rio de Janeiro, Brazil. Mem Inst Oswaldo Cruz. 111(6):403–406. https://doi.org/10.1590/0074-02760160030
Primo D, Pacheco GT, Timenetsky MDCST et al (2018) Surveillance and molecular characterization of human adenovirus in patients with acute gastroenteritis in the era of rotavirus vaccine, Brazil, 2012–2017. J Clin Virol 109:35–40. https://doi.org/10.1016/j.jcv.2018.10.010
Banyai K, Martella V, Meleg E et al (2009) Searching for HAdV-52, the putative gastroenteritis-associated human adenovirus serotype in Southern Hungary. New Microbiol. 32(2):185–188
Magwalivha M, Wolfaardt M, Kiulia NM et al (2010) High prevalence of species D human adenoviruses in fecal specimens from Urban Kenyan children with diarrhea. J Med Virol. 82(1):77–84. https://doi.org/10.1002/jmv.21673
Gelaw A, Pietsch C, Liebert UG (2019) Genetic diversity of human adenovirus and human astrovirus in children with acute gastroenteritis in Northwest Ethiopia. Arch Virol. 164(12):2985–2993. https://doi.org/10.1007/s00705-019-04421-8
Harb A, Abraham S, Rusdi B et al (2019) Molecular detection and epidemiological features of selected bacterial, viral, and parasitic enteropathogens in stool specimens from children with acute diarrhea in Thi-Qar Governorate, Iraq. Int J Environ Res Public Health. 16(9):E1573. https://doi.org/10.3390/ijerph16091573
Kumthip K, Khamrin P, Ushijima H et al (2019) Enteric and non-enteric adenovirus associated with acute gastroenteritis in pediatric patients in Thailand, 2011 to 2017. PLoS ONE 14(8):e0220263. https://doi.org/10.1371/journal.pone.0220263
Sanaei Dashti PA, Ghahremani T, Hashempoor T et al (2016) Molecular epidemiology of enteric adenovirus gastroeneteritis in under-five-old children in Iran. Gastroenterol Res Pract. 2016:2045697. https://doi.org/10.1155/2016/2045697
Afrad MH, Avzun T, Haque J et al (2018) Detection of enteric- and non-enteric adenoviruses in gastroenteritis patients, Bangladesh, 2012–2015. J Med Virol. 90(4):677–684. https://doi.org/10.1002/jmv.25008
La Rosa G, Della Libera S, Petricca S et al (2015) Genetic diversity of human adenovirus in children with acute gastroenteritis, Albania, 2013–2015. Biomed Res Int. 2015:142912. https://doi.org/10.1155/2015/142912
Liu L, Qian Y, Zhang Y et al (2014) Adenoviruses associated with acute diarrhea in children in Beijing, China. PLoS ONE 9(2):e88791. https://doi.org/10.1371/journal.pone.0088791
Moyo SJ, Hanevik K, Blomberg B et al (2014) Prevalence and molecular characterisation of human adenovirus in diarrhoeic children in Tanzania; a case control study. BMC Infect Dis. 14:666. https://doi.org/10.1186/s12879-014-0666-1
Mayindou BG, Ngokana A, Sidibé V et al (2016) Molecular epidemiology and surveillance of circulating rotavirus and adenovirus in Congolese children with gastroenteritis. J Med Virol. 88(4):596–605. https://doi.org/10.1002/jmv.24382
Ozsari T, Bora G, Kaya B et al (2016) The prevalence of rotavirus and adenovirus in the childhood gastroenteritis. Jundishapur J Microbiol. 9(6):e34867. https://doi.org/10.5812/jjm.34867
Gray JJ, Kohli E, Ruggeri FM et al (2007) European multicenter evaluation of commercial enzyme immunoassays for detecting norovirus antigen in fecal samples. Clin Vaccine Immunol. 14(10):1349–1355
Arowolo KO, Ayolabi CI, Lapinski B et al (2019) Epidemiology of enteric viruses in children with gastroenteritis in Ogun State, Nigeria. J Med Virol. 91(6):1022–1029. https://doi.org/10.1002/jmv.25399
Amaral MS, Estevam GK, Penatti M et al (2015) The prevalence of norovirus, astrovirus and adenovirus infections among hospitalised children with acute gastroenteritis in Porto Velho, state of Rondônia, western Brazilian Amazon. Mem Inst Oswaldo Cruz. 110(2):215–221
Raboni SM, Damasio GA, Ferreira CE et al (2014) Acute gastroenteritis and enteric viruses in hospitalised children in southern Brazil: aetiology, seasonality and clinical outcomes. Mem Inst Oswaldo Cruz. 109(4):428–435
Cardoso DDP, Martins RMB, Kitajima EW et al (1992) Rotavirus and adenovirus in 0- to 5-year-old children hospitalized with or without gastroenteritis in Goiâna, GO, Brazil. Rev Inst Med Trop São Paulo. 34(5):433–439
Andreasi MS, Cardoso DD, Fernandes SM et al (2008) Adenovirus, calicivirus and astrovirus detection in fecal samples of hospitalized children with acute gastroenteritis from Campo Grande, MS, Brazil. Mem Inst Oswaldo Cruz 103(7):741–744
Duarte RJ, Mendes EN, Penna FJ et al (2012) Prevalência baixa de adenovirus em crianças com diarréia em Belo Horizonte-MG. J Bras Patol Med Lab. 48(4):259–263
Reis TA, Assis AS, do Valle DA, et al (2016) The role of human adenoviruses type 41 in acute diarrheal disease in Minas Gerais after rotavirus vaccination. Braz J Microbiol 47(1):243–250. https://doi.org/10.1016/j.bjm.2015.11.011
Timenetsky Mdo C, Kisielius JJ, Grisi SJ et al (1993) Rotavirus, adenovirus, astrovirus, calicivirus and small round virus particles in feces of children with and without acute diarrhea, from 1987 to 1988, in the greater São Paulo. Rev Inst Med Trop Sao Paulo. 35(3):275–280
Costa LCPDN, Siqueira JAM, Portal TM et al (2017) Detection and genotyping of human adenovirus and sapovirus in children with acute gastroenteritis in Belém, Pará, between 1990 and 1992: first detection of GI.7 and GV.2 sapoviruses in Brazil. Rev Soc Bras Med Trop. 50(5):621–628. https://doi.org/10.1590/0037-8682-0198-2017
Magalhães GF, Nogueira PA, Grava AF et al (2007) Rotavirus and adenovirus in Rondônia. Mem Inst Oswaldo Cruz. 102(5):555–557
Gouvea V, Glass RI, Woods P et al (1990) Polymerase chain reaction amplification and typing of rotavirus nucleic acid from stool specimens. J Clin Microbiol. 28(2):276–282
Gentsch JR, Glass RI, Woods P, Gouvea V, Gorziglia M, Flores J, Das BK, Bhan MK (1992) Identification of group A rotavirus gene 4 types by polymerase chain reaction. J Clin Microbiol. 30(6):1365–1373
Ando T, Monroe SS, Noel JS et al (1997) A one-tube method of reverse transcription-PCR to efficiently amplify a 3-kilobase region from the RNA polymerase gene to the poly(A) tail of small round-structured viruses (Norwalk-like viruses). J Clin Microbiol. 35(3):570–577
Kageyama T, Kojima S, Shinohara M et al (2003) Broadly reactive and highly sensitive assay for Norwalk-like viruses based on real-time quantitative reverse transcription-PCR. J Clin Microbiol. 41(4):1548–1557
Dey RS, Ghosh S, Chawla-Sarkar M et al (2011) Circulation of a novel pattern of infections by enteric adenovirus serotype 41 among children below 5 years of age in Kolkata, India. J Clin Microbiol. 49(2):500–5005. https://doi.org/10.1128/JCM.01834-10
Xu W, McDonough MC, Erdman DD (2000) Species-specific identification of human adenoviruses by a multiplex PCR assay. J Clin Microbiol. 38(11):4114–4120
Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22(22):4673–4680
Tamura K, Stecher G, Peterson D et al (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol. 30(12):2725–2729. https://doi.org/10.1093/molbev/mst197
Akello JO, Kamgang R, Barbani MT et al (2020) Epidemiology of human adenovirus: a 20-year retrospective observational study in hospitalized patients in Bern, Switzerland. Clin Epidemiol. 12:353–366. https://doi.org/10.2147/CLEP.S246352
Lee JI, Lee GC, Chung JY et al (2012) Detection and molecular characterization of adenoviruses in Korean children hospitalized with acute gastroenteritis. Microbiol Immunol. 56(8):523–528. https://doi.org/10.1111/j.1348-0421.2012.00469.x
Kotloff KL, Blackwelder WC, Nasrin D et al (2012) The global enteric multicenter study (GEMS) of diarrheal disease in infants and young children in developing countries: epidemiologic and clinical methods of the case/control study. Clin Infect Dis. 55(Suppl 4):S232–S245. https://doi.org/10.1093/cid/cis753
Binder AM, Biggs HM, Haynes AK et al (2017) Human adenovirus surveillance—United States, 2003–2016. MMWR Morb Mortal Wkly Rep. 66(39):1039–1042. https://doi.org/10.15585/mmwr.mm6639a2
Kim JS, Lee SK, Ko DH et al (2017) Associations of adenovirus genotypes in korean acute gastroenteritis patients with respiratory symptoms and intussusception. Biomed Res Int. 2017:1602054. https://doi.org/10.1155/2017/1602054
Soares CC, Volotão EM, Albuquerque MC et al (2002) Prevalence of enteric adenoviruses among children with diarrhea in four Brazilian cities. J Clin Virol. 23(3):171–177
McIver CJ, Hansman G, White P et al (2001) Diagnosis of enteric pathogens in children with gastroenteritis. Pathology. 33(3):353–358
Banerjee A, De P, Manna B et al (2017) Molecular characterization of enteric adenovirus genotypes 40 and 41 identified in children with acute gastroenteritis in Kolkata, India during 2013–2014. J Med Virol. 89(4):606–614. https://doi.org/10.1002/jmv.24672
Filho EP, da Costa Faria NR, Fialho AM et al (2007) Adenoviruses associated with acute gastroenteritis in hospitalized and community children up to 5 years old in Rio de Janeiro and Salvador, Brazil. J Med Microbiol. 56(Pt 3):313–319. https://doi.org/10.1099/jmm.0.46685-0
Khor CS, Sam IC, Hooi PS, Quek KF, Chan YF (2012) Epidemiology and seasonality of respiratory viral infections in hospitalized children in Kuala Lumpur, Malaysia: a retrospective study of 27 years. BMC Pediatr. 12:32
Shimizu H, Phan TG, Nishimura S et al (2007) An outbreak of adenovirus serotype 41 infection in infants and children with acute gastroenteritis in Maizuru City, Japan. Infect Genet Evol. 7(2):279–284
Sriwanna P, Chieochansin T, Vuthitanachot C et al (2013) Molecular characterization of human adenovirus infection in Thailand, 2009–2012. Virol J. 10:193. https://doi.org/10.1186/1743-422X-10-193
Ghebremedhin B (2014) Human adenovirus: Viral pathogen with increasing importance. Eur J Microbiol Immunol (Bp). 4(1):26–33. https://doi.org/10.1556/EuJMI.4.2014.1.2
Pfortmueller CA, Barbani MT, Schefold JC et al (2019) Severe acute respiratory syndrome (ARDS) induced by human adenovirus B21: report on 2 cases and literature review. J Crit Care. 51:99–104. https://doi.org/10.1016/j.jcrc.2019.02.019
Maranhão AG, Soares CC, Albuquerque MC et al (2009) Molecular epidemiology of adenovírus conjunctivitis in Rio de Janeiro, Brazil, between 2004 and 2007. Rev Inst Med Trop Sao Paulo. 51(4):227–229
Scott MK, Chommanard C, Lu X et al (2016) Human adenovirus associated with severe respiratory infection, Oregon, USA, 2013–2014. Emerg Infect Dis. 22(6):1044–1051. https://doi.org/10.3201/eid2206.151898
Lee YC, Chen N, Huang IT et al (2015) Human adenovirus type 8 epidemic keratoconjunctivitis with large corneal epithelial full-layer detachment: an endemic outbreak with uncommon manifestations. Clin Ophthalmol. 9:953–957. https://doi.org/10.2147/OPTH.S79697
Acknowledgements
We thank the Enteric Diseases Laboratory of Adolfo Lutz Institute staff for technical assistance: Antonio Erculiani Junior, Audrey Cilli, Giselle Aparecida Schiavelli, Rita de Cassia Compagnoli Carmona, Simone Guadagnucci Morillo and Sirlene Henrique Rodrigues Silva. We are grateful to Centers for Surveillance (CVE), São Paulo State Health Department; Public Health Laboratories (LACENs) and CGLAB/DEVEP/SVS/Ministry of Health, Brasília, for assistance in sample collection and epidemiological data.
Funding
Adriana Luchs is funded by Conselho Nacional de Desenvolvimento Científico e Tecnológico/CNPq grant #400450/2016-0. Ellen Viana de Souza and Roberta Salzone Medeiros are supported by a fellowship of Institutional Program for Scientific Initiation Scholarships (Programa Institucional de Bolsas de Iniciação Científica/PIBIC-CNPq). Yasmin França Viana Pires de Souza is supported by a fellowship of Scientific Initiation (Iniciação Científica/CNPq) grant #400450/2016-0. Lais Sampaio de Azevedo and Talita Gonçalves Aires de Queiroz are supported by a fellowship of Training Program for Scientific Research at Instituto Adolfo Lutz (Programa de Formação para Investigação Científica do Instituto Adolfo Lutz/FEDIAL).
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AL conceived the study; AL and MCSTT designed the study protocol; EVS, YFVPS, RSM, LSA, TGAQ and AL participated in the conduct of the study; EVS, YFVPS, RSM, LSA, TGAQ and AL acquired the data and performed the PCR assays; EVS, YFVPS, RSM, LSA, TGAQ, RLSD, RSSM, SVK and AL conducted the sequencing assays; EVS, YFVPS, RSM, LSA, TGAQ and AL analyzed and interpreted the data; AL drafted the manuscript; EVS, YFVPS, RSM, LSA, TGAQ, RLSD, RSSM, SVK and MCSTT critically revised the manuscript for intellectual content. All authors read and approved the final version. AL is the guarantor of the paper.
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This study was carried out in accordance with the Declaration of Helsinki as revised in 2000 and approved by the Ethics Committee of the Adolfo Lutz Institute, São Paulo, Brazil (CTC 42-H/2015; CEP 1624723). Study participants were not required to provide informed consent, as this study was considered by the Ethics Committee to be part of routine surveillance activities.
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Souza, E.V., de Souza, Y.F.V.P., Medeiros, R.S. et al. Diversity of enteric and non-enteric human adenovirus strains in Brazil, 2006-2011. Arch Virol 166, 897–903 (2021). https://doi.org/10.1007/s00705-020-04946-3
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DOI: https://doi.org/10.1007/s00705-020-04946-3