Skip to main content

Advertisement

SpringerLink
Log in

Isolation and molecular characterization of Adenovirus in suspected acute flaccid paralysis patients: A preliminary report from Pakistan

  • Original Article
  • Published:
Archives of Virology Aims and scope Submit manuscript

Abstract

Human adenoviruses (HAdVs) usually cause asymptomatic or mild infection, but infrequently, they are responsible for various severe syndromes including neurological disorders. Various research studies have investigated the association of HAdVs with acute flaccid paralysis (AFP). The purpose of this study was to investigate the genetic diversity of HAdVs and their association with AFP. Stool samples from patients ≤ 12 years of age with suspected AFP were collected from all over Pakistan within the framework of poliovirus surveillance. Poliovirus- and enterovirus-negative samples were screened for HAdVs. For virus isolation, the human epithelial cell line HEp-2c was used, culture-positive samples were screened by nested PCR assay, and partial hexon gene sequences were used for genotype identification. Out of 172 samples, 94 were positive by virus isolation, 89 were positive by PCR, and 32 isolates were genotyped successfully. Phylogenetic analysis showed that the HAdVs belonged to species A (HAdV-A12 and A31), B (HAdV-B3 and B7), C (HAdV-C1 and C6), D (HAdV-D19 and D93), and F (HAdV-F41), showing 99-100% nucleotide sequence identity and 98.3-100% amino acid sequence identity). Most of these genotypes have been reported previously in AFP cases, but this is the first report of the detection of HAdV-D93 in stool samples from AFP cases. The detection of a significant fraction of the HAdVs genotypes indicates that these genetically distinct genotypes are circulating in Pakistan and suggests their possible role in the pathogenesis of AFP.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Haddad-Boubaker S et al (2019) Metagenomic analysis identifies human adenovirus 31 in children with acute flaccid paralysis in Tunisia. Adv Virol 164(3):747–755

    CAS  Google Scholar 

  2. Ghebremedhin B (2014) Human adenovirus: Viral pathogen with increasing importance. Eur J Microbiol Immunol 4(1):26–33

    Article  CAS  Google Scholar 

  3. Radke JR, Cook JL (2018) Human adenovirus infections: update and consideration of mechanisms of viral persistence. Curr Opin Infect Dis 31(3):251

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Sharma A et al (2009) Adenovirus receptors and their implications in gene delivery. Virus Res 143(2):184–194

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Yao L-H et al (2019) Human adenovirus among hospitalized children with respiratory tract infections in Beijing, China, 2017–2018. Virol J 16(1):1–8

    Article  Google Scholar 

  6. Lion T (2014) Adenovirus infections in immunocompetent and immunocompromised patients. Clin Microbiol Rev 27(3):441–462

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Abelson M, Shapiro A (2010) A guide to understanding adenovirus, the diseases it causes and the best ways to treat these conditions. Rev Ophthalmol. Available at: https://www.reviewofophthalmology.com/article/a-guide-to-understanding-adenovirus-thediseases-it-causes-and-the-best-ways-to-treat-these-conditions

  8. Hofmayer S et al (2009) Unique sequence features of the Human Adenovirus 31 complete genomic sequence are conserved in clinical isolates. BMC Genom 10(1):1–14

    Article  Google Scholar 

  9. Venard V et al (2000) Genotyping of adenoviruses isolated in an outbreak in a bone marrow transplant unit shows that diverse strains are involved. J Hosp Infect 44(1):71–74

    Article  CAS  PubMed  Google Scholar 

  10. Matsushima Y et al (2011) Genomic characterization of a novel human adenovirus type 31 recombinant in the hexon gene. J Gen Virol 92(12):2770–2775

    Article  CAS  PubMed  Google Scholar 

  11. Frange P et al (2011) Adenoviral infection presenting as an isolated central nervous system disease without detectable viremia in two children after stem cell transplantation. J Clin Microbiol 49(6):2361–2364

    Article  PubMed  PubMed Central  Google Scholar 

  12. Dubberke ER et al (2006) Acute meningoencephalitis caused by adenovirus serotype 26. J Neurovirol 12(3):235–240

    Article  PubMed  Google Scholar 

  13. Ooi MH et al (2003) Adenovirus type 21—associated acute flaccid paralysis during an outbreak of hand-foot-and-mouth disease in Sarawak, Malaysia. Clin Infect Dis 36(5):550–559

    Article  PubMed  Google Scholar 

  14. Hsu CH et al (2019) Progress toward poliomyelitis eradication—Pakistan, January 2018–September 2019. Morb Mortal Wkly Rep 68(45):1029

    Article  Google Scholar 

  15. World Health Organization (2004) Polio laboratory manual

  16. Allard A, Albinsson B, Wadell G (2001) Rapid typing of human adenoviruses by a general PCR combined with restriction endonuclease analysis. J Clin Microbiol 39(2):498–505

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Darriba D et al (2012) jModelTest 2: more models, new heuristics and parallel computing. Nat Methods 9(8):772–772

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52(5):696–704

    Article  PubMed  Google Scholar 

  19. Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22(22):4673–4680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16(2):111–120

    Article  CAS  PubMed  Google Scholar 

  21. Jones DT, Taylor WR, Thornton JM (1992) The rapid generation of mutation data matrices from protein sequences. Bioinformatics 8(3):275–282

    Article  CAS  Google Scholar 

  22. Casas I et al (2005) Molecular identification of adenoviruses in clinical samples by analyzing a partial hexon genomic region. J Clin Microbiol 43(12):6176–6182

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Pattengale ND et al (2010) How many bootstrap replicates are necessary? J Comput Biol 17(3):337–354

    Article  CAS  PubMed  Google Scholar 

  24. Felsenstein J (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39(4):783–791

    Article  PubMed  Google Scholar 

  25. Ivanova OE et al (2012) Adenovirus isolation rates in acute flaccid paralysis patients. J Med Virol 84(1):75–80

    Article  PubMed  Google Scholar 

  26. World Health Organization (2018) Manual for the virological investigation of poliomyelitis: WHO. 2004. Geneva, Switzerland

  27. Similä S et al (1970) Encephalomeningitis in children associated with an adenovirus type 7 epidemic. Acta Paediatrica 59(3):310–316

    Article  Google Scholar 

  28. Cardosa MJ et al (1999) Isolation of subgenus B adenovirus during a fatal outbreak of enterovirus 71-associated hand, foot, and mouth disease in Sibu, Sarawak. The Lancet 354(9183):987–991

    Article  CAS  Google Scholar 

  29. Bowles NE et al (2003) Detection of viruses in myocardial tissues by polymerase chain reaction: evidence of adenovirus as a common cause of myocarditis in children and adults. J Am Coll Cardiol 42(3):466–472

    Article  PubMed  Google Scholar 

  30. Lum LCS et al (2000) Adenovirus in EV71-associated hand, foot, and mouth disease. The Lancet 355(9198):146–147

    Article  CAS  Google Scholar 

  31. de Azevedo JP et al (2004) Characterization of species B adenoviruses isolated from fecal specimens taken from poliomyelitis-suspected cases. J Clin Virol 31(4):248–252

    Article  PubMed  Google Scholar 

  32. Ohtsuki N, Kimura S, Nezu A (2000) Three cases with acute encephalopathy related with adenovirus type 7 infection. No to hattatsu= Brain Develop 32(1):68

  33. Chan DY (2014) Fifteen years of acute flaccid paralysis surveillance in Hong Kong: Findings from 1997 to 2011. J Paediatrics Child Health 50(7):545–552

    Article  Google Scholar 

  34. Huang Y-C et al (2013) Adenovirus infection associated with central nervous system dysfunction in children. J Clin Virol 57(4):300–304

    Article  PubMed  Google Scholar 

  35. Yousefi M et al (2018) Enteroviruses and Adenoviruses in stool specimens of paralytic children-can they be the cause of paralysis? Iranian J Microbiol 10(3):194

    Google Scholar 

  36. Belsy A et al (2009) Molecular characterization of adenoviral infections in Cuba: report of an unusual association of species D adenoviruses with different clinical syndromes. Adv Virol 154(4):619–627

    CAS  Google Scholar 

  37. Victoria JG et al (2009) Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. J Virol 83(9):4642–4651

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Lelong M et al (1956) La pneumonie a virus du groupe APC chez le Nourrisson Isolement du virus: les lesions anatomohistologiques. Arch Fr Pediatr 13:1092

    PubMed  Google Scholar 

  39. Chany C et al (1958) Severe and fatal pneumonia in infants and young children associated with adenovirus infections. Am J Hyg 67(3):367–378

    CAS  PubMed  Google Scholar 

  40. Kelsey DS (1978) Adenovirus meningoencephalitis. Pediatrics 61(2):291–293

    Article  CAS  PubMed  Google Scholar 

  41. Davis D, Henslee PJ, Markesbery WR (1988) Fatal adenovirus meningoencephalitis in a bone marrow transplant patient. Ann Neurol 23(4):385–389

    Article  CAS  PubMed  Google Scholar 

  42. Huttunen L (1970) Adenovirus type 7—associated encephalitis. Scand J Infect Dis 2(2):151–153

    Article  CAS  PubMed  Google Scholar 

  43. Straussberg R et al (2001) A syndrome of transient encephalopathy associated with adenovirus infection. Pediatrics 107(5):e69–e69

    Article  CAS  PubMed  Google Scholar 

  44. Dupuis M et al (2011) Molecular detection of viral causes of encephalitis and meningitis in New York State. J Med Virol 83(12):2172–2181

    Article  CAS  PubMed  Google Scholar 

  45. Chen S-Y et al (2020) Epidemiology and genetic variabilities of human adenovirus type 55 reveal relative genome stability across time and geographic space in China. Front Microbiol 11:3033

    Article  Google Scholar 

  46. Cook J, Radke J (2017) Mechanisms of pathogenesis of emerging adenoviruses. F1000Research, p1-10. https://doi.org/10.12688/f1000research.10152.1

  47. Houng H-SH et al (2010) Genome sequences of human adenovirus 14 isolates from mild respiratory cases and a fatal pneumonia, isolated during 2006–2007 epidemics in North America. Respir Res 11(1):1–8

    Article  Google Scholar 

Download references

Acknowledgement

The authors gratefully acknowledge the support provided by the National Institute of Health Islamabad

Author information

Authors and Affiliations

  1. Department of Microbiology, Faculty of Biological Sciences, Quaid-i-Azam University, Islamabad, Pakistan

    Zainab Khattak, Aamer Ali Shah & Yasir Arshid

  2. Department of Virology, National Institute of Health, Park Road, Chak Shahzad, Islamabad, 45500, Pakistan

    Syed Sohail Zahoor Zaidi, Nayab Mahmood, Muhammad Masroor Alam, Salmaan Sharif, Ribqa Akhtar, Yasir Arshid & Muhammad Suleman Rana

Authors
  1. Zainab Khattak
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aamer Ali Shah
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Syed Sohail Zahoor Zaidi
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Nayab Mahmood
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Muhammad Masroor Alam
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Salmaan Sharif
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Ribqa Akhtar
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yasir Arshid
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Muhammad Suleman Rana
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Muhammad Suleman Rana.

Ethics declarations

Conflict of interest

None to declare

Additional information

Handling Editor: Tim Skern.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (TXT 6 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Khattak, Z., Shah, A.A., Zaidi, S.S.Z. et al. Isolation and molecular characterization of Adenovirus in suspected acute flaccid paralysis patients: A preliminary report from Pakistan. Arch Virol 167, 483–491 (2022). https://doi.org/10.1007/s00705-021-05346-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00705-021-05346-x

Search

Navigation