Parechovirus and enteroviruses among young infants with sepsis in Iran
-
Manoochehr Makvandi
,
Ali Teimoori
,
Roya Pirmoradi
,
Chiman Karami
,
Ahmad Shamsizadeh
,
Abdolnabi Shabani
,
Kambiz Ahmadi Angali
Abstract
Background and Objectives: Human parechoviruses (HPeV) and Human enteroviruses (EV) frequently cause a sepsis-like illness in young infants (younger than three months). Therefore, this study was conducted to determine the frequency of HPeV and EV among the young infants with clinical signs and symptoms of sepsis in Ahvaz city, Iran.
Materials and Methods: The blood specimens were collected from 100 (younger than 90 days hospitalized infants) including 54 (56.25%) males and 46 (43.75%) females with clinical signs and symptoms of sepsis-like disease. The RNA was extracted and tested for detection of VP1 region of HPeV and 5 UTR (Untranslated Region) of EV by RT-PCR. The sequences of positive of HPeV were further analyzed to determine HPeV genotyping.
Results: 5/100 (5%) of patients including 2/46 (2%) females and 3/54 (3%) males tested positive for HPeV (P=0.85). The analysis of 5 positive VP1 region of HPeV revealed the genotype 1. The analysis of sequencing and phylogenetic tree revealed that the isolated HPeVs were genotype 1. While 38/100 (38%) specimens including 16 (16%) females and 22 (22%) males were tested positive for EV (P=0.68).
Conclusion: The frequency of HPeV genotype 1 was 5% among the young infants with sepsis. While frequency of EV was 38% among the young infants with sepsis. This study showed HPeV genotype 1 and EV are dominant in this region.
1. Brent AJ. Sepsis. Medicine 2018;45:649-653.
2. Dolin HH, Papadimos TJ, Chen X, Pan ZK. Characterization of pathogenic sepsis etiologies and patient profiles: a novel approach to triage and treatment. Microbiol Insights 2019;12:1178636118825081.
3. Bone RC. The sepsis syndrome. definition and general approach to management. Clin Chest Med 1996;17:175-181.
4. Gupta N, Richter R, Robert S, Kong M. Viral sepsis in children. Front Pediatr 2018;6:252.
5. Tapparel C, Siegrist F, Petty TJ, Kaiser L. Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol 2013;14:282-293.
6. Stanway G, Joki-Korpela P, Hyypia T, Human parechoviruses--biology and clinical significance. Rev Med Virol 2000;10:57-69.
7. Sridhar A, Karelehto E, Brouwer L, Pajkrt D, Wolthers KC. Parechovirus a pathogenesis and the enigma of genotype A‐3. Viruses 2019;11:1062.
8. Olijve L, Jennings L, Walls T. Human parechovirus: an increasingly recognized cause of sepsis-like illness in young infants. Clin Microbiol Rev 2017;31(1):e00047-17.
9. Alam MM, Khurshid A, Shaukat S, Rana MS, Sharif S, Angez M, et al. Viral etiologies of acute dehydrating gastroenteritis in Pakistani children: confounding role of parechoviruses. Viruses 2015;7:378-393.
10. Patil PR, Ganorkar NN, Gopalkrishna V. Epidemiology and genetic diversity of human parechovirus circulating among children hospitalized with acute gastroenteritis in Pune, western India: a 5-years study. Epidemiol Infect 2018;146:11-18.
11. Zhong H, Lin Y, Sun J, Su L, Cao L, Yang Y, et al. Prevalence and genotypes of human parechovirus in stool samples from hospitalized children in Shanghai, China, 2008 and 2009. J Med Virol 2011;83:1428-1434.
12. Graul S, Bottcher S, Eibach D, Krumkamp R, Kasmaier J, Adu-Sarkodie Y, et al. High diversity of human parechovirus including novel types in stool samples from Ghanaian children. J Clin Virol 2017;96:116-119.
13. Rahimi P, Naser HM, Siadat SD, Sohrabi A, Mostafavi E, Motamedirad M, et al. Genotyping of human parechovirus in Iranian young children with aseptic meningitis and sepsis-like illness. J Neurovirol 2013;19:595-600.
14. Shokrollahi MR, Noorbakhsh S, Monavari HR, Darestani SG, Motlagh AV, Javadinia S. Acute nonbacterial gastroenteritis in hospitalized children: a cross sectional study. Jundishapur J Microbiol 2014;7(12):e11840.
15. Ghazi F, Ataei Z, Dabirmanesh B. Molecular detection of human parechovirus type 1 in stool samples from children with diarrhea. Int J Infect Dis 2012;16(9):e673-676.
16. Ito M, Yamashita T, Tsuzuki H, Kabashima Y, Hasegawa A, Nagaya S, et al. Detection of human parechovirus from clinical stool samples in Aichi, Japan. J Clin Microbiol 2010;48:2683-2688.
17. Chiang GPK, Chen Z, Chan MCW, Lee SHM, Kwok AK, Yeung ACM, et al. Clinical features and seasonality of parechovirus infection in an Asian subtropical city, Hong Kong. PLoS One 2017;12(9):e0184533.
18. Ito M, Yamashita T, Tsuzuki H, Takeda N, Sakae K. Isolation and identification of a novel human parechovirus. J Gen Virol 2004;85:391-398.
19. Verboon-Maciolek MA, Groenendaal F, Hahn CD, Hellmann J, van Loon AM, Boivin G, et al. Human parechovirus causes encephalitis with white matter injury in neonates. Ann Neurol 2008;64:266-273.
20. B'Krong NTTC, Minh NNQ, Qui PT, Chau TTH, Nghia HDT, Do LAH, et al. Enterovirus serotypes in patients with central nervous system and respiratory infections in Viet Nam 1997-2010. Virol J 2018;15:69.
21. Ahmad S, Dalwai A, Al-Nakib W. Frequency of enterovirus detection in blood samples of neonates admitted to hospital with sepsis-like illness in Kuwait. J Med Virol 2013;85:1280-1285.
22. Harvala H, McLeish N, Kondracka J, McIntyre CL, McWilliam Leitch EC, Templeton K, et al. Comparison of human parechovirus and enterovirus detection frequencies in cerebrospinal fluid samples collected over a 5‐year period in Edinburgh: parechovirus type 3 identified as the most common picornavirus type. J Med Virol 2011;83:889-896.
23. Maguire HC, Atkinson P, Sharland M, Bendig J. Enterovirus infections in England and Wales: laboratory surveillance data: 1975 to 1994. Commun Dis Public Health 1999;2:122-125.
24. Khetsuriani N, Lamonte-Fowlkes A, Oberste S, Pallansch MA. Enterovirus surveillance--United States, 1970-2005. MMWR Surveill Summ 2006;55:1-20.
25. Kapusinszky B, Szomor KN, Farkas Á, Takács M, Berencsi G. Detection of non-polio enteroviruses in Hungary 2000–2008 and molecular epidemiology of enterovirus 71, coxsackievirus A16, and echovirus 30. Virus Genes 2010;40:163-173.
26. Wildenbeest JG, Benschop KS, Bouma-de Jongh S, Wolthers KC, Pajkrt D. Prolonged shedding of human parechovirus in feces of young children after symptomatic infection. Pediatr Infect Dis J 2016;35:580-583
27. Sharp J, Bell J, Harrison CJ, Nix WA, Oberste MS, Selvarangan R. Human parechovirus in respiratory specimens from children in Kansas city, Missouri. J Clin Microbiol 2012;50:4111-4113.
28. Yen MH, Tsao KC, Huang YC, Huang CG, Huang YL, Lin R, et al. Viral load in blood is correlated with disease severity of neonatal coxsackievirus B3 infection: early diagnosis and predicting disease severity is possible in severe neonatal enterovirus infection. Clin Infect Dis 2007;44(10):e78-81.
29. Esposito S, Rahamat-Langendoen J, Ascolese B, Senatore L, Castellazzi L, Niesters HG. Pediatric parechovirus infections. J Clin Virol 2014;60:84-89.
30. Nix WA, Maher K, Pallansch MA, Oberste MS. Parechovirus typing in clinical specimens by nested or semi-nested PCR coupled with sequencing. J Clin Virol 2010;48:202-207.
31. Mohamadpoor T, Nabavinia M, Gholoobi A, Alavi M, Meshkat Z. Enteroviruses in acute myocardial infarction. Iran J Public Health 2012;41:71-74.
32. Studier JA, Keppler KJ. A note on the neighbor-joining algorithm of Saitou and Nei. Mol Biol Evol 1988;5:729-731.
33. Wolthers KC, Benschop KS, Schinkel J, Molenkamp R, Bergevoet RM, Spijkerman IJ, et al. Human parechovirus as an important viral cause of sepsis like illness and meningitis in young children. Clin Infect Dis 2008;47:358-363.
34. Harvala H, Robertson I, Chieochansin T, McWilliam Leitch EC, Templeton K, Simmonds P. Specific association of human parechovirus type 3 with sepsis and fever in young infants, as identified by direct typing of cerebrospinal fluid samples. J Infect Dis 2009;199:1753-1760.
35. Shahroodi MJG, Ghazvini K, Sadeghi R, Sasan MS. Enteroviral meningitis in neonates and children of Mashhad, Iran. Jundishapur J Microbiol 2016;9(5):e19955.
36. Rahimi P, Mahdian Naser H, Sohrabi A. The association of non-polio enteroviruses with aseptic meningitis in children in Iran. JoMMID 2014;2:56-60.
37. Rasti M, Samarbaf-Zadeh AR, Makvandi M, Shamsi-Zadeh A. Relative frequency of enteroviruses in children with aseptic meningitis referred to Aboozar hospital in Ahvaz. Jundishapur J Microbiol 2012;5:456-459.
38. Jordan I, Esteva C, Esteban E, Noguera A, García JJ, Muñoz-Almagro C. Severe enterovirus disease in febrile neonates. Enferm Infecc Microbiol Clin 2009;27:399-402.
39. Seo JH, Yeom JS, Youn HS, Han TH, Chung JY. Prevalence of human parechovirus and enterovirus in cerebrospinal fluid samples in children in Jinju, Korea. Korean J Pediatr 2015;58:102-107.
40. Fragkou PC, Moschopoulos CD, Karofylakis E, Kelesidis T, Tsiodras S. Update in viral infections in the intensive care unit. Front Med (Lausanne) 2021;8:575580.
41. Upperman JS, Potoka DA, Zhang X, Wong K, Zamora R, Ford HR. Mechanism of intestinal-derived fungal sepsis by gliotoxin, a fungal metabolite. J Pediatr Surg 2003;38:966-970.
42. Delaloye J, Calandra T. Invasive candidiasis as a cause of sepsis in the critically ill patient. Virulence 2014;5:161-169.
2. Dolin HH, Papadimos TJ, Chen X, Pan ZK. Characterization of pathogenic sepsis etiologies and patient profiles: a novel approach to triage and treatment. Microbiol Insights 2019;12:1178636118825081.
3. Bone RC. The sepsis syndrome. definition and general approach to management. Clin Chest Med 1996;17:175-181.
4. Gupta N, Richter R, Robert S, Kong M. Viral sepsis in children. Front Pediatr 2018;6:252.
5. Tapparel C, Siegrist F, Petty TJ, Kaiser L. Picornavirus and enterovirus diversity with associated human diseases. Infect Genet Evol 2013;14:282-293.
6. Stanway G, Joki-Korpela P, Hyypia T, Human parechoviruses--biology and clinical significance. Rev Med Virol 2000;10:57-69.
7. Sridhar A, Karelehto E, Brouwer L, Pajkrt D, Wolthers KC. Parechovirus a pathogenesis and the enigma of genotype A‐3. Viruses 2019;11:1062.
8. Olijve L, Jennings L, Walls T. Human parechovirus: an increasingly recognized cause of sepsis-like illness in young infants. Clin Microbiol Rev 2017;31(1):e00047-17.
9. Alam MM, Khurshid A, Shaukat S, Rana MS, Sharif S, Angez M, et al. Viral etiologies of acute dehydrating gastroenteritis in Pakistani children: confounding role of parechoviruses. Viruses 2015;7:378-393.
10. Patil PR, Ganorkar NN, Gopalkrishna V. Epidemiology and genetic diversity of human parechovirus circulating among children hospitalized with acute gastroenteritis in Pune, western India: a 5-years study. Epidemiol Infect 2018;146:11-18.
11. Zhong H, Lin Y, Sun J, Su L, Cao L, Yang Y, et al. Prevalence and genotypes of human parechovirus in stool samples from hospitalized children in Shanghai, China, 2008 and 2009. J Med Virol 2011;83:1428-1434.
12. Graul S, Bottcher S, Eibach D, Krumkamp R, Kasmaier J, Adu-Sarkodie Y, et al. High diversity of human parechovirus including novel types in stool samples from Ghanaian children. J Clin Virol 2017;96:116-119.
13. Rahimi P, Naser HM, Siadat SD, Sohrabi A, Mostafavi E, Motamedirad M, et al. Genotyping of human parechovirus in Iranian young children with aseptic meningitis and sepsis-like illness. J Neurovirol 2013;19:595-600.
14. Shokrollahi MR, Noorbakhsh S, Monavari HR, Darestani SG, Motlagh AV, Javadinia S. Acute nonbacterial gastroenteritis in hospitalized children: a cross sectional study. Jundishapur J Microbiol 2014;7(12):e11840.
15. Ghazi F, Ataei Z, Dabirmanesh B. Molecular detection of human parechovirus type 1 in stool samples from children with diarrhea. Int J Infect Dis 2012;16(9):e673-676.
16. Ito M, Yamashita T, Tsuzuki H, Kabashima Y, Hasegawa A, Nagaya S, et al. Detection of human parechovirus from clinical stool samples in Aichi, Japan. J Clin Microbiol 2010;48:2683-2688.
17. Chiang GPK, Chen Z, Chan MCW, Lee SHM, Kwok AK, Yeung ACM, et al. Clinical features and seasonality of parechovirus infection in an Asian subtropical city, Hong Kong. PLoS One 2017;12(9):e0184533.
18. Ito M, Yamashita T, Tsuzuki H, Takeda N, Sakae K. Isolation and identification of a novel human parechovirus. J Gen Virol 2004;85:391-398.
19. Verboon-Maciolek MA, Groenendaal F, Hahn CD, Hellmann J, van Loon AM, Boivin G, et al. Human parechovirus causes encephalitis with white matter injury in neonates. Ann Neurol 2008;64:266-273.
20. B'Krong NTTC, Minh NNQ, Qui PT, Chau TTH, Nghia HDT, Do LAH, et al. Enterovirus serotypes in patients with central nervous system and respiratory infections in Viet Nam 1997-2010. Virol J 2018;15:69.
21. Ahmad S, Dalwai A, Al-Nakib W. Frequency of enterovirus detection in blood samples of neonates admitted to hospital with sepsis-like illness in Kuwait. J Med Virol 2013;85:1280-1285.
22. Harvala H, McLeish N, Kondracka J, McIntyre CL, McWilliam Leitch EC, Templeton K, et al. Comparison of human parechovirus and enterovirus detection frequencies in cerebrospinal fluid samples collected over a 5‐year period in Edinburgh: parechovirus type 3 identified as the most common picornavirus type. J Med Virol 2011;83:889-896.
23. Maguire HC, Atkinson P, Sharland M, Bendig J. Enterovirus infections in England and Wales: laboratory surveillance data: 1975 to 1994. Commun Dis Public Health 1999;2:122-125.
24. Khetsuriani N, Lamonte-Fowlkes A, Oberste S, Pallansch MA. Enterovirus surveillance--United States, 1970-2005. MMWR Surveill Summ 2006;55:1-20.
25. Kapusinszky B, Szomor KN, Farkas Á, Takács M, Berencsi G. Detection of non-polio enteroviruses in Hungary 2000–2008 and molecular epidemiology of enterovirus 71, coxsackievirus A16, and echovirus 30. Virus Genes 2010;40:163-173.
26. Wildenbeest JG, Benschop KS, Bouma-de Jongh S, Wolthers KC, Pajkrt D. Prolonged shedding of human parechovirus in feces of young children after symptomatic infection. Pediatr Infect Dis J 2016;35:580-583
27. Sharp J, Bell J, Harrison CJ, Nix WA, Oberste MS, Selvarangan R. Human parechovirus in respiratory specimens from children in Kansas city, Missouri. J Clin Microbiol 2012;50:4111-4113.
28. Yen MH, Tsao KC, Huang YC, Huang CG, Huang YL, Lin R, et al. Viral load in blood is correlated with disease severity of neonatal coxsackievirus B3 infection: early diagnosis and predicting disease severity is possible in severe neonatal enterovirus infection. Clin Infect Dis 2007;44(10):e78-81.
29. Esposito S, Rahamat-Langendoen J, Ascolese B, Senatore L, Castellazzi L, Niesters HG. Pediatric parechovirus infections. J Clin Virol 2014;60:84-89.
30. Nix WA, Maher K, Pallansch MA, Oberste MS. Parechovirus typing in clinical specimens by nested or semi-nested PCR coupled with sequencing. J Clin Virol 2010;48:202-207.
31. Mohamadpoor T, Nabavinia M, Gholoobi A, Alavi M, Meshkat Z. Enteroviruses in acute myocardial infarction. Iran J Public Health 2012;41:71-74.
32. Studier JA, Keppler KJ. A note on the neighbor-joining algorithm of Saitou and Nei. Mol Biol Evol 1988;5:729-731.
33. Wolthers KC, Benschop KS, Schinkel J, Molenkamp R, Bergevoet RM, Spijkerman IJ, et al. Human parechovirus as an important viral cause of sepsis like illness and meningitis in young children. Clin Infect Dis 2008;47:358-363.
34. Harvala H, Robertson I, Chieochansin T, McWilliam Leitch EC, Templeton K, Simmonds P. Specific association of human parechovirus type 3 with sepsis and fever in young infants, as identified by direct typing of cerebrospinal fluid samples. J Infect Dis 2009;199:1753-1760.
35. Shahroodi MJG, Ghazvini K, Sadeghi R, Sasan MS. Enteroviral meningitis in neonates and children of Mashhad, Iran. Jundishapur J Microbiol 2016;9(5):e19955.
36. Rahimi P, Mahdian Naser H, Sohrabi A. The association of non-polio enteroviruses with aseptic meningitis in children in Iran. JoMMID 2014;2:56-60.
37. Rasti M, Samarbaf-Zadeh AR, Makvandi M, Shamsi-Zadeh A. Relative frequency of enteroviruses in children with aseptic meningitis referred to Aboozar hospital in Ahvaz. Jundishapur J Microbiol 2012;5:456-459.
38. Jordan I, Esteva C, Esteban E, Noguera A, García JJ, Muñoz-Almagro C. Severe enterovirus disease in febrile neonates. Enferm Infecc Microbiol Clin 2009;27:399-402.
39. Seo JH, Yeom JS, Youn HS, Han TH, Chung JY. Prevalence of human parechovirus and enterovirus in cerebrospinal fluid samples in children in Jinju, Korea. Korean J Pediatr 2015;58:102-107.
40. Fragkou PC, Moschopoulos CD, Karofylakis E, Kelesidis T, Tsiodras S. Update in viral infections in the intensive care unit. Front Med (Lausanne) 2021;8:575580.
41. Upperman JS, Potoka DA, Zhang X, Wong K, Zamora R, Ford HR. Mechanism of intestinal-derived fungal sepsis by gliotoxin, a fungal metabolite. J Pediatr Surg 2003;38:966-970.
42. Delaloye J, Calandra T. Invasive candidiasis as a cause of sepsis in the critically ill patient. Virulence 2014;5:161-169.
| Files | ||
| Issue | Vol 13 No 3 (2021) | |
| Section | Original Article(s) | |
| DOI | https://doi.org/10.18502/ijm.v13i3.6393 | |
| Keywords | ||
| Sepsis; Parechovirus; Enterovirus; Reverse transcriptase polymerase chain reaction; Genotype | ||
| Rights and permissions | |
|
This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License. |
How to Cite
1.
Makvandi M, Teimoori A, Pirmoradi R, Karami C, Shamsizadeh A, Shabani A, Ahmadi Angali K. Parechovirus and enteroviruses among young infants with sepsis in Iran. Iran J Microbiol. 2021;13(3):312-318.
