J Korean Med Sci.  2017 Oct;32(10):1647-1656. 10.3346/jkms.2017.32.10.1647.

Epidemiological Correlation between Fecal Adenovirus Subgroups and Pediatric Intussusception in Korea

• Jang J
• Lee YJ
• Kim JS
• Chung JY
• Chang S
• Lee K
• Choe BH
• Hong SJ
• Song JS
• Park KY

• KMID: 2400437
• DOI: http://doi.org/10.3346/jkms.2017.32.10.1647

Abstract

We investigated the adenoviral etiology and seasonal epidemic trends in intussusception and each adenoviral subgroup. Also we confirmed whether we can use the adenovirus data of Acute Infectious Agents Laboratory Surveillance Report (AIALSR) as an epidemic predictor of intussusception. Patients with intussusception (n = 126), < 5 years old, were enrolled and matched by age and sex with controls suffering acute gastroenteritis without intussusception (n = 106), all recruited at 8 centers. All fecal specimens were assayed for adenovirus, including subgroups A, B, C, E, and F, with reverse transcriptase-polymerase chain reaction (RT-PCR). Adenovirus was detected in 53 cases and 13 controls (P < 0.001). Nonenteric adenoviruses (NEAds) were detected in 51 cases and four controls (P < 0.001). We used Spearman's correlation analysis to analyze the incidence of intussusception and adenoviral epidemic trends, and compared them with fecal and respiratory adenoviral epidemic trends in the AIALSR. The trend of intussusception correlated with total NEAds (r = 0.635; P = 0.011), as did the fecal AIALSR adenovirus trends (r = 0.572; P = 0.026). Among the NEAd subgroups, subgroup C was dominant (P < 0.001), but subgroups B (P = 0.007) and E (P = 0.013) were also significant to intussusception. However, only subgroup C showed a significant epidemic correlation (r = 0.776; P = 0.001) with intussusception. Not respiratory but fecal AIALSR adenovirus trends correlated with the incidence of NEAds and intussusception. We suggest the possibility of using fecal AIALSR adenovirus data as an approximate epidemic predictor of intussusception.

Keyword

Intussusception; Adenoviridae; Epidemics; Reverse Transcriptase-Polymerase Chain Reaction; Child

MeSH Terms

Adenoviridae*
Child
Gastroenteritis
Humans
Incidence
Intussusception*
Korea*
Seasons

Figure

• 

  Fig. 1 Cases of intussusceptions and the virus detected, according to age. NEAd = nonenteric adenovirus.

• 

  Fig. 2 Comparisons of the seasonal epidemic trends. (A) Adenovirus data from AIALSR, intussusception, and NEAd, and (B) intussusception and NEAd subgroups. AIALSR = Acute Infectious Agents Laboratory Surveillance Report, NEAd = nonenteric adenovirus, Ad =adenovirus.

• 

  Fig. 3 Seasonal epidemic trends in each virus in the fecal AIALSR data and our results (sum of cases and controls). (A) Norovirus, (B) rotavirus, and (C) astrovirus and sapovirus in this study. AIALSR = Acute Infectious Agents Laboratory Surveillance Report.

Reference

1. Kennedy M, Liacouras CA. Intussusception. In : Kliegman RM, Stanton BF, St. Geme JW, Schor NF, editors. Nelson Textbook of Pediatrics. 20th ed. Philadelphia, PA: Elsevier;2016. p. 1812–1814.

2. Bell TM, Steyn JH. Viruses in lymph nodes of children with mesenteric adenitis and intussusception. BMJ. 1962; 2:700–702.

3. Kim JS, Lee SK, Ko DH, Hyun J, Kim HS, Song W, Kim HS. Associations of adenovirus genotypes in Korean acute gastroenteritis patients with respiratory symptoms and intussusception. Biomed Res Int. 2017; 2017:1602054.

4. Moore SW, Kirsten M, Müller EW, Numanoglu A, Chitnis M, Le Grange E, Banieghbal B, Hadley GP. Retrospective surveillance of intussusception in South Africa, 1998–2003. J Infect Dis. 2010; 202:Suppl. S156–S161.

5. Bruce J, Huh YS, Cooney DR, Karp MP, Allen JE, Jewett TC Jr. Intussusception: evolution of current management. J Pediatr Gastroenterol Nutr. 1987; 6:663–674.

6. Pang LC. Intussusception revisited: clinicopathologic analysis of 261 cases, with emphasis on pathogenesis. South Med J. 1989; 82:215–228.

7. Arbizu RA, Aljomah G, Kozielski R, Baker SS, Baker RD. Intussusception associated with adenovirus. J Pediatr Gastroenterol Nutr. 2014; 59:e41.

8. Murphy TV, Gargiullo PM, Massoudi MS, Nelson DB, Jumaan AO, Okoro CA, Zanardi LR, Setia S, Fair E, LeBaron CW, Rotavirus Intussusception Investigation Team, et al. Intussusception among infants given an oral rotavirus vaccine. N Engl J Med. 2001; 344:564–572.

9. El-Hodhod MA, Nassar MF, Ezz El-Arab S, Ahmed EF. Rotavirus fecal antigen retrieval in infantile intussusception. Eur J Clin Microbiol Infect Dis. 2008; 27:879–881.

10. Hsu HY, Kao CL, Huang LM, Ni YH, Lai HS, Lin FY, Chang MH. Viral etiology of intussusception in Taiwanese childhood. Pediatr Infect Dis J. 1998; 17:893–898.

11. Aminu M, Ameh EA, Geyer A, Esona MD, Taylor MB, Steele AD. Role of astrovirus in intussusception in Nigerian infants. J Trop Pediatr. 2009; 55:192–194.

12. Okimoto S, Hyodo S, Yamamoto M, Nakamura K, Kobayashi M. Association of viral isolates from stool samples with intussusception in children. Int J Infect Dis. 2011; 15:e641–e645.

13. Khalifa AB, Jebali A, Kedher M, Trabelsi A. Infectious etiology of acute idiopathic intussusception in children. Ann Biol Clin (Paris). 2013; 71:389–393.

14. Kaemmerer E, Tischendorf JJ, Steinau G, Wagner N, Gassler N. Ileocecal intussusception with histomorphological features of inflammatory neuropathy in adenovirus infection. Gastroenterol Res Pract. 2009; 2009:579501.

15. Chhabra P, Payne DC, Szilagyi PG, Edwards KM, Staat MA, Shirley SH, Wikswo M, Nix WA, Lu X, Parashar UD, et al. Etiology of viral gastroenteritis in children <5 years of age in the United States, 2008–2009. J Infect Dis. 2013; 208:790–800.

16. Jakab F, Péterfai J, Verebély T, Meleg E, Bányai K, Mitchell DK, Szûcs G. Human astrovirus infection associated with childhood intussusception. Pediatr Int. 2007; 49:103–105.

17. Lappalainen S, Ylitalo S, Arola A, Halkosalo A, Räsänen S, Vesikari T. Simultaneous presence of human herpesvirus 6 and adenovirus infections in intestinal intussusception of young children. Acta Paediatr. 2012; 101:663–670.

18. Bines JE, Liem NT, Justice FA, Son TN, Kirkwood CD, de Campo M, Barnett P, Bishop RF, Robins-Browne R, Carlin JB; Intussusception Study Group. Risk factors for intussusception in infants in Vietnam and Australia: adenovirus implicated, but not rotavirus. J Pediatr. 2006; 149:452–460.

19. Lee YW, Yang SI, Kim JM, Kim JY. Clinical features and role of viral isolates from stool samples of intussuception in children. Pediatr Gastroenterol Hepatol Nutr. 2013; 16:162–170.

20. Korea Centers for Disease Control & Prevention. Weekly viral epidemic reports of acute diarrheal disease: no. 213–278 [Internet]. accessed on 6 June 2017. Available at http://www.cdc.go.kr/CDC/info/CdcKrInfo0503.jsp?menuIds=HOME001-MNU1154-MNU0005-MNU0048-MNU0051<fid=478<q_type=<q_value=&pageNum=.

21. Korea Centers for Disease Control & Prevention. Weekly viral epidemic report of influenza and respiratory virus: no. 209–268 [Internet]. accessed on 6 June 2017. Available at http://www.cdc.go.kr/CDC/info/CdcKrInfo0502.jsp?menuIds=HOME001-MNU1154-MNU0005-MNU0048-MNU0050&fid=477&q_type=&q_value=&pageNum=26.

22. Liu L, Qian Y, Zhang Y, Deng J, Jia L, Dong H. Adenoviruses associated with acute diarrhea in children in Beijing, China. PLoS One. 2014; 9:e88791.

23. Lee JI, Lee GC, Chung JY, Han TH, Lee YK, Kim MS, Lee CH. Detection and molecular characterization of adenoviruses in Korean children hospitalized with acute gastroenteritis. Microbiol Immunol. 2012; 56:523–528.

24. Chen SC, Wang JD, Hsu HY, Leong MM, Tok TS, Chin YY. Epidemiology of childhood intussusception and determinants of recurrence and operation: analysis of national health insurance data between 1998 and 2007 in Taiwan. Pediatr Neonatol. 2010; 51:285–291.

25. Takeuchi M, Osamura T, Yasunaga H, Horiguchi H, Hashimoto H, Matsuda S. Intussusception among Japanese children: an epidemiologic study using an administrative database. BMC Pediatr. 2012; 12:36.

26. Yang CM, Hsu HY, Tsao PN, Chang MH, Lin FY. Recurrence of intussusception in childhood. Acta Paediatr Taiwan. 2001; 42:158–161.

27. Wang GD, Liu SJ. Enema reduction of intussusception by hydrostatic pressure under ultrasound guidance: a report of 377 cases. J Pediatr Surg. 1988; 23:814–818.

28. Nicolas JC, Ingrand D, Fortier B, Bricout F. A one-year virological survey of acute intussusception in childhood. J Med Virol. 1982; 9:267–271.

29. Guarner J, de Leon-Bojorge B, Lopez-Corella E, Ferebee-Harris T, Gooding L, Garnett CT, Shieh WJ, Dawson J, Erdman D, Zaki SR. Intestinal intussusception associated with adenovirus infection in Mexican children. Am J Clin Pathol. 2003; 120:845–850.

30. Selvaraj G, Kirkwood C, Bines J, Buttery J. Molecular epidemiology of adenovirus isolates from patients diagnosed with intussusception in Melbourne, Australia. J Clin Microbiol. 2006; 44:3371–3373.

31. Ghebremedhin B. Human adenovirus: viral pathogen with increasing importance. Eur J Microbiol Immunol (Bp). 2014; 4:26–33.

32. Mandelboim M, Dror P, Azar R, Bromberg M, Mendelson E. Adenovirus infections in hospitalized patients in Israel: epidemiology and molecular characterization. J Clin Microbiol. 2011; 49:597–601.