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Comparative Study
. 2017 Sep 13;12(9):e0184699.
doi: 10.1371/journal.pone.0184699. eCollection 2017.

PCR detection of human herpesviruses in colonic mucosa of individuals with inflammatory bowel disease: Comparison with individuals with immunocompetency and HIV infection

Takayuki Shimada  1 , Naoyoshi Nagata  1 , Koki Okahara  1 , Akane Joya  2 , Tsunefusa Hayashida  2 , Shinichi Oka  2 , Toshiyuki Sakurai  1 , Junichi Akiyama  1 , Naomi Uemura  3 , Hiroyuki Gatanaga  2
Affiliations
Comparative Study

PCR detection of human herpesviruses in colonic mucosa of individuals with inflammatory bowel disease: Comparison with individuals with immunocompetency and HIV infection

Takayuki Shimada et al. PLoS One. .

Abstract

Background: Detection of human herpesviruses (HHVs) other than cytomegalovirus (CMV) in colonic mucosa of individuals with inflammatory bowel disease (IBD) remains unknown. This study identified eight HHVs in the colonic mucosa of individuals with IBD and compared the results with immunocompetent and human immunodeficiency virus (HIV)-infected individuals.

Methods: A total of 89 individuals who had colorectal ulcer on colonoscopy were enrolled: 26 with immunocompetency (n = 26), 41 with IBD, and 22 with HIV infection. We examined the colonic ulcers for the presence of eight HHVs-herpes simplex virus (HSV)-1/2, varicella zoster virus (VZV), CMV, Epstein-Barr virus (EBV), HHV-6, HHV-7, and HHV-8-using mucosal PCR.

Results: The IBD group had positivity rates of 0%, 0%, 0%, 53.7%, 24.4%, 39%, 39%, and 0% for HSV-1, HSV-2, VZV, EBV, CMV, HHV-6, HHV-7, and HHV-8, respectively. The positivity rates of EBV and CMV in colonic mucosa increased significantly in the order of the immunocompetent, IBD, and HIV groups (EBV: 23.1%, 53.7%, 72.7%, P for trend = 0.0005; CMV, 7.7%, 24.4%, 54.5%, P for trend = 0.0003, respectively), but no increase was found in the other HHVs. Median mucosal EBV DNA values in the immunocompetent, IBD, and HIV groups were 0, 76, and 287 copies/μg DNA, respectively (P for trend = 0.002). Corresponding median mucosal CMV DNA values were 0, 0, and 17 copies/μg DNA (P for trend = 0.0001). There was no significant difference in the positivity rates of the eight HHVs between ulcerative colitis and Crohn's disease.

Conclusion: The HHVs of EBV, CMV, HHV-6, and HHV-7, but not of HSV-1, HSV-2, VZV, or HHV-8, were identified in the colonic mucosa of IBD individuals. EBV and CMV in colonic mucosa was correlated with host immune status in increasing order of immunocompetent, IBD, and HIV-infected individuals.

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Conflict of interest statement

Competing Interests: The authors have declared that no competing interests exist.

Figures

Fig 1
Fig 1. Mucosal HHV PCR positivity rate in the IC, IBD, and HIV-infected groups.
Note: Bars represent standard error. Abbreviations: CMV, cytomegalovirus; EBV, Epstein–Barr virus; HHV, human herpesvirus; HIV, human immunodeficiency virus; HSV-1/2, herpes simplex virus-1/2; IBD, inflammatory bowel disease; IC, immunocompetent; NA, not applicable; VZV, varicella zoster virus.
Fig 2
Fig 2. Quantitative mucosal EBV and CMV in the IC, IBD, and HIV-infected groups.
Note: a95,286 copies/μg DNA, b172,000 and 498,000 copies/μg DNA. Abbreviations: CMV, cytomegalovirus; EBV, Epstein–Barr virus; HHV, human herpesvirus; HIV, human immunodeficiency virus; IBD, inflammatory bowel disease; IC, immunocompetent.
Fig 3
Fig 3. Mucosal HHV PCR positivity rate in UC and CD individuals (n = 41).
Note: Bars represent standard error. Abbreviations: CMV, cytomegalovirus; EBV, Epstein–Barr virus; HHV, human herpesvirus; HIV, human immunodeficiency virus; HSV-1/2, herpes simplex virus-1/2; IBD, inflammatory bowel disease; IC, immunocompetent; NA, not applicable; VZV, varicella zoster virus.
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Grants and funding

This study was funded by a Grant-in-Aid for Research from the National Center for Global Health and Medicine (26A-201 and 29-2001). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.