Skip to main content
Top
Published in: Virology Journal 1/2012

Open Access 01-12-2012 | Research

Simultaneous investigation of influenza and enteric viruses in the stools of adult patients consulting in general practice for acute diarrhea

Authors: Christophe Arena, Jean Pierre Amoros, Véronique Vaillant, Katia Balay, Roxane Chikhi-Brachet, Laurent Varesi, Jean Arrighi, Thierry Blanchon, Fabrice Carrat, Thomas Hanslik, Alessandra Falchi

Published in: Virology Journal | Issue 1/2012

Login to get access

Abstract

Background

Gastrointestinal symptoms are not an uncommon manifestation of an influenza virus infection. In the present study, we aimed to investigate the presence of influenza viruses in the stools of adult patients consulting their general practitioner for uncomplicated acute diarrhea (AD) and the proportion of concurrent infections by enteric and influenza viruses.

Method

A case-control study was conducted from December 2010 to April 2011. Stool specimens were collected and tested for influenza viruses A (seasonal A/H3N2 and pandemic A/H1N1) and B, and for four enteric viruses (astrovirus, group A rotavirus, human enteric adenovirus, norovirus of genogroups I – NoVGI - and genogroup II - NoVGII).

Results

General practitioners enrolled 138 cases and 93 controls. Of the 138 stool specimens collected, 92 (66.7%) were positive for at least one of the four enteric viruses analysed and 10 (7.2%) tested positive for one influenza virus. None of these 10 influenza positive patients reported respiratory symptoms. In five influenza-positive patients (3.6%), we also detected one enteric virus, with 4 of them being positive for influenza B (2 had co-detection with NoVGI, 1 with NoVGII, and 1 with astrovirus). None of the 93 controls tested positive for one of the enteric and/or other influenza viruses we investigated.

Conclusions

In this study we showed that the simultaneous detection of influenza and enteric viruses is not a rare event. We have also reported, for the first time in general practice, the presence of seasonal and pandemic influenza viruses in the stools of adult patients consulting for uncomplicated AD. A simultaneous investigation of enteric and influenza viruses in patients complaining of gastrointestinal symptoms could be useful for future studies to better identify the agents responsible for AD.
Literature
1.
go back to reference Kerr AA, McQuillin J, Downham MA, Gardner PS: Gastric 'flu influenza B causing abdominal symptons in children. Lancet 1975,1(7902):291-295.PubMedCrossRef Kerr AA, McQuillin J, Downham MA, Gardner PS: Gastric 'flu influenza B causing abdominal symptons in children. Lancet 1975,1(7902):291-295.PubMedCrossRef
2.
go back to reference Chi CY, Wang SM, Lin CC, Wang HC, Wang JR, Su IJ, Liu CC: Clinical features of children infected with different strains of influenza B in southern Taiwan. Pediatr Infect Dis J 2008,27(7):640-645. 10.1097/INF.0b013e31816be008PubMedCrossRef Chi CY, Wang SM, Lin CC, Wang HC, Wang JR, Su IJ, Liu CC: Clinical features of children infected with different strains of influenza B in southern Taiwan. Pediatr Infect Dis J 2008,27(7):640-645. 10.1097/INF.0b013e31816be008PubMedCrossRef
3.
go back to reference Chan PA, Mermel LA, Andrea SB, McCulloh R, Mills JP, Echenique I, Leveen E, Rybak N, Cunha C, Machan JT, et al.: Distinguishing characteristics between pandemic 2009-2010 influenza A (H1N1) and other viruses in patients hospitalized with respiratory illness. PLoS One 2011,6(9):e24734. 10.1371/journal.pone.0024734PubMedPubMedCentralCrossRef Chan PA, Mermel LA, Andrea SB, McCulloh R, Mills JP, Echenique I, Leveen E, Rybak N, Cunha C, Machan JT, et al.: Distinguishing characteristics between pandemic 2009-2010 influenza A (H1N1) and other viruses in patients hospitalized with respiratory illness. PLoS One 2011,6(9):e24734. 10.1371/journal.pone.0024734PubMedPubMedCentralCrossRef
4.
go back to reference Price DA, Postlethwaite RJ, Longson M: Influenzavirus A2 infections presenting with febril convulsions and gastrointestinal symptoms in young children. Clin Pediatr (Phila) 1976,15(4):361-367. 10.1177/000992287601500408CrossRef Price DA, Postlethwaite RJ, Longson M: Influenzavirus A2 infections presenting with febril convulsions and gastrointestinal symptoms in young children. Clin Pediatr (Phila) 1976,15(4):361-367. 10.1177/000992287601500408CrossRef
5.
go back to reference Armstrong KL, Fraser DK, Faoagali JL: Gastrointestinal bleeding with influenza virus. Med J Aust 1991,154(3):180-182.PubMed Armstrong KL, Fraser DK, Faoagali JL: Gastrointestinal bleeding with influenza virus. Med J Aust 1991,154(3):180-182.PubMed
6.
go back to reference Peltola V, Ziegler T, Ruuskanen O: Influenza A and B virus infections in children. Clin Infect Dis 2003,36(3):299-305. 10.1086/345909PubMedCrossRef Peltola V, Ziegler T, Ruuskanen O: Influenza A and B virus infections in children. Clin Infect Dis 2003,36(3):299-305. 10.1086/345909PubMedCrossRef
7.
go back to reference Wootton SH, Scheifele DW, Mak A, Petric M, Skowronski DM: Detection of human influenza virus in the stool of children. Pediatr Infect Dis J 2006,25(12):1194-1195.PubMedCrossRef Wootton SH, Scheifele DW, Mak A, Petric M, Skowronski DM: Detection of human influenza virus in the stool of children. Pediatr Infect Dis J 2006,25(12):1194-1195.PubMedCrossRef
8.
go back to reference Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, Garten RJ, Gubareva LV, Xu X, Bridges CB, Uyeki TM: Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 2009,360(25):2605-2615.PubMedCrossRef Dawood FS, Jain S, Finelli L, Shaw MW, Lindstrom S, Garten RJ, Gubareva LV, Xu X, Bridges CB, Uyeki TM: Emergence of a novel swine-origin influenza A (H1N1) virus in humans. N Engl J Med 2009,360(25):2605-2615.PubMedCrossRef
9.
go back to reference Dilantika C, Sedyaningsih ER, Kasper MR, Agtini M, Listiyaningsih E, Uyeki TM, Burgess TH, Blair PJ, Putnam SD: Influenza virus infection among pediatric patients reporting diarrhea and influenza-like illness. BMC Infect Dis 2010, 10: 3. 10.1186/1471-2334-10-3PubMedPubMedCentralCrossRef Dilantika C, Sedyaningsih ER, Kasper MR, Agtini M, Listiyaningsih E, Uyeki TM, Burgess TH, Blair PJ, Putnam SD: Influenza virus infection among pediatric patients reporting diarrhea and influenza-like illness. BMC Infect Dis 2010, 10: 3. 10.1186/1471-2334-10-3PubMedPubMedCentralCrossRef
10.
go back to reference Chan MC, Lee N, Chan PK, Leung TF, Sung JJ: Fecal detection of influenza A virus in patients with concurrent respiratory and gastrointestinal symptoms. J Clin Virol 2009,45(3):208-211. 10.1016/j.jcv.2009.06.011PubMedCrossRef Chan MC, Lee N, Chan PK, Leung TF, Sung JJ: Fecal detection of influenza A virus in patients with concurrent respiratory and gastrointestinal symptoms. J Clin Virol 2009,45(3):208-211. 10.1016/j.jcv.2009.06.011PubMedCrossRef
11.
go back to reference Chan MC, Lee N, Chan PK, To KF, Wong RY, Ho WS, Ngai KL, Sung JJ: Seasonal influenza A virus in feces of hospitalized adults. Emerg Infect Dis 2011,17(11):2038-2042.PubMedPubMedCentralCrossRef Chan MC, Lee N, Chan PK, To KF, Wong RY, Ho WS, Ngai KL, Sung JJ: Seasonal influenza A virus in feces of hospitalized adults. Emerg Infect Dis 2011,17(11):2038-2042.PubMedPubMedCentralCrossRef
12.
go back to reference Yoo SJ, Moon SJ, Kuak EY, Yoo HM, Kim CK, Chey MJ, Shin BM: Frequent detection of pandemic (H1N1) 2009 virus in stools of hospitalized patients. J Clin Microbiol 2010,48(6):2314-2315. 10.1128/JCM.00325-10PubMedPubMedCentralCrossRef Yoo SJ, Moon SJ, Kuak EY, Yoo HM, Kim CK, Chey MJ, Shin BM: Frequent detection of pandemic (H1N1) 2009 virus in stools of hospitalized patients. J Clin Microbiol 2010,48(6):2314-2315. 10.1128/JCM.00325-10PubMedPubMedCentralCrossRef
13.
go back to reference Buchy P, Mardy S, Vong S, Toyoda T, Aubin JT, Miller M, Touch S, Sovann L, Dufourcq JB, Richner B, et al.: Influenza A/H5N1 virus infection in humans in Cambodia. J Clin Virol 2007,39(3):164-168. 10.1016/j.jcv.2007.04.010PubMedCrossRef Buchy P, Mardy S, Vong S, Toyoda T, Aubin JT, Miller M, Touch S, Sovann L, Dufourcq JB, Richner B, et al.: Influenza A/H5N1 virus infection in humans in Cambodia. J Clin Virol 2007,39(3):164-168. 10.1016/j.jcv.2007.04.010PubMedCrossRef
14.
go back to reference Uiprasertkul M, Puthavathana P, Sangsiriwut K, Pooruk P, Srisook K, Peiris M, Nicholls JM, Chokephaibulkit K, Vanprapar N, Auewarakul P: Influenza A H5N1 replication sites in humans. Emerg Infect Dis 2005,11(7):1036-1041. 10.3201/eid1107.041313PubMedPubMedCentralCrossRef Uiprasertkul M, Puthavathana P, Sangsiriwut K, Pooruk P, Srisook K, Peiris M, Nicholls JM, Chokephaibulkit K, Vanprapar N, Auewarakul P: Influenza A H5N1 replication sites in humans. Emerg Infect Dis 2005,11(7):1036-1041. 10.3201/eid1107.041313PubMedPubMedCentralCrossRef
15.
go back to reference Zhang Z, Zhang J, Huang K, Li KS, Yuen KY, Guan Y, Chen H, Ng WF: Systemic infection of avian influenza A virus H5N1 subtype in humans. Hum Pathol 2009,40(5):735-739. 10.1016/j.humpath.2008.08.015PubMedCrossRef Zhang Z, Zhang J, Huang K, Li KS, Yuen KY, Guan Y, Chen H, Ng WF: Systemic infection of avian influenza A virus H5N1 subtype in humans. Hum Pathol 2009,40(5):735-739. 10.1016/j.humpath.2008.08.015PubMedCrossRef
16.
go back to reference von Linstow ML, Eugen-Olsen J, Koch A, Winther TN, Westh H, Hogh B: Excretion patterns of human metapneumovirus and respiratory syncytial virus among young children. Eur J Med Res 2006,11(8):329-335.PubMed von Linstow ML, Eugen-Olsen J, Koch A, Winther TN, Westh H, Hogh B: Excretion patterns of human metapneumovirus and respiratory syncytial virus among young children. Eur J Med Res 2006,11(8):329-335.PubMed
17.
go back to reference Hung IF, Cheng VC, Wu AK, Tang BS, Chan KH, Chu CM, Wong MM, Hui WT, Poon LL, Tse DM, et al.: Viral loads in clinical specimens and SARS manifestations. Emerg Infect Dis 2004,10(9):1550-1557. 10.3201/eid1009.040058PubMedPubMedCentralCrossRef Hung IF, Cheng VC, Wu AK, Tang BS, Chan KH, Chu CM, Wong MM, Hui WT, Poon LL, Tse DM, et al.: Viral loads in clinical specimens and SARS manifestations. Emerg Infect Dis 2004,10(9):1550-1557. 10.3201/eid1009.040058PubMedPubMedCentralCrossRef
18.
go back to reference 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(9):e641-e645. 10.1016/j.ijid.2011.05.008PubMedCrossRef 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(9):e641-e645. 10.1016/j.ijid.2011.05.008PubMedCrossRef
19.
go back to reference Chow BD, Ou Z, Esper FP: Newly recognized bocaviruses (HBoV, HBoV2) in children and adults with gastrointestinal illness in the United States. J Clin Virol 2010,47(2):143-147. 10.1016/j.jcv.2009.11.030PubMedCrossRef Chow BD, Ou Z, Esper FP: Newly recognized bocaviruses (HBoV, HBoV2) in children and adults with gastrointestinal illness in the United States. J Clin Virol 2010,47(2):143-147. 10.1016/j.jcv.2009.11.030PubMedCrossRef
20.
go back to reference Hayase Y, Tobita K, Sato H: Detection of type B influenza virus genes from biopsied gastric mucosa. J Gastroenterol 2002,37(2):101-105. 10.1007/s005350200003PubMedCrossRef Hayase Y, Tobita K, Sato H: Detection of type B influenza virus genes from biopsied gastric mucosa. J Gastroenterol 2002,37(2):101-105. 10.1007/s005350200003PubMedCrossRef
21.
go back to reference Kaji M, Watanabe A, Aizawa H: Differences in clinical features between influenza A H1N1, A H3N2, and B in adult patients. Respirology 2003,8(2):231-233. 10.1046/j.1440-1843.2003.00457.xPubMedCrossRef Kaji M, Watanabe A, Aizawa H: Differences in clinical features between influenza A H1N1, A H3N2, and B in adult patients. Respirology 2003,8(2):231-233. 10.1046/j.1440-1843.2003.00457.xPubMedCrossRef
22.
go back to reference To KK, Chan KH, Li IW, Tsang TY, Tse H, Chan JF, Hung IF, Lai ST, Leung CW, Kwan YW, et al.: Viral load in patients infected with pandemic H1N1 2009 influenza A virus. J Med Virol 2010,82(1):1-7. 10.1002/jmv.21664PubMedCrossRef To KK, Chan KH, Li IW, Tsang TY, Tse H, Chan JF, Hung IF, Lai ST, Leung CW, Kwan YW, et al.: Viral load in patients infected with pandemic H1N1 2009 influenza A virus. J Med Virol 2010,82(1):1-7. 10.1002/jmv.21664PubMedCrossRef
23.
go back to reference Brandt CD, Kim HW, Rodriguez WJ, Arrobio JO, Jeffries BC, Parrott RH: Simultaneous infections with different enteric and respiratory tract viruses. J Clin Microbiol 1986,23(1):177-179.PubMedPubMedCentral Brandt CD, Kim HW, Rodriguez WJ, Arrobio JO, Jeffries BC, Parrott RH: Simultaneous infections with different enteric and respiratory tract viruses. J Clin Microbiol 1986,23(1):177-179.PubMedPubMedCentral
24.
go back to reference Chan MC, Lee N, Wong RY, Ho WS, Sung JJ: A 75-year-old woman with seasonal influenza A (H3N2) virus infection and diarrhea. J Clin Virol 2010,48(4):231-233. 10.1016/j.jcv.2010.02.017PubMedCrossRef Chan MC, Lee N, Wong RY, Ho WS, Sung JJ: A 75-year-old woman with seasonal influenza A (H3N2) virus infection and diarrhea. J Clin Virol 2010,48(4):231-233. 10.1016/j.jcv.2010.02.017PubMedCrossRef
25.
go back to reference Shu Y, Li CK, Li Z, Gao R, Liang Q, Zhang Y, Dong L, Zhou J, Dong J, Wang D, et al.: Avian influenza A(H5N1) viruses can directly infect and replicate in human gut tissues. J Infect Dis 2010,201(8):1173-1177. 10.1086/651457PubMedCrossRef Shu Y, Li CK, Li Z, Gao R, Liang Q, Zhang Y, Dong L, Zhou J, Dong J, Wang D, et al.: Avian influenza A(H5N1) viruses can directly infect and replicate in human gut tissues. J Infect Dis 2010,201(8):1173-1177. 10.1086/651457PubMedCrossRef
26.
go back to reference Zeng H, Pappas C, Katz JM, Tumpey TM: The 2009 pandemic H1N1 and triple-reassortant swine H1N1 influenza viruses replicate efficiently but elicit an attenuated inflammatory response in polarized human bronchial epithelial cells. J Virol 2011,85(2):686-696. 10.1128/JVI.01568-10PubMedPubMedCentralCrossRef Zeng H, Pappas C, Katz JM, Tumpey TM: The 2009 pandemic H1N1 and triple-reassortant swine H1N1 influenza viruses replicate efficiently but elicit an attenuated inflammatory response in polarized human bronchial epithelial cells. J Virol 2011,85(2):686-696. 10.1128/JVI.01568-10PubMedPubMedCentralCrossRef
27.
go back to reference Zhirnov OP, Vorobjeva IV, Saphonova OA, Malyshev NA, Ovcharenko AV, Klenk HD: Specific biochemical features of replication of clinical influenza viruses in human intestinal cell culture. Biochemistry (Mosc) 2007,72(4):398-408. 10.1134/S0006297907040062CrossRef Zhirnov OP, Vorobjeva IV, Saphonova OA, Malyshev NA, Ovcharenko AV, Klenk HD: Specific biochemical features of replication of clinical influenza viruses in human intestinal cell culture. Biochemistry (Mosc) 2007,72(4):398-408. 10.1134/S0006297907040062CrossRef
28.
go back to reference Qu B, Li X, Gao W, Sun W, Jin Y, Cardona CJ, Xing Z: Human intestinal epithelial cells are susceptible to influenza virus subtype H9N2. Virus Res 2012,163(1):151-159. 10.1016/j.virusres.2011.09.007PubMedCrossRef Qu B, Li X, Gao W, Sun W, Jin Y, Cardona CJ, Xing Z: Human intestinal epithelial cells are susceptible to influenza virus subtype H9N2. Virus Res 2012,163(1):151-159. 10.1016/j.virusres.2011.09.007PubMedCrossRef
29.
go back to reference Valleron AJ, Bouvet E, Garnerin P, Menares J, Heard I, Letrait S, Lefaucheux J: A computer network for the surveillance of communicable diseases: the French experiment. Am J Public Health 1986,76(11):1289-1292. 10.2105/AJPH.76.11.1289PubMedPubMedCentralCrossRef Valleron AJ, Bouvet E, Garnerin P, Menares J, Heard I, Letrait S, Lefaucheux J: A computer network for the surveillance of communicable diseases: the French experiment. Am J Public Health 1986,76(11):1289-1292. 10.2105/AJPH.76.11.1289PubMedPubMedCentralCrossRef
30.
go back to reference Barber RD, Harmer DW, Coleman RA, Clark BJ: GAPDH as a housekeeping gene: analysis of GAPDH mRNA expression in a panel of 72 human tissues. Physiol Genomics 2005,21(3):389-395. 10.1152/physiolgenomics.00025.2005PubMedCrossRef Barber RD, Harmer DW, Coleman RA, Clark BJ: GAPDH as a housekeeping gene: analysis of GAPDH mRNA expression in a panel of 72 human tissues. Physiol Genomics 2005,21(3):389-395. 10.1152/physiolgenomics.00025.2005PubMedCrossRef
31.
go back to reference Selvaraju SB, Selvarangan R: Evaluation of three influenza A and B real-time reverse transcription-PCR assays and a new 2009 H1N1 assay for detection of influenza viruses. J Clin Microbiol 2010,48(11):3870-3875. 10.1128/JCM.02464-09PubMedPubMedCentralCrossRef Selvaraju SB, Selvarangan R: Evaluation of three influenza A and B real-time reverse transcription-PCR assays and a new 2009 H1N1 assay for detection of influenza viruses. J Clin Microbiol 2010,48(11):3870-3875. 10.1128/JCM.02464-09PubMedPubMedCentralCrossRef
32.
go back to reference Nakauchi M, Yasui Y, Miyoshi T, Minagawa H, Tanaka T, Tashiro M, Kageyama T: One-step real-time reverse transcription-PCR assays for detecting and subtyping pandemic influenza A/H1N1 2009, seasonal influenza A/H1N1, and seasonal influenza A/H3N2 viruses. J Virol Methods 2011,171(1):156-162. 10.1016/j.jviromet.2010.10.018PubMedCrossRef Nakauchi M, Yasui Y, Miyoshi T, Minagawa H, Tanaka T, Tashiro M, Kageyama T: One-step real-time reverse transcription-PCR assays for detecting and subtyping pandemic influenza A/H1N1 2009, seasonal influenza A/H1N1, and seasonal influenza A/H3N2 viruses. J Virol Methods 2011,171(1):156-162. 10.1016/j.jviromet.2010.10.018PubMedCrossRef
33.
go back to reference Duchamp MB, Casalegno JS, Gillet Y, Frobert E, Bernard E, Escuret V, Billaud G, Valette M, Javouhey E, Lina B, et al.: Pandemic A(H1N1)2009 influenza virus detection by real time RT-PCR: is viral quantification useful? Clin Microbiol Infect 2010,16(4):317-321. 10.1111/j.1469-0691.2010.03169.xPubMedCrossRef Duchamp MB, Casalegno JS, Gillet Y, Frobert E, Bernard E, Escuret V, Billaud G, Valette M, Javouhey E, Lina B, et al.: Pandemic A(H1N1)2009 influenza virus detection by real time RT-PCR: is viral quantification useful? Clin Microbiol Infect 2010,16(4):317-321. 10.1111/j.1469-0691.2010.03169.xPubMedCrossRef
34.
go back to reference Higgins RR, Beniprashad M, Cardona M, Masney S, Low DE, Gubbay JB: Evaluation and Verification of the Seeplex(R) Diarrhea-V ACE Assay for the Simultaneous Detection of Adenovirus, Rotavirus and Norovirus Genogroups I and II in Clinical Stool Specimens. J Clin Microbiol 2011,49(9):3154-3162. 10.1128/JCM.00599-11PubMedPubMedCentralCrossRef Higgins RR, Beniprashad M, Cardona M, Masney S, Low DE, Gubbay JB: Evaluation and Verification of the Seeplex(R) Diarrhea-V ACE Assay for the Simultaneous Detection of Adenovirus, Rotavirus and Norovirus Genogroups I and II in Clinical Stool Specimens. J Clin Microbiol 2011,49(9):3154-3162. 10.1128/JCM.00599-11PubMedPubMedCentralCrossRef
Metadata
Title
Simultaneous investigation of influenza and enteric viruses in the stools of adult patients consulting in general practice for acute diarrhea
Authors
Christophe Arena
Jean Pierre Amoros
Véronique Vaillant
Katia Balay
Roxane Chikhi-Brachet
Laurent Varesi
Jean Arrighi
Thierry Blanchon
Fabrice Carrat
Thomas Hanslik
Alessandra Falchi
Publication date
01-12-2012
Publisher
BioMed Central
Published in
Virology Journal / Issue 1/2012
Electronic ISSN: 1743-422X
DOI
https://doi.org/10.1186/1743-422X-9-116

Other articles of this Issue 1/2012

Virology Journal 1/2012 Go to the issue
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.