ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
GBD 2016 Diarrhoeal Disease Collaborators , 2018. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of diarrhoea in 195 countries: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect Dis 18: 1211–1228.
-
2.
Newman KL , Moe CL , Kirby AE , Flanders WD , Parkos CA , Leon JS , 2016. Norovirus in symptomatic and asymptomatic individuals: cytokines and viral shedding. Clin Exp Immunol 184: 347–357.
-
3.
Jeong AY et al., 2013. Occurrence of norovirus infections in asymptomatic food handlers in South Korea. J Clin Microbiol 51: 598–600.
-
4.
Okitsu S et al., 2020. Molecular detection of enteric viruses in the stool samples of children without diarrhea in Bangladesh. Infect Genet Evol 77: 104055.
-
5.
Horwood PF et al., 2017. A high burden of asymptomatic gastrointestinal infections in traditional communities in Papua New Guinea. Am J Trop Med Hyg 97: 1872–1875.
-
6.
Kobayashi D , Yokota K , Yamagata-Uyama S , Saito M , 2022. Factors associated with the detection of norovirus among asymptomatic adults. Clin Microbiol Infect 28: 299.e1–299.e8.
-
7.
Phillips G , Tam CC , Rodrigues LC , Lopman B , 2010. Prevalence and characteristics of asymptomatic norovirus infection in the community in England. Epidemiol Infect 138: 1454–1458.
-
8.
Phillips G , Lopman B , Rodrigues LC , Tam CC , 2010. Asymptomatic rotavirus infections in England: prevalence, characteristics, and risk factors. Am J Epidemiol 171: 1023–1030.
-
9.
Zheng D , Liwinski T , Elinav E , 2020. Interaction between microbiota and immunity in health and disease. Cell Res 30: 492–506.
-
10.
Mori K et al., 2018. Comparison between patients with norovirus-related gastroenteritis and asymptomatic carriers with respect to distribution of antibody-complexed viral particles and intestinal flora. J Med Virol 90: 1882–1887.
-
11.
Patin NV , Peña-Gonzalez A , Hatt JK , Moe C , Kirby A , Konstantinidis KT , 2020. The role of the gut microbiome in resisting norovirus infection as revealed by a human challenge study. mBio 11: e02634-20.
-
12.
Zhang L , Dong D , Jiang C , Li Z , Wang X , Peng Y , 2015. Insight into alteration of gut microbiota in Clostridium difficile infection and asymptomatic C. difficile colonization. Anaerobe 34: 1–7.
-
13.
Kibe M , Tomita S , Umezaki M , 2022. Divergence in nutritional intake and physical activity patterns among households in a village of ethnic minorities in northern Laos at the initial stage of health transition. Hum Ecol 50: 287–305.
-
14.
Kibe M , Mizuno Y , Masuoka H , Kosaka S , Natsuhara K , Hirayama K , Inthavong N , Kounnavong S , Tomita S , Umezaki M , 2023. Transition to a market economy and chronic psychosocial stress in northern Laos: an exploratory study of urinary free cortisol in rural residents. Am J Hum Biol 36: e23976.
-
15.
Mizuno Y , Masuoka H , Kibe M , Kosaka S , Natsuhara K , Hirayama K , Inthavong N , Kounnavong S , Tomita S , Umezaki M , 2022. Impact of modernization on urinary concentrations of arsenic, cadmium, lead, and selenium in rural residents of northern Laos. Am J Hum Biol 34: e23685.
-
16.
Mizuno Y et al., 2023. Determinants of oxidative stress among indigenous populations in northern Laos: trace element exposures and dietary patterns. Sci Total Environ 868: 161516.
-
17.
Yan H , Yagyu F , Okitsu S , Nishio O , Ushijima H , 2003. Detection of norovirus (GI, GII), sapovirus and astrovirus in fecal samples using reverse transcription single-round multiplex PCR. J Virol Methods 114: 37–44.
-
18.
Thongprachum A , Khamrin P , Pham NT , Takanashi S , Okitsu S , Shimizu H , Maneekarn N , Hayakawa S , Ushijima H , 2017. Multiplex RT-PCR for rapid detection of viruses commonly causing diarrhea in pediatric patients. J Med Virol 89: 818–824.
-
19.
Kumar S , Stecher G , Li M , Knyaz C , Tamura K , 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35: 1547–1549.
-
20.
Stecher G , Tamura K , Kumar S , 2020. Molecular evolutionary genetics analysis (MEGA) for macOS. Mol Biol Evol 37: 1237–1239.
-
21.
Saitou N , Nei M , 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
-
22.
Kimura M , 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111–120.
-
23.
Felsenstein J , 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.
-
24.
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: 4673–4680.
-
25.
Morita H , Kuwahara T , Ohshima K , Sasamoto H , Itoh K , Hattori M , Hayashi T , Takami H , 2007. An improved DNA isolation method for metagenomic analysis of the microbial flora of the human intestine. Microbes Environ 22: 214–222.
-
26.
Masuoka H , Suda W , Tomitsuka E , Shindo C , Takayasu L , Horwood P , Greenhill AR , Hattori M , Umezaki M , Hirayama K , 2020. The influences of low protein diet on the intestinal microbiota of mice. Sci Rep 10: 17077.
-
27.
Lee JE , Lee S , Sung J , Ko G , 2011. Analysis of human and animal fecal microbiota for microbial source tracking. ISME J 5: 362–365.
-
28.
Jonduo ME et al., 2020. Gut microbiota composition in obese and non-obese adult relatives from the highlands of Papua New Guinea. FEMS Microbiol Lett 367: fnaa161.
-
29.
Sato M , Suzuki Y , 2022. Alterations in intestinal microbiota in ultramarathon runners. Sci Rep 12: 6984.
-
30.
Good IJ , 1953. The population frequencies of species and the estimation of population parameters. Biometrika 40: 237–264.
-
31.
Singleton DR , Furlong MA , Rathbun SL , Whitman WB , 2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67: 4374–4376.
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32.
Lozupone C , Knight R , 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228–8235.
-
33.
Lynch JP 3rd , Kajon AE , 2016. Adenovirus: epidemiology, global spread of novel serotypes, and advances in treatment and prevention. Semin Respir Crit Care Med 37: 586–602.
-
34.
Amar CF , East CL , Gray J , Iturriza-Gomara M , Maclure EA , McLauchlin J , 2007. Detection by PCR of eight groups of enteric pathogens in 4,627 faecal samples: re-examination of the English case-control Infectious Intestinal Disease Study (1993–1996). Eur J Clin Microbiol Infect Dis 26: 311–323.
-
35.
Rouhani S et al., 2016. Norovirus infection and acquired immunity in 8 countries: results from the MAL-ED study. Clin Infect Dis 62: 1210–1217.
-
36.
Phillips G , Tam CC , Rodrigues LC , Lopman B , 2011. Risk factors for symptomatic and asymptomatic norovirus infection in the community. Epidemiol Infect 139: 1676–1686.
-
37.
Xiong L , Li Y , Li J , Yang J , Shang L , He X , Liu L , Luo Y , Xie X , 2021. Intestinal microbiota profiles in infants with acute gastroenteritis caused by rotavirus and norovirus infection: a prospective cohort study. Int J Infect Dis 111: 76–84.
-
38.
Almand EA , Moore MD , Jaykus LA , 2019. Characterization of human norovirus binding to gut-associated bacterial ligands. BMC Res Notes 12: 607.
-
39.
Jones MK et al., 2014. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346: 755–759.
-
40.
Santiso-Bellón C , Gozalbo-Rovira R , Buesa J , Rubio-Del-Campo A , Peña-Gil N , Navarro-Lleó N , Cárcamo-Calvo R , Yebra MJ , Monedero V , RodrÃguez-DÃaz J , 2022. Replication of human norovirus in mice after antibiotic-mediated intestinal bacteria depletion. Int J Mol Sci 23: 10643.
-
41.
Makki K , Deehan EC , Walter J , Bäckhed F , 2018. The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe 23: 705–715.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1776 | 1776 | 34 |
| Full Text Views | 153 | 153 | 14 |
| PDF Downloads | 122 | 122 | 18 |
Asymptomatic Enteric Virus Infections and Association with the Gut Microbiome in Rural Residents of Northern Laos
Sae Sekiya
Sae Sekiya
Department of Human Ecology, School of International Health, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan;
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Hiroaki Masuoka
Hiroaki Masuoka
Laboratory for Microbiome Science, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan;
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Yuki Mizuno
Yuki Mizuno
Department of Human Ecology, School of International Health, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan;
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Mihoko Kibe
Mihoko Kibe
Department of Human Ecology, School of International Health, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan;
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Satoko Kosaka
Satoko Kosaka
Department of Human Ecology, School of International Health, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan;
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Kazumi Natsuhara
Kazumi Natsuhara
Faculty of Nursing, Toho University, Tokyo, Japan;
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Kazuhiro Hirayama
Kazuhiro Hirayama
Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan;
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Nouhak Inthavong
Nouhak Inthavong
Ministry of Health, Lao Tropical and Public Health Institute, Vientiane, Laos;
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Sengchanh Kounnavong
Sengchanh Kounnavong
Ministry of Health, Lao Tropical and Public Health Institute, Vientiane, Laos;
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Shinsuke Tomita
Shinsuke Tomita
Graduate School of Environmental Studies, Nagoya University, Nagoya, Japan;
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Lena Takayasu
Lena Takayasu
Department of Human Ecology, School of International Health, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan;
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Wataru Suda
Wataru Suda
Laboratory for Microbiome Science, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan;
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Fumihiro Yagyu
Fumihiro Yagyu
Graduate School of International Development and Cooperation, Kibi International University, Hyogo, Japan
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Masahiro Umezaki
Masahiro Umezaki
Department of Human Ecology, School of International Health, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan;
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ABSTRACT.
Viral gastrointestinal infections are an important public health concern, and the occurrence of asymptomatic enteric virus infections makes it difficult to prevent and control their spread. This study aimed to determine the prevalence of and factors associated with asymptomatic enteric virus infection in adults in northern Laos. Fecal samples were collected from apparently healthy participants who did not report diarrhea or high fever at the time of the survey in northern Laos, and enteric viruses were detected using polymerase chain reaction (PCR) and reverse transcription (RT)-PCR. Individual characteristics, including the gut microbiome, were compared between asymptomatic carriers and noncarriers of each enteric virus. Of the participants (N = 255), 12 (4.7%) were positive for norovirus genogroup I (GI), 8 (3.1%) for human adenovirus, and 1 (0.4%) for norovirus GII; prevalence tended to be higher in less-modernized villages. Gut microbial diversity (evaluated by the number of operational taxonomic units) was higher in asymptomatic carriers of norovirus GI or human adenovirus than in their noncarriers. Gut microbiome compositions differed significantly between asymptomatic carriers and noncarriers of norovirus GI or human adenovirus (permutational analysis of variance, P <0.05). These findings imply an association between asymptomatic enteric virus infection and modernization and/or the gut microbiome in northern Laos.
- Supplemental Materials (PDF 795.91 KB)
Author Notes
Financial support: Financial support was provided by
Author’s addresses: Sae Sekiya, Yuki Mizuno, Mihoko Kibe, Satoko Kosaka, Lena Takayasu, and Masahiro Umezaki, Department of Human Ecology, School of International Health, Graduate School of Medicine, The University of Tokyo, Tokyo, Japan, E-mails: sekiya@humeco.m.u-tokyo.ac.jp, mizuno@humeco.m.u-tokyo.ac.jp, mihoko.k@humeco.m.u-tokyo.ac.jp, skosaka@nagasaki-u.ac.jp, lt425@cornell.edu, and umezaki@humeco.m.u-tokyo.ac.jp. Hiroaki Masuoka and Wataru Suda, Laboratory for Microbiome Science, RIKEN Center for Integrative Medical Sciences, Yokohama, Japan, E-mails: hiroaki.masuoka@riken.jp and wataru.suda@riken.jp. Kazumi Natsuhara, Faculty of Nursing, Toho University, Tokyo, Japan, E-mail: kazumi.natsuhara@med.toho-u.ac.jp. Kazuhiro Hirayama, Graduate School of Agricultural and Life Sciences, The University of Tokyo, Tokyo, Japan, E-mail: akazu@g.ecc.u-tokyo.ac.jp. Nouhak Inthavong and Sengchanh Kounnavong, Ministry of Health, Lao Tropical and Public Health Institute, Vientiane, Lao People’s Democratic Republic, E-mails: nouhak_25@yahoo.com and sengchanhkounnavong@hotmail.com. Shinsuke Tomita, Graduate School of Environmental Studies, Nagoya University, Nagoya, Japan, E-mail: tomishing@nagoya-u.jp. Fumihiro Yagyu, Graduate School of International Development and Cooperation, Kibi International University, Hyogo, Japan, E-mail: fyagyu@gmail.com.
ProCite
RefWorks
Reference Manager
BibTeX
Zotero
EndNote
-
1.
GBD 2016 Diarrhoeal Disease Collaborators , 2018. Estimates of the global, regional, and national morbidity, mortality, and aetiologies of diarrhoea in 195 countries: a systematic analysis for the Global Burden of Disease Study 2016. Lancet Infect Dis 18: 1211–1228.
-
2.
Newman KL , Moe CL , Kirby AE , Flanders WD , Parkos CA , Leon JS , 2016. Norovirus in symptomatic and asymptomatic individuals: cytokines and viral shedding. Clin Exp Immunol 184: 347–357.
-
3.
Jeong AY et al., 2013. Occurrence of norovirus infections in asymptomatic food handlers in South Korea. J Clin Microbiol 51: 598–600.
-
4.
Okitsu S et al., 2020. Molecular detection of enteric viruses in the stool samples of children without diarrhea in Bangladesh. Infect Genet Evol 77: 104055.
-
5.
Horwood PF et al., 2017. A high burden of asymptomatic gastrointestinal infections in traditional communities in Papua New Guinea. Am J Trop Med Hyg 97: 1872–1875.
-
6.
Kobayashi D , Yokota K , Yamagata-Uyama S , Saito M , 2022. Factors associated with the detection of norovirus among asymptomatic adults. Clin Microbiol Infect 28: 299.e1–299.e8.
-
7.
Phillips G , Tam CC , Rodrigues LC , Lopman B , 2010. Prevalence and characteristics of asymptomatic norovirus infection in the community in England. Epidemiol Infect 138: 1454–1458.
-
8.
Phillips G , Lopman B , Rodrigues LC , Tam CC , 2010. Asymptomatic rotavirus infections in England: prevalence, characteristics, and risk factors. Am J Epidemiol 171: 1023–1030.
-
9.
Zheng D , Liwinski T , Elinav E , 2020. Interaction between microbiota and immunity in health and disease. Cell Res 30: 492–506.
-
10.
Mori K et al., 2018. Comparison between patients with norovirus-related gastroenteritis and asymptomatic carriers with respect to distribution of antibody-complexed viral particles and intestinal flora. J Med Virol 90: 1882–1887.
-
11.
Patin NV , Peña-Gonzalez A , Hatt JK , Moe C , Kirby A , Konstantinidis KT , 2020. The role of the gut microbiome in resisting norovirus infection as revealed by a human challenge study. mBio 11: e02634-20.
-
12.
Zhang L , Dong D , Jiang C , Li Z , Wang X , Peng Y , 2015. Insight into alteration of gut microbiota in Clostridium difficile infection and asymptomatic C. difficile colonization. Anaerobe 34: 1–7.
-
13.
Kibe M , Tomita S , Umezaki M , 2022. Divergence in nutritional intake and physical activity patterns among households in a village of ethnic minorities in northern Laos at the initial stage of health transition. Hum Ecol 50: 287–305.
-
14.
Kibe M , Mizuno Y , Masuoka H , Kosaka S , Natsuhara K , Hirayama K , Inthavong N , Kounnavong S , Tomita S , Umezaki M , 2023. Transition to a market economy and chronic psychosocial stress in northern Laos: an exploratory study of urinary free cortisol in rural residents. Am J Hum Biol 36: e23976.
-
15.
Mizuno Y , Masuoka H , Kibe M , Kosaka S , Natsuhara K , Hirayama K , Inthavong N , Kounnavong S , Tomita S , Umezaki M , 2022. Impact of modernization on urinary concentrations of arsenic, cadmium, lead, and selenium in rural residents of northern Laos. Am J Hum Biol 34: e23685.
-
16.
Mizuno Y et al., 2023. Determinants of oxidative stress among indigenous populations in northern Laos: trace element exposures and dietary patterns. Sci Total Environ 868: 161516.
-
17.
Yan H , Yagyu F , Okitsu S , Nishio O , Ushijima H , 2003. Detection of norovirus (GI, GII), sapovirus and astrovirus in fecal samples using reverse transcription single-round multiplex PCR. J Virol Methods 114: 37–44.
-
18.
Thongprachum A , Khamrin P , Pham NT , Takanashi S , Okitsu S , Shimizu H , Maneekarn N , Hayakawa S , Ushijima H , 2017. Multiplex RT-PCR for rapid detection of viruses commonly causing diarrhea in pediatric patients. J Med Virol 89: 818–824.
-
19.
Kumar S , Stecher G , Li M , Knyaz C , Tamura K , 2018. MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35: 1547–1549.
-
20.
Stecher G , Tamura K , Kumar S , 2020. Molecular evolutionary genetics analysis (MEGA) for macOS. Mol Biol Evol 37: 1237–1239.
-
21.
Saitou N , Nei M , 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4: 406–425.
-
22.
Kimura M , 1980. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16: 111–120.
-
23.
Felsenstein J , 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783–791.
-
24.
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: 4673–4680.
-
25.
Morita H , Kuwahara T , Ohshima K , Sasamoto H , Itoh K , Hattori M , Hayashi T , Takami H , 2007. An improved DNA isolation method for metagenomic analysis of the microbial flora of the human intestine. Microbes Environ 22: 214–222.
-
26.
Masuoka H , Suda W , Tomitsuka E , Shindo C , Takayasu L , Horwood P , Greenhill AR , Hattori M , Umezaki M , Hirayama K , 2020. The influences of low protein diet on the intestinal microbiota of mice. Sci Rep 10: 17077.
-
27.
Lee JE , Lee S , Sung J , Ko G , 2011. Analysis of human and animal fecal microbiota for microbial source tracking. ISME J 5: 362–365.
-
28.
Jonduo ME et al., 2020. Gut microbiota composition in obese and non-obese adult relatives from the highlands of Papua New Guinea. FEMS Microbiol Lett 367: fnaa161.
-
29.
Sato M , Suzuki Y , 2022. Alterations in intestinal microbiota in ultramarathon runners. Sci Rep 12: 6984.
-
30.
Good IJ , 1953. The population frequencies of species and the estimation of population parameters. Biometrika 40: 237–264.
-
31.
Singleton DR , Furlong MA , Rathbun SL , Whitman WB , 2001. Quantitative comparisons of 16S rRNA gene sequence libraries from environmental samples. Appl Environ Microbiol 67: 4374–4376.
-
32.
Lozupone C , Knight R , 2005. UniFrac: a new phylogenetic method for comparing microbial communities. Appl Environ Microbiol 71: 8228–8235.
-
33.
Lynch JP 3rd , Kajon AE , 2016. Adenovirus: epidemiology, global spread of novel serotypes, and advances in treatment and prevention. Semin Respir Crit Care Med 37: 586–602.
-
34.
Amar CF , East CL , Gray J , Iturriza-Gomara M , Maclure EA , McLauchlin J , 2007. Detection by PCR of eight groups of enteric pathogens in 4,627 faecal samples: re-examination of the English case-control Infectious Intestinal Disease Study (1993–1996). Eur J Clin Microbiol Infect Dis 26: 311–323.
-
35.
Rouhani S et al., 2016. Norovirus infection and acquired immunity in 8 countries: results from the MAL-ED study. Clin Infect Dis 62: 1210–1217.
-
36.
Phillips G , Tam CC , Rodrigues LC , Lopman B , 2011. Risk factors for symptomatic and asymptomatic norovirus infection in the community. Epidemiol Infect 139: 1676–1686.
-
37.
Xiong L , Li Y , Li J , Yang J , Shang L , He X , Liu L , Luo Y , Xie X , 2021. Intestinal microbiota profiles in infants with acute gastroenteritis caused by rotavirus and norovirus infection: a prospective cohort study. Int J Infect Dis 111: 76–84.
-
38.
Almand EA , Moore MD , Jaykus LA , 2019. Characterization of human norovirus binding to gut-associated bacterial ligands. BMC Res Notes 12: 607.
-
39.
Jones MK et al., 2014. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 346: 755–759.
-
40.
Santiso-Bellón C , Gozalbo-Rovira R , Buesa J , Rubio-Del-Campo A , Peña-Gil N , Navarro-Lleó N , Cárcamo-Calvo R , Yebra MJ , Monedero V , RodrÃguez-DÃaz J , 2022. Replication of human norovirus in mice after antibiotic-mediated intestinal bacteria depletion. Int J Mol Sci 23: 10643.
-
41.
Makki K , Deehan EC , Walter J , Bäckhed F , 2018. The impact of dietary fiber on gut microbiota in host health and disease. Cell Host Microbe 23: 705–715.
| Past two years | Past Year | Past 30 Days | |
|---|---|---|---|
| Abstract Views | 1776 | 1776 | 34 |
| Full Text Views | 153 | 153 | 14 |
| PDF Downloads | 122 | 122 | 18 |