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Published in: EJNMMI Research 1/2017

Open Access 01-12-2017 | Original research

Gut microbiota and physiologic bowel 18F-FDG uptake

Authors: Ji Yeon Kang, Han-Na Kim, Yoosoo Chang, Yeojun Yun, Seungho Ryu, Hocheol Shin, Hyung-Lae Kim

Published in: EJNMMI Research | Issue 1/2017

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Abstract

Background

We investigated the association between physiologic bowel FDG uptake and gut microbiota. FDG uptake in the normal large and small intestine is widely variable both in distribution and intensity. The etiology of physiologic bowel 18F-FDG activity remains unknown.

Results

We included 63 healthy male subjects. After overnight fasting, blood samples and 18F-FDG PET/CT scans were taken. Fecal samples were collected, and gut microbiota were analyzed by 16S rRNA gene-pyrosequencing. The physiologic bowel FDG uptake was classified into three groups by visual assessment and measured using the maximum and mean standardized uptake value. We used the total bowel to liver uptake ratio (TBRmax and TBRmean). There was no significant difference in age, BMI, or lipid profiles between groups. To identify specific microbial taxa associated with the bowel FDG uptake while accounting for age and BMI, we performed a generalized linear model. At the genus level, the group with focal or intense FDG uptake in the intestine was associated with low abundance of unclassified Clostridiales. The group with intestinal FDG uptake lower than the liver was associated with high abundance of Klebsiella. TBRmax and TBRmean were negatively associated with abundance of unclassified Enterobacteriaceae.

Conclusion

We cautiously speculate that physiologic bowel FDG activity might be caused by an increase in intestinal permeability and may reflect an impaired barrier function in the intestine.
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Literature
1.
go back to reference Kim S, Chung JK, Kim BT, Kim SJ, Jeong JM, Lee DS, et al. Relationship between gastrointestinal F-18-fluorodeoxyglucose accumulation and gastrointestinal symptoms in whole-body PET. Clin Positron Imaging. 1999;2:273–9.CrossRefPubMed Kim S, Chung JK, Kim BT, Kim SJ, Jeong JM, Lee DS, et al. Relationship between gastrointestinal F-18-fluorodeoxyglucose accumulation and gastrointestinal symptoms in whole-body PET. Clin Positron Imaging. 1999;2:273–9.CrossRefPubMed
2.
go back to reference Soyka JD, Strobel K, Veit-Haibach P, Schaefer NG, Schmid DT, Tschopp A, et al. Influence of bowel preparation before 18F-FDG PET/CT on physiologic 18F-FDG activity in the intestine. J Nucl Med. 2010;51:507–10.CrossRefPubMed Soyka JD, Strobel K, Veit-Haibach P, Schaefer NG, Schmid DT, Tschopp A, et al. Influence of bowel preparation before 18F-FDG PET/CT on physiologic 18F-FDG activity in the intestine. J Nucl Med. 2010;51:507–10.CrossRefPubMed
3.
go back to reference Toriihara A, Yoshida K, Umehara I, Shibuya H. Normal variants of bowel FDG uptake in dual-time-point PET/CT imaging. Ann Nucl Med. 2011;25:173–8.CrossRefPubMed Toriihara A, Yoshida K, Umehara I, Shibuya H. Normal variants of bowel FDG uptake in dual-time-point PET/CT imaging. Ann Nucl Med. 2011;25:173–8.CrossRefPubMed
4.
go back to reference Franquet E, Palmer MR, Gifford AE, Selen DJ, Chen YC, Sedora-Roman N, et al. Rifaximin suppresses background intestinal 18F-FDG uptake on PET/CT scans. Nucl Med Commun. 2014;35:1026–31.CrossRefPubMed Franquet E, Palmer MR, Gifford AE, Selen DJ, Chen YC, Sedora-Roman N, et al. Rifaximin suppresses background intestinal 18F-FDG uptake on PET/CT scans. Nucl Med Commun. 2014;35:1026–31.CrossRefPubMed
5.
go back to reference Yoon HJ, Kim HN, Yun Y, Kim Y, Ha AN, Kim HL, et al. Background intestinal 18F-FDG uptake is related to serum lipid profile and obesity in breast cancer patients. PLoS One. 2015;10:e0141473.CrossRefPubMedPubMedCentral Yoon HJ, Kim HN, Yun Y, Kim Y, Ha AN, Kim HL, et al. Background intestinal 18F-FDG uptake is related to serum lipid profile and obesity in breast cancer patients. PLoS One. 2015;10:e0141473.CrossRefPubMedPubMedCentral
6.
go back to reference Lee JW, Oh JK, Chung YA, Na SJ, Hyun SH, Hong IK, et al. Prognostic significance of 18F-FDG uptake in Hepatocellular carcinoma treated with Transarterial Chemoembolization or concurrent Chemoradiotherapy: a multicenter retrospective cohort study. J Nucl Med. 2016;57:509–16.CrossRefPubMed Lee JW, Oh JK, Chung YA, Na SJ, Hyun SH, Hong IK, et al. Prognostic significance of 18F-FDG uptake in Hepatocellular carcinoma treated with Transarterial Chemoembolization or concurrent Chemoradiotherapy: a multicenter retrospective cohort study. J Nucl Med. 2016;57:509–16.CrossRefPubMed
7.
go back to reference Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4516–22.CrossRefPubMed Caporaso JG, Lauber CL, Walters WA, Berg-Lyons D, Lozupone CA, Turnbaugh PJ, et al. Global patterns of 16S rRNA diversity at a depth of millions of sequences per sample. Proc Natl Acad Sci U S A. 2011;108(Suppl 1):4516–22.CrossRefPubMed
8.
go back to reference Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.CrossRefPubMedPubMedCentral Kozich JJ, Westcott SL, Baxter NT, Highlander SK, Schloss PD. Development of a dual-index sequencing strategy and curation pipeline for analyzing amplicon sequence data on the MiSeq Illumina sequencing platform. Appl Environ Microbiol. 2013;79:5112–20.CrossRefPubMedPubMedCentral
9.
go back to reference Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome. 2014;2:6.CrossRefPubMedPubMedCentral Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, et al. An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome. 2014;2:6.CrossRefPubMedPubMedCentral
10.
go back to reference Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.CrossRefPubMedPubMedCentral Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, et al. QIIME allows analysis of high-throughput community sequencing data. Nat Methods. 2010;7:335–6.CrossRefPubMedPubMedCentral
11.
go back to reference DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–72.CrossRefPubMedPubMedCentral DeSantis TZ, Hugenholtz P, Larsen N, Rojas M, Brodie EL, Keller K, et al. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol. 2006;72:5069–72.CrossRefPubMedPubMedCentral
12.
go back to reference Navas-Molina JA, Peralta-Sanchez JM, Gonzalez A, McMurdie PJ, Vazquez-Baeza Y, Xu Z, et al. Advancing our understanding of the human microbiome using QIIME. Methods Enzymol. 2013;531:371–444.CrossRefPubMedPubMedCentral Navas-Molina JA, Peralta-Sanchez JM, Gonzalez A, McMurdie PJ, Vazquez-Baeza Y, Xu Z, et al. Advancing our understanding of the human microbiome using QIIME. Methods Enzymol. 2013;531:371–444.CrossRefPubMedPubMedCentral
13.
15.
go back to reference Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York; 2009. Wickham H. ggplot2: Elegant Graphics for Data Analysis. Springer-Verlag New York; 2009.
17.
go back to reference Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312:1355–9.CrossRefPubMedPubMedCentral Gill SR, Pop M, Deboy RT, Eckburg PB, Turnbaugh PJ, Samuel BS, et al. Metagenomic analysis of the human distal gut microbiome. Science. 2006;312:1355–9.CrossRefPubMedPubMedCentral
18.
go back to reference Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–8.CrossRefPubMedPubMedCentral Eckburg PB, Bik EM, Bernstein CN, Purdom E, Dethlefsen L, Sargent M, et al. Diversity of the human intestinal microbial flora. Science. 2005;308:1635–8.CrossRefPubMedPubMedCentral
19.
go back to reference Verdam FJ, Fuentes S, de Jonge C, Zoetendal EG, Erbil R, Greve JW, et al. Human intestinal microbiota composition is associated with local and systemic inflammation in obesity. Obesity (Silver Spring). 2013;21:E607–15.CrossRef Verdam FJ, Fuentes S, de Jonge C, Zoetendal EG, Erbil R, Greve JW, et al. Human intestinal microbiota composition is associated with local and systemic inflammation in obesity. Obesity (Silver Spring). 2013;21:E607–15.CrossRef
20.
go back to reference Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57:1470–81.CrossRefPubMed Cani PD, Bibiloni R, Knauf C, Waget A, Neyrinck AM, Delzenne NM, et al. Changes in gut microbiota control metabolic endotoxemia-induced inflammation in high-fat diet-induced obesity and diabetes in mice. Diabetes. 2008;57:1470–81.CrossRefPubMed
21.
go back to reference Moreira AP, Texeira TF, Ferreira AB, Peluzio Mdo C, Alfenas RC. Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. Br J Nutr. 2012;108:801–9.CrossRefPubMed Moreira AP, Texeira TF, Ferreira AB, Peluzio Mdo C, Alfenas RC. Influence of a high-fat diet on gut microbiota, intestinal permeability and metabolic endotoxaemia. Br J Nutr. 2012;108:801–9.CrossRefPubMed
22.
go back to reference Teixeira TF, Collado MC, Ferreira CL, Bressan J, Peluzio MC. Potential mechanisms for the emerging link between obesity and increased intestinal permeability. Nutr Res. 2012;32:637–47.CrossRefPubMed Teixeira TF, Collado MC, Ferreira CL, Bressan J, Peluzio MC. Potential mechanisms for the emerging link between obesity and increased intestinal permeability. Nutr Res. 2012;32:637–47.CrossRefPubMed
23.
24.
go back to reference Simrén M, Barbara G, Flint HJ, Spiegel BMR, Spiller RC, Vanner S, et al. Intestinal microbiota in functional bowel disorders: a Rome foundation report. Gut. 2012;62:159–76.CrossRefPubMedPubMedCentral Simrén M, Barbara G, Flint HJ, Spiegel BMR, Spiller RC, Vanner S, et al. Intestinal microbiota in functional bowel disorders: a Rome foundation report. Gut. 2012;62:159–76.CrossRefPubMedPubMedCentral
26.
go back to reference Xu D, Gao J, Gillilland M 3rd, Wu X, Song I, Kao JY, et al. Rifaximin alters intestinal bacteria and prevents stress-induced gut inflammation and visceral hyperalgesia in rats. Gastroenterology. 2014;146:484–96. e4CrossRefPubMed Xu D, Gao J, Gillilland M 3rd, Wu X, Song I, Kao JY, et al. Rifaximin alters intestinal bacteria and prevents stress-induced gut inflammation and visceral hyperalgesia in rats. Gastroenterology. 2014;146:484–96. e4CrossRefPubMed
28.
go back to reference Levine GM, Shiau YF, Deren JA. Characteristics of intestinal glucose secretion in normal and diabetic rats. Am J Phys. 1982;242:G455–9. Levine GM, Shiau YF, Deren JA. Characteristics of intestinal glucose secretion in normal and diabetic rats. Am J Phys. 1982;242:G455–9.
29.
go back to reference Bardhan KD, Cullis J, Williams NR, Arasaradnam RP, Wilson AJ. Quantification of 18FDG in the normal Colon-a first step in investigating whether its presence is a marker of a physiological process. PLoS One. 2016;11:e0147838.CrossRefPubMedPubMedCentral Bardhan KD, Cullis J, Williams NR, Arasaradnam RP, Wilson AJ. Quantification of 18FDG in the normal Colon-a first step in investigating whether its presence is a marker of a physiological process. PLoS One. 2016;11:e0147838.CrossRefPubMedPubMedCentral
30.
go back to reference Wang K, Chen YC, Palmer MR, Tal I, Ahmed A, Moss AC, et al. Focal physiologic fluorodeoxyglucose activity in the gastrointestinal tract is located within the colonic lumen. Nucl Med Commun. 2012;33:641–7.CrossRefPubMed Wang K, Chen YC, Palmer MR, Tal I, Ahmed A, Moss AC, et al. Focal physiologic fluorodeoxyglucose activity in the gastrointestinal tract is located within the colonic lumen. Nucl Med Commun. 2012;33:641–7.CrossRefPubMed
31.
go back to reference Andoh A, Nishida A, Takahashi K, Inatomi O, Imaeda H, Bamba S, et al. Comparison of the gut microbial community between obese and lean peoples using 16S gene sequencing in a Japanese population. J Clin Biochem Nutr. 2016;59:65–70.CrossRefPubMedPubMedCentral Andoh A, Nishida A, Takahashi K, Inatomi O, Imaeda H, Bamba S, et al. Comparison of the gut microbial community between obese and lean peoples using 16S gene sequencing in a Japanese population. J Clin Biochem Nutr. 2016;59:65–70.CrossRefPubMedPubMedCentral
32.
go back to reference McCoy AN, Araujo-Perez F, Azcarate-Peril A, Yeh JJ, Sandler RS, Keku TO. Fusobacterium is associated with colorectal adenomas. PLoS One. 2013;8:e53653.CrossRefPubMedPubMedCentral McCoy AN, Araujo-Perez F, Azcarate-Peril A, Yeh JJ, Sandler RS, Keku TO. Fusobacterium is associated with colorectal adenomas. PLoS One. 2013;8:e53653.CrossRefPubMedPubMedCentral
33.
go back to reference Bashir A, Miskeen AY, Hazari YM, Asrafuzzaman S, Fazili KM. Fusobacterium nucleatum, inflammation, and immunity: the fire within human gut. Tumour Biol. 2016;37:2805–10.CrossRefPubMed Bashir A, Miskeen AY, Hazari YM, Asrafuzzaman S, Fazili KM. Fusobacterium nucleatum, inflammation, and immunity: the fire within human gut. Tumour Biol. 2016;37:2805–10.CrossRefPubMed
34.
go back to reference Lee KE, Moon CM, Yoon HJ, Kim BS, Chang JY, Son HM, et al. Background colonic 18F-Fluoro-2-Deoxy-D-glucose uptake on positron emission tomography is associated with the presence of colorectal adenoma. PLoS One. 2016;11:e0160886.CrossRefPubMedPubMedCentral Lee KE, Moon CM, Yoon HJ, Kim BS, Chang JY, Son HM, et al. Background colonic 18F-Fluoro-2-Deoxy-D-glucose uptake on positron emission tomography is associated with the presence of colorectal adenoma. PLoS One. 2016;11:e0160886.CrossRefPubMedPubMedCentral
35.
go back to reference Lee S, Sung J, Lee J, Ko G. Comparison of the gut microbiotas of healthy adult twins living in South Korea and the United States. Appl Environ Microbiol. 2011;77:7433–7.CrossRefPubMedPubMedCentral Lee S, Sung J, Lee J, Ko G. Comparison of the gut microbiotas of healthy adult twins living in South Korea and the United States. Appl Environ Microbiol. 2011;77:7433–7.CrossRefPubMedPubMedCentral
Metadata
Title
Gut microbiota and physiologic bowel 18F-FDG uptake
Authors
Ji Yeon Kang
Han-Na Kim
Yoosoo Chang
Yeojun Yun
Seungho Ryu
Hocheol Shin
Hyung-Lae Kim
Publication date
01-12-2017
Publisher
Springer Berlin Heidelberg
Published in
EJNMMI Research / Issue 1/2017
Electronic ISSN: 2191-219X
DOI
https://doi.org/10.1186/s13550-017-0318-8

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