Administration of Bifidobacterium bifidum CGMCC 15068 modulates gut microbiota and metabolome in azoxymethane (AOM)/dextran sulphate sodium (DSS)-induced colitis-associated colon cancer (CAC) in mice.


Journal

Applied microbiology and biotechnology
ISSN: 1432-0614
Titre abrégé: Appl Microbiol Biotechnol
Pays: Germany
ID NLM: 8406612

Informations de publication

Date de publication:
Jul 2020
Historique:
received: 08 12 2019
accepted: 09 04 2020
revised: 31 03 2020
pubmed: 6 5 2020
medline: 27 1 2021
entrez: 6 5 2020
Statut: ppublish

Résumé

The gut microbiota plays an important role in colorectal cancer (CRC), and the use of probiotics might be a promising intervention method. The aim of our study was to investigate the beneficial effect of Bifidobacterium bifidum CGMCC 15068 on an azoxymethane (AOM)/dextran sulphate sodium (DSS)-induced colitis-associated CRC (CAC) mouse model. CAC was induced by an intra-peritoneal injection of AOM (10 mg/kg) and three 7-day cycles of 2% DSS in drinking water with a 14-day recovery period between two consecutive DSS administrations. B. bifidum CGMCC 15068 (3 × 10

Identifiants

pubmed: 32367312
doi: 10.1007/s00253-020-10621-z
pii: 10.1007/s00253-020-10621-z
doi:

Substances chimiques

Dextran Sulfate 9042-14-2
Azoxymethane MO0N1J0SEN

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Pagination

5915-5928

Subventions

Organisme : National Natural Science Foundation of China
ID : 81790631
Organisme : National Natural Science Foundation of China
ID : 81570512

Références

Abdelhamid AG, El-Masry SS, El-Dougdoug NK (2019) Probiotic Lactobacillus and Bifidobacterium strains possess safety characteristics, antiviral activities and host adherence factors revealed by genome mining. EPMA J 10:337–350. https://doi.org/10.1007/s13167-019-00184-z
doi: 10.1007/s13167-019-00184-z pubmed: 31832110
Anderson NM, Mucka P, Kern JG, Feng H (2018) The emerging role and targetability of the TCA cycle in cancer metabolism. Protein Cell 9:216–237. https://doi.org/10.1007/s13238-017-0451-1
doi: 10.1007/s13238-017-0451-1 pubmed: 28748451
Arthur JC, Jobin C (2011) The struggle within: microbial influences on colorectal cancer. Inflamm Bowel Dis 17:396–409. https://doi.org/10.1002/ibd.21354
doi: 10.1002/ibd.21354 pubmed: 20848537 pmcid: 3376405
Bian X, Wu W, Yang L, Lv L, Wang Q, Li Y, Ye J, Fang D, Wu J, Jiang X, Shi D, Li L (2019) Administration of Akkermansia muciniphila ameliorates dextran sulfate sodium-induced ulcerative colitis in mice. Front Microbiol 10: . https://doi.org/10.3389/fmicb.2019.02259
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120. https://doi.org/10.1093/bioinformatics/btu170
doi: 10.1093/bioinformatics/btu170 pubmed: 4103590 pmcid: 4103590
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68:394–424. https://doi.org/10.3322/caac.21492
doi: 10.3322/caac.21492
Canani RB, Costanzo MD, Leone L, Pedata M, Meli R, Calignano A (2011) Potential beneficial effects of butyrate in intestinal and extraintestinal diseases. World J Gastroenterol 17:1519–1528. https://doi.org/10.3748/wjg.v17.i12.1519
doi: 10.3748/wjg.v17.i12.1519 pubmed: 3070119 pmcid: 3070119
Caporaso JG, Kuczynski J, Stombaugh J, Bittinger K, Bushman FD, Costello EK, Fierer N, Peña AG, Goodrich JK, Gordon JI, Huttley GA, Kelley ST, Knights D, Koenig JE, Ley RE, Lozupone CA, McDonald D, Muegge BD, Pirrung M, Reeder J, Sevinsky JR, Turnbaugh PJ, Walters WA, Widmann J, Yatsunenko T, Zaneveld J, Knight R (2010) QIIME allows analysis of high-throughput community sequencing data. Nat Methods 7:335–336. https://doi.org/10.1038/nmeth.f.303
doi: 10.1038/nmeth.f.303 pubmed: 3156573 pmcid: 3156573
Chen W, Liu F, Ling Z, Tong X, Xiang C (2012) Human intestinal lumen and mucosa-associated microbiota in patients with colorectal cancer. PLoS One 7:e39743. https://doi.org/10.1371/journal.pone.0039743
doi: 10.1371/journal.pone.0039743 pubmed: 22761885 pmcid: 22761885
Chen Y-J, Wu H, Wu S-D, Lu N, Wang Y-T, Liu H-N, Dong L, Liu T-T, Shen X-Z (2018) Parasutterella, in association with irritable bowel syndrome and intestinal chronic inflammation. J Gastroenterol Hepatol 33:1844–1852. https://doi.org/10.1111/jgh.14281
doi: 10.1111/jgh.14281 pubmed: 29744928
Cole JR, Wang Q, Fish JA, Chai B, McGarrell DM, Sun Y, Brown CT, Porras-Alfaro A, Kuske CR, Tiedje JM (2014) Ribosomal Database Project: data and tools for high throughput rRNA analysis. Nucleic Acids Res 42:D633–D642. https://doi.org/10.1093/nar/gkt1244
doi: 10.1093/nar/gkt1244 pubmed: 24288368
Collins JW, Chervaux C, Raymond B, Derrien M, Brazeilles R, Kosta A, Chambaud I, Crepin VF, Frankel G (2014) Fermented dairy products modulate Citrobacter rodentium-induced colonic hyperplasia. J Infect Dis 210:1029–1041. https://doi.org/10.1093/infdis/jiu205
doi: 10.1093/infdis/jiu205 pubmed: 24706936 pmcid: 4157696
Currie E, Schulze A, Zechner R, Walther TC, Farese RV (2013) Cellular fatty acid metabolism and Cancer. Cell Metab 18:153–161. https://doi.org/10.1016/j.cmet.2013.05.017
doi: 10.1016/j.cmet.2013.05.017 pubmed: 23791484 pmcid: 3742569
de las Rivas B, Marcobal A, Carrascosa AV, Muñoz R (2006) PCR detection of foodborne bacteria producing the biogenic amines histamine, tyramine, putrescine, and cadaverine. J Food Prot 69:2509–2514. https://doi.org/10.4315/0362-028x-69.10.2509
doi: 10.4315/0362-028x-69.10.2509 pubmed: 17066936
De Robertis M, Massi E, Poeta ML, Carotti S, Morini S, Cecchetelli L, Signori E, Fazio VM (2011) The AOM/DSS murine model for the study of colon carcinogenesis: from pathways to diagnosis and therapy studies. J Carcinog 10:9. https://doi.org/10.4103/1477-3163.78279
doi: 10.4103/1477-3163.78279 pubmed: 21483655 pmcid: 3072657
Derrien M, Vaughan EE, Plugge CM, De WV (2004) Akkermansia muciniphila gen. nov., sp. nov., a human intestinal mucin-degrading bacterium. Int J Syst Evol Microbiol 54:1469–1476. https://doi.org/10.1099/ijs.0.02873-0
doi: 10.1099/ijs.0.02873-0 pubmed: 15388697
Everard A, Belzer C, Geurts L, Ouwerkerk JP, Druart C, Bindels LB, Guiot Y, Derrien M, Muccioli GG, Delzenne NM, de Vos WM, Cani PD (2013) Cross-talk between Akkermansia muciniphila and intestinal epithelium controls diet-induced obesity. PNAS 110:9066–9071. https://doi.org/10.1073/pnas.1219451110
doi: 10.1073/pnas.1219451110 pubmed: 23671105
Foo N-P, Ou Yang H, Chiu H-H, Chan H-Y, Liao C-C, Yu C-K, Wang Y-J (2011) Probiotics prevent the development of 1,2-dimethylhydrazine (DMH)-induced colonic tumorigenesis through suppressed colonic mucosa cellular proliferation and increased stimulation of macrophages. J Agric Food Chem 59:13337–13345. https://doi.org/10.1021/jf203444d
doi: 10.1021/jf203444d pubmed: 22049926
Gao Z, Guo B, Gao R, Zhu Q, Qin H (2015) Microbiota disbiosis is associated with colorectal cancer. Front Microbiol 6: . https://doi.org/10.3389/fmicb.2015.00020
Gareau MG, Sherman PM, Walker WA (2010) Probiotics and the gut microbiota in intestinal health and disease. Nat Rev Gastroenterol Hepatol 7:503–514. https://doi.org/10.1038/nrgastro.2010.117
doi: 10.1038/nrgastro.2010.117 pubmed: 4748966 pmcid: 4748966
Grimm V, Radulovic K, Riedel CU (2015) Colonization of C57BL/6 mice by a potential probiotic Bifidobacterium bifidum strain under germ-free and specific pathogen-free conditions and during experimental colitis. PLoS One 10:e0139935. https://doi.org/10.1371/journal.pone.0139935
doi: 10.1371/journal.pone.0139935 pubmed: 26439388 pmcid: 4595203
Hibberd AA, Lyra A, Ouwehand AC, Rolny P, Lindegren H, Cedgård L, Wettergren Y (2017) Intestinal microbiota is altered in patients with colon cancer and modified by probiotic intervention. BMJ Open Gastroenterol 4:e000145. https://doi.org/10.1136/bmjgast-2017-000145
doi: 10.1136/bmjgast-2017-000145 pubmed: 28944067 pmcid: 5609083
Jacouton E, Chain F, Sokol H, Langella P, Bermúdez-Humarán LG (2017) Probiotic strain Lactobacillus casei BL23 prevents colitis-associated colorectal cancer. Front Immunol 8:1553. https://doi.org/10.3389/fimmu.2017.01553
doi: 10.3389/fimmu.2017.01553 pubmed: 29209314 pmcid: 5702231
Jess T, Gamborg M, Matzen P, Munkholm P, Sørensen TIA (2005) Increased risk of intestinal cancer in Crohn’s disease: a meta-analysis of population-based cohort studies. Am J Gastroenterol 100:2724–2729. https://doi.org/10.1111/j.1572-0241.2005.00287.x
doi: 10.1111/j.1572-0241.2005.00287.x pubmed: 16393226
Kim MJ, Ku S, Kim SY, Lee HH, Jin H, Kang S, Li R, Johnston TV, Park MS, Ji GE (2018) Safety evaluations of Bifidobacterium bifidum BGN4 and Bifidobacterium longum BORI. Int J Mol Sci 19. https://doi.org/10.3390/ijms19051422
Kinross JM, Darzi AW, Nicholson JK (2011) Gut microbiome-host interactions in health and disease. Genome Med 3:14. https://doi.org/10.1186/gm228
doi: 10.1186/gm228 pubmed: 21392406 pmcid: 3092099
Kitaoka M (2012) Bifidobacterial enzymes involved in the metabolism of human milk oligosaccharides123. Adv Nutr 3:422S–429S. https://doi.org/10.3945/an.111.001420
doi: 10.3945/an.111.001420 pubmed: 22585921 pmcid: 3649479
Kovács T, Mikó E, Vida A, Sebő É, Toth J, Csonka T, Boratkó A, Ujlaki G, Lente G, Kovács P, Tóth D, Árkosy P, Kiss B, Méhes G, Goedert JJ, Bai P (2019) Cadaverine, a metabolite of the microbiome, reduces breast cancer aggressiveness through trace amino acid receptors. Sci Rep 9:1–14. https://doi.org/10.1038/s41598-018-37664-7
doi: 10.1038/s41598-018-37664-7
Langille MGI, Zaneveld J, Caporaso JG, McDonald D, Knights D, Reyes JA, Clemente JC, Burkepile DE, Vega Thurber RL, Knight R, Beiko RG, Huttenhower C (2013) Predictive functional profiling of microbial communities using 16S rRNA marker gene sequences. Nat Biotechnol 31:814–821. https://doi.org/10.1038/nbt.2676
doi: 10.1038/nbt.2676 pubmed: 23975157 pmcid: 23975157
Liberti MV, Locasale JW (2016) The Warburg effect: how does it benefit cancer cells? Trends Biochem Sci 41:211–218. https://doi.org/10.1016/j.tibs.2015.12.001
doi: 10.1016/j.tibs.2015.12.001 pubmed: 26778478 pmcid: 4783224
Lin C-C, Cheng T-L, Tsai W-H, Tsai H-J, Hu K-H, Chang H-C, Yeh C-W, Chen Y-C, Liao C-C, Chang W-T (2012) Loss of the respiratory enzyme citrate synthase directly links the Warburg effect to tumor malignancy. Sci Rep 2:785. https://doi.org/10.1038/srep00785
doi: 10.1038/srep00785 pubmed: 23139858 pmcid: 3492867
Louis P, Hold GL, Flint HJ (2014) The gut microbiota, bacterial metabolites and colorectal cancer. Nat Rev Microbiol 12:661–672. https://doi.org/10.1038/nrmicro3344
doi: 10.1038/nrmicro3344 pubmed: 25198138
Macchione IG, Lopetuso LR, Ianiro G, Napoli M, Gibiino G, Rizzatti G, Petito V, Gasbarrini A, Scaldaferri F (2019) Akkermansia muciniphila: key player in metabolic and gastrointestinal disorders. Eur Rev Med Pharmacol Sci 23:8075–8083. https://doi.org/10.26355/eurrev_201909_19024
doi: 10.26355/eurrev_201909_19024 pubmed: 31599433
Magoč T, Salzberg SL (2011) FLASH: fast length adjustment of short reads to improve genome assemblies. Bioinformatics 27:2957–2963. https://doi.org/10.1093/bioinformatics/btr507
doi: 10.1093/bioinformatics/btr507 pubmed: 21903629 pmcid: 3198573
Meehan CJ, Beiko RG (2014) A phylogenomic view of ecological specialization in the Lachnospiraceae, a family of digestive tract-associated bacteria. Genome Biol Evol 6:703–713. https://doi.org/10.1093/gbe/evu050
doi: 10.1093/gbe/evu050 pubmed: 24625961 pmcid: 24625961
Mendes MCS, Paulino DS, Brambilla SR, Camargo JA, Persinoti GF, Carvalheira JBC (2018) Microbiota modification by probiotic supplementation reduces colitis associated colon cancer in mice. World J Gastroenterol 24:1995–2008. https://doi.org/10.3748/wjg.v24.i18.1995
doi: 10.3748/wjg.v24.i18.1995 pubmed: 29760543 pmcid: 5949713
Milani C, Ticinesi A, Gerritsen J, Nouvenne A, Lugli GA, Mancabelli L, Turroni F, Duranti S, Mangifesta M, Viappiani A, Ferrario C, Maggio M, Lauretani F, De Vos W, van Sinderen D, Meschi T, Ventura M (2016) Gut microbiota composition and Clostridium difficile infection in hospitalized elderly individuals: a metagenomic study. Sci Rep 6:1–12. https://doi.org/10.1038/srep25945
doi: 10.1038/srep25945
O’Callaghan A, van Sinderen D (2016) Bifidobacteria and their role as members of the human gut microbiota. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.00925
Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glöckner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res 41:D590–D596. https://doi.org/10.1093/nar/gks1219
doi: 10.1093/nar/gks1219 pubmed: 23193283
R Core Team (2013) R: The R Project for Statistical Computing
Ren J-G, Seth P, Ye H, Guo K, Hanai J, Husain Z, Sukhatme VP (2017) Citrate suppresses tumor growth in multiple models through inhibition of glycolysis, the tricarboxylic acid cycle and the IGF-1R pathway. Sci Rep 7:1–13. https://doi.org/10.1038/s41598-017-04626-4
doi: 10.1038/s41598-017-04626-4
Rivière A, Selak M, Lantin D, Leroy F, De Vuyst L (2016) Bifidobacteria and butyrate-producing colon bacteria: importance and strategies for their stimulation in the human gut. Front Microbiol 7. https://doi.org/10.3389/fmicb.2016.00979
Rognes T, Flouri T, Nichols B, Quince C, Mahé F (2016) VSEARCH: a versatile open source tool for metagenomics. PeerJ 4:e2584. https://doi.org/10.7717/peerj.2584
doi: 10.7717/peerj.2584 pubmed: 27781170 pmcid: 5075697
Rohart F, Gautier B, Singh A, Cao K-AL (2017) mixOmics: an R package for ‘omics feature selection and multiple data integration. PLoS Comput Biol 13:e1005752 . https://doi.org/10.1371/journal.pcbi.1005752
Russell WR, Gratz SW, Duncan SH, Holtrop G, Ince J, Scobbie L, Duncan G, Johnstone AM, Lobley GE, Wallace RJ, Duthie GG, Flint HJ (2011) High-protein, reduced-carbohydrate weight-loss diets promote metabolite profiles likely to be detrimental to colonic health. Am J Clin Nutr 93:1062–1072. https://doi.org/10.3945/ajcn.110.002188
doi: 10.3945/ajcn.110.002188 pubmed: 21389180
Sato T, Matsumoto K, Okumura T, Yokoi W, Naito E, Yoshida Y, Nomoto K, Ito M, Sawada H (2008) Isolation of lactate-utilizing butyrate-producing bacteria from human feces and in vivo administration of Anaerostipes caccae strain L2 and galacto-oligosaccharides in a rat model. FEMS Microbiol Ecol 66:528–536. https://doi.org/10.1111/j.1574-6941.2008.00528.x
doi: 10.1111/j.1574-6941.2008.00528.x pubmed: 18554304
Scharlau D, Borowicki A, Habermann N, Hofmann T, Klenow S, Miene C, Munjal U, Stein K, Glei M (2009) Mechanisms of primary cancer prevention by butyrate and other products formed during gut flora-mediated fermentation of dietary fibre. Mutat Res 682:39–53. https://doi.org/10.1016/j.mrrev.2009.04.001
doi: 10.1016/j.mrrev.2009.04.001 pubmed: 19383551
Segata N, Izard J, Waldron L, Gevers D, Miropolsky L, Garrett WS, Huttenhower C (2011) Metagenomic biomarker discovery and explanation. Genome Biol 12:R60. https://doi.org/10.1186/gb-2011-12-6-r60
doi: 10.1186/gb-2011-12-6-r60 pubmed: 3218848 pmcid: 3218848
Song H, Wang W, Shen B, Jia H, Hou Z, Chen P, Sun Y (2018) Pretreatment with probiotic Bifico ameliorates colitis-associated cancer in mice: transcriptome and gut flora profiling. Cancer Sci 109:666–677. https://doi.org/10.1111/cas.13497
doi: 10.1111/cas.13497 pubmed: 29288512 pmcid: 5834773
Tan J, Chen Y-X (2016) Dietary and lifestyle factors associated with colorectal cancer risk and interactions with microbiota: fiber, red or processed meat and alcoholic drinks. Gastrointest Tumors 3:17–24. https://doi.org/10.1159/000442831
doi: 10.1159/000442831 pubmed: 27722153
Tsugawa H, Cajka T, Kind T, Ma Y, Higgins B, Ikeda K, Kanazawa M, VanderGheynst J, Fiehn O, Arita M (2015) MS-DIAL: data independent MS/MS deconvolution for comprehensive metabolome analysis. Nat Methods 12:523–526. https://doi.org/10.1038/nmeth.3393
doi: 10.1038/nmeth.3393 pubmed: 4449330 pmcid: 4449330
Turroni F, Peano C, Pass DA, Foroni E, Severgnini M, Claesson MJ, Kerr C, Hourihane J, Murray D, Fuligni F, Gueimonde M, Margolles A, De Bellis G, O’Toole PW, van Sinderen D, Marchesi JR, Ventura M (2012) Diversity of bifidobacteria within the infant gut microbiota. PLoS One 7:e36957. https://doi.org/10.1371/journal.pone.0036957
doi: 10.1371/journal.pone.0036957 pubmed: 22606315 pmcid: 3350489
Wang T-A, Zhang X-D, Guo X-Y, Xian S-L, Lu Y-F (2016) 3-bromopyruvate and sodium citrate target glycolysis, suppress survivin, and induce mitochondrial-mediated apoptosis in gastric cancer cells and inhibit gastric orthotopic transplantation tumor growth. Oncol Rep 35:1287–1296. https://doi.org/10.3892/or.2015.4511
doi: 10.3892/or.2015.4511 pubmed: 26708213
Zarrinpar A, Chaix A, Xu ZZ, Chang MW, Marotz CA, Saghatelian A, Knight R, Panda S (2018) Antibiotic-induced microbiome depletion alters metabolic homeostasis by affecting gut signaling and colonic metabolism. Nat Commun 9:2872. https://doi.org/10.1038/s41467-018-05336-9
doi: 10.1038/s41467-018-05336-9 pubmed: 30030441 pmcid: 6054678
Zhu J, Zhu C, Ge S, Zhang M, Jiang L, Cui J, Ren F (2014) Lactobacillus salivarius Ren prevent the early colorectal carcinogenesis in 1, 2-dimethylhydrazine-induced rat model. J Appl Microbiol 117:208–216. https://doi.org/10.1111/jam.12499
doi: 10.1111/jam.12499 pubmed: 24754742
Zierer J, Jackson MA, Kastenmüller G, Mangino M, Long T, Telenti A, Mohney RP, Small KS, Bell JT, Steves CJ, Valdes AM, Spector TD, Menni C (2018) The fecal metabolome as a functional readout of the gut microbiome. Nat Genet 50:790–795. https://doi.org/10.1038/s41588-018-0135-7
doi: 10.1038/s41588-018-0135-7 pubmed: 29808030 pmcid: 6104805
Zou S, Fang L, Lee M-H (2018) Dysbiosis of gut microbiota in promoting the development of colorectal cancer. Gastroenterol Rep (Oxf) 6:1–12. https://doi.org/10.1093/gastro/gox031
doi: 10.1093/gastro/gox031

Auteurs

Qing Wang (Q)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Kaicen Wang (K)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Wenrui Wu (W)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Longxian Lv (L)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Xiaoyuan Bian (X)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Liya Yang (L)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Qiangqiang Wang (Q)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Yating Li (Y)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Jianzhong Ye (J)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Daiqiong Fang (D)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Jingjing Wu (J)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Xianwan Jiang (X)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Jiaojiao Xie (J)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Yanmeng Lu (Y)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China.

Lanjuan Li (L)

State Key Laboratory for Diagnosis and Treatment of Infectious Diseases, The First Affiliated Hospital, School of Medicine, Zhejiang University, Hangzhou, 310003, China. ljli@zju.edu.cn.
Collaborative Innovation Centre for Diagnosis and Treatment of Infectious Diseases, Hangzhou, 310003, China. ljli@zju.edu.cn.
National Clinical Research Center for Infectious Diseases, Hangzhou, 310003, China. ljli@zju.edu.cn.

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