A gut butyrate‑producing bacterium Butyricicoccus pullicaecorum regulates short‑chain fatty acid transporter and receptor to reduce the progression of 1,2‑dimethylhydrazine‑associated colorectal cancer
- Authors:
- Shih-Chang Chang
- Ming-Hung Shen
- Chih-Yi Liu
- Chi-Ming Pu
- Je-Ming Hu
- Chi-Jung Huang
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Affiliations: Division of Colorectal Surgery, Department of Surgery, Cathay General Hospital, Taipei 10630, Taiwan, R.O.C., Department of Surgery, Fu Jen Catholic University Hospital, New Taipei City 24352, Taiwan, R.O.C., Department of Pathology, Sijhih Cathay General Hospital, New Taipei City 22174, Taiwan, R.O.C., Division of Plastic Surgery, Cathay General Hospital, Taipei 10630, Taiwan, R.O.C., Division of Colorectal Surgery, Department of Surgery, Tri‑Service General Hospital, Taipei 11490, Taiwan, R.O.C., School of Medicine, College of Medicine, Fu Jen Catholic University, New Taipei City 24205, Taiwan, R.O.C. - Published online on: October 5, 2020 https://doi.org/10.3892/ol.2020.12190
- Article Number: 327
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Copyright: © Chang et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
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Abstract
Mima K, Ogino S, Nakagawa S, Sawayama H, Kinoshita K, Krashima R, Ishimoto T, Imai K, Iwatsuki M, Hashimoto D, et al: The role of intestinal bacteria in the development and progression of gastrointestinal tract neoplasms. Surg Oncol. 26:368–376. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zarkavelis G, Boussios S, Papadaki A, Katsanos KH, Christodoulou DK and Pentheroudakis G: Current and future biomarkers in colorectal cancer. Ann Gastroenterol. 30:613–621. 2017.PubMed/NCBI | |
Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA and Jemal A: Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 68:394–424. 2018. View Article : Google Scholar : PubMed/NCBI | |
Gonzalez-Vallinas M, Vargas T, Moreno-Rubio J, Molina S, Herranz J, Cejas P, Burgos E, Aguayo C, Custodio A, Reglero G, et al: Clinical relevance of the differential expression of the glycosyltransferase gene GCNT3 in colon cancer. Eur J Cancer. 51:1–8. 2015. View Article : Google Scholar : PubMed/NCBI | |
Takakura Y, Ikeda S, Imaoka Y, Urushihara T and Itamoto T: An elevated preoperative serum carbohydrate antigen 19-9 level is a significant predictor for peritoneal dissemination and poor survival in colorectal cancer. Colorectal Dis. 17:417–425. 2015. View Article : Google Scholar : PubMed/NCBI | |
Tilg H, Adolph TE, Gerner RR and Moschen AR: The intestinal microbiota in colorectal cancer. Cancer Cell. 33:954–964. 2018. View Article : Google Scholar : PubMed/NCBI | |
Kisiel JB, Klepp P, Allawi HT, Taylor WR, Giakoumopoulos M, Sander T, Yab TC, Moum BA, Lidgard GP, Brackmann S, et al: Analysis of DNA methylation at specific loci in stool samples detects colorectal cancer and high-grade dysplasia in patients with inflammatory bowel disease. Clin Gastroenterol Hepatol. 17:914–921.e5. 2019. View Article : Google Scholar : PubMed/NCBI | |
Huang CJ, Yang SH, Lee CL, Cheng YC, Tai SY and Chien CC: Ribosomal protein S27-like in colorectal cancer: A candidate for predicting prognoses. PLoS One. 8:e670432013. View Article : Google Scholar : PubMed/NCBI | |
Huang CJ, Lee CL, Yang SH, Chien CC, Huang CC, Yang RN and Chang CC: Upregulation of the growth arrest-specific-2 in recurrent colorectal cancers, and its susceptibility to chemotherapy in a model cell system. Biochim Biophys Acta. 1862:1345–1353. 2016. View Article : Google Scholar : PubMed/NCBI | |
Kimura Y, Sumiyoshi M and Baba K: Antitumor activities of synthetic and natural stilbenes through antiangiogenic action. Cancer Sci. 99:2083–2096. 2008.PubMed/NCBI | |
Watine JC and Bunting PS: Mass colorectal cancer screening: Methodological quality of practice guidelines is not related to their content validity. Clin Biochem. 41:459–466. 2008. View Article : Google Scholar : PubMed/NCBI | |
Cremonesi E, Governa V, Garzon JFG, Mele V, Amicarella F, Muraro MG, Trella E, Galati-Fournier V, Oertli D, Däster SR, et al: Gut microbiota modulate T cell trafficking into human colorectal cancer. Gut. 67:1984–1994. 2018. View Article : Google Scholar : PubMed/NCBI | |
Ahmed FE: miRNA as markers for the diagnostic screening of colon cancer. Expert Rev Anticancer Ther. 14:463–485. 2014. View Article : Google Scholar : PubMed/NCBI | |
Nishioka Y, Ueki T, Hokazono K, Nagayoshi K and Tanaka M: Comparative detection of aberrantly methylated DNA in preoperative and postoperative stool from patients with colorectal cancers. Int J Biol Markers. 30:e81–e87. 2015. View Article : Google Scholar : PubMed/NCBI | |
Pittman ME: Fecal microbiota and screening for colorectal cancer. Clin Chem. 64:1273–1274. 2018. View Article : Google Scholar : PubMed/NCBI | |
Bishop KS, Xu H and Marlow G: Epigenetic regulation of gene expression induced by butyrate in colorectal cancer: Involvement of MicroRNA. Genet Epigenet. 9:1179237X177299002017. View Article : Google Scholar : PubMed/NCBI | |
Wang T, Cai G, Qiu Y, Fei N, Zhang M, Pang X, Jia W, Cai S and Zhao L: Structural segregation of gut microbiota between colorectal cancer patients and healthy volunteers. ISME J. 6:320–329. 2012. View Article : Google Scholar : PubMed/NCBI | |
Wang Y, Huang D, Chen KY, Cui M, Wang W, Huang X, Awadellah A, Li Q, Friedman A, Xin WW, et al: Fucosylation deficiency in mice leads to colitis and adenocarcinoma. Gastroenterology. 152:193–205.e10. 2017. View Article : Google Scholar : PubMed/NCBI | |
Puertollano E, Kolida S and Yaqoob P: Biological significance of short-chain fatty acid metabolism by the intestinal microbiome. Curr Opin Clin Nutr Metab Care. 17:139–144. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang G, Yu Y, Wang YZ, Wang JJ, Guan R, Sun Y, Shi F, Gao J and Fu XL: Role of SCFAs in gut microbiome and glycolysis for colorectal cancer therapy. J Cell Physiol. 234:17023–17049. 2019. View Article : Google Scholar : PubMed/NCBI | |
Huang CC, Shen MH, Chen SK, Yang SH, Liu CY, Guo JW, Chang KW and Huang CJ: Gut butyrate-producing organisms correlate to placenta specific 8 protein: Importance to colorectal cancer progression. J Adv Res. 22:7–20. 2019. View Article : Google Scholar : PubMed/NCBI | |
Li JY, Yu M, Pal S, Tyagi AM, Dar H, Adams J, Weitzmann MN, Jones RM and Pacifici R: Parathyroid hormone-dependent bone formation requires butyrate production by intestinal microbiota. J Clin Invest. 130:1767–1781. 2020. View Article : Google Scholar : PubMed/NCBI | |
Rosser EC, Piper CJM, Matei DE, Blair PA, Rendeiro AF, Orford M, Alber DG, Krausgruber T, Catalan D, Klein N, et al: Microbiota-derived metabolites suppress arthritis by amplifying aryl-hydrocarbon receptor activation in regulatory B cells. Cell Metab. 31:837–851.e10. 2020. View Article : Google Scholar : PubMed/NCBI | |
Ganapathy V, Thangaraju M, Prasad PD, Martin PM and Singh N: Transporters and receptors for short-chain fatty acids as the molecular link between colonic bacteria and the host. Curr Opin Pharmacol. 13:869–874. 2013. View Article : Google Scholar : PubMed/NCBI | |
Bartoszek A, Moo EV, Binienda A, Fabisiak A, Krajewska JB, Mosińska P, Niewinna K, Tarasiuk A, Martemyanov K, Salaga M and Fichna J: Free fatty acid receptors as new potential therapeutic target in inflammatory bowel diseases. Pharmacol Res. 152:1046042020. View Article : Google Scholar : PubMed/NCBI | |
Zhao Y, Chen F, Wu W, Sun M, Bilotta AJ, Yao S, Xiao Y, Huang X, Eaves-Pyles TD, Golovko G, et al: GPR43 mediates microbiota metabolite SCFA regulation of antimicrobial peptide expression in intestinal epithelial cells via activation of mTOR and STAT3. Mucosal Immunol. 11:752–762. 2018. View Article : Google Scholar : PubMed/NCBI | |
Chen J, Xuan YH, Luo MX, Ni XG, Ling LQ, Hu SJ, Chen JQ, Xu JY, Jiang LY, Si WZ, et al: Kaempferol alleviates acute alcoholic liver injury in mice by regulating intestinal tight junction proteins and butyrate receptors and transporters. Toxicology. 429:1523382020. View Article : Google Scholar : PubMed/NCBI | |
Boesmans L, Valles-Colomer M, Wang J, Eeckhaut V, Falony G, Ducatelle R, Van Immerseel F, Raes J and Verbeke K: Butyrate producers as potential next-generation probiotics: Safety assessment of the administration of Butyricicoccus pullicaecorum to healthy volunteers. mSystems. 3:e00094–18. 2018. View Article : Google Scholar : PubMed/NCBI | |
Eeckhaut V, Wang J, Van Parys A, Haesebrouck F, Joossens M, Falony G, Raes J, Ducatelle R and Van Immerseel F: The Probiotic Butyricicoccus pullicaecorum reduces feed conversion and protects from potentially harmful intestinal microorganisms and necrotic enteritis in broilers. Front Microbiol. 7:14162016. View Article : Google Scholar : PubMed/NCBI | |
McGrath JC, Drummond GB, McLachlan EM, Kilkenny C and Wainwright CL: Guidelines for reporting experiments involving animals: The ARRIVE guidelines. Br J Pharmacol. 160:1573–1576. 2010. View Article : Google Scholar : PubMed/NCBI | |
Hampshire VA and Gilbert SH: Refinement, reduction, and replacement (3R) strategies in preclinical testing of medical devices. Toxicol Pathol. 47:329–338. 2019. View Article : Google Scholar : PubMed/NCBI | |
Vidali S, Aminzadeh-Gohari S, Feichtinger RG, Vatrinet R, Koller A, Locker F, Rutherford T, O'Donnell M, Stöger-Kleiber A, Lambert B, et al: The ketogenic diet is not feasible as a therapy in a CD-1 nu/nu mouse model of renal cell carcinoma with features of Stauffer's syndrome. Oncotarget. 8:57201–57215. 2017. View Article : Google Scholar : PubMed/NCBI | |
De Robertis M, Massi E, Poeta ML, Carotti S, Morini S, Cecchetelli L, Signori E and Fazio VM: The AOM/DSS murine model for the study of colon carcinogenesis: From pathways to diagnosis and therapy studies. J Carcinog. 10:92011. View Article : Google Scholar : PubMed/NCBI | |
Rueden CT, Schindelin J, Hiner MC, DeZonia BE, Walter AE, Arena ET and Eliceiri KW: ImageJ2: ImageJ for the next generation of scientific image data. BMC Bioinformatics. 18:5292017. View Article : Google Scholar : PubMed/NCBI | |
Hung CS, Wang YC, Guo JW, Yang RN, Lee CL, Shen MH, Huang CC, Huang CJ, Yang JY and Liu CY: Expression pattern of placenta specific 8 and keratin 20 in different types of gastrointestinal cancer. Mol Med Rep. 21:659–666. 2020.PubMed/NCBI | |
Livak KJ and Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods. 25:402–408. 2001. View Article : Google Scholar : PubMed/NCBI | |
Fischer AH, Jacobson KA, Rose J and Zeller R: Hematoxylin and eosin staining of tissue and cell sections. CSH Protoc. 2008:pdb.prot4986. 2008. | |
Kim JJ, Shajib MS, Manocha MM and Khan WI: Investigating intestinal inflammation in DSS-induced model of IBD. J Vis Exp. 60:36782012. | |
Vargason AM and Anselmo AC: Clinical translation of microbe-based therapies: Current clinical landscape and preclinical outlook. Bioeng Transl Med. 3:124–137. 2018. View Article : Google Scholar : PubMed/NCBI | |
Shah MS, DeSantis T, Yamal JM, Weir T, Ryan EP, Cope JL and Hollister EB: Re-purposing 16S rRNA gene sequence data from within case paired tumor biopsy and tumor-adjacent biopsy or fecal samples to identify microbial markers for colorectal cancer. PLoS One. 13:e02070022018. View Article : Google Scholar : PubMed/NCBI | |
Gao C, Ganesh BP, Shi Z, Shah RR, Fultz R, Major A, Venable S, Lugo M, Hoch K, Chen X, et al: Gut microbe-mediated suppression of inflammation-associated colon carcinogenesis by luminal histamine production. Am J Pathol. 187:2323–2336. 2017. View Article : Google Scholar : PubMed/NCBI | |
Eeckhaut V, Van Immerseel F, Teirlynck E, Pasmans F, Fievez V, Snauwaert C, Haesebrouck F, Ducatelle R, Louis P and Vandamme P: Butyricicoccus pullicaecorum gen. nov., sp. nov., an anaerobic, butyrate-producing bacterium isolated from the caecal content of a broiler chicken. Int J Syst Evol Microbiol. 58:2799–2802. 2008. View Article : Google Scholar : PubMed/NCBI | |
Sitkin S and Pokrotnieks J: Clinical potential of anti-inflammatory effects of faecalibacterium prausnitzii and butyrate in inflammatory bowel disease. Inflamm Bowel Dis. 25:e40–e41. 2019. View Article : Google Scholar : PubMed/NCBI | |
Eeckhaut V, Machiels K, Perrier C, Romero C, Maes S, Flahou B, Steppe M, Haesebrouck F, Sas B, Ducatelle R, et al: Butyricicoccus pullicaecorum in inflammatory bowel disease. Gut. 62:1745–1752. 2013. View Article : Google Scholar : PubMed/NCBI | |
Kurata N, Tokashiki N, Fukushima K, Hasuoka N, Kitagawa K, Mashimo M, Regan JW, Murayama T and Fujino H: Short chain fatty acid butyrate uptake reduces expressions of prostanoid EP4 receptors and their mediation of cyclooxygenase-2 induction in HCA-7 human colon cancer cells. Eur J Pharmacol. 853:308–315. 2019. View Article : Google Scholar : PubMed/NCBI | |
Kazemi Sefat NA, Mohammadi MM, Hadjati J, Talebi S, Ajami M and Daneshvar H: Sodium butyrate as a histone deacetylase inhibitor affects toll-like receptor 4 expression in colorectal cancer cell lines. Immunol Invest. 48:759–769. 2019. View Article : Google Scholar : PubMed/NCBI | |
Luo S, Li Z, Mao L, Chen S and Sun S: Sodium butyrate induces autophagy in colorectal cancer cells through LKB1/AMPK signaling. J Physiol Biochem. 75:53–63. 2019. View Article : Google Scholar : PubMed/NCBI | |
Zhou Q, Li G, Zuo S, Zhu W and Yuan X: RNA sequencing analysis of molecular basis of sodium butyrate-induced growth inhibition on colorectal cancer cell lines. Biomed Res Int. 2019:14278712019. View Article : Google Scholar : PubMed/NCBI | |
Pirozzi C, Francisco V, Guida FD, Gómez R, Lago F, Pino J, Meli R and Gualillo O: Butyrate modulates inflammation in chondrocytes via GPR43 receptor. Cell Physiol Biochem. 51:228–243. 2018. View Article : Google Scholar : PubMed/NCBI | |
Gopal E, Miyauchi S, Martin PM, Ananth S, Roon P, Smith SB and Ganapathy V: Transport of nicotinate and structurally related compounds by human SMCT1 (SLC5A8) and its relevance to drug transport in the mammalian intestinal tract. Pharm Res. 24:575–584. 2007. View Article : Google Scholar : PubMed/NCBI | |
Cimadamore A, Santoni M, Massari F, Gasparrini S, Cheng L, Lopez-Beltran A, Montironi R and Scarpelli M: Microbiome and cancers, with focus on genitourinary tumors. Front Oncol. 9:1782019. View Article : Google Scholar : PubMed/NCBI | |
Gurav A, Sivaprakasam S, Bhutia YD, Boettger T, Singh N and Ganapathy V: Slc5a8, a Na+-coupled high-affinity transporter for short-chain fatty acids, is a conditional tumour suppressor in colon that protects against colitis and colon cancer under low-fibre dietary conditions. Biochem J. 469:267–278. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zaiss MM, Jones RM, Schett G and Pacifici R: The gut-bone axis: How bacterial metabolites bridge the distance. J Clin Invest. 129:3018–3028. 2019. View Article : Google Scholar : PubMed/NCBI | |
Chen JS, Faller DV and Spanjaard RA: Short-chain fatty acid inhibitors of histone deacetylases: Promising anticancer therapeutics? Curr Cancer Drug Targets. 3:219–236. 2003. View Article : Google Scholar : PubMed/NCBI | |
Singh N, Thangaraju M, Prasad PD, Martin PM, Lambert NA, Boettger T, Offermanns S and Ganapathy V: Blockade of dendritic cell development by bacterial fermentation products butyrate and propionate through a transporter (Slc5a8)-dependent inhibition of histone deacetylases. J Biol Chem. 285:27601–27608. 2010. View Article : Google Scholar : PubMed/NCBI | |
Turowski GA, Rashid Z, Hong F, Madri JA and Basson MD: Glutamine modulates phenotype and stimulates proliferation in human colon cancer cell lines. Cancer Res. 54:5974–5980. 1994.PubMed/NCBI | |
Leibovitz A, Stinson JC, McCombs WB III, McCoy CE, Mazur KC and Mabry ND: Classification of human colorectal adenocarcinoma cell lines. Cancer Res. 36:4562–4569. 1976.PubMed/NCBI | |
Gupta N, Martin PM, Prasad PD and Ganapathy V: SLC5A8 (SMCT1)-mediated transport of butyrate forms the basis for the tumor suppressive function of the transporter. Life Sci. 78:2419–2425. 2006. View Article : Google Scholar : PubMed/NCBI | |
Tang Y, Chen Y, Jiang H, Robbins GT and Nie D: G-protein-coupled receptor for short-chain fatty acids suppresses colon cancer. Int J Cancer. 128:847–856. 2011. View Article : Google Scholar : PubMed/NCBI | |
Thangaraju M, Cresci GA, Liu K, Ananth S, Gnanaprakasam JP, Browning DD, Mellinger JD, Smith SB, Digby GJ, Lambert NA, et al: GPR109A is a G-protein-coupled receptor for the bacterial fermentation product butyrate and functions as a tumor suppressor in colon. Cancer Res. 69:2826–2832. 2009. View Article : Google Scholar : PubMed/NCBI | |
Eslami M, Yousefi B, Kokhaei P, Hemati M, Nejad ZR, Arabkari V and Namdar A: Importance of probiotics in the prevention and treatment of colorectal cancer. J Cell Physiol. 234:17127–17143. 2019. View Article : Google Scholar : PubMed/NCBI | |
Gui Q, Li H, Wang A, Zhao X, Tan Z, Chen L, Xu K and Xiao C: The association between gut butyrate-producing bacteria and non-small-cell lung cancer. J Clin Lab Anal. 34:e233182020. View Article : Google Scholar : PubMed/NCBI | |
Zeng X, Gao X, Peng Y, Wu Q, Zhu J, Tan C, Xia G, You C, Xu R, Pan S, et al: Higher risk of stroke is correlated with increased opportunistic pathogen load and reduced levels of butyrate-producing bacteria in the gut. Front Cell Infect Microbiol. 9:42019. View Article : Google Scholar : PubMed/NCBI | |
Chen D, Jin D, Huang S, Wu J, Xu M, Liu T, Dong W, Liu X, Wang S, Zhong W, et al: Clostridium butyricum, a butyrate-producing probiotic, inhibits intestinal tumor development through modulating Wnt signaling and gut microbiota. Cancer Lett. 469:456–467. 2020. View Article : Google Scholar : PubMed/NCBI | |
Hagihara M, Kuroki Y, Ariyoshi T, Higashi S, Fukuda K, Yamashita R, Matsumoto A, Mori T, Mimura K, Yamaguchi N, et al: Clostridium butyricum modulates the microbiome to protect intestinal barrier function in mice with antibiotic-induced dysbiosis. iScience. 23:1007722020. View Article : Google Scholar : PubMed/NCBI | |
Sun M, Wu W, Liu Z and Cong Y: Microbiota metabolite short chain fatty acids, GPCR, and inflammatory bowel diseases. J Gastroenterol. 52:1–8. 2017. View Article : Google Scholar : PubMed/NCBI | |
Alvarez-Mercado AI, Navarro-Oliveros M, Robles-Sánchez C, Plaza-Díaz J, Sáez-Lara MJ, Muñoz-Quezada S, Fontana L and Abadía-Molina F: Microbial population changes and their relationship with human health and disease. Microorganisms. 7:682019. View Article : Google Scholar | |
Roduit C, Frei R, Ferstl R, Loeliger S, Westermann P, Rhyner C, Schiavi E, Barcik W, Rodriguez-Perez N, Wawrzyniak M, et al: High levels of butyrate and propionate in early life are associated with protection against atopy. Allergy. 74:799–809. 2019. View Article : Google Scholar : PubMed/NCBI | |
Li M, van Esch BCAM, Henricks PAJ, Folkerts G and Garssen J: The anti-inflammatory effects of short chain fatty acids on lipopolysaccharide- or tumor necrosis factor α-stimulated endothelial cells via activation of GPR41/43 and inhibition of HDACs. Front Pharmacol. 9:5332018. View Article : Google Scholar : PubMed/NCBI | |
Scorletti E, Afolabi PR, Miles EA, Smith DE, Almehmadi A, Alshathry A, Moyses HE, Clough GF, Wright M, Patel J, et al: Design and rationale of the INSYTE study: A randomised, placebo controlled study to test the efficacy of a synbiotic on liver fat, disease biomarkers and intestinal microbiota in non-alcoholic fatty liver disease. Contemp Clin Trials. 71:113–123. 2018. View Article : Google Scholar : PubMed/NCBI | |
Lau WL and Vaziri ND: Gut microbial short-chain fatty acids and the risk of diabetes. Nat Rev Nephrol. 15:389–390. 2019. View Article : Google Scholar : PubMed/NCBI | |
Cornejo-Pareja I, Muñoz-Garach A, Clemente-Postigo M and Tinahones FJ: Importance of gut microbiota in obesity. Eur J Clin Nutr. 72 (Suppl 1):S26–S37. 2019. View Article : Google Scholar | |
Gill PA, van Zelm MC, Muir JG and Gibson PR: Review article: Short chain fatty acids as potential therapeutic agents in human gastrointestinal and inflammatory disorders. Aliment Pharmacol Ther. 48:15–34. 2018. View Article : Google Scholar : PubMed/NCBI | |
Esser D, Lange J, Marinos G, Sieber M, Best L, Prasse D, Bathia J, Rühlemann MC, Boersch K, Jaspers C and Sommer F: Functions of the microbiota for the physiology of animal metaorganisms. J Innate Immun. 11:393–404. 2019. View Article : Google Scholar : PubMed/NCBI | |
Koliarakis I, Messaritakis I, Nikolouzakis TK, Hamilos G, Souglakos J and Tsiaoussis J: Oral bacteria and intestinal dysbiosis in colorectal cancer. Int J Mol Sci. 20:41462019. View Article : Google Scholar | |
Chen J and Vitetta L: Inflammation-modulating effect of butyrate in the prevention of colon cancer by dietary fiber. Clin Colorectal Cancer. 17:e541–e544. 2018. View Article : Google Scholar : PubMed/NCBI |