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Published in: BMC Complementary Medicine and Therapies 1/2020

01-12-2020 | Pneumococcus | Research article

Shen-ling-bai-zhu-san ameliorates inflammation and lung injury by increasing the gut microbiota in the murine model of Streptococcus pneumonia-induced pneumonia

Authors: Jinli Feng, Weibo Dai, Cheng Zhang, Houjun Chen, Ziliang Chen, Yongfeng Chen, Qianyi Pan, Yongmao Zhou

Published in: BMC Complementary Medicine and Therapies | Issue 1/2020

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Abstract

Background

Shen-ling-bai-zhu-san (SLBZS) regulates inflammation and gut microbiota which are associated with Streptococcus pneumoniae (Spn)-induced pneumonia. So, we studied the therapeutic effect of SLBZS and evaluated whether gut microbiota is associated with the effects of SLBZS in improving Spn-induced pneumonia.

Methods

Spn-induced pneumonia NIH mice were treated by SLBZS and cefixime. A CT scan was performed and Myeloperoxidase (MPO) activity in lung homogenates was determined using the MPO Colorimetric Assay Kit. Inflammation levels in lung homogenates were measured using ELISA. Bacterial load was coated on a TSAII sheep blood agar. Intestinal gut microbiota information was analyzed according to sequencing libraries.

Results

SLBZS decreased bacterial load, reduced wet/dry weight ratio, inhibited myeloperoxidase activity, reduced the neutrophils count, and ameliorated lung injury. Furthermore, SLBZS inhibited interleukin (IL)-1β, IL-6, tumor necrosis factor-α, IL-2, IL-8, IL-12, and interferon-γ secretion and enhanced IL-10 secretion. These results suggest that SLBZS ameliorates lung injury in mice with Spn-induced pneumonia. Moreover, SLBZS reduced inflammatory cytokine levels in a concentration-dependent manner and increased gut microbiota abundance and diversity. After SLBZS treatment, bacteria such as Epsilonbacteraeota, Bacteroidetes, Actinobacteria, Proteobacteria, and Patescibacteria were significantly reduced, while Tenericutes and Firmicutes were significantly increased.

Conclusion

SLBZS ameliorates inflammation, lung injury, and gut microbiota in mice with S. pneumoniae-induced pneumonia.
Literature
1.
go back to reference Cilloniz C, Liapikou A, Martin-Loeches I, Garcia-Vidal C, Gabarrus A, Ceccato A, Magdaleno D, Mensa J, Marco F, Torres A. Twenty-year trend in mortality among hospitalized patients with pneumococcal community-acquired pneumonia. PLoS One. 2018;13:e0200504.CrossRef Cilloniz C, Liapikou A, Martin-Loeches I, Garcia-Vidal C, Gabarrus A, Ceccato A, Magdaleno D, Mensa J, Marco F, Torres A. Twenty-year trend in mortality among hospitalized patients with pneumococcal community-acquired pneumonia. PLoS One. 2018;13:e0200504.CrossRef
2.
go back to reference Amin R, Hatakeyama Y, Kitazawa T, Matsumoto K, Fujita S, Seto K, Hasegawa T. Capturing the trends in hospital standardized mortality ratios for pneumonia: a retrospective observational study in Japan (2010 to 2018). Environ Health Prev Med. 2020;25:2.CrossRef Amin R, Hatakeyama Y, Kitazawa T, Matsumoto K, Fujita S, Seto K, Hasegawa T. Capturing the trends in hospital standardized mortality ratios for pneumonia: a retrospective observational study in Japan (2010 to 2018). Environ Health Prev Med. 2020;25:2.CrossRef
3.
go back to reference Pick H, Daniel P, Rodrigo C, Bewick T, Ashton D, Lawrence H, Baskaran V, Edwards-Pritchard RC, Sheppard C, Eletu SD, et al. Pneumococcal serotype trends, surveillance and risk factors in UK adult pneumonia, 2013-18. Thorax. 2020;75:38–49.CrossRef Pick H, Daniel P, Rodrigo C, Bewick T, Ashton D, Lawrence H, Baskaran V, Edwards-Pritchard RC, Sheppard C, Eletu SD, et al. Pneumococcal serotype trends, surveillance and risk factors in UK adult pneumonia, 2013-18. Thorax. 2020;75:38–49.CrossRef
4.
go back to reference Ghia CJ, Dhar R, Koul PA, Rambhad G, Fletcher MA. Streptococcus pneumoniae as a cause of community-acquired pneumonia in Indian adolescents and adults: a systematic review and meta-analysis. Clin Med Insights Circ Respir Pulm Med. 2019;13:1179548419862790.CrossRef Ghia CJ, Dhar R, Koul PA, Rambhad G, Fletcher MA. Streptococcus pneumoniae as a cause of community-acquired pneumonia in Indian adolescents and adults: a systematic review and meta-analysis. Clin Med Insights Circ Respir Pulm Med. 2019;13:1179548419862790.CrossRef
5.
go back to reference Kim GL, Seon SH, Rhee DK. Pneumonia and Streptococcus pneumoniae vaccine. Arch Pharm Res. 2017;40:885–93.CrossRef Kim GL, Seon SH, Rhee DK. Pneumonia and Streptococcus pneumoniae vaccine. Arch Pharm Res. 2017;40:885–93.CrossRef
6.
go back to reference Amalakuhan B, Echevarria KL, Restrepo MI. Managing community acquired pneumonia in the elderly - the next generation of pharmacotherapy on the horizon. Expert Opin Pharmacother. 2017;18:1039–48.CrossRef Amalakuhan B, Echevarria KL, Restrepo MI. Managing community acquired pneumonia in the elderly - the next generation of pharmacotherapy on the horizon. Expert Opin Pharmacother. 2017;18:1039–48.CrossRef
7.
go back to reference Deng D, Chen Z, Jia L, Bu J, Ye M, Sun L, Gen Y, Zhang W, Chen G, Fang B. Treatment of hospital-acquired pneumonia with multi-drug resistant organism by Buzhong Yiqi decoction based on Fuzheng Quxie classical prescription: study protocol for a randomized controlled trial. Trials. 2019;20:817.CrossRef Deng D, Chen Z, Jia L, Bu J, Ye M, Sun L, Gen Y, Zhang W, Chen G, Fang B. Treatment of hospital-acquired pneumonia with multi-drug resistant organism by Buzhong Yiqi decoction based on Fuzheng Quxie classical prescription: study protocol for a randomized controlled trial. Trials. 2019;20:817.CrossRef
8.
go back to reference Song Y, Yao C, Yao Y, Han H, Zhao X, Yu K, Liu L, Xu Y, Liu Z, Zhou Q, et al. XueBiJing injection versus placebo for critically ill patients with severe community-acquired pneumonia: a randomized controlled trial. Crit Care Med. 2019;47:e735–43.CrossRef Song Y, Yao C, Yao Y, Han H, Zhao X, Yu K, Liu L, Xu Y, Liu Z, Zhou Q, et al. XueBiJing injection versus placebo for critically ill patients with severe community-acquired pneumonia: a randomized controlled trial. Crit Care Med. 2019;47:e735–43.CrossRef
9.
go back to reference Wang H, Li J, Yu X, Li SY. Integrated traditional Chinese and conventional medicine in treatment of severe community-acquired pneumonia: study protocol for a randomized placebo-controlled trial. Trials. 2018;19:620.CrossRef Wang H, Li J, Yu X, Li SY. Integrated traditional Chinese and conventional medicine in treatment of severe community-acquired pneumonia: study protocol for a randomized placebo-controlled trial. Trials. 2018;19:620.CrossRef
10.
go back to reference Li DM, Qi RH, Zhang HC, Liao X, Xie YM, Zhang JH, Zhang BL. Clinical application evaluation and revision suggestions of clinical practice guideline on traditional Chinese medicine therapy alone or combined with antibiotics for community acquired pneumonia. Zhongguo Zhong Yao Za Zhi. 2018;43:4759–64.PubMed Li DM, Qi RH, Zhang HC, Liao X, Xie YM, Zhang JH, Zhang BL. Clinical application evaluation and revision suggestions of clinical practice guideline on traditional Chinese medicine therapy alone or combined with antibiotics for community acquired pneumonia. Zhongguo Zhong Yao Za Zhi. 2018;43:4759–64.PubMed
11.
go back to reference Huang YH, Chen ST, Liu FH, Hsieh SH, Lin CH, Liou MJ, Wang CC, Huang CH, Liu GH, Lin JR, et al. The efficacy and safety of concentrated herbal extract granules, YH1, as an add-on medication in poorly controlled type 2 diabetes: a randomized, double-blind, placebo-controlled pilot trial. PLoS One. 2019;14:e0221199.CrossRef Huang YH, Chen ST, Liu FH, Hsieh SH, Lin CH, Liou MJ, Wang CC, Huang CH, Liu GH, Lin JR, et al. The efficacy and safety of concentrated herbal extract granules, YH1, as an add-on medication in poorly controlled type 2 diabetes: a randomized, double-blind, placebo-controlled pilot trial. PLoS One. 2019;14:e0221199.CrossRef
12.
go back to reference Yang QH, Xu YJ, Liu YZ, Liang YJ, Feng GF, Zhang YP, Xing HJ, Yan HZ, Li YY. Effects of Chaihu-Shugan-san and Shen-Ling-Bai-Zhu-san on p38 MAPK pathway in Kupffer cells of nonalcoholic Steatohepatitis. Evid Based Complement Alternat Med. 2014;2014:671013.PubMedPubMedCentral Yang QH, Xu YJ, Liu YZ, Liang YJ, Feng GF, Zhang YP, Xing HJ, Yan HZ, Li YY. Effects of Chaihu-Shugan-san and Shen-Ling-Bai-Zhu-san on p38 MAPK pathway in Kupffer cells of nonalcoholic Steatohepatitis. Evid Based Complement Alternat Med. 2014;2014:671013.PubMedPubMedCentral
13.
go back to reference Yang L, Song Y, Jin P, Liu Y, Wang Y, Qiao H, Huang Y. Shen-Ling-Bai-Zhu-san for ulcerative colitis: protocol for a systematic review and meta-analysis. Medicine (Baltimore). 2018;97:e12337.CrossRef Yang L, Song Y, Jin P, Liu Y, Wang Y, Qiao H, Huang Y. Shen-Ling-Bai-Zhu-san for ulcerative colitis: protocol for a systematic review and meta-analysis. Medicine (Baltimore). 2018;97:e12337.CrossRef
14.
go back to reference Zhang Y, Tang K, Deng Y, Chen R, Liang S, Xie H, He Y, Chen Y, Yang Q. Effects of shenling baizhu powder herbal formula on intestinal microbiota in high-fat diet-induced NAFLD rats. Biomed Pharmacother. 2018;102:1025–36.CrossRef Zhang Y, Tang K, Deng Y, Chen R, Liang S, Xie H, He Y, Chen Y, Yang Q. Effects of shenling baizhu powder herbal formula on intestinal microbiota in high-fat diet-induced NAFLD rats. Biomed Pharmacother. 2018;102:1025–36.CrossRef
15.
go back to reference Tamburini S, Clemente JC. Gut microbiota: Neonatal gut microbiota induces lung immunity against pneumonia. Nat Rev Gastroenterol Hepatol. 2017;14:263–4.CrossRef Tamburini S, Clemente JC. Gut microbiota: Neonatal gut microbiota induces lung immunity against pneumonia. Nat Rev Gastroenterol Hepatol. 2017;14:263–4.CrossRef
16.
go back to reference Peng S, Du TH, Zhang M. Changes in gut microbiota and serum D-lactate level and correlation analysis in children with recurrent pneumonia. Zhongguo Dang Dai Er Ke Za Zhi. 2016;18:113–6.PubMed Peng S, Du TH, Zhang M. Changes in gut microbiota and serum D-lactate level and correlation analysis in children with recurrent pneumonia. Zhongguo Dang Dai Er Ke Za Zhi. 2016;18:113–6.PubMed
17.
go back to reference Schuijt TJ, Lankelma JM, Scicluna BP, de Sousa e Melo F, Roelofs JJ, de Boer JD, Hoogendijk AJ, de Beer R, de Vos A, Belzer C, et al. The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut. 2016;65:575–83.CrossRef Schuijt TJ, Lankelma JM, Scicluna BP, de Sousa e Melo F, Roelofs JJ, de Boer JD, Hoogendijk AJ, de Beer R, de Vos A, Belzer C, et al. The gut microbiota plays a protective role in the host defence against pneumococcal pneumonia. Gut. 2016;65:575–83.CrossRef
18.
go back to reference Mahmoodpoor A, Hamishehkar H, Asghari R, Abri R, Shadvar K, Sanaie S. Effect of a probiotic preparation on ventilator-associated pneumonia in critically ill patients admitted to the intensive care unit: a prospective double-blind randomized controlled trial. Nutr Clin Pract. 2019;34:156–62.CrossRef Mahmoodpoor A, Hamishehkar H, Asghari R, Abri R, Shadvar K, Sanaie S. Effect of a probiotic preparation on ventilator-associated pneumonia in critically ill patients admitted to the intensive care unit: a prospective double-blind randomized controlled trial. Nutr Clin Pract. 2019;34:156–62.CrossRef
19.
go back to reference Ige OM, Okesola AO. Comparative efficacy and safety of CEFIXIME and ciprofloxacin in the management of adults with community-acquired pneumonia in IBADAN, NIGERIA. Ann Ib Postgrad Med. 2015;13:72–8.PubMedPubMedCentral Ige OM, Okesola AO. Comparative efficacy and safety of CEFIXIME and ciprofloxacin in the management of adults with community-acquired pneumonia in IBADAN, NIGERIA. Ann Ib Postgrad Med. 2015;13:72–8.PubMedPubMedCentral
20.
go back to reference Minami M, Konishi T, Takase H, Jiang Z, Arai T, Makino T. Effect of Shin'iseihaito (Xinyiqingfeitang) on acute Streptococcus pneumoniae murine sinusitis via macrophage activation. Evid Based Complement Alternat Med. 2017;2017:4293291.CrossRef Minami M, Konishi T, Takase H, Jiang Z, Arai T, Makino T. Effect of Shin'iseihaito (Xinyiqingfeitang) on acute Streptococcus pneumoniae murine sinusitis via macrophage activation. Evid Based Complement Alternat Med. 2017;2017:4293291.CrossRef
21.
go back to reference Cui P, Xin H, Yao Y, Xiao S, Zhu F, Gong Z, Tang Z, Zhan Q, Qin W, Lai Y, et al. Human amnion-derived mesenchymal stem cells alleviate lung injury induced by white smoke inhalation in rats. Stem Cell Res Ther. 2018;9:101.CrossRef Cui P, Xin H, Yao Y, Xiao S, Zhu F, Gong Z, Tang Z, Zhan Q, Qin W, Lai Y, et al. Human amnion-derived mesenchymal stem cells alleviate lung injury induced by white smoke inhalation in rats. Stem Cell Res Ther. 2018;9:101.CrossRef
22.
go back to reference Yang Z, Zou X, Feng P, Zhan H, Xiong D, Lang J. Inhibition of the PI3K/AKT signaling pathway or overexpression of Beclin1 blocks reinfection of Streptococcus pneumoniae after infection of influenza a virus in severe community-acquired pneumonia. Inflammation. 2019.42:1741–753.CrossRef Yang Z, Zou X, Feng P, Zhan H, Xiong D, Lang J. Inhibition of the PI3K/AKT signaling pathway or overexpression of Beclin1 blocks reinfection of Streptococcus pneumoniae after infection of influenza a virus in severe community-acquired pneumonia. Inflammation. 2019.42:1741–753.CrossRef
23.
go back to reference Yang X, Liu L, Chen J, Xiao A. Response of intestinal bacterial Flora to the long-term feeding of Aflatoxin B1 (AFB1) in mice. Toxins (Basel). 2017;9. Yang X, Liu L, Chen J, Xiao A. Response of intestinal bacterial Flora to the long-term feeding of Aflatoxin B1 (AFB1) in mice. Toxins (Basel). 2017;9.
24.
go back to reference Gu S, Chen D, Zhang JN, Lv X, Wang K, Duan LP, Nie Y, Wu XL. Bacterial community mapping of the mouse gastrointestinal tract. PLoS One. 2013;8:e74957.CrossRef Gu S, Chen D, Zhang JN, Lv X, Wang K, Duan LP, Nie Y, Wu XL. Bacterial community mapping of the mouse gastrointestinal tract. PLoS One. 2013;8:e74957.CrossRef
25.
go back to reference Ji HJ, Kang N, Chen T, Lv L, Ma XX, Wang FY, Tang XD. Shen-ling-bai-zhu-san, a spleen-tonifying Chinese herbal formula, alleviates lactose-induced chronic diarrhea in rats. J Ethnopharmacol. 2019;231:355–62.CrossRef Ji HJ, Kang N, Chen T, Lv L, Ma XX, Wang FY, Tang XD. Shen-ling-bai-zhu-san, a spleen-tonifying Chinese herbal formula, alleviates lactose-induced chronic diarrhea in rats. J Ethnopharmacol. 2019;231:355–62.CrossRef
26.
go back to reference Lv WJ, Liu C, Li YF, Chen WQ, Li ZQ, Li Y, Xiong Y, Chao LM, Xu XL, Guo SN. Systems pharmacology and microbiome dissection of Shen Ling Bai Zhu san reveal multiscale treatment strategy for IBD. Oxidative Med Cell Longev. 2019;2019:8194804. Lv WJ, Liu C, Li YF, Chen WQ, Li ZQ, Li Y, Xiong Y, Chao LM, Xu XL, Guo SN. Systems pharmacology and microbiome dissection of Shen Ling Bai Zhu san reveal multiscale treatment strategy for IBD. Oxidative Med Cell Longev. 2019;2019:8194804.
27.
go back to reference Zhou Y, Gao H, Mihindukulasuriya KA, La Rosa PS, Wylie KM, Vishnivetskaya T, Podar M, Warner B, Tarr PI, Nelson DE, et al. Biogeography of the ecosystems of the healthy human body. Genome Biol. 2013;14:R1.CrossRef Zhou Y, Gao H, Mihindukulasuriya KA, La Rosa PS, Wylie KM, Vishnivetskaya T, Podar M, Warner B, Tarr PI, Nelson DE, et al. Biogeography of the ecosystems of the healthy human body. Genome Biol. 2013;14:R1.CrossRef
28.
go back to reference Dai W, Wang H, Zhou Q, Feng X, Lu Z, Li D, Yang Z, Liu Y, Li Y, Xie G, et al. The concordance between upper and lower respiratory microbiota in children with mycoplasma pneumoniae pneumonia. Emerg Microbes Infect. 2018;7:92.PubMedPubMedCentral Dai W, Wang H, Zhou Q, Feng X, Lu Z, Li D, Yang Z, Liu Y, Li Y, Xie G, et al. The concordance between upper and lower respiratory microbiota in children with mycoplasma pneumoniae pneumonia. Emerg Microbes Infect. 2018;7:92.PubMedPubMedCentral
29.
go back to reference Shankar J, Nguyen MH, Crespo MM, Kwak EJ, Lucas SK, McHugh KJ, Mounaud S, Alcorn JF, Pilewski JM, Shigemura N, et al. Looking beyond respiratory cultures: microbiome-cytokine signatures of bacterial pneumonia and Tracheobronchitis in lung transplant recipients. Am J Transplant. 2016;16:1766–78.CrossRef Shankar J, Nguyen MH, Crespo MM, Kwak EJ, Lucas SK, McHugh KJ, Mounaud S, Alcorn JF, Pilewski JM, Shigemura N, et al. Looking beyond respiratory cultures: microbiome-cytokine signatures of bacterial pneumonia and Tracheobronchitis in lung transplant recipients. Am J Transplant. 2016;16:1766–78.CrossRef
30.
go back to reference Wang H, Dai W, Qiu C, Li S, Wang W, Xu J, Li Z, Wang H, Li Y, Yang Z, et al. Mycoplasma pneumoniae and Streptococcus pneumoniae caused different microbial structure and correlation network in lung microbiota. J Thorac Dis. 2016;8:1316–22.CrossRef Wang H, Dai W, Qiu C, Li S, Wang W, Xu J, Li Z, Wang H, Li Y, Yang Z, et al. Mycoplasma pneumoniae and Streptococcus pneumoniae caused different microbial structure and correlation network in lung microbiota. J Thorac Dis. 2016;8:1316–22.CrossRef
31.
go back to reference Prazak J, Iten M, Cameron DR, Save J, Grandgirard D, Resch G, Goepfert C, Leib SL, Takala J, Jakob SM, et al. Bacteriophages improve outcomes in experimental Staphylococcus aureus ventilator-associated pneumonia. Am J Respir Crit Care Med. 2019;200:1126–33.CrossRef Prazak J, Iten M, Cameron DR, Save J, Grandgirard D, Resch G, Goepfert C, Leib SL, Takala J, Jakob SM, et al. Bacteriophages improve outcomes in experimental Staphylococcus aureus ventilator-associated pneumonia. Am J Respir Crit Care Med. 2019;200:1126–33.CrossRef
32.
go back to reference Loughran AJ, Orihuela CJ, Tuomanen EI. Streptococcus pneumoniae: invasion and inflammation. Microbiol Spectr. 2019;7:10. Loughran AJ, Orihuela CJ, Tuomanen EI. Streptococcus pneumoniae: invasion and inflammation. Microbiol Spectr. 2019;7:10.
33.
go back to reference Smith MW, Schmidt JE, Rehg JE, Orihuela CJ, McCullers JA. Induction of pro- and anti-inflammatory molecules in a mouse model of pneumococcal pneumonia after influenza. Comp Med. 2007;57:82–9.PubMedPubMedCentral Smith MW, Schmidt JE, Rehg JE, Orihuela CJ, McCullers JA. Induction of pro- and anti-inflammatory molecules in a mouse model of pneumococcal pneumonia after influenza. Comp Med. 2007;57:82–9.PubMedPubMedCentral
34.
go back to reference Duell BL, Tan CK, Carey AJ, Wu F, Cripps AW, Ulett GC. Recent insights into microbial triggers of interleukin-10 production in the host and the impact on infectious disease pathogenesis. FEMS Immunol Med Microbiol. 2012;64:295–313.CrossRef Duell BL, Tan CK, Carey AJ, Wu F, Cripps AW, Ulett GC. Recent insights into microbial triggers of interleukin-10 production in the host and the impact on infectious disease pathogenesis. FEMS Immunol Med Microbiol. 2012;64:295–313.CrossRef
35.
go back to reference Penaloza HF, Nieto PA, Munoz-Durango N, Salazar-Echegarai FJ, Torres J, Parga MJ, Alvarez-Lobos M, Riedel CA, Kalergis AM, Bueno SM. Interleukin-10 plays a key role in the modulation of neutrophils recruitment and lung inflammation during infection by Streptococcus pneumoniae. Immunology. 2015;146:100–12.CrossRef Penaloza HF, Nieto PA, Munoz-Durango N, Salazar-Echegarai FJ, Torres J, Parga MJ, Alvarez-Lobos M, Riedel CA, Kalergis AM, Bueno SM. Interleukin-10 plays a key role in the modulation of neutrophils recruitment and lung inflammation during infection by Streptococcus pneumoniae. Immunology. 2015;146:100–12.CrossRef
36.
go back to reference Yang Q, Xu Y, Feng G, Hu C, Zhang Y, Cheng S, Wang Y, Gong X. p38 MAPK signal pathway involved in anti-inflammatory effect of Chaihu-Shugan-san and Shen-ling-bai-zhu-san on hepatocyte in non-alcoholic steatohepatitis rats. Afr J Tradit Complement Altern Med. 2014;11:213–21.CrossRef Yang Q, Xu Y, Feng G, Hu C, Zhang Y, Cheng S, Wang Y, Gong X. p38 MAPK signal pathway involved in anti-inflammatory effect of Chaihu-Shugan-san and Shen-ling-bai-zhu-san on hepatocyte in non-alcoholic steatohepatitis rats. Afr J Tradit Complement Altern Med. 2014;11:213–21.CrossRef
37.
go back to reference Kanmani P, Clua P, Vizoso-Pinto MG, Rodriguez C, Alvarez S, Melnikov V, Takahashi H, Kitazawa H, Villena J. Respiratory commensal Bacteria Corynebacterium pseudodiphtheriticum improves resistance of infant mice to respiratory syncytial virus and Streptococcus pneumoniae Superinfection. Front Microbiol. 2017;8:1613.CrossRef Kanmani P, Clua P, Vizoso-Pinto MG, Rodriguez C, Alvarez S, Melnikov V, Takahashi H, Kitazawa H, Villena J. Respiratory commensal Bacteria Corynebacterium pseudodiphtheriticum improves resistance of infant mice to respiratory syncytial virus and Streptococcus pneumoniae Superinfection. Front Microbiol. 2017;8:1613.CrossRef
38.
go back to reference Dubourg G, Lagier JC, Armougom F, Robert C, Hamad I, Brouqui P, Raoult D. The gut microbiota of a patient with resistant tuberculosis is more comprehensively studied by culturomics than by metagenomics. Eur J Clin Microbiol Infect Dis. 2013;32:637–45.CrossRef Dubourg G, Lagier JC, Armougom F, Robert C, Hamad I, Brouqui P, Raoult D. The gut microbiota of a patient with resistant tuberculosis is more comprehensively studied by culturomics than by metagenomics. Eur J Clin Microbiol Infect Dis. 2013;32:637–45.CrossRef
39.
go back to reference Gauguet S, D'Ortona S, Ahnger-Pier K, Duan B, Surana NK, Lu R, Cywes-Bentley C, Gadjeva M, Shan Q, Priebe GP, Pier GB. Intestinal microbiota of mice influences resistance to Staphylococcus aureus pneumonia. Infect Immun. 2015;83:4003–14.CrossRef Gauguet S, D'Ortona S, Ahnger-Pier K, Duan B, Surana NK, Lu R, Cywes-Bentley C, Gadjeva M, Shan Q, Priebe GP, Pier GB. Intestinal microbiota of mice influences resistance to Staphylococcus aureus pneumonia. Infect Immun. 2015;83:4003–14.CrossRef
40.
go back to reference Felix KM, Jaimez IA, Nguyen TV, Ma H, Raslan WA, Klinger CN, Doyle KP, Wu HJ. Gut microbiota contributes to resistance against pneumococcal pneumonia in Immunodeficient rag(−/−) mice. Front Cell Infect Microbiol. 2018;8:118.CrossRef Felix KM, Jaimez IA, Nguyen TV, Ma H, Raslan WA, Klinger CN, Doyle KP, Wu HJ. Gut microbiota contributes to resistance against pneumococcal pneumonia in Immunodeficient rag(−/−) mice. Front Cell Infect Microbiol. 2018;8:118.CrossRef
41.
go back to reference Shi Y, Zhai Q, Li D, Mao B, Liu X, Zhao J, Zhang H, Chen W. Restoration of cefixime-induced gut microbiota changes by Lactobacillus cocktails and fructooligosaccharides in a mouse model. Microbiol Res. 2017;200:14–24.CrossRef Shi Y, Zhai Q, Li D, Mao B, Liu X, Zhao J, Zhang H, Chen W. Restoration of cefixime-induced gut microbiota changes by Lactobacillus cocktails and fructooligosaccharides in a mouse model. Microbiol Res. 2017;200:14–24.CrossRef
42.
go back to reference Lv W, Liu C, Ye C, Sun J, Tan X, Zhang C, Qu Q, Shi D, Guo S. Structural modulation of gut microbiota during alleviation of antibiotic-associated diarrhea with herbal formula. Int J Biol Macromol. 2017;105:1622–9.CrossRef Lv W, Liu C, Ye C, Sun J, Tan X, Zhang C, Qu Q, Shi D, Guo S. Structural modulation of gut microbiota during alleviation of antibiotic-associated diarrhea with herbal formula. Int J Biol Macromol. 2017;105:1622–9.CrossRef
Metadata
Title
Shen-ling-bai-zhu-san ameliorates inflammation and lung injury by increasing the gut microbiota in the murine model of Streptococcus pneumonia-induced pneumonia
Authors
Jinli Feng
Weibo Dai
Cheng Zhang
Houjun Chen
Ziliang Chen
Yongfeng Chen
Qianyi Pan
Yongmao Zhou
Publication date
01-12-2020
Publisher
BioMed Central
Published in
BMC Complementary Medicine and Therapies / Issue 1/2020
Electronic ISSN: 2662-7671
DOI
https://doi.org/10.1186/s12906-020-02958-9

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