Skip to main content
SpringerLink
Log in

Effects of Dietary Supplementation with Lactobacillus acidophilus and Bacillus subtilis on Mucosal Immunity and Intestinal Barrier Are Associated with Its Modulation of Gut Metabolites and Microbiota in Late-Phase Laying Hens

  • Published:
Probiotics and Antimicrobial Proteins Aims and scope Submit manuscript

Abstract

We investigated the effects of dietary supplementation with Lactobacillus acidophilus and Bacillus subtilis on the intestinal immune response, intestinal barrier function, cecal microbiota profile, and metabolite profile in late-phase laying hens. Hens were divided into three groups and fed with the basal diet (NC group), basal diet supplementation with 250 mg/kg B. subtilis and L. acidophilus mixture powder (LD group), and basal diet supplementation with 500 mg/kg B. subtilis and L. acidophilus mixture powder (HD group), respectively. The results indicated that the dietary supplementation with L. acidophilus and B. subtilis increased the integrity of the intestinal barrier as evidenced by the significant increase in the number of ileal goblet cells and improve the expression of occludin, claudin-1, and ZO-1 genes in the HD group. Moreover, the levels of IL-6, TNF-α, and IFN-γ were significantly decreased in the LD and HD groups. The levels of immunoglobulin G (IgG) increased in the LD and HD group, and the levels of secretory immunoglobulin A (sIgA) increased with the HD treatment. Furthermore, 16 s rRNA sequencing revealed L. acidophilus in combination with B. subtilis increased the diversity of gut microbiota. The metabolomic analysis revealed beneficial changes in the amino acid metabolism and lipid metabolism (decrease in LysoPC and LysoPE levels). In conclusion, dietary supplementation with L. acidophilus and B. subtilis could improve intestinal barrier function and maintain immune homeostasis. These beneficial effects may be associated with the modulation of the intestinal microbiome and metabolites.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Data Availability

The datasets used or analyzed during the current study are available from the corresponding author on reasonable request.

References

  1. Ge YT, Lin SM, Li BW, Yang YH, Tang X, Shi YH, Sun J, Le GW (2020) Oxidized pork induces oxidative stress and inflammation by altering gut microbiota in mice. Mol Nutr Food Res 64(2):e1901012. https://doi.org/10.1002/mnfr.201901012

    Article  CAS  PubMed  Google Scholar 

  2. Li X, Mao MY, Zhang YN, Yu KF, Zhu WY (2019) Succinate modulates intestinal barrier function and inflammation response in pigs. Biomolecules 9(9):486. https://doi.org/10.3390/biom9090486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Bron PA, Kleerebezem M, Brummer RJ, Cani PD, Mercenier A, MacDonald TT, Garcia-Rodenas CL, Wells JM (2017) Can probiotics modulate human disease by impacting intestinal barrier function? Br J Nutr 117(1):93–107. https://doi.org/10.1017/S0007114516004037

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  4. Paone P, Cani PD (2020) Mucus barrier, mucins and gut microbiota: the expected slimy partners? Gut 69(12):2232–2243. https://doi.org/10.1136/gutjnl-2020-322260

    Article  CAS  PubMed  Google Scholar 

  5. Honda K, Littman DR (2016) The microbiota in adaptive immune homeostasis and disease. Nature 535(7610):75–84. https://doi.org/10.1038/nature18848

    Article  CAS  PubMed  Google Scholar 

  6. Johansson ME, Hansson GC (2016) Immunological aspects of intestinal mucus and mucins. Nat Rev Immunol 16(10):639–649. https://doi.org/10.1038/nri.2016.88

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Kayama H, Okumura R, Takeda K (2020) Interaction between the microbiota, epithelia, and immune cells in the intestine. Annu Rev Immunol 38:23–48. https://doi.org/10.1146/annurev-immunol-070119-115104

    Article  CAS  PubMed  Google Scholar 

  8. Ji YY, Groer M, Dutra SVO, Sarkar A, McSkimming DI (2020) Gut microbiota and immune system interactions. Microorganisms 8(10):1587. https://doi.org/10.3390/microorganisms8101587

    Article  CAS  Google Scholar 

  9. Gu YF, Chen YP, Jin R, Wang C, Wen C, Zhou YM (2021) A comparison of intestinal integrity, digestive function, and egg quality in laying hens with different ages. Poult Sci 100(3):100949. https://doi.org/10.1016/j.psj.2020.12.046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Arnold JW, Roach J, Fabela S, Moorfield E, Ding S, Blue E, Dagher S, Magness S, Tamayo R, Bruno-Barcena JM et al (2021) The pleiotropic effects of prebiotic galacto-oligosaccharides on the aging gut. Microbiome 9(1):31. https://doi.org/10.1186/s40168-020-00980-0

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Li J, Wu T, Li N, Wang XN, Chen GY, Lyu XL (2019) Bilberry anthocyanin extract promotes intestinal barrier function and inhibits digestive enzyme activity by regulating the gut microbiota in aging rats. Food Funct 10(1):333–343. https://doi.org/10.1039/c8fo01962b

    Article  CAS  PubMed  Google Scholar 

  12. Pan J, Yin J, Zhang K, Xie PF, Ding H, Huang XG, Blachier F, Kong XF (2019) Dietary xylo-oligosaccharide supplementation alters gut microbial composition and activity in pigs according to age and dose. AMB Express 9(1):134. https://doi.org/10.1186/s13568-019-0858-6

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Wang YY, Heng C, Zhou XH, Cao GT, Jiang L, Wang JS, Li KX, Wang DC, Zhan XA (2021) Supplemental Bacillus subtilis DSM 29784 and enzymes, alone or in combination, as alternatives for antibiotics to improve growth performance, digestive enzyme activity, anti-oxidative status, immune response and the intestinal barrier of broiler chickens. Br J Nutr 125(5):494–507. https://doi.org/10.1017/S0007114520002755

    Article  CAS  PubMed  Google Scholar 

  14. Liu ZH, Ma YL, Shen TY, Chen HQ, Zhou YK, Zhang P, Zhang M, Chu ZX, Qin HL (2010) Identification of DC-SIGN as the receptor during the interaction of Lactobacillus plantarum CGMCC 1258 and dendritic cells. World J Microbiol Biotechnol 27(3):603–611. https://doi.org/10.1007/s11274-010-0495-3

    Article  CAS  Google Scholar 

  15. Xie JH, Nie SP, Yu Q, Yin JY, Xiong T, Gong DM, Xie MY (2016) Lactobacillus plantarum NCU116 attenuates cyclophosphamide-induced immunosuppression and regulates Th17/Treg cell immune responses in mice. J Agric Food Chem 64(6):1291–1297. https://doi.org/10.1021/acs.jafc.5b06177

    Article  CAS  PubMed  Google Scholar 

  16. Dowarah R, Verma AK, Agarwal N, Singh P, Singh BR (2018) Selection and characterization of probiotic lactic acid bacteria and its impact on growth, nutrient digestibility, health and antioxidant status in weaned piglets. PLoS One 13(3):e0192978. https://doi.org/10.1371/journal.pone.0192978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Chen YQ, Ouyang XY, Laaksonen O, Liu XY, Shao Y, Zhao HF, Zhang BL, Zhu BQ (2019) Effect of Lactobacillus acidophilus, Oenococcus oeni, and Lactobacillus brevis on composition of bog bilberry juice. Foods 8(10):430. https://doi.org/10.3390/foods8100430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Cutting SM (2011) Bacillus probiotics. Food Microbiol 28(2):214–220. https://doi.org/10.1016/j.fm.2010.03.007

    Article  PubMed  Google Scholar 

  19. He YJ, Jinno C, Kim K, Wu ZH, Tan B, Li XD, Whelan R, Liu YH (2020) Dietary Bacillus spp. enhanced growth and disease resistance of weaned pigs by modulating intestinal microbiota and systemic immunity. J Anim Sci Biotechnol 11(1):101. https://doi.org/10.1186/s40104-020-00498-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Chapman CM, Gibson GR, Rowland I (2011) Health benefits of probiotics: are mixtures more effective than single strains? Eur J Nutr 50(1):1–17. https://doi.org/10.1007/s00394-010-0166-z

    Article  CAS  PubMed  Google Scholar 

  21. Liu X, Xia B, He T, Li D, Su JH, Guo L, Wang JF, Zhu YH (2019) Oral administration of a select mixture of Lactobacillus and Bacillus alleviates inflammation and maintains mucosal barrier integrity in the ileum of pigs challenged with Salmonella infantis. Microorganisms 7(5):135. https://doi.org/10.3390/microorganisms7050135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Perini MP, Rentas MF, Pedreira R, Amaral AR, Zafalon RVA, Rodrigues RBA, Henriquez LBF, Zanini L, Vendramini THA, Balieiro JCC et al (2020) Duration of prebiotic intake is a key-factor for diet-induced modulation of immunity and fecal fermentation products in dogs. Microorganisms 8(12):1916. https://doi.org/10.3390/microorganisms8121916

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Ren HY, Liu TC, Lu YP, Zhang K, Xu Y, Zhou P, Tang X (2021) A comparison study of the influence of milk protein versus whey protein in high-protein diets on adiposity in rats. Food Funct 12(3):1008–1019. https://doi.org/10.1039/d0fo01960g

    Article  CAS  PubMed  Google Scholar 

  24. Li JJ, Zhang L, Li YF, Wu Y, Wu T, Feng H, Xu ZJ, Liu YH, Ruan Z, Zhou SC (2020) Puerarin improves intestinal barrier function through enhancing goblet cells and mucus barrier. J Funct Foods 75:10426. https://doi.org/10.1016/j.jff.2020.104246

    Article  CAS  Google Scholar 

  25. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262

    Article  CAS  PubMed  Google Scholar 

  26. Sarah JC, Simon RC (2018) Diet, the intestinal microbiota and immune health in aging. Crit Rev Food Sci Nutr 58(4):651–661. https://doi.org/10.1080/10408398.2016.1211086

    Article  Google Scholar 

  27. Hagan T, Cortese M, Rouphael N, Boudreau C, Linde C et al (2019) Antibiotics-driven gut microbiome perturbation alters immunity to vaccines in humans. Cell 178(6):1313–1328. https://doi.org/10.1016/j.cell.2019.08.010

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Feng J, Lu MY, Wang J, Zhang HJ, Qiu K, Qi GH, Wu SG (2021) Dietary oregano essential oil supplementation improves intestinal functions and alters gut microbiota in late-phase laying hens. J Anim Sci Biotechnol 12(1):72. https://doi.org/10.1186/s40104-021-00600-3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Ge HF, Cai ZZ, Chai JL, Liu JY, Liu BQ, Yu YD, Liu JB, Zhang T (2021) Egg white peptides ameliorate dextran sulfate sodium-induced acute colitis symptoms by inhibiting the production of pro-inflammatory cytokines and modulation of gut microbiota composition. Food Chem 360(30):129981. https://doi.org/10.1016/j.foodchem.2021.129981

    Article  CAS  PubMed  Google Scholar 

  30. Hu RJ, Lin H, Wang MM, Zhao YZ, Liu HJ, Min YN, Yang XJ, Gao YP, Yang MM (2021) Lactobacillus reuteri-derived extracellular vesicles maintain intestinal immune homeostasis against lipopolysaccharide-induced inflammatory responses in broilers. J Anim Sci Biotechnol 12(1):25. https://doi.org/10.1186/s40104-020-00532-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Ding MF, Yang B, Ross RP, Stanton C, Zhao JX, Zhang H, Chen W (2021) Crosstalk between sIgA-coated bacteria in infant gut and early-life health. Trends Microbiol 29(8):725–735. https://doi.org/10.1016/j.tim.2021.01.012

    Article  CAS  PubMed  Google Scholar 

  32. Zhuang Y, Wu HR, Wang XX, He JY, He SP, Yin YL (2019) Resveratrol attenuates oxidative stress-induced intestinal barrier injury through PI3K/Akt-mediated Nrf2 signaling pathway. Oxid Med Cell Longev 2019:7591840. https://doi.org/10.1155/2019/7591840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Lee SH (2015) Intestinal permeability regulation by tight junction: implication on inflammatory bowel diseases. Intest Res 13(1):11–18. https://doi.org/10.5217/ir.2015.13.1.11

    Article  PubMed  PubMed Central  Google Scholar 

  34. Khoder G, Al-Yassir F, Al Menhali A, Saseedharan P, Sugathan S, Tomasetto C, Karam SM (2019) Probiotics upregulate trefoil factors and downregulate pepsinogen in the mouse stomach. Int J Mol Sci 20(16):3901. https://doi.org/10.3390/ijms20163901

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Xie S, Zhao SY, Jiang L, Lu LH, Yang Q, Yu QH (2019) Lactobacillus reuteri stimulates intestinal epithelial proliferation and induces differentiation into goblet cells in young chickens. J Agric Food Chem 67(49):13758–13766. https://doi.org/10.1021/acs.jafc.9b06256

    Article  CAS  PubMed  Google Scholar 

  36. Wang WW, Wang J, Zhang HJ, Wu SG, Qi GH (2020) Effects of Clostridium butyricum on production performance and intestinal absorption function of laying hens in the late phase of production. Anim Feed Sci Technol 264:114476. https://doi.org/10.1016/j.anifeedsci.2020.114476

    Article  CAS  Google Scholar 

  37. Fouhse JM, Zijlstra RT, Willing BP (2016) The role of gut microbiota in the health and disease of pigs. Anim Front 6(3):30–36. https://doi.org/10.2527/af.2016-0031

    Article  Google Scholar 

  38. Hui Y, Tamez-Hidalgo P, Cieplak T, Satessa GD, Kot W, Kjaerulff S, Nielsen MO, Nielsen DS, Krych L (2021) Supplementation of a Lacto-fermented rapeseed-seaweed blend promotes gut microbial-and gut immune-modulation in weaner piglets. J Anim Sci Biotechnol 12(1):85. https://doi.org/10.1186/s40104-021-00601-2

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Galley JD, Mackos AR, Varaljay VA, Bailey MT (2017) Stressor exposure has prolonged effects on colonic microbial community structure in Citrobacter rodentium-challenged mice. Sci Rep 7:45012. https://doi.org/10.1038/srep45012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Yang M, Bose S, Lim S, Seo J, Shin J, Lee D, Chung WH, Song EJ, Nam YD, Kim H (2020) Beneficial effects of newly isolated Akkermansia muciniphila strains from the human gut on obesity and metabolic dysregulation. Microorganisms 8(9):1413. https://doi.org/10.3390/microorganisms8091413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Lee G, You HJ, Bajaj JS, Joo SK, Yu J, Park S, Kang H, Park JH, Kim JH, Lee DH et al (2020) Distinct signatures of gut microbiome and metabolites associated with significant fibrosis in non-obese NAFLD. Nat Commun 11(1):4982. https://doi.org/10.1038/s41467-020-18754-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Mazon-Moya MJ, Willis AR, Torraca V, Boucontet L, Shenoy AR, Colucci-Guyon E, Mostowy S (2017) Septins restrict inflammation and protect zebrafish larvae from Shigella infection. PLoS Pathog 13(6):e1006467. https://doi.org/10.1371/journal.ppat.1006467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Srisawat N, Tungsanga S, Lumlertgul N, Komaenthammasophon C, PeerapornratanaS TN, Tiranathanagul K, Praditpornsilpa K, Eiam-Ong S, Tungsanga K et al (2018) The effect of polymyxin B hemoperfusion on modulation of human leukocyte antigen DR in severe sepsis patients. Crit Care 22:279. https://doi.org/10.1186/s13054-018-2077-y

    Article  PubMed  PubMed Central  Google Scholar 

  44. Wang S, Ahmadi S, Nagpal R, Jain S, Mishra SP, Kavanagh K, Zhu X, Wang Z, McClain DA, Kritchevsky SB et al (2020) Lipoteichoic acid from the cell wall of a heat killed Lactobacillus paracasei D3–5 ameliorates aging-related leaky gut, inflammation and improves physical and cognitive functions: from C. elegans to mice. Geroscience 42(1):333–352. https://doi.org/10.1007/s11357-019-00137-4

    Article  CAS  PubMed  Google Scholar 

  45. Lu XM, Ce Q, Jin L, Zheng J, Sun M, Tang X, Li D, Sun J (2021) Deoiled sunflower seeds ameliorate depression by promoting the production of monoamine neurotransmitters and inhibiting oxidative stress. Food Funct 12(2):573–586. https://doi.org/10.1039/d0fo01978j

    Article  CAS  PubMed  Google Scholar 

  46. Dai D, Wu SG, Zhang HJ, Qi GH, Wang J (2020) Dynamic alterations in early intestinal development, microbiota and metabolome induced by in ovo feeding of L-arginine in a layer chick model. J Anim Sci Biotechnol 11(1):19. https://doi.org/10.1186/s40104-020-0427-5

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hui ST, Parks BW, Org E, Norheim F, Che N, Pan C, Castellani LW, Charugundla S, Dirks DL, Psychogios N et al (2015) The genetic architecture of NAFLD among inbred strains of mice. Elife 4:e05607. https://doi.org/10.7554/eLife.05607

    Article  PubMed  PubMed Central  Google Scholar 

  48. Zhang BB, Lv ZP, Li Z, Wang WW, Li G, Guo YM (2018) Dietary l-arginine supplementation alleviates the intestinal injury and modulates the gut microbiota in broiler chickens challenged by Clostridium perfringens. Front Microbiol 9:1716. https://doi.org/10.3389/fmicb.2018.01716

    Article  PubMed  PubMed Central  Google Scholar 

  49. Dahal RH, Nguyen TM, Shim DS, Kim JY, Lee J, Kim J (2020) Development of multifunctional cosmetic cream using bioactive materials from Streptomyces sp. T65 with synthesized mesoporous silica particles SBA-15. Antioxidants 9(4):27–28. https://doi.org/10.3390/antiox9040278

    Article  CAS  Google Scholar 

  50. Kim M, Yoo HJ, Ko J, Lee JH (2020) Metabolically unhealthy overweight individuals have high lysophosphatide levels, phospholipase activity, and oxidative stress. Clin Nutr 39(4):1137–1145. https://doi.org/10.1016/j.clnu.2019.04.025

    Article  CAS  PubMed  Google Scholar 

  51. Ha CY, Kim JY, Paik JK, Kim OY, Paik YH, Lee EJ, Lee JH (2012) The association of specific metabolites of lipid metabolism with markers of oxidative stress, inflammation and arterial stiffness in men with newly diagnosed type 2 diabetes. Clin Endocrinology 76(5):674–682. https://doi.org/10.1111/j.1365-2265.2011.04244.x

    Article  CAS  Google Scholar 

  52. Kim M, Yoo HJ, Lee D, Lee JH (2020) Oxidized LDL induces procoagulant profiles by increasing lysophosphatidylcholine levels, lysophosphatidylethanolamine levels, and Lp-PLA2 activity in borderline hypercholesterolemia. Nutr Metab Cardiovasc Dis 30(7):1137–1146. https://doi.org/10.1016/j.numecd.2020.03.015

    Article  CAS  PubMed  Google Scholar 

  53. Yang L, Zhang B, Wang X, Liu Z, Li J, Zhang S, Gu X, Jia M, Guo H, Feng N et al (2020) P53/PANK1/miR-107 signalling pathway spans the gap between metabolic reprogramming and insulin resistance induced by high-fat diet. J Cell Mol Med 24(6):3611–3624. https://doi.org/10.1111/jcmm.15053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Hong Y, Li B, Zheng N, Wu G, Ma J, Tao X, Chen L, Zhong J, Sheng L, Li H (2020) Integrated metagenomic and metabolomic analyses of the effect of astragalus polysaccharides on alleviating high-fat diet-induced metabolic disorders. Front Pharmacol 11:833. https://doi.org/10.3389/fphar.2020.00833

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Funding

The study was supported by Standard Foods (China) Co., Ltd, Jiangsu, P.R. China, and the National Key Research and Development Program of China (2017YFD0400600).

Author information

Authors and Affiliations

  1. Centre for Food Nutrition and Functional Food Engineering, School of Food Science and Technology, Jiangnan University, Jiangsu, 214122, China

    Xin Chen, Weiwen Chen, Wenjia Ci, Yingying Zheng & Jianjin Zhu

  2. Key Laboratory of Animal Nutrition and Feed Science in East China, Ministry of Agriculture, College of Animal Science, Zhejiang University, Hangzhou, 310058, China

    Xinyan Han

  3. Food Processing Technology Laboratory, School of Food Science and Technology, Jiangnan University, Jiangsu, 214122, China

    Jianping Huang

Authors
  1. Xin Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Weiwen Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Wenjia Ci
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yingying Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Xinyan Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jianping Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Jianjin Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Conceptualization, JJX, and XYH. Methodology, JJZ and XC. Validation, JJZ, XC, and WC. Formal analysis, WJC, YYZ. Data curation, JPH, and XC. Writing–original draft preparation, XC. Writing–review and editing, YYZ, XYH, and JJZ. Supervision, WWC and WJC. Funding acquisition, JJZ. All authors have read and agreed to the published version of the manuscript.

Corresponding author

Correspondence to Jianjin Zhu.

Ethics declarations

Ethics Approval

The Animal Care and Use Committee of Zhejiang University (permit number SYXK 2012–0178) approved all experimental protocol, and all animal research procedures of this study were performed based on the institutional guidelines.

Conflict of Interest

The authors declare no competing interests.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

Below is the link to the electronic supplementary material.

Supplementary file1 (DOCX 371 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Chen, X., Chen, W., Ci, W. et al. Effects of Dietary Supplementation with Lactobacillus acidophilus and Bacillus subtilis on Mucosal Immunity and Intestinal Barrier Are Associated with Its Modulation of Gut Metabolites and Microbiota in Late-Phase Laying Hens. Probiotics & Antimicro. Prot. 15, 912–924 (2023). https://doi.org/10.1007/s12602-022-09923-7

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12602-022-09923-7

Keywords

Search

Navigation