Skip to main content

Advertisement

SpringerLink
Log in

Bifidobacterium animalis subsp. lactis HN019 has antimicrobial activity against endodontic pathogens in vitro

  • Human Microbiome - Research Paper
  • Published:
Brazilian Journal of Microbiology Aims and scope Submit manuscript

Abstract

The aim of the present study was to evaluate, in vitro, the antimicrobial activity of the probiotic Bifidobacterium animalis subsp. lactis HN019, through the well technique, against 10 microorganisms can be found involved in endodontic infections. The antimicrobial activity of the probiotic was performed on Streptococcus mutans, Streptococcus sobrinus, Lacticaseibacillus casei, Enterococcus faecalis, Staphylococcus aureus, Candida albicans, Porphyromonas gingivalis, Porphyromonas endodontalis, Fusobacterium nucleatum and Prevotella intermedia. For the control group, it was used non-pathogenic bacteria Escherichia coli, Saccharomyces cerevisiae, and Kocuria rizhopilla. After 48 to 72 h of incubation of the petri dishes containing the culture medium, the microorganism strains, and the probiotic, the plates were examined to assess the uniformity of microbial growth, presence of contaminants, and the halo of inhibition. After visual inspection, the reading of the halo of inhibition was performed with the aid of a digital caliper using a reflected light source to illuminate the inverted plate on a black, opaque background after removing the cap. Thus, 3 values were obtained from each bacterial inoculum, which were added and divided by three to obtain the average of the values. The results of the in vitro study demonstrated that the probiotic B. animalis subsp. lactis HN019 promoted the inhibition of all strains of the pathogens evaluated, with the exception of Candida albicans, demonstrating antimicrobial activity on these microorganisms.

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

Similar content being viewed by others

Data Availability

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

References

  1. Food and Agriculture Organization and World Health Organization Expert Consultation (2001) Evaluation of health and nutritional properties of powder milk and live lactic acid bacteria. Córdoba, Argentina: Food and Agriculture Organization of the United Nations and World Health Organization; [cited 2005 September 8]. Available from: ftp://ftp.fao.org/es/esn/food/probio_report_en.pdf

  2. Mahasneh SA, Mahasneh AD (2017) Probiotics: a promising role in dental health. Dent J 5(4):26. https://doi.org/10.3390/dj5040026

    Article  Google Scholar 

  3. Keller MK, Hasslöf P, Dahlén G, Stecksén-Blicks G, Twetman S (2012) Probiotic supplements (lactobacillus reuteri dsm 17938 and atcc pta 5289) do not affect regrowth of mutans streptococci after full-mouth disinfection with chlorhexidine: a randomized controlled multicenter trial. Caries Res 46:140–146. https://doi.org/10.1159/000337098

    Article  CAS  PubMed  Google Scholar 

  4. McCabe LR, Parameswaran N (2018) Advances in probiotic regulation of bone and mineral metabolism. Calcif Tissue Int 102:480–488. https://doi.org/10.1007/s00223-018-0403-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Aggarwal N, Breedon AME, Davis CM, Hwang IY, Chang MW (2020) Engineering probiotics for therapeutic applications: recent examples and translational outlook. Curr Opin Biotechnol 65:171–179. https://doi.org/10.1016/j.copbio.2020.02.016

    Article  CAS  PubMed  Google Scholar 

  6. Singh D, Khan MA, Siddique HR (2021) Therapeutic implications of probiotics in microbiota dysbiosis: a special reference to the liver and oral cancers. Life Sci 285:120008. https://doi.org/10.1016/j.lfs.2021.120008

    Article  CAS  PubMed  Google Scholar 

  7. Twetman L, Larsen U, Fiehn NE, Stecksén-Blicks C, Twetman S (2009) Coaggregation between probiotic bacteria and caries-associated strains: an in vitro study. Acta Odontol Scand 67:284–288. https://doi.org/10.1080/00016350902984237

    Article  PubMed  Google Scholar 

  8. Islam SU (2016) Clinical uses of probiotics. Medicine (Baltimore) 95(5):e2658. https://doi.org/10.1097/MD.0000000000002658

    Article  PubMed  Google Scholar 

  9. Meurman JH, Stamatova IV (2018) Probiotics: evidence of oral health implications. Folia Med (Plovdiv) 60:21–29. https://doi.org/10.1515/folmed-2017-0080

    Article  PubMed  Google Scholar 

  10. Butler MI, Mörkl S, Sandhu KV, Cryan JF, Dinan TG (2019) The gut microbiome and mental health: what should we tell our patients?: Le microbiote Intestinal et la Santé Mentale : que Devrions-Nous dire à nos Patients? Can J Psychiatry 64(11):747–760. https://doi.org/10.1177/0706743719874168

    Article  PubMed  PubMed Central  Google Scholar 

  11. Seminario-Amez M, López-López J, Estrugo-Devesa A, Ayuso-Montero R, Jané-Salas E (2017) Probiotics and oral health: a systematic review. Med Oral Patol Oral Cir Bucal 22(3):e282–e288. https://doi.org/10.4317/medoral.21494

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Radaic A, Ye C, Parks B, Gao L, Kuraji R, Malone E, Kamarajan P, Zhan L, Kapila YL (2020) Modulation of pathogenic oral biofilms towards health with nisin probiotic. J Oral Microbiol 12(1):1809302. https://doi.org/10.1080/20002297.2020.1809302

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Hirasawa M, Kurita-Ochia T (2020) Probiotic potential of Lactobacilli isolated from saliva of periodontally healthy individuals. Oral Health Prev Dent 18(1):563–570. https://doi.org/10.3290/j.ohpd.a44693

    Article  PubMed  Google Scholar 

  14. Vestman N, Chen T, Lif Holgerson P, Öhman C, Johansson I (2015) Oral microbiota shift after 12-week supplementation with Lactobacillus reuteri DSM 17938 and PTA 5289: a randomized control trial. PLoS One 6(10):e0125812. https://doi.org/10.1371/journal.pone.0125812

    Article  CAS  Google Scholar 

  15. Bustamante M, Oomah BD, Mosi-Roa Y, Rubilar M, Burgos-Díaz C (2020) Probiotics as an adjunct therapy for the treatment of halitosis, dental caries and periodontitis. Probiotics Antimicrob Proteins 12(2):325–334. https://doi.org/10.1007/s12602-019-9521-4

    Article  CAS  PubMed  Google Scholar 

  16. Kraft-Bodi E, Jørgensen MR, Keller MK, Kragelund C, Twetman S (2015) Effect of probiotic bacteria on oral Candida in frail elderly. J Dent Res 94(9 Suppl):181S–186S. https://doi.org/10.1177/0022034515595950

    Article  CAS  PubMed  Google Scholar 

  17. Matsubara VH, Bandara HM, Mayer MP, Samaranayake LP (2016) Probiotics as antifungals in mucosal candidiasis. Clin Infect Dis 62(9):1143–1153. https://doi.org/10.1093/cid/ciw038

    Article  PubMed  Google Scholar 

  18. York A (2019) A probiotic for candidiasis? Nat Rev Microbiol 17(12):723. https://doi.org/10.1038/s41579-019-0296-0

    Article  CAS  PubMed  Google Scholar 

  19. Keller MK, Hasslöf P, Stecksén-Blicks C, Twetman S (2011) Co-aggregation and growth inhibition of probiotic lactobacilli and clinical isolates of mutans streptococci: an in vitro study. Acta Odontol Scand 69:263–268. https://doi.org/10.3109/00016357.2011.554863

    Article  PubMed  Google Scholar 

  20. Jiang Q, Stamatova I, Kainulainen V, Korpela R, Meurman JH (2016) Interactions between Lactobacillus rhamnosus GG and oral micro-organisms in an in vitro biofilm model. BMC Microbiol 12(16):149. https://doi.org/10.1186/s12866-016-0759-7

    Article  CAS  Google Scholar 

  21. Lin TH, Lin CH, Pan TM (2018) The implication of probiotics in the prevention of dental caries. Appl Microbiol Biotechnol 102(2):577–586. https://doi.org/10.1007/s00253-017-8664-z

    Article  CAS  PubMed  Google Scholar 

  22. Zaura E, Twetman S (2019) Critical appraisal of oral pre- and probiotics for caries prevention and care. Caries Res 53(5):514–526. https://doi.org/10.1159/000499037

    Article  PubMed  Google Scholar 

  23. Ricoldi MST, Furlaneto FAC, Oliveira LFF, Teixeira GC, Pischiotini JP, Moreira ALG, Ervolino E, de Oliveira MN, Bogsan CSB, Salvador SL, Messora MR (2017) Effects of the probiotic Bifidobacterium animalis subsp. lactis on the non-surgical treatment of periodontitis. A histomorphometric, microtomographic and immunohistochemical study in rats. PLoS One 12(6). https://doi.org/10.1371/journal.pone.0179946

  24. Morales A, Gandolfo A, Bravo J, Carvajal P, Silva N, Godoy C, Garcia-Sesnich J, Hoare A, Diaz P, Gamonal J (2018) Microbiological and clinical effects of probiotics and antibiotics on nonsurgical treatment of chronic periodontitis: a randomized placebo- controlled trial with 9-month follow-up. J Appl Oral Sci 26:e20170075. https://doi.org/10.1590/1678-7757-2017-0075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Schmitter T, Fiebich BL, Fischer JT, Gajfulin M, Larsson N, Rose T, Goetz MR (2018) Ex vivo anti- inflammatory effects of probiotics for periodontal health. J Oral Microbiol 25(10):1502027. https://doi.org/10.1080/20002297.2018.1502027

    Article  CAS  Google Scholar 

  26. Messora MR, Oliveira LF, Foureaux RC, Taba M Jr, Zangerônimo MG, Furlaneto FA, Pereira LJ (2013) Probiotic therapy reduces periodontal tissue destruction and improves the intestinal morphology in rats with ligature-induced periodontitis. J Periodontol 84(12):1818–1826. https://doi.org/10.1902/jop.2013.120644

    Article  PubMed  Google Scholar 

  27. Grusovin MG, Bossini S, Calza S, Cappa V, Garzetti G, Scotti E, Gherlone EF, Mensi M (2020) Clinical efficacy of Lactobacillus reuteri-containing lozenges in the supportive therapy of generalized periodontitis stage III and IV, grade C: 1-year results of a double-blind randomized placebo-controlled pilot study. Clin Oral Investig 24(6):2015–2024. https://doi.org/10.1007/s00784-019-03065-x

    Article  PubMed  Google Scholar 

  28. Messora MR, Pereira LJ, Foureaux R, Oliveira LF, Sordi CG, Alves AJ, Napimoga MH, Nagata MJ, Ervolino E, Furlaneto FA (2016) Favourable effects of Bacillus subtilis and Bacillus licheniformis on experimental periodontitis in rats. Arch Oral Biol 66:108–119. https://doi.org/10.1016/j.archoralbio.2016.02.014

    Article  PubMed  Google Scholar 

  29. Oliveira LF, Salvador SL, Silva PHF, Furlaneto FAC, Figueiredo L, Casarin R, Ervolino E, Palioto DB, Souza SLS, Taba MJ, Novaes ABNJ, Messora MR (2017) Benefits of Bifidobacterium animalis subsp. lactis Probiotic in Experimental Periodontitis. J Periodontol 88:197–208. https://doi.org/10.1902/jop.2016.160217

    Article  PubMed  Google Scholar 

  30. Luo W, Li H, Ye F (2021) Clinical therapeutic effects of probiotics in combination with antibiotics on periodontitis: a protocol for systematic review and meta-analysis. Medicine (Baltimore) 100(4):e23755. https://doi.org/10.1097/MD.0000000000023755

    Article  CAS  PubMed  Google Scholar 

  31. Gomez A, Nelson KE (2017) The oral microbiome of children: development, disease, and implications beyond oral health. Microb Ecol 73(2):492–503. https://doi.org/10.1007/s00248-016-0854-1

    Article  CAS  PubMed  Google Scholar 

  32. Sharma N, Bhatia S, Sodhi AS, Batra N (2018) Oral microbiome and health. AIMS Microbiol 4(1):42–66. https://doi.org/10.3934/microbiol.2018.1.42

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Belibasakis GN, Bostanci N, Marsh PD, Zaura E (2019) Applications of the oral microbiome in personalized dentistry. Arch Oral Biol 104:7–12. https://doi.org/10.1016/j.archoralbio.2019.05.023

    Article  PubMed  Google Scholar 

  34. Xiao J, Fiscella KA, Gill SR (2020) Oral microbiome: possible harbinger for children’s health. Int J Oral Sci 12(1):12. https://doi.org/10.1038/s41368-020-0082-x

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Sasaki H, Okamatsu Y, Kawai T, Kent R, Taubman M, Stashenko P (2004) The interleukin-10 knockout mouse is highly susceptible to Porphyromonas gingivalis-induced alveolar bone loss. J Periodontal Res 39:432–441. https://doi.org/10.1111/j.1600-0765.2004.00760.x

    Article  CAS  PubMed  Google Scholar 

  36. Neelakantan P, Romero M, Vera J, Daood U, Khan AU, Yan A, Cheung GSP (2017) Biofilms in endodontics-current status and future directions. Int J Mol Sci 18(8):1748. https://doi.org/10.3390/ijms18081748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Iqbal A (2012) Antimicrobial irrigants in the endodontic therapy. Int J Health Sci 6:186–192

    Google Scholar 

  38. Marsh PD (2010) Microbiology of dental plaque biofilms and their role in oral health and caries. Dent Clin N Am 54:441–454. https://doi.org/10.1016/j.cden.2010.03.002

    Article  PubMed  Google Scholar 

  39. Allaker RP, Stephen AS (2017) Use of probiotics and oral health. Curr Oral Health Rep 4:309–318. https://doi.org/10.1007/s40496-017-0159-6

    Article  PubMed  PubMed Central  Google Scholar 

  40. Samaranayake L, Matsubara VH (2017) Normal oral flora and the oral ecosystem. Dent Clin N Am 61:199–215. https://doi.org/10.1016/j.cden.2016.11.002

    Article  PubMed  Google Scholar 

  41. Brook I (2003) Microbiology and management of endodontic infections in children. J Clin Pediatr Dent 28:13–18. https://doi.org/10.17796/jcpd.28.1.uwjxq61753506255

    Article  PubMed  Google Scholar 

  42. Siqueira JF, Roças I (2014) Present status and future directions in endodontic microbiology. Endod Topics 30:3–22. https://doi.org/10.1111/iej.13677

    Article  Google Scholar 

  43. Bohora A, Kokate S (2017) Evaluation of the role of probiotics in endodontic treatment: a preliminary study. J Int Soc Prev Community Dent 7(1):46–51. https://doi.org/10.4103/2231-0762.200710

    Article  PubMed  PubMed Central  Google Scholar 

  44. Bohora AA, Kokate SR, Khedkar S, Vankudre A (2019) Antimicrobial activity of probiotics against endodontic pathogens: - a preliminary study. Indian J Med Microbiol 37(1):5–11. https://doi.org/10.4103/ijmm.IJMM_18_333

    Article  PubMed  Google Scholar 

  45. El-Sayed H, Aly Y, Elgamily H, Nagy MM (2019) A promising probiotic irrigant: an in vitro study. Open Access Maced J Med Sci 7(3):407–411. https://doi.org/10.3889/oamjms.2019.074

    Article  PubMed  PubMed Central  Google Scholar 

  46. Cosme-Silva L, Dal-Fabbro R, Cintra LTA, Dos Santos VR, Duque C, Ervolino E, Mogami Bomfim S, Gomes-Filho JE (2019) Systemic administration of probiotics reduces the severity of apical periodontitis. Int Endod J 52(12):1738–1749. https://doi.org/10.1111/iej.13192

    Article  CAS  PubMed  Google Scholar 

  47. Cosme-Silva L, Dal-Fabbro R, Cintra LTA, Ervolino E, Plazza F, Mogami Bomfim S, Duarte PCT, Junior VEDS, Gomes-Filho JE (2020) Reduced bone resorption and inflammation in apical periodontitis evoked by dietary supplementation with probiotics in rats. Int Endod J 53(8):1084–1092. https://doi.org/10.1111/iej.13311

    Article  CAS  PubMed  Google Scholar 

  48. Kumar G, Tewari S, Tagg J, Chikindas ML, Popov IV, Tiwari SK (2021) Can probiotics emerge as effective therapeutic agents in apical periodontitis? A review. Probiotics Antimicrob Proteins 13(2):299–314. https://doi.org/10.1007/s12602-021-09750-2

    Article  CAS  PubMed  Google Scholar 

  49. Rakhimova O, Schmidt A, Landström M, Johansson A, Kelk P, Romani Vestman N (2021) Cytokine secretion, viability, and real-time proliferation of apical-papilla stem cells upon exposure to oral bacteria. Front Cell Infect Microbiol 10:620801. https://doi.org/10.3389/fcimb.2020.620801

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Invernici MM, Furlaneto FAC, Salvador SL, Ouwehand AC, Salminen S, Mantziari A, Vinderola G, Ervolino E, Santana SI, Silva PHF, Messora MR (2020) Bifidobacterium animalis subsp. lactis HN019 presents antimicrobial potential against periodontopathogens and modulates the immunological response of oral mucosa in periodontitis patients. PLoS One 15(9):e0238425. https://doi.org/10.1371/journal.pone.0238425

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Vives-Soler A, Chimenos-Küstner E (2020) Effect of probiotics as a complement to non-surgical periodontal therapy in chronic periodontitis: a systematic review. Med Oral Patol Oral Cir Bucal 25(2):e161–e167. https://doi.org/10.4317/medoral.23147

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Hu L, Zhou M, Young A, Zhao W, Yan Z (2019) In vivo effectiveness and safety of probiotics on prophylaxis and treatment of oral candidiasis: a systematic review and meta-analysis. BMC Oral Health 19(1):140. https://doi.org/10.1186/s12903-019-0841-2

    Article  PubMed  PubMed Central  Google Scholar 

  53. Cheng B, Zeng X, Liu S, Zou J, Wang Y (2020) The efficacy of probiotics in management of recurrent aphthous stomatitis: a systematic review and meta-analysis. Sci Rep 10(1):21181. https://doi.org/10.1038/s41598-020-78281-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. İnce G, Gürsoy H, İpçi ŞD, Cakar G, Emekli-Alturfan E, Yılmaz S (2015) Clinical and biochemical evaluation of lozenges containing Lactobacillus reuteri as an adjunct to non-surgical periodontal therapy in chronic periodontitis. J Periodontol 86(6):746–754. https://doi.org/10.1902/jop.2015.140612

    Article  PubMed  Google Scholar 

  55. Tekce M, Ince G, Gursoy H, Dirikan Ipci S, Cakar G, Kadir T, Yılmaz S (2015) Clinical and microbiological effects of probiotic lozenges in the treatment of chronic periodontitis: a 1-year follow-up study. J Clin Periodontol 42(4):363–372. https://doi.org/10.1111/jcpe.12387

    Article  PubMed  Google Scholar 

  56. Morales A, Carvajal P, Silva N, Hernandez M, Godoy C, Rodriguez G, Cabello R, Garcia-Sesnich J, Hoare A, Diaz PI, Gamonal J (2016) Clinical effects of Lactobacillus rhamnosus in non-surgical treatment of chronic periodontitis: a randomized placebo-controlled trial with 1-year follow-up. J Periodontol 87(8):944–952. https://doi.org/10.1902/jop.2016.150665

    Article  PubMed  Google Scholar 

  57. Gill HS, Rutherfurd KJ, Prasad J, Gopal PK (2000) Enhancement of natural and acquired immunity by Lactobacillus rhamnosus (HN001), Lactobacillus acidophilus (HN017) and Bifidobacterium lactis (HN019). Br J Nutr 83(2):167–176. https://doi.org/10.1017/s0007114500000210

    Article  CAS  PubMed  Google Scholar 

  58. Toiviainen A, Jalasvuori H, Lahti E, Gursoy U, Salminen S, Fontana M, Flannagan S, Eckert G, Kokaras A, Paster B, Söderling E (2015) Impact of orally administered lozenges with Lactobacillus rhamnosus GG and Bifidobacterium animalis subsp. lactis BB-12 on the number of salivary mutans streptococci, amount of plaque, gingival inflammation and the oral microbiome in healthy adults. Clin Oral Investig 19(1):77–83. https://doi.org/10.1007/s00784-014-1221-6

    Article  PubMed  Google Scholar 

  59. Dahlén G (2017) Culture-based analysis of endodontic infections. In: Fouad AF (ed) Endodontic microbiology, 2nd edn. Wiley, New York, pp 57–79

    Google Scholar 

  60. Hernández-Bautista LM, Márquez-Preciado R, Ortiz-Magdaleno M, Pozos-Guillén A, Aranda-Romo S, Sánchez-Vargas LO (2020) Effect of five commercial probiotic formulations on Candida albicans growth: in vitro study. J Clin Pediatr Dent 44(5):315–322. https://doi.org/10.17796/1053-4625-44.5.5

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Pediatric Dentistry, Faculty of Dentistry of Ribeirão Preto, University of São Paulo, Ribeirão Preto, Brazil

    Lisa Danielly Curcino Araujo, Raquel Assed Bezerra da Silva, Clara Marina Pereira Cavalcanti Silva, Carolina Maschietto Pucinelli & Léa Assed Bezerra da Silva

  2. Department of Clinical Analyses, School of Pharmaceutical Sciences of Ribeirão Preto, University of São Paulo, Ribeirão Preto, Brazil

    Sérgio Luiz Sousa Salvador & Marina Del Arco Mastrange

  3. Department of Oral and Maxillofacial Surgery and Periodontology, School of Dentistry of Ribeirão Preto, University of São Paulo, Ribeirão Preto, Brazil

    Michel Reis Messora & Flávia Aparecida Chaves Furlaneto

Authors
  1. Lisa Danielly Curcino Araujo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Raquel Assed Bezerra da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Clara Marina Pereira Cavalcanti Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sérgio Luiz Sousa Salvador
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Michel Reis Messora
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Flávia Aparecida Chaves Furlaneto
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marina Del Arco Mastrange
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Carolina Maschietto Pucinelli
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Léa Assed Bezerra da Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Lisa Danielly Curcino Araujo.

Ethics declarations

Conflict of interest

The authors declare no competing interests.

Additional information

Responsible Editor: Carla Taddei

Publisher’s note

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

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Araujo, L.D.C., da Silva, R.A.B., Silva, C.M.P.C. et al. Bifidobacterium animalis subsp. lactis HN019 has antimicrobial activity against endodontic pathogens in vitro. Braz J Microbiol 54, 2289–2295 (2023). https://doi.org/10.1007/s42770-023-01083-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s42770-023-01083-2

Keywords

Search

Navigation