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Article

Topical Administration of Lactiplantibacillus plantarum Accelerates the Healing of Chronic Diabetic Foot Ulcers through Modifications of Infection, Angiogenesis, Macrophage Phenotype and Neutrophil Response

by
Julio Nicolás Argañaraz Aybar
1,
Sonia Ortiz Mayor
2,
Luis Olea
3,
Juan José Garcia
3,
Sebastian Nisoria
3,
Yanina Kolling
1,
Constanza Melian
1,
Mirta Rachid
1,
Rafael Torres Dimani
1,
Cecilia Werenitzky
4,
Cecilia Lorca
4,
Susana Salva
5,
Nadia Gobbato
1,
Julio Villena
5,* and
Juan C. Valdez
1,*
1
Cátedra de Inmunología, Instituto de Microbiología, Facultad de Bioquímica, Química y Farmacia, Universidad Nacional de Tucumán, San Miguel de Tucuman CP4000, Tucumán, Argentina
2
Laboratorio de Anatomía Patológica, Hospital Ángel C. Padilla, Sistema Provincial de Salud, San Miguel de Tucuman CP4000, Tucumán, Argentina
3
Servicio de Traumatología, Hospital Ángel C. Padilla, Sistema Provincial de Salud, San Miguel de Tucuman CP4000, Tucumán, Argentina
4
Cátedra de Bacteriología, Instituto de Microbiología, Facultad de Bioquímica, Química y Farmacia, Universidad Nacional de Tucumán, San Miguel de Tucuman CP4000, Tucumán, Argentina
5
Laboratorio de Inmunobiotecnología, Centro de Referencia para Lactobacilos (CERELA-CONICET), San Miguel de Tucuman CP4000, Tucumán, Argentina
*
Authors to whom correspondence should be addressed.
Microorganisms 2022, 10(3), 634; https://doi.org/10.3390/microorganisms10030634
Submission received: 21 December 2021 / Revised: 11 January 2022 / Accepted: 17 January 2022 / Published: 17 March 2022
(This article belongs to the Special Issue Probiotics for Next Generations)
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Abstract

This work aimed to evaluate the adjuvant treatment to surgical debridement using topical applications of Lactiplantibacillus plantarum ATCC 10241 cultures in complicated diabetic foot ulcers as compared to diabetic foot ulcers receiving surgical wound debridement. A randomised controlled trial was performed involving 22 outpatients with complicated diabetic foot ulcers that either received surgical debridement (SuDe, n = 12) or surgical debridement plus topical applications of L. plantarum cultures (SuDe + Lp, n = 10) every week during a 12 week treatment period. Compared to patients receiving SuDe, patients treated with SuDe + Lp exhibited significantly increased fibroplasia and angiogenesis, as determined by Masson’s trichrome staining and the study of CD34 cells, α-smooth muscle actin to semi-quantify vascular area, number of vessels and endothelial cells. In addition, a promotion of the polarisation of macrophages from M1 (CD68) to M2 (CD163) phenotype was observed in SuDe + Lp patients with remarkable differences in the tissue localisation. Bacterial counts were significantly diminished in the SuDe + Lp group compared to the SuDe group. Ex vivo assays, using polymorphonuclears isolated from peripheral blood of patients with diabetes and healthy individuals and challenged with Staphylococcus aureus demonstrated that the addition of L. plantarum supernatants significantly improved the phagocytosis of these cells. L. plantarum-secreted components increased the neutrophils bactericidal activity and regulated the netosis induced by S. aureus. At day 49, the average wound area reduction with SuDe + Lp was 73.5% compared with 45.8% for SuDe (p < 0.05). More patients progressed to closure with SuDe + Lp compared with SuDe treatment, indicating the ability of L. plantarum to accelerate the healing. At day 60, 60% of patients treated with SuDe + Lp achieved 100% of wound area reduction compared with 40% for SuDe. We propose that SuDe + Lp could be an effective adjuvant to surgical debridement when SuDe is not satisfactory for patients with complicated diabetic foot ulcers. The treatment is cheap and easy to apply and the product is easy to obtain.
Keywords: diabetic foot ulcers; Lactiplantibacillus plantarum; healing acceleration; macrophages; angiogenesis; neutrophil response; topical probiotic diabetic foot ulcers; Lactiplantibacillus plantarum; healing acceleration; macrophages; angiogenesis; neutrophil response; topical probiotic

Share and Cite

MDPI and ACS Style

Argañaraz Aybar, J.N.; Ortiz Mayor, S.; Olea, L.; Garcia, J.J.; Nisoria, S.; Kolling, Y.; Melian, C.; Rachid, M.; Torres Dimani, R.; Werenitzky, C.; et al. Topical Administration of Lactiplantibacillus plantarum Accelerates the Healing of Chronic Diabetic Foot Ulcers through Modifications of Infection, Angiogenesis, Macrophage Phenotype and Neutrophil Response. Microorganisms 2022, 10, 634. https://doi.org/10.3390/microorganisms10030634

AMA Style

Argañaraz Aybar JN, Ortiz Mayor S, Olea L, Garcia JJ, Nisoria S, Kolling Y, Melian C, Rachid M, Torres Dimani R, Werenitzky C, et al. Topical Administration of Lactiplantibacillus plantarum Accelerates the Healing of Chronic Diabetic Foot Ulcers through Modifications of Infection, Angiogenesis, Macrophage Phenotype and Neutrophil Response. Microorganisms. 2022; 10(3):634. https://doi.org/10.3390/microorganisms10030634

Chicago/Turabian Style

Argañaraz Aybar, Julio Nicolás, Sonia Ortiz Mayor, Luis Olea, Juan José Garcia, Sebastian Nisoria, Yanina Kolling, Constanza Melian, Mirta Rachid, Rafael Torres Dimani, Cecilia Werenitzky, and et al. 2022. "Topical Administration of Lactiplantibacillus plantarum Accelerates the Healing of Chronic Diabetic Foot Ulcers through Modifications of Infection, Angiogenesis, Macrophage Phenotype and Neutrophil Response" Microorganisms 10, no. 3: 634. https://doi.org/10.3390/microorganisms10030634

APA Style

Argañaraz Aybar, J. N., Ortiz Mayor, S., Olea, L., Garcia, J. J., Nisoria, S., Kolling, Y., Melian, C., Rachid, M., Torres Dimani, R., Werenitzky, C., Lorca, C., Salva, S., Gobbato, N., Villena, J., & Valdez, J. C. (2022). Topical Administration of Lactiplantibacillus plantarum Accelerates the Healing of Chronic Diabetic Foot Ulcers through Modifications of Infection, Angiogenesis, Macrophage Phenotype and Neutrophil Response. Microorganisms, 10(3), 634. https://doi.org/10.3390/microorganisms10030634

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