In Vitro Antibacterial and Anti-Inflammatory Activity of Arctostaphylos uva-ursi Leaf Extract against Cutibacterium acnes
Abstract
:1. Introduction
2. Materials and Methods
2.1. Bacterial Strain, Compounds and Materials
2.2. Characterization of Arctostaphylos uva-ursi Extract
2.2.1. FT-IR/ATR Analysis
2.2.2. Thermal Analysis
2.2.3. XPS Characterization
2.2.4. Total Polyphenol Content (TPC) Determination
2.2.5. Preparation of a Toning Lotion Loaded with Arctostaphylos uva-ursi Leaf Extract
2.2.6. HPLC Analysis
2.2.7. In Vitro Skin Permeation Studies
2.3. Kirby–Bauer Disk Diffusion Test
2.4. Determination of the Minimum Inhibitory Concentration (MIC)
2.5. Time-Killing Assay
2.6. LIVE/DEAD Staining
2.7. Biofilm Inhibition and Degradation
2.8. Cytotoxicity and Hemolysis Profile
2.9. Enzyme-linked Immunosorbent Assay (ELISA)
2.10. Antioxidant Activity
2.11. Statistical Analysis
3. Results
3.1. Chemical–Physical Characterization of Arctostaphylos uva-ursi Leaf Extract
3.2. Total Phenol Content (TPC)
3.3. Franz Cell Permeation Tests
3.4. Antibacterial Activity on Planktonic C. acnes
3.5. Fluorescence Microscopy of Live/Dead Cells
3.6. Effect of Arctostaphylos uva-ursi on C. acnes Biofilm
3.7. Cytotoxicity Profile
3.8. Induction of Inflammatory Cytokines by C. acnes In Vitro
3.9. Antioxidant Activity
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Aydemir, E.H. Acne vulgaris. Turk. Arch. Pediatrics 2014, 49, 13–16. [Google Scholar] [CrossRef] [PubMed]
- Balch, C.M.; Riley, L.B.; Bae, Y.J.; Salmeron, M.A.; Platsoucas, C.D.; von Eschenbach, A.; Itoh, K. Patterns of human tumor-infiltrating lymphocytes in 120 human cancers. Arch. Surg. 1990, 125, 200–205. [Google Scholar] [CrossRef]
- Tan, J.K.L.; Bhate, K. A global perspective on the epidemiology of acne. Br. J. Dermatol. 2015, 172 (Suppl S1), 3–12. [Google Scholar] [CrossRef] [PubMed]
- Tan, A.U.; Schlosser, B.J.; Paller, A.S. A review of diagnosis and treatment of acne in adult female patients. Int. J. Womens Dermatol. 2018, 4, 56–71. [Google Scholar] [CrossRef] [PubMed]
- Toyoda, M.; Morohashi, M. Pathogenesis of acne. Med. Electron Microsc. Off. J. Clin. Electron Microsc. Soc. Jpn. 2001, 34, 29–40. [Google Scholar] [CrossRef] [PubMed]
- Lolis, M.S.; Bowe, W.P.; Shalita, A.R. Acne and systemic disease. Med. Clin. 2009, 93, 1161–1181. [Google Scholar] [CrossRef] [PubMed]
- Collier, C.N.; Harper, J.C.; Cafardi, J.A.; Cantrell, W.C.; Wang, W.; Foster, K.W.; Elewski, B.E. The prevalence of acne in adults 20 years and older. J. Am. Acad. Dermatol. 2008, 58, 56–59. [Google Scholar] [CrossRef] [PubMed]
- Frénard, C.; Mansouri, S.; Corvec, S.; Boisrobert, A.; Khammari, A.; Dréno, B. Prepubertal acne: A retrospective study. Int. J. Womens Dermatol. 2021, 7, 482–485. [Google Scholar] [CrossRef]
- Claudel, J.-P.; Auffret, N.; Leccia, M.-T.; Poli, F.; Corvec, S.; Dréno, B. Staphylococcus epidermidis: A Potential New Player in the Physiopathology of Acne? Dermatology 2019, 235, 287–294. [Google Scholar] [CrossRef]
- Byrd, A.L.; Belkaid, Y.; Segre, J.A. The human skin microbiome. Nat. Rev. Microbiol. 2018, 16, 143–155. [Google Scholar] [CrossRef]
- Mayslich, C.; Grange, P.A.; Dupin, N. Cutibacterium acnes as an Opportunistic Pathogen: An Update of Its Virulence-Associated Factors. Microorganisms 2021, 9, 303. [Google Scholar] [CrossRef]
- Fang, F.; Xie, Z.; Quan, J.; Wei, X.; Wang, L.; Yang, L. Baicalin suppresses Propionibacterium acnes-induced skin inflammation by downregulating the NF-κB/MAPK signaling pathway and inhibiting activation of NLRP3 inflammasome. Braz. J. Med. Biol. Res. 2020, 53, e9949. [Google Scholar] [CrossRef]
- Kraft, J.; Freiman, A. Management of acne. CMAJ Can. Med. Assoc. J. 2011, 183, E430–E435. [Google Scholar] [CrossRef]
- Platsidaki, E.; Dessinioti, C. Recent advances in understanding Propionibacterium acnes (Cutibacterium acnes) in acne. F1000Research 2018, 7, 1953. [Google Scholar] [CrossRef]
- Ochsendorf, F. Systemic antibiotic therapy of acne vulgaris. J. Der Dtsch. Dermatol. Ges. 2006, 4, 828–841. [Google Scholar] [CrossRef]
- Baldwin, H. Oral Antibiotic Treatment Options for Acne Vulgaris. J. Clin. Aesthetic Dermatol. 2020, 13, 26–32. [Google Scholar]
- Geria, A.N.; Tajirian, A.L.; Kihiczak, G.; Schwartz, R.A. Minocycline-induced skin pigmentation: An update. Acta Dermatovenerol. Croat. ADC 2009, 17, 123–126. [Google Scholar]
- Bagatin, E.; de Freitas, T.H.P.; Rivitti-Machado, M.C.; Machado, M.C.R.; Ribeiro, B.M.; Nunes, S.; da Rocha, M.A.D. Adult female acne: A guide to clinical practice. An. Bras. Dermatol. 2019, 94, 62–75. [Google Scholar] [CrossRef]
- Patel, M.; Bowe, W.P.; Heughebaert, C.; Shalita, A.R. The development of antimicrobial resistance due to the antibiotic treatment of acne vulgaris: A review. J. Drugs Dermatol. 2010, 9, 655–664. [Google Scholar]
- Blaskovich, M.A.T.; Elliott, A.G.; Kavanagh, A.M.; Ramu, S.; Cooper, M.A. In vitro Antimicrobial Activity of Acne Drugs Against Skin-Associated Bacteria. Sci. Rep. 2019, 9, 14658. [Google Scholar] [CrossRef]
- Vora, J.; Srivastava, A.; Modi, H. Antibacterial and antioxidant strategies for acne treatment through plant extracts. Inform. Med. Unlocked 2018, 13, 128–132. [Google Scholar] [CrossRef]
- Gonçalves, L.A.; Lorenzo, J.M.; Trindade, M.A. Fruit and Agro-Industrial Waste Extracts as Potential Antimicrobials in Meat Products: A Brief Review. Foods 2021, 10, 1469. [Google Scholar] [CrossRef] [PubMed]
- Leichtweis, M.G.; Oliveira, M.B.P.P.; Ferreira, I.C.F.R.; Pereira, C.; Barros, L. Sustainable Recovery of Preservative and Bioactive Compounds from Food Industry Bioresidues. Antioxidants 2021, 10, 1827. [Google Scholar] [CrossRef] [PubMed]
- Ekor, M. The growing use of herbal medicines: Issues relating to adverse reactions and challenges in monitoring safety. Front. Pharmacol. 2014, 4, 177. [Google Scholar] [CrossRef] [PubMed]
- Amroun, D.; Hamoudi, M.; Khennouf, S.; Boutefnouchet, S.; Harzallah, D.; Amrane, M.; Dahamna, S. In-vivo anti-inflammatory activity and safety assessment of the aqueous extract of Algerian Erica arborea L. (Ericaceae) aerial parts. J. Ethnopharmacol. 2021, 271, 113881. [Google Scholar] [CrossRef] [PubMed]
- Dell’Annunziata, F.; Dell’Aversana, C.; Doti, N.; Donadio, G.; Dal Piaz, F.; Izzo, V.; De Filippis, A.; Galdiero, M.; Altucci, L.; Boccia, G.; et al. Outer Membrane Vesicles Derived from Klebsiella pneumoniae Are a Driving Force for Horizontal Gene Transfer. Int. J. Mol. Sci. 2021, 22, 8732. [Google Scholar] [CrossRef] [PubMed]
- Mohd Azman, N.A.; Gallego, M.G.; Segovia, F.; Abdullah, S.; Shaarani, S.M.; Almajano Pablos, M.P. Study of the Properties of Bearberry Leaf Extract as a Natural Antioxidant in Model Foods. Antioxid. Basel Switz. 2016, 5, E11. [Google Scholar] [CrossRef] [PubMed]
- Das, S. Natural therapeutics for urinary tract infections-a review. Future J. Pharm. Sci. 2020, 6, 64. [Google Scholar] [CrossRef]
- Asensio, E.; Vitales, D.; Pérez, I.; Peralba, L.; Viruel, J.; Montaner, C.; Vallès, J.; Garnatje, T.; Sales, E. Phenolic Compounds Content and Genetic Diversity at Population Level across the Natural Distribution Range of Bearberry (Arctostaphylos uva-ursi, Ericaceae) in the Iberian Peninsula. Plants 2020, 9, 1250. [Google Scholar] [CrossRef]
- Amarowicz, R.; Pegg, R.B. Inhibition of proliferation of human carcinoma cell lines by phenolic compounds from a bearberry-leaf crude extract and its fractions. J. Funct. Foods 2013, 5, 660–667. [Google Scholar] [CrossRef]
- Jeverica, S.; El Sayed, F.; Čamernik, P.; Kocjančič, B.; Sluga, B.; Rottman, M.; Papst, L. Growth detection of Cutibacterium acnes from orthopaedic implant-associated infections in anaerobic bottles from BACTEC and BacT/ALERT blood culture systems and comparison with conventional culture media. Anaerobe 2020, 61, 102133. [Google Scholar] [CrossRef] [PubMed]
- Csukás, Z.; Banizs, B.; Rozgonyi, F. Studies on the cytotoxic effects of Propionibacterium acnes strains isolated from cornea. Microb. Pathog. 2004, 36, 171–174. [Google Scholar] [CrossRef] [PubMed]
- Fabiano, A.; Migone, C.; Cerri, L.; Piras, A.M.; Mezzetta, A.; Maisetta, G.; Esin, S.; Batoni, G.; Di Stefano, R.; Zambito, Y. Combination of Two Kinds of Medicated Microparticles Based on Hyaluronic Acid or Chitosan for a Wound Healing Spray Patch. Pharmaceutics 2021, 13, 2195. [Google Scholar] [CrossRef] [PubMed]
- Bonifacio, M.A.; Cerqueni, G.; Cometa, S.; Licini, C.; Sabbatini, L.; Mattioli-Belmonte, M.; De Giglio, E. Insights into Arbutin Effects on Bone Cells: Towards the Development of Antioxidant Titanium Implants. Antioxidants 2020, 9, 579. [Google Scholar] [CrossRef]
- Cometa, S.; Bonifacio, M.A.; Licini, C.; Bellissimo, A.; Pinto, L.; Baruzzi, F.; Mattioli-Belmonte, M.; De Giglio, E. Innovative Eco-Friendly Hydrogel Film for Berberine Delivery in Skin Applications. Molecules 2021, 26, 4901. [Google Scholar] [CrossRef]
- Folliero, V.; Dell’Annunziata, F.; Roscetto, E.; Cammarota, M.; De Filippis, A.; Schiraldi, C.; Catania, M.R.; Casolaro, V.; Perrella, A.; Galdiero, M.; et al. Niclosamide as a Repurposing Drug against Corynebacterium striatum Multidrug-Resistant Infections. Antibiotics 2022, 11, 651. [Google Scholar] [CrossRef]
- Morone, M.V.; Dell’Annunziata, F.; Giugliano, R.; Chianese, A.; De Filippis, A.; Rinaldi, L.; Gambardella, U.; Franci, G.; Galdiero, M.; Morone, A. Pulsed laser ablation of magnetic nanoparticles as a novel antibacterial strategy against gram positive bacteria. Appl. Surf. Sci. Adv. 2022, 7, 100213. [Google Scholar] [CrossRef]
- Gerlier, D.; Thomasset, N. Use of MTT colorimetric assay to measure cell activation. J. Immunol. Methods 1986, 94, 57–63. [Google Scholar] [CrossRef]
- Folliero, V.; Dell’Annunziata, F.; Roscetto, E.; Amato, A.; Gasparro, R.; Zannella, C.; Casolaro, V.; De Filippis, A.; Catania, M.R.; Franci, G.; et al. Rhein: A novel antibacterial compound against Streptococcus mutans infection. Microbiol. Res. 2022, 261, 127062. [Google Scholar] [CrossRef]
- Evans, B.C.; Nelson, C.E.; Yu, S.S.; Beavers, K.R.; Kim, A.J.; Li, H.; Nelson, H.M.; Giorgio, T.D.; Duvall, C.L. Ex vivo red blood cell hemolysis assay for the evaluation of pH-responsive endosomolytic agents for cytosolic delivery of biomacromolecular drugs. J. Vis. Exp. JoVE 2013, 73, e50166. [Google Scholar] [CrossRef]
- Xie, J.; Schaich, K.M. Re-evaluation of the 2,2-diphenyl-1-picrylhydrazyl free radical (DPPH) assay for antioxidant activity. J. Agric. Food Chem. 2014, 62, 4251–4260. [Google Scholar] [CrossRef]
- Shahidi, F.; Ho, C.-T. (Eds.) Phenolic Compounds in Foods and Natural Health Products; ACS Symposium Series; American Chemical Society: Washington, DC, USA, 2005; Volume 909, ISBN 978-0-8412-3891-6. [Google Scholar]
- Sugier, P.; Sęczyk, Ł.; Sugier, D.; Krawczyk, R.; Wójcik, M.; Czarnecka, J.; Okoń, S.; Plak, A. Chemical Characteristics and Antioxidant Activity of Arctostaphylos uva-ursi L. Spreng. at the Southern Border of the Geographical Range of the Species in Europe. Mol. Basel Switz. 2021, 26, 7692. [Google Scholar] [CrossRef]
- Takebayashi, J.; Ishii, R.; Chen, J.; Matsumoto, T.; Ishimi, Y.; Tai, A. Reassessment of antioxidant activity of arbutin: Multifaceted evaluation using five antioxidant assay systems. Free Radic. Res. 2010, 44, 473–478. [Google Scholar] [CrossRef]
- Castillo, D.E.; Nanda, S.; Keri, J.E. Propionibacterium (Cutibacterium) acnes Bacteriophage Therapy in Acne: Current Evidence and Future Perspectives. Dermatol. Ther. 2019, 9, 19–31. [Google Scholar] [CrossRef]
- Nasri, H.; Bahmani, M.; Shahinfard, N.; Moradi Nafchi, A.; Saberianpour, S.; Rafieian Kopaei, M. Medicinal Plants for the Treatment of Acne Vulgaris: A Review of Recent Evidences. Jundishapur J. Microbiol. 2015, 8, e25580. [Google Scholar] [CrossRef]
- Hassan, H.M.; Jiang, Z.-H.; Asmussen, C.; McDonald, E.; Qin, W. Antibacterial activity of northern Ontario medicinal plant extracts. Can. J. Plant Sci. 2014, 94, 417–424. [Google Scholar] [CrossRef]
- Jahodár, L.; Jílek, P.; Páktová, M.; Dvoráková, V. Antimicrobial effect of arbutin and an extract of the leaves of Arctostaphylos uva-ursi in vitro. Cesk. Farm. 1985, 34, 174–178. [Google Scholar]
- Kruszewska, H.; Zareba, T.; Tyski, S. Examination of antimicrobial activity of selected non-antibiotic medicinal preparations. Acta Pol. Pharm. 2012, 69, 1368–1371. [Google Scholar]
- Wynn, S.G.; Fougère, B.J. Veterinary Herbal Medicine; Mosby: Saint-Louis, MO, USA, 2007; ISBN 978-0-323-02998-8. [Google Scholar]
- Dell’Annunziata, F.; Martora, F.; Della Pepa, M.E.; Folliero, V.; Luongo, L.; Bocelli, S.; Guida, F.; Mascolo, P.; Campobasso, C.P.; Maione, S.; et al. Post-mortem interval assessment by MALDI-TOF mass spectrometry analysis in murine cadavers. J. Appl. Microbiol. 2021, 132, 707–714. [Google Scholar] [CrossRef]
- Kim, J.; Ochoa, M.-T.; Krutzik, S.R.; Takeuchi, O.; Uematsu, S.; Legaspi, A.J.; Brightbill, H.D.; Holland, D.; Cunliffe, W.J.; Akira, S.; et al. Activation of toll-like receptor 2 in acne triggers inflammatory cytokine responses. J. Immunol. Baltim. Md. 1950 2002, 169, 1535–1541. [Google Scholar] [CrossRef]
- Nagy, I.; Pivarcsi, A.; Kis, K.; Koreck, A.; Bodai, L.; McDowell, A.; Seltmann, H.; Patrick, S.; Zouboulis, C.C.; Kemény, L. Propionibacterium acnes and lipopolysaccharide induce the expression of antimicrobial peptides and proinflammatory cytokines/chemokines in human sebocytes. Microbes Infect. 2006, 8, 2195–2205. [Google Scholar] [CrossRef] [PubMed]
- Tanghetti, E.A. The role of inflammation in the pathology of acne. J. Clin. Aesthetic Dermatol. 2013, 6, 27–35. [Google Scholar]
- Sugisaki, H.; Yamanaka, K.; Kakeda, M.; Kitagawa, H.; Tanaka, K.; Watanabe, K.; Gabazza, E.C.; Kurokawa, I.; Mizutani, H. Increased interferon-gamma, interleukin-12p40 and IL-8 production in Propionibacterium acnes-treated peripheral blood mononuclear cells from patient with acne vulgaris: Host response but not bacterial species is the determinant factor of the disease. J. Dermatol. Sci. 2009, 55, 47–52. [Google Scholar] [CrossRef] [PubMed]
- Nguyen, A.T.; Kim, K.-Y. Rhein inhibits the growth of Propionibacterium acnes by blocking NADH dehydrogenase-2 activity. J. Med. Microbiol. 2020, 69, 689–696. [Google Scholar] [CrossRef]
- Schink, A.; Neumann, J.; Leifke, A.L.; Ziegler, K.; Fröhlich-Nowoisky, J.; Cremer, C.; Thines, E.; Weber, B.; Pöschl, U.; Schuppan, D.; et al. Screening of herbal extracts for TLR2- and TLR4-dependent anti-inflammatory effects. PLoS ONE 2018, 13, e0203907. [Google Scholar] [CrossRef]
- Lee, H.-J.; Kim, K.-W. Anti-inflammatory effects of arbutin in lipopolysaccharide-stimulated BV2 microglial cells. Inflamm. Res. Off. J. Eur. Histamine Res. Soc. Al 2012, 61, 817–825. [Google Scholar] [CrossRef]
- Alkhawaja, E.; Hammadi, S.; Abdelmalek, M.; Mahasneh, N.; Alkhawaja, B.; Abdelmalek, S.M. Antibiotic resistant Cutibacterium acnes among acne patients in Jordan: A cross sectional study. BMC Dermatol. 2020, 20, 17. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2022 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Dell’Annunziata, F.; Cometa, S.; Della Marca, R.; Busto, F.; Folliero, V.; Franci, G.; Galdiero, M.; De Giglio, E.; De Filippis, A. In Vitro Antibacterial and Anti-Inflammatory Activity of Arctostaphylos uva-ursi Leaf Extract against Cutibacterium acnes. Pharmaceutics 2022, 14, 1952. https://doi.org/10.3390/pharmaceutics14091952
Dell’Annunziata F, Cometa S, Della Marca R, Busto F, Folliero V, Franci G, Galdiero M, De Giglio E, De Filippis A. In Vitro Antibacterial and Anti-Inflammatory Activity of Arctostaphylos uva-ursi Leaf Extract against Cutibacterium acnes. Pharmaceutics. 2022; 14(9):1952. https://doi.org/10.3390/pharmaceutics14091952
Chicago/Turabian StyleDell’Annunziata, Federica, Stefania Cometa, Roberta Della Marca, Francesco Busto, Veronica Folliero, Gianluigi Franci, Massimiliano Galdiero, Elvira De Giglio, and Anna De Filippis. 2022. "In Vitro Antibacterial and Anti-Inflammatory Activity of Arctostaphylos uva-ursi Leaf Extract against Cutibacterium acnes" Pharmaceutics 14, no. 9: 1952. https://doi.org/10.3390/pharmaceutics14091952