Abstract
Canine skin is often a source of bacterial strains that are characterized by the presence of important virulence factors and a high antimicrobial resistance. These bacteria are involved in the pathogenesis of infectious skin diseases, which are very frequent in dogs. Moreover, canine skin isolates are easily spread to other animals and humans. The aim of this study was to evaluate the inhibitory and bactericidal activity of eight organic acids (L-lactic, acetic, propionic, butyric, citric, succinic, glycolic, L-ascorbic acid) against 14 canine skin isolates (11 Gram-positive and three Gram-negative species). The advantages of the tested organic acids are their gentleness to the skin and their affordability. The minimum inhibitory concentration (MIC) and minimum bactericidal concentration (MBC) were determined by the broth microdilution method. All tested acids showed a bactericidal effect against the selected bacteria, with the exception of their bacteriostatic effect against the Bacillus cereus strain. The lowest MIC showed acetic acid (MIC between 0.5 and 2.0 mg/mL) and propionic acid (MIC 0.8 – 3.3 mg/mL), whereas L-ascorbic acid (MIC 4.0 – 16.0 mg/mL) seems to be weaker among the tested acids. Two Staphylococcus aureus strains and a strain of Escherichia coli were observed to be more resistant compared to coagulase-negative staphylococci.
Highlights
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The canine skin is common source of multiresistant and biofilm-forming bacteria
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Organic acids could represent alternative antimicrobial means for skin
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Acetic and propionic acids were showed lowest MIC among tested acids
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The higher minimal inhibitory concentrations were observed for S. aureus and E. coli
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All data generated or analysed during this study are included in this published article.
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References
Adamczak A, Ożarowski M, Karpiński TM (2020) Antibacterial activity of some flavonoids and organic acids widely distributed in plants. J Clin Med 9:109. https://doi.org/10.3390/jcm9010109
Balouri M, Sadiki M, Ibnsouda SK (2016) Methods for in vitro evaluating antimicrobial activity: a review. J Pharm Anal 6:71–79. https://doi.org/10.1016/j.jpha.2015.11.005
Bertelloni F, Cagnoli G, Ebani VV (2021) Virulence and antimicrobial resistance in canine Staphylococcus spp. isolates. Microorganisms 9:515. https://doi.org/10.3390/microorganisms9030515
Bessede E, Angla-Gre M, Delagarde Y, Sep Hieng S, Ménard A, Mégraud F (2011) Matrix-assisted laser-desorption/ionization biotyper: experience in the routine of a University hospital. Clin Mcrobiol Infect 17:533–538. https://doi.org/10.1111/j.1469-0691.2010.03274.x
Draelos ZD (2018) The science behind skin care: moisturizers. J Cosmet Dermatol 17:138–144. https://doi.org/10.1111/jocd.12490
Ferrer L, García-Fonticoba R, Pérez D, Viñes J, Fàbregas N, Madroñero S, Meroni G, Martino PA, Martínez S, Maté ML, Sánchez-Bruni S, Cuscó A, Migura-García L, Francino O (2021) Whole genome sequencing and de novo assembly of Staphylococcus pseudintermedius: a pangenome approach to unravelling pathogenesis of canine pyoderma. Vet Dermatol 32:654–663. https://doi.org/10.1111/vde.13040
Gao Z, Shao J, Sun H, Zhong W, Zhuang W, Zhang Z (2012) Evaluation of different kinds of organic acids and their antibacterial activity in Japanese Apricot fruits. Afr J Agric Res 7:4911–4918. https://doi.org/10.5897/AJAR12.1347
Halstead FD, Rauf M, Moiemen NS, Bamford A, Wearn CM, Fraise AP, Lund PA, Oppenheim BA, Webber MA (2015) The antibacterial activity of acetic acid against biofilm-producing pathogens of relevance to burns patients. PLoS ONE 10:e0136190. https://doi.org/10.1371/journal.pone.0136190
Hirshfield IN, Terzulli S, O’Byrne C (2003) Weak organic acids: a panoply of effexts on bacteria. Sci pro 86:245–269. https://doi.org/10.3184/003685003783238626
Hoffmann AR, Patterson AP, Diesel A, Lawhon SD, Ly HJ, Stephenson CE, Mansell J, Steiner JM, Dowd SE, Olivry T, Suchodolski JS (2014) The skin microbiome in healthy and allergic dogs. PLoS ONE 9:e83197. https://doi.org/10.1371/journal.pone.0083197
Kovanda L, Zhang W, Wei X, Luo J, Wu X, Atwill ER, Vaessen S, Li X, Liu Y (2019) In vitro antimicrobial activities of organic acids and their derivatives on several species of Gram-negative and Gram-positive bacteria. Molecules 24:3770. https://doi.org/10.3390/molecules24203770
Loeffler A, Lloyd DH (2018) What has changed in canine pyoderma? A narrative review. The Vet J 235:73–82. https://doi.org/10.1016/j.tvjl.2018.04.002
Lloyd DH, Garthwaite G (1982) Epidermal structure and surface topography of canine skin. Res Vet 33:99–104
Meroni G, Filipe JFS, Drago L, Martino PA (2019) Investigation on antibiotic-resistance, biofilm formation and virulence factors in multi drug resistant and non multi drug resistant Staphylococcus pseudintermedius. Microorganisms 7:702. https://doi.org/10.3390/microorganisms7120702
Mogana R, Adhikari A, Tzar MN, Ramliza R, Wiart C (2020) Antibacterial activities of the extracts, fractions and isolated compounds from Canarium patentinervium Miq. against bacterial clinical isolates. BMC Complement Med Ther 20:55. https://doi.org/10.1186/s12906-020-2837-5
Nagoba BS, Selkar SP, Wadher BJ, Gandhi RC (2013) Acetic acid treatment of pseudomonal wound infections–a review. J Infect Public Health 6:410–415. https://doi.org/10.1016/j.jiph.2013.05.005
Pangprasit N, Srithanasuwan A, Suriyasathaporn W, Pikulkaew S, Bernard JK, Chaisri W (2020) Antibacterial activities of acetic acid against major and minor pathogens isolated from mastitis in dairy cows. Pathogens 9:961. https://doi.org/10.3390/pathogens9110961
Papatsiros VG, Billinis C (2012) The prophylactic use of acidifiers as antibacterial agents in swine. Antimicrobial Agents; Bobbrala, V., Ed.; IntechOpen: London, Uk, pp. 295–310
Ravetti S, Clemente C, Brignone S, Hergert L, Allemandi D, Palma S (2019) Ascorbic acid in skin health. Cosmetics 6:58. https://doi.org/10.3390/cosmetics6040058
Ryssel H, Kloeters O, Germann G, Schäfer Th, Wiedemann G, Oehlbauer M (2009) The antimicrobial effect of acetic acid – an alternative to common local antiseptics? J Inter Soc Burn Injuries 35:695–700. https://doi.org/10.1016/j.burns.2008.11.009
Stanojević-Nikolić S, Dimić G, Mojović L, Pejin J, Djukić-Vuković A, Kocić-Tanackov S (2016) Antimicrobial activity of lactic acid against pathogen and spoilage microorganisms. J Food Process Preserv 40:990–998. https://doi.org/10.1111/jfpp.12679
Štempelová L, Kubašová I, Bujňáková D, Kačírová J, Farbáková J, Maďar M, Karahutová L, Strompfová V (2022) Distribution and characterization of staphylococci isolated from healthy canine skin. Topics Comp Anim Med 49:100665. https://doi.org/10.1016/j.tcam.2022.100665
Tang S-C, Yang J-H (2018) Dual effects of alpha-hydroxy acids on the skin. Molecules 23(4):863. https://doi.org/10.3390/molecules23040863
Vallarino JG, Osorio S (2019) Organic acids, Chapter 10. Postharvest Physiol Biochem Fruits Vegetables: 207–224. https://doi.org/10.1016/B978-0-12-813278-4.00010-5
Xiao-yan D, Yu-hui B, Qi Z, He-Jia W, Shi-Xin X (2021) Study on the bactericidal effect of different organic acids on Escherichia coli and its application in slaughterhouse. Int J Vet Sci Res 7:033–039. https://doi.org/10.17352/ijvsr.000078
Acknowledgements
This work was financed by the Slovak scientific agency VEGA (Vedecká grantová agentúra Ministerstva školstva, vedy, výskumu a športu Slovenskej republiky a Slovenskej akadémie vied; project no. 2/0006/20 and no. VEGA 2/0010/21).
Funding
This work was financed by the Slovak scientific agency VEGA (Vedecká grantová agentúra Ministerstva školstva, vedy, výskumu a športu Slovenskej republiky a Slovenskej akadémie vied; project no. 2/0006/20 and no. VEGA 2/0010/21).
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Viola Strompfová conceived the study design. Lucia Štempelová, Viola Strompfová, Dobroslava Bujňáková and Ivana Kubašová performed the analysis of the MIC and testing of bacterial properties. Lívia Karahutová detected the virulence factors of the strains by the PCR method. Canine skin samples provided Jana Gálová and Erik Kužma. The first draft of the manuscript was written by Lucia Štempelová, and all the authors commented on previous versions of the manuscript. All authors have read and approved the final manuscript.
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All procedures involving dogs were in accordance with standard veterinary practices according Slovak legislation (no. 377/2012 and 436/2012).
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Štempelová, L., Kubašová, I., Bujňáková, D. et al. Antimicrobial activity of organic acids against canine skin bacteria. Vet Res Commun 47, 999–1005 (2023). https://doi.org/10.1007/s11259-022-10056-z
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DOI: https://doi.org/10.1007/s11259-022-10056-z