Antibiotic resistance profile of gram-negative bacteria isolated from dog nasal swab samples, and antibacterial and antioxidant activities of aqueous extracts of Alpinia purpurta (Vieill.) K. Schum (Zingiberaceae)

Camila de Cuffa Matusaiki, Rafaela Galves Ferreira, Luciana Kazue Otutumi, Isabela Carvalho dos Santos, Felipe André Pereira Ramos, Taniara Suelen Mezalira, Ezilda Jacomassi, Lidiane Nunes Barbosa, Daniela Dib Gonçalves, Andréia Assunção Soares

Abstract


The indiscriminate use of antibiotics in veterinary medicine and their negligent use among dog owners have contributed to the rise of antibiotic resistance in microorganisms found in pets. In addition, the search for medicinal plants with antibacterial properties has made the evaluation of aqueous extracts of Alpinia purpurata (Vieill.) K. Schum an important issue. Thus, the aim of this work was to determine the antibiotic resistance profile of gram-negative bacteria isolated from nasal swab samples of dogs and assess the antibacterial activity of the aqueous extracts of leaves and rhizomes of A. purpurata. The bacteria identified were tested using the agar disc diffusion assay for the evaluation of antibiotic resistance. A total of 16 isolates were obtained from the 19 samples collected, with a high prevalence of Escherichia coli (n=5). There was a high rate of resistance to ?-lactams, where the highest percentage was seen for amoxicillin (72.5%). Aqueous leaf extracts had high levels of total phenolic compounds (637.47 µg GAE mg-1), differing significantly (p < 0.05) from aqueous rhizome extracts (228.64 µg GAE mg-1). There was no significant difference in EC50 of DPPH values between the aqueous extracts; however, the antioxidant capacity of rhizome extracts had higher values than leaf extracts. The minimum inhibitory concentration (MIC) of leaves and rhizomes for the evaluated bacteria ranged from 9000 to 32,000 µg mL-1. For the minimum bactericidal concentration (MBC), most bacteria showed an MBC over 38,400 µg mL-1 for the rhizome. In conclusion, the bacteria isolated from dog nasal swabs showed a high resistance profile for the antibiotics of the penicillin class. Additionally, the results from the analysis of the aqueous extracts of rhizomes and leaves of A. purpurata showed an antimicrobial effect possibly associated with a high content of total phenolic compounds; these results can create a scope for using these extracts together with conventional antibiotics to control the emergence of antibiotic resistance among microbial species.

Keywords


Antimicrobial; Escherichia coli; Ginger; Serratia liquefaciens; Hafnia alvei; Pantoea agglomerans.

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References


Argudín, M. A., Deplano, A., Meghraoui, A., Dodémont, M., Heinrichs, A., Denis, O. Nonhoff, C. & Roisin, S. (2017). Bacteria from animals as a pool of antimicrobial resistance genes. Antibiotics (Basel), 6(2), 1-12. doi: 10.3390/antibiotics6020012

Ayres, M., Ayres Júnior, M., Ayres, D. L. & Santos, A. S. (2007). BioEstat: aplicações estatísticas nas áreas das ciências biomédicas. Belém: Universidade Federal do Pará. 364 p.

Bahr Arias, M. V., Carrilho, C. M. D. M. (2012). Resistência antimicrobiana nos animais e no ser humano. Há motivo para preocupação? Semina: Ciências Agrárias, 33(2), 775-790. doi: 10.5433/1679-0359.2012v33n2p775

Barbosa, L. N., Alves, F. C. B., Andrade, B. F. M. T., Albano, M., Castilho, I. G., Rall, V. L. M., Athayde N. B., Delbem, N. L. C., Roca, R. O. & Fernandes Júnior, A. (2014). Effects of Ocimun basilicum Linn essential oil and sodium hexametaphosphate on the shelf life of fresh chicken sausage. Journal of Food Protection, 77(6), 981-986. doi: 10.4315/0362-028X.JFP-13-498

Bona, E. A. M., Pinto, F. G. S., Fruet, T. K., Jorge, T. C. M. & Moura, A. C. (2014). Comparação de métodos para a avaliação da atividade antimicrobiana e determinação da concentração inibitória minima (CIM) de extratos vegetais aquosos e etanólicos. Arquivos Instituto Biológico São Paulo, 81(3), 218-225. doi: 10.1590/1808-1657001192012

Bozdogan, B., Berrezouga, L., Kuo, M. S., Yurek, D. A., Farley, K. A., Stockman, B. J. & Leclercq, R. (1999). A new resistance gene, linB, conferring resistance to lincosamides by nucleotidylation in Enterococcus faecium HM1025. Antimicrobial Agents and Chemotherapy, 43(4), 925-999.

CLSI. Clinical and Laboratory Standards Institute. (2018). Performance standars for antimicrobial susceptibility testing. CLSI document M100. Wayne (PA).

CLSI. Clinical Laboratory Standards Institute. (2003). Metodologia dos testes de sensibilidade a agentes antimicrobianos por diluição para bactérias de crescimento aeróbico: norma aprovada. 6.ed. São Paulo, v.23, M7-A6.

Costa, S. L. P. & Silva Júnior, A. C. S. (2017). Resistência bacteriana aos antibióticos e saúde pública: uma breve revisão de literatura. Estação Científica UNIFAP, 7(2), 45-57. doi: 10.18468/estcien.2017v7n2.p45-57

Cox, G. & Wright, G. D. (2013). Intrinsic antibiotic resistance: mechanisms, origins, challenges and solutions. International Journal of Medical Microbiology, 303(6-7), 287-292. doi: 10.1016/j.ijmm.2013.02.009.

Chan, E. W. C. & Wong, S. K. (2015). Phytochemistry and pharmacology of ornamental gingers, Hedychium coronarium and Alpinia purpurata: a review. Journal of Integrative Medicine, 13(6), 368-379. doi: 10.1016/S2095-4964(15)60208-4

Cutrim, E. S. M., Teles, A. M., Mouchrek, A. N., Mouchrek Filho, V. E., & Everton, G. O. (2019). Avaliação da atividade antimicrobiana e antioxidante dos óleos essenciais e extratos hidroalcoólicos de Zingiber officinale (gengibre) e Rosmarinus officinalis (alecrim). Revista Virtual de Química, 11(1), 60-81. doi: 10.21577/1984-6835.20190006

Dalgê, J. J. (2014). Estudo da capacidade antioxidante, antimicrobiana e anti-hemolítica do gengibre (Zingiber officinale). 2014. 72f. Dissertação (Mestrado em engenharia de alimentos) – Universidade de São Paulo, Pirassununga.

Del Fio, F. S., Matos Filho, T. R. & Groppo, F. C. (2000). Resistência Bacteriana. Revista Brasileira de Medicina, 57(10), 1129-1140.

Drougka, G. E., Foka, A., Koutinas, C. K., Jelastopulu, E., Giormezis, N., Farmaki, O., Sarrou, S., Anastassiou, E. D., Petinaki, E., & Spiliopoulou, I. (2016). Interspecies spread of Staphylococcus aureus clones among companionanimals and human close contacts in a veterinary teaching hospital. Across-sectional study in Greece. Preventive Veterinary Medicine, 126, 190-198. doi: 10.1016/j.prevetmed.2016.02.004

Ghosh, S., & Rangan, L. (2013). Alpinia: the gold mine of future therapeutics. 3 Biotech, 3(3), 173-183. doi: 10.1007/s13205-012-0089-x

Kadwalia, A., Bhoomika, A. K., Thakur, P., Vivekanandhan, R., Jaiswal, S., Patel, K. P., & Bhawana, R. (2019). Antimicrobial resistant: a glance on emergence, spread and combat. Journal of Pharmacognosy and Phytochemistry, 8(2), 995-998.

Kuete, V. (2010). Potential of Cameroonian plants and derived products against microbial infections: a review. Planta Med, 76(14),1479-1491. doi: 10.1055/s-0030-1250027

Kona, L. A., Thofeeq, M. D. & Venkata, R. (2015). In vitro studies and antibacterial activity of Alpinia purpurata. Austin Journal of Biotechnology & Bioengineering, 2(4), 1-2.

Leite-Martins, L. R., Mahú, M. I. M., Costa, A. L., Mendes, A., Lopes, E., Mendonça, D. M. V., Niza-Ribeiro, J. J. R., Matos, A. J. F., & Costa, P. M. (2014). Prevalence of antimicrobial resistance in enteric Escherichia coli from domestic pets and assessment of associated risk markers using a generalized linear mixed model. Preventive Veterinary Medicine, 117, 28-39. doi: 10.1016/j.prevetmed.2014.09.008

Leite-Martins, L. R., Meireles, D., Beça, N., Bessa, L. J., Matos, A. J. F., & Costa, P. M. (2015). Spread of multidrug-resistant Escherichia coli within domestic aggregates (humans, pets, and household environment). Journal of Veterinary Behavior, 10, 549-555. doi: 10.1016/j.jveb.2015.07.040

Lima, A. P. C. S., Gallani, N. R., Toledo, M. I. & Lopes, L. C. (2008). Utilização de um sistema de gerenciamento de benefícios farmacêuticos (PBM) para a caracterização do perfil de prescrição e aquisição de antibióticos. Revista Brasileira de Ciências Farmacêuticas, 44(2), 215-223. doi: 10.1590/S1516-93322008000200007

Lim, C. S. H., & Lim, S. L. (2013). Ferric reducing capacity versus ferric reducing antioxidant power for measuring total antioxidant capacity. Laboratory Medicine, 44(1), 51-55. doi:10.1309/LM93W7KTFNPZIXRR

Macedo Júnior, A. M. Multiresistência bacteriana e a consequência do uso irracional dos antibióticos. (2019). Scire Salutis, 9(2), 1-8. doi: 10.6008/CBPC2236-9600.2019.002.0001

Manandhar, S., Luitel, S. & Dahal, R. K. (2019). In vitro antimicrobial activity of some medicinal plants against human pathogenic bacteria. Journal of Tropical Medicine, 2019, 1-6. doi: 10.1155/2019/1895340

Negi, P. S. (2012). Plant extracts for the control of bacterial growth: Efficacy, stability and safety issues for food application. International Journal of Food Microbiology, 156(1), 7-17. doi: 10.1016/j.ijfoodmicro.2012.03.006

Otunola, G. A., Oloyede, O. B., Oladiji, A.T., & Afolayan, A. J. (2014). Selected spices and their combination modulate hypercholesterolemia-induced oxidative stress in experimental rats. Biological Research, 47(1), 1-6. doi: 10.1186/0717-6287-47-5

Paula, C. G. D. (2014). Análise de prescrições de medicamentos antimicrobianos dispensados em uma farmácia comunitária no município de João Pessoa, Paraíba. Revista Especialize on-line IPOG, 1(9), 1-14.

Pyrzynska, K., & Pekal, A. (2013). Application of free radical diphenylpicrylhydrazyl (DPPH) to estimate the antioxidant capacity of food samples. Analytical Methods, 5(17), 6-11. doi: 10.1039/C3AY40367J

Quinn, P. J., Carter, M. E., Markey, B. & Carter, G. R. (1994). Clinical veterinary microbiology. St. Louis: Mosby. 627 p.

Romaniuk, J. A. H. & Cegelski, L. (2015). Bacteria cell wall composition and the of antibiotics by cell-wall and whole-cell NMR. Philosophical Transactions of the Royal Society B, 370(1), 1-14. doi: 10.1098/rstb.2015.0024.

Sahoo, S., Singhi, S. & Nayak, S. (2014). Chemical composition, antioxidant and antimicrobial activity of essential oil and extract of Alpinia malaccensis Roscoe (Zingiberaceae). International Journal of Pharmacy and Pharmaceutical Sciences, 6(7), 183-188.

Shareef, H. K., Muhammed, H. J., Hussein, H. M., & Hameed, I. H. (2016). Antibacterial Effect of Gingiber officinale Roscoe and Bioactive Chemical Analysus using Gas Chromatography Mass Spectrum. Oriental Journal of Chemistry, 32(2), 817-837. doi: 10.13005/ojc/320207

Silva, N. C. C., & Fernandes-Júnior, A. (2010). Biological properties of medicinal plants: a riview of their antimicobial activity. The Journal of Venomous Animals and Toxins including Tropical Diseases, 16(3), 402-413. doi: 10.1590/S1678-91992010000300006

Singleton, V. L., & Rossi, J. A. (1965). Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. American Journal of Enology and Viticulture, 16, 144-158.

Soares, A. A., Jacomassi, E., Mata, R., Lopes, K. F. C., Borges, J. L., Pereira, U. P., Germano, R. M., Otutumi, L. K., Martins, L. A., & Gonçalves, D. D. (2018). Antimicrobial activity of species Zingiber officinale Roscoe and Alpinia purpurata (Vieill.) K. Schum (Zingiberaceae) - review. Semina: Ciências Agrárias, 39(4), 1849-1862. doi: 10.5433/1679-0359.2018v39n4p1849

Sumabranian, V., & Suja, S. (2011). Phytochemical screening of Alpinia purpurata (Vieill). Research Journal of Pharmaceutical, Biological and Chemical Sciences, 2(3), 866-871.

Urrea-Victoria, V., Pires, J., Torres, P. B., Santos, D. Y. A. C., & Chow, F. (2016). Ensaio antioxidante em microplaca do poder de redução do ferro (FRAP) para extratos de algas. Instituto de Biociências: Universidade de São Paulo, 2016.

Villafolres, O. B., Macabeo, A. P. G., Gehle, D., Krohn, K., Franzblau, S. G., & Aguinaldo, A. M. (2011). Phytoconstituints from Alpinia purpurata and their in vitro inhibitory activity against Mycobacterium tuberculosis. Pharmacognosy Magazine, 6(24), 339-344.

Wendlandt, S., Shen, J., Kadlec, K., Wang, Y., Li, B., Zhang, W., Febler, A. T., Wu, C., & Schwarz, S. Multidrug resistance genes in staphylococci from animals that confer resistance to critically and highly important antimicrobial agents in human medicine. (2015). Trends in Microbiology, 23(1), 1-11. doi: 10.1016/j.tim.2014.10.002

Wieler, L. H., Ewers, C., Guenther, S., Walther, B., & Lubke-Becker, A. (2011). International Journal of Medical Microbiology, 301, 635-641. doi:10.1016/j.ijmm.2011.09.009

Wong, L. F., Lim, Y. Y., & Omar, M. (2009). Antioxidant and antimicrobial activities of some Alpinia species. Journal of Food Biochemistry, 33(6), 835-851. doi: 10.1111/j.1745-4514.2009.00258.x




DOI: http://dx.doi.org/10.5433/1679-0359.2021v42n1p179

Semina: Ciênc. Agrár.
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DOI: 10.5433 / 1679-0359
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