Evaluation of a Product Intended for Microbiological Control in Animal Production, and Its Combination With Halquinol

Alberto Gonçalves Evangelista , Lucas dos Santos Janotto , Adriana Paula Possamai , Carolina Cini Perry , Francine Lemes Ribeiro , Rafael Canonenco de Araujo , Fernando Bittencourt Luciano

Animal Research and One Health ›› 2026, Vol. 4 ›› Issue (3) : 302 -313.

PDF (541KB)
Animal Research and One Health ›› 2026, Vol. 4 ›› Issue (3) :302 -313. DOI: 10.1002/aro2.70030
ARTICLE
Evaluation of a Product Intended for Microbiological Control in Animal Production, and Its Combination With Halquinol
Author information +
History +
PDF (541KB)

Abstract

Antimicrobial resistance is an increasingly pressing global concern, with one of its contributing factors being the use of subtherapeutic doses of antibiotics in animal production for zootechnical purposes. Halquinol (HA) remains one of the few compounds still permitted in certain regions; however, the development of alternative solutions is imperative. This study evaluated the in vitro effects of a formulation composed of essential oils and organic acids against Salmonella and Escherichia coli as well as its interaction with HA. The formulation demonstrated both inhibitory and bactericidal activity against the bacteria, with effective concentrations ranging from 2.0 to 8.0 mL/L. In contrast, HA exhibited solely bacteriostatic effects, with minimum inhibitory concentrations ranging from 37.5 to 300 μg/mL. When used in combination, the compounds predominantly resulted in additive or indifferent interactions: 51.35% of the assays showed additive effects, 43.24% exhibited no interaction, and only 5.41% demonstrated antagonistic interactions. Importantly, the formulation did not induce bacterial resistance or adaptation following sublethal exposure. Conversely, sublethal exposure to HA led to an approximately tenfold increase in its bacteriostatic dose. Moreover, the formulation showed potential to mitigate resistance induced by sublethal HA exposure. In a simulated swine digestion, the combination of the formulation with HA was particularly effective against E. coli, with the co-administration reducing the required concentrations of the individual compounds to achieve sustained bacterial suppression throughout the digestive process. Based on these findings, the tested formulation demonstrates promising potential for bacterial control and may be used in combination with HA to reduce its required dosage.

Keywords

animal production / antimicrobial combination / antimicrobial resistance / halquinol

Cite this article

Download citation ▾
Alberto Gonçalves Evangelista, Lucas dos Santos Janotto, Adriana Paula Possamai, Carolina Cini Perry, Francine Lemes Ribeiro, Rafael Canonenco de Araujo, Fernando Bittencourt Luciano. Evaluation of a Product Intended for Microbiological Control in Animal Production, and Its Combination With Halquinol. Animal Research and One Health, 2026, 4 (3) : 302-313 DOI:10.1002/aro2.70030

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

A. G. Evangelista, J. A. F Corrêa, A. C. S. M. Pinto, and F. B. Luciano, “The Impact of Essential Oils on Antibiotic Use in Animal Production Regarding Antimicrobial Resistance—A Review,” Critical Reviews in Food Science and Nutrition 62, no. 19 (2022): 5267–5283, https://doi.org/10.1080/10408398.2021.1883548.

[2]

F. Ma, S. Xu, Z. Tang, Z. Li, and L. Zhang, “Use of Antimicrobials in Food Animals and Impact of Transmission of Antimicrobial Resistance on Humans,” Biosafety and Health 3, no. 1 (2021): 32–38, https://doi.org/10.1016/j.bsheal.2020.09.004.

[3]

T. H. Lee, S. Y. Park, J. Y. Kim, J.-D. Choi, and G. Moon, “Establishment of Analysis Method for the Quantification of Residues of Halquinol and Its Metabolites in Livestock and Fishery Products Using Liquid Chromatography–Tandem Mass Spectrometry,” Applied Biological Chemistry 66, no. 1 (2023): 38, https://doi.org/10.1186/s13765-023-00793-3.

[4]

A. G. Evangelista, L. dS. Janotto, E. H. C. Matté, C. C. Perry, F. L. Ribeiro, and F. B. Luciano, “In Vitro Interaction Between Essential Oil Compounds and Halquinol Against Zoonotic Pathogenic Bacteria,” Biocatalysis and Agricultural Biotechnology (2023): e102672, https://doi.org/10.1016/j.bcab.2023.102672.

[5]

J. A. F. Corrêa, J. V. G. dos Santos, A. G. Evangelista, A. C. S. M Pinto, R. E. F. de Macedo, and F. B. Luciano, “Combined Application of Phenolic Acids and Essential Oil Components Against Salmonella Enteritidis and Listeria monocytogenes in Vitro and in Ready-to-Eat Cooked Ham,” LWT 149 (2021): e111881, https://doi.org/10.1016/j.lwt.2021.111881.

[6]

E. H. C. Matté, F. B. Luciano, and A. G. Evangelista, “Essential Oils and Essential Oil Compounds in Animal Production as Antimicrobials and Anthelmintics: An Updated Review,” Animal Health Research Reviews 24, no. 1 (2023): 1–11, https://doi.org/10.1017/S1466252322000093.

[7]

G. R. Oliveira, W. K. Oliveira, C. Andrade, et al., “Natural Antimicrobials for Control of Salmonella Enteritidis in Feed and in Vitro Model of the Chicken Digestive Process,” Journal of Animal Physiology and Animal Nutrition 103, no. 3 (2019): 756–765, http://doi.wiley.com/10.1111/jpn.13070.

[8]

L. dS. Janotto, T. dM. Nazareth, G. Meca, F. B. Luciano, and A. G. Evangelista, “Exploring the Efficacy of Antibiotic-Essential Oil Combinations: Implications for Combating Antimicrobial Resistance,” Bioresource Technology Reports 24 (2023): e101679, https://doi.org/10.1016/j.biteb.2023.101679.

[9]

B. V. Pearlin, S. Muthuvel, P. Govidasamy, et al., “Role of Acidifiers in Livestock Nutrition and Health: A Review,” Journal of Animal Physiology and Animal Nutrition 104, no. 2 (2020): 558–569, https://doi.org/10.1111/jpn.13282.

[10]

B. Tugnoli, G. Giovagnoni, A. Piva, and E. Grilli, “From Acidifiers to Intestinal Health Enhancers: How Organic Acids Can Improve Growth Efficiency of Pigs,” Animals 10, no. 1 (2020): e134, https://doi.org/10.3390/ani10010134.

[11]

A. E. Kholif, G. A. Gouda, O. A. Olafadehan, S. M. Sallam, and U. Y. Anele, “‘Acidifiers and Organic Acids in Livestock Nutrition and Health’ Organic Feed Additives for Livestock,” Organic Feed Additives for Livestock (2025): 43–56, https://doi.org/10.1016/B978-0-443-13510-1.00003-7.

[12]

GRASP. Linha Aves (2023), https://www.grasp.ind.br/linha-aves/.

[13]

EW Nutrition. Activo (2023), https://ew-nutrition.com/animal-nutrition/products/activo/.

[14]

M. Ryan, “‘Evaluating the Economic Benefits and Costs of Antimicrobial Use in Food-Producing Animals’ OECD Food,” Agriculture and Fisheries Papers 40 (2019), https://doi.org/10.1787/f859f644-en.

[15]

Clinical and Laboratory Standards Institute. Performance Standards for Antimicrobial Susceptibility Testing, 32nd ed. (2022).

[16]

K. Palaniappan and R. A. Holley, “Use of Natural Antimicrobials to Increase Antibiotic Susceptibility of Drug Resistant Bacteria,” International Journal of Food Microbiology 140, no. 2–3 (2010): 164–168, https://doi.org/10.1016/j.ijfoodmicro.2010.04.001.

[17]

H. Yoon, B.-Y. Park, M.-H. Oh, K.-H. Choi, and Y. Yoon, “Effect of Nacl on Heat Resistance, Antibiotic Susceptibility, and Caco-2 Cell Invasion of Salmonella,” BioMed Research International 2013 (2013): 1–5, https://doi.org/10.1155/2013/274096.

[18]

A. G. Evangelista, J. A. F. Corrêa, J. V. G. dos Santos, et al., “Cell-Free Supernatants Produced by Lactic Acid Bacteria Reduce Salmonella Population in Vitro,” Microbiology 167 (2021): 11, https://doi.org/10.1099/mic.0.001102.

[19]

D. H. Nguyen, W. J. Seok, and I. H. Kim, “Organic Acids Mixture as a Dietary Additive for Pigs—A Review,” Animals 10, no. 6 (2020): e952, https://doi.org/10.3390/ani10060952.

[20]

O. A. Odeyemi, O. O. Alegbeleye, M. Strateva, and D. Stratev, “Understanding Spoilage Microbial Community and Spoilage Mechanisms in Foods of Animal Origin,” Comprehensive Reviews in Food Science and Food Safety 19, no. 2 (2020): 311–331, https://doi.org/10.1111/1541-4337.12526.

[21]

C.-Q. Gao, H.-Q. Shi, W.-Y. Xie, et al., “Dietary Supplementation With Acidifiers Improves the Growth Performance, Meat Quality and Intestinal Health of Broiler Chickens,” Animal Nutrition 7, no. 3 (2021): 762–769, https://doi.org/10.1016/j.aninu.2021.01.005.

[22]

M.-C. Meunier-Salaün, J. Chiron, F. Etore, et al., “Drinking Water for Liquid-Fed Pigs,” Animal 11, no. 5 (2017): 836–844, https://doi.org/10.1017/S1751731116002202.

[23]

Quadragen VetHealth. Quadra Gen Nutrition Hal-Q (2022), https://www.indiamart.com/proddetail/nutrition-hal-q-19013618362.html.

[24]

E. M. Adamowicz and W. R. Harcombe, “Weakest-Link Dynamics Predict Apparent Antibiotic Interactions in a Model Cross-Feeding Community,” Antimicrobial Agents and Chemotherapy 64 (2020): 11, https://doi.org/10.1128/AAC.00465-20.

[25]

T. Liu, J. Kang, and L. Liu, “Thymol as a Critical Component of Thymus vulgaris L. Essential Oil Combats Pseudomonas aeruginosa by Intercalating DNA and Inactivating Biofilm,” LWT 136 (2021): e110354, https://doi.org/10.1016/j.lwt.2020.110354.

[26]

I. Sutradhar, C. Ching, D. Desai, Z. Heins, A. S. Khalil, and M. H. Zaman, “Effects of Antibiotic Interaction on Antimicrobial Resistance Development in Wastewater,” Scientific Reports 13, no. 1 (2023): e7801, https://doi.org/10.1038/s41598-023-34935-w.

[27]

A. Ait-Ouazzou, L. Espina, T. K. Gelaw, S. de Lamo-Castellví, R. Pagán, and D. García-Gonzalo, “New Insights in Mechanisms of Bacterial Inactivation by Carvacrol,” Journal of Applied Microbiology 114, no. 1 (2013): 173–185, https://doi.org/10.1111/jam.12028.

[28]

P. V. Pesingi, B. R. Singh, P. K. Pesingi, et al., “MexAB-OprM Efflux Pump of Pseudomonas aeruginosa Offers Resistance to Carvacrol: A Herbal Antimicrobial Agent,” Frontiers in Microbiology 10 (2019): 2664, https://doi.org/10.3389/fmicb.2019.02664.

[29]

A. Tetard, A. Zedet, C. Girard, P. Plésiat, and C. Llanes, “Cinnamaldehyde Induces Expression of Efflux Pumps and Multidrug Resistance in Pseudomonas aeruginosa,” Antimicrobial Agents and Chemotherapy 63 (2019): 10, https://doi.org/10.1128/AAC.01081-19.

[30]

M. A. A. Agreles, I. D. L. Cavalcanti, and I. M. F. Cavalcanti, “The Role of Essential Oils in the Inhibition of Efflux Pumps and Reversion of Bacterial Resistance to Antimicrobials,” Current Microbiology 78, no. 10 (2021): 3609–3619, https://doi.org/10.1007/s00284-021-02635-1.

[31]

R. U. Khan, S. Naz, F. Raziq, et al., “Prospects of Organic Acids as Safe Alternative to Antibiotics in Broiler Chickens Diet,” Environmental Science & Pollution Research 29, no. 22 (2022): 32594–32604, https://doi.org/10.1007/s11356-022-19241-8.

[32]

V. H. Pham, W. Abbas, J. Huang, et al., “Effect of Blending Encapsulated Essential Oils and Organic Acids as an Antibiotic Growth Promoter Alternative on Growth Performance and Intestinal Health in Broilers With Necrotic Enteritis,” Poultry Science 101, no. 1 (2022): e101563, https://doi.org/10.1016/j.psj.2021.101563.

[33]

P. S. X. Yap, B. C. Yiap, H. C. Ping, and S. H. E. Lim, “Essential Oils, a New Horizon in Combating Bacterial Antibiotic Resistance,” Open Microbiology Journal 8, no. 1 (2014): 6–14, https://doi.org/10.2174/1874285801408010006.

[34]

R. I. Carvalho, A. S. de Jesus Medeiros, M. Chaves, E. L. de Souza, and M. Magnani, “Lipids, Ph, and Their Interaction Affect the Inhibitory Effects of Carvacrol Against Salmonella Typhimurium PT4 and Escherichia coli O157:H7,” Frontiers in Microbiology 8 (2018): 2701, https://doi.org/10.3389/fmicb.2017.02701.

[35]

V. Laviniki, C. Simoni, A. F. Carloto, and G. V. Lopes, “The Biofilm-Forming Ability of Salmonella enterica Subsp. Enterica Isolated From Swine-Feed Mills,” Ciência Rural 54 (2024): 4, https://doi.org/10.1590/0103-8478cr20230146.

Rights & permissions

2025 The Author(s). Animal Research and One Health published by John Wiley & Sons Australia, Ltd on behalf of Institute of Animal Science, Chinese Academy of Agricultural Sciences.

PDF (541KB)

0

Accesses

0

Citation

Detail

Sections
Recommended

/

〈 〉