Artificial insemination, as an essential pillar of the modern poultry industry, primarily depends on the quality of semen collected from stud roosters. Since the collection and storage of ejaculates is not a sterile process, antimicrobial agents have become essential supplements to semen extenders. While the use of traditional antibiotics has been challenged because of rising bacterial resistance, natural biomolecules represent an appealing alternative because of their antibacterial and antioxidant properties. As such, this study strived to compare the effects of 50 μmol/L curcumin (CUR) with 31.2 µg/mL kanamycin (KAN) as a conventional antibiotic on rooster sperm quality in the presence of Salmonella enterica, Escherichia coli and Pseudomonas aeruginosa. Changes in sperm structural integrity and functional activity were monitored at 2 and 24 h of culture. Computer-assisted semen analysis revealed significant sperm motility preservation following treatment with KAN, particularly in the case of Salmonella enterica and Pseudomonas aeruginosa (p < 0.001) after 24 h. On the other hand, CUR was more effective in opposing ROS overproduction by all bacteria (p < 0.05), as determined by luminol-based luminometry, and maintained sperm mitochondrial activity (p < 0.001 in the case of Salmonella enterica; p < 0.05 with respect to Escherichia coli and Pseudomonas aeruginosa), as assessed by the fluorometric JC-1 assay. The TUNEL assay revealed that CUR readily preserved the DNA integrity of rooster sperm exposed to Salmonella enterica (p < 0.01) and Escherichia coli (p < 0.001). The bacteriological analysis showed higher efficiency of KAN in preventing the growth of all selected bacterial species (p < 0.0001) as opposed to CUR. In conclusion, CUR provided protection to rooster spermatozoa against alterations caused by uropathogens, most likely through its antioxidant activity. Hence, CUR supplementation to poultry semen extenders in combination with properly selected antibacterial substances may become an interesting strategy in the management of bacterial contamination during semen storage.

AgroBioTech Research Centre Slovak University of Agriculture in Nitra Tr A Hlinku 2 949 76 Nitra Slovakia

Department of Bioenergetics Food Analysis and Microbiology Institute of Food Technology and Nutrition University of Rzeszow Cwiklinskiej 1 35 601 Rzeszow Poland

Department of Fruit Science Viticulture and Enology Faculty of Horticulture and Landscape Engineering Slovak University of Agriculture in Nitra Tr A Hlinku 2 949 76 Nitra Slovakia

Department of Neuroscience 2nd Faculty of Medicine 5 Úvalu 84 150 06 Prague Czech Republic

Institute of Applied Biology Faculty of Biotechnology and Food Sciences Slovak University of Agriculture in Nitra Tr A Hlinku 2 949 76 Nitra Slovakia

Institute of Biotechnology Faculty of Biotechnology and Food Sciences Slovak University of Agriculture in Nitra Tr A Hlinku 2 949 76 Nitra Slovakia

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Mohan J., Sharma S., Kolluri G., Dhama K. History of artificial insemination in poultry, its components and significance. Poult. Sci. J. 2018;74:475–488. doi: 10.1017/S0043933918000430. DOI

Ombelet W., Van Robays J. Artificial insemination history: Hurdles and milestones. Facts Views Vis. Obgyn. 2015;7:137–143. PubMed PMC

Wen C., Mai C., Cai R., Gou Q., Zhang B., Li J., Sun C., Yang N. Inheritance of the duration of fertility in chickens and its correlation with laying performance. Genet. Sel. Evol. 2022;54:41. doi: 10.1186/s12711-022-00733-7. PubMed DOI PMC

Englmaierová M., Tumová E., Charvátová V., Skřivan M. Effects of laying hens housing system on laying performance, egg quality characteristics, and egg microbial contamination. Czech J. Anim. Sci. 2014;59:345–352. doi: 10.17221/7585-CJAS. DOI

Lenický M., Slanina T., Kačániová M., Galovičová L., Petrovičová M., Ďuračka M., Benko F., Kováč J., Tvrdá E. Identification of Bacterial Profiles and Their Interactions with Selected Quality, Oxidative, and Immunological Parameters of Turkey Semen. Animals. 2021;11:1771. doi: 10.3390/ani11061771. PubMed DOI PMC

Gale C., Brown K. The Identification of Bacteria Contaminating Collected Semen and the Use of Antibiotics in Their Control. Poult. Sci. 1961;40:50–55. doi: 10.3382/ps.0400050. DOI

Reiber M.A., McInroy J.A., Conner D.E. Enumeration and identification of bacteria in chicken semen. Poult. Sci. 1995;74:795–799. doi: 10.3382/ps.0740795. PubMed DOI

Cox N.A., Stern N.J., Wilson J.L., Musgrove M.T., Buhr R.J., Hiett K.L. Isolation of Campylobacter spp. from semen samples of commercial broiler breeder roosters. Avian Dis. 2002;46:717–720. doi: 10.1637/0005-2086(2002)046[0717:IOCSFS]2.0.CO;2. PubMed DOI

Haines M.D., Parker H.M., McDaniel C.D., Kiess A.S. Impact of 6 different intestinal bacteria on broiler breeder sperm motility in vitro. Poult. Sci. 2013;92:2174–2181. doi: 10.3382/ps.2013-03109. PubMed DOI

Donoghue A.M., Blore P.J., Cole K., Loskutoff N.M., Donoghue D.J. Detection of Campylobacter or Salmonella in turkey semen and the ability of poultry semen extenders to reduce their concentrations. Poult. Sci. 2004;83:1728–1733. doi: 10.1093/ps/83.10.1728. PubMed DOI

Tvrdá E., Bučko O., Rojková K., Ďuračka M., Kunová S., Kováč J., Benko F., Kačániová M. The Efficiency of Selected Extenders against Bacterial Contamination of Boar Semen in a Swine Breeding Facility in Western Slovakia. Animals. 2021;11:3320. doi: 10.3390/ani11113320. PubMed DOI PMC

Ďuračka M., Belić L., Tokárová K., Žiarovská J., Kačániová M., Lukáč N., Tvrdá E. Bacterial communities in bovine ejaculates and their impact on the semen quality. Syst. Biol. Reprod. Med. 2021;67:438–449. doi: 10.1080/19396368.2021.1958028. PubMed DOI

Tvrdá E., Kačániová M., Baláži A., Vašíček J., Vozaf J., Jurčík R., Ďuračka M., Žiarovská J., Kováč J., Chrenek P. The Impact of Bacteriocenoses on Sperm Vitality, Immunological and Oxidative Characteristics of Ram Ejaculates: Does the Breed Play a Role? Animals. 2022;12:54. doi: 10.3390/ani12010054. PubMed DOI PMC

Jacobs L.A., McDaniel G.R., Broughton C.W. Microbial flora observed within sections of the oviduct in naturally mated, artificially inseminated, and virgin hens. Poult. Sci. 1978;57:1550–1553. doi: 10.3382/ps.0571550. PubMed DOI

Moyle T., Drake K., Gole V., Chousalka K., Hazel S. Bacterial contamination of eggs and behaviour of poultry flocks in the free range environment. Comp. Immunol. Microbiol. Infect. Dis. 2016;49:88–94. doi: 10.1016/j.cimid.2016.10.005. PubMed DOI

Rouger A., Tresse O., Zagorec M. Bacterial Contaminants of Poultry Meat: Sources, Species, and Dynamics. Microorganisms. 2017;5:50. doi: 10.3390/microorganisms5030050. PubMed DOI PMC

Brillard J.P. Practical aspects of fertility in poultry. World’s Poult. Sci. J. 2003;59:441–446. doi: 10.1079/WPS20030027. DOI

Alkali I.M., Asuku S.O., Umar M.B., Abba A., Mustapha A., Bukar M.M., Waziri M.A. Microbial Contaminants in Fresh and Extended Turkey Semen and their Sensitivity to Antibiotics. Nig. Vet. J. 2020;41:1–6. doi: 10.4314/nvj.v41i1.1. DOI

Murugesan S., Mahapatra R. Cryopreservation of Ghagus chicken semen: Effect of cryoprotectants, diluents and thawing temperature. Reprod. Domest. Anim. 2020;55:951–957. doi: 10.1111/rda.13734. PubMed DOI

Morrell J.M., Wallgren M. Alternatives to Antibiotics in Semen Extenders: A Review. Pathogens. 2014;3:934–946. doi: 10.3390/pathogens3040934. PubMed DOI PMC

El B., Bouchicha A., Kalem A., Mimoune N., Djouadi S., Khelef D., Kaidi R. Study of antibiotics and symbiotic effects on sperm quality using the CASA system. Vet. Stan. 2022;53:377–388. doi: 10.46419/vs.53.4.2. DOI

Cauwerts K., Decostere A., De Graef E.M., Haesebrouck F., Pasmans F. High prevalence of tetracycline resistance in Enterococcus isolates from broilers carrying the erm(B) gene. Avian Pathol. 2007;36:395–399. doi: 10.1080/03079450701589167. PubMed DOI

Tvrdá E., Greifová H., Mackovich A., Hashim F., Lukáč N. Curcumin offers antioxidant protection to cryopreserved bovine semen. Czech J. Anim. Sci. 2018;63:247–255. doi: 10.17221/33/2017-CJAS. DOI

Abdelnour S.A., Hassan M.A.E., Mohammed A.K., Alhimaidi A.R., Al-Gabri N., Al-Khaldi K.O., Swelum A.A. The Effect of Adding Different Levels of Curcumin and Its Nanoparticles to Extender on Post-Thaw Quality of Cryopreserved Rabbit Sperm. Animals. 2020;10:1508. doi: 10.3390/ani10091508. PubMed DOI PMC

Lee A.S., Lee S.H., Lee S., Yang B.K. Effects of Curcumin on Sperm Motility, Viability, Mitochondrial Activity and Plasma Membrane Integrity in Boar Semen. Biomed. Sci. Lett. 2017;23:406–410. doi: 10.15616/BSL.2017.23.4.406. DOI

Bucak M.N., Sariozkan S., Tuncer P.B., Sakin F., Atessahin A., Kulaksiz R., Cevik M. The effect of antioxidants on post-thawed Angora goat (Capra hircus ancryrensis) sperm parameters, lipid peroxidation and antioxidant activities. Small Rum. Res. 2010;89:24–30. doi: 10.1016/j.smallrumres.2009.11.015. PubMed DOI

Jalili F., Zareh-Shahneh A., Zeinoaldini S., Yousefi A.R., Kazemizadeh A. The effect of curcumin on frozen-thawed sperm quality and fertility of broiler breeder roosters. Iran J. Anim. Sci. 2020;50:295–306. doi: 10.22059/ijas.2018.252502.653618. DOI

Jakubczyk K., Drużga A., Katarzyna J., Skonieczna-Żydecka K. Antioxidant Potential of Curcumin—A Meta-Analysis of Randomized Clinical Trials. Antioxidants. 2020;9:1092. doi: 10.3390/antiox9111092. PubMed DOI PMC

Sharifian P., Yaslianifard S., Fallah P., Aynesazi S., Bakhtiyari M., Mohammadzadeh M. Investigating the Effect of Nano-Curcumin on the Expression of Biofilm Regulatory Genes of Pseudomonas aeruginosa. Infect. Drug Resist. 2020;13:2477–2484. doi: 10.2147/IDR.S263387. PubMed DOI PMC

Adamczak A., Ożarowski M., Karpiński T.M. Curcumin, a Natural Antimicrobial Agent with Strain-Specific Activity. Pharmaceuticals. 2020;13:153. doi: 10.3390/ph13070153. PubMed DOI PMC

Duracka M., Lukac N., Kacaniova M., Kantor A., Hleba L., Ondruska L., Tvrda E. Antibiotics Versus Natural Biomolecules: The Case of In Vitro Induced Bacteriospermia by Enterococcus faecalis in Rabbit Semen. Molecules. 2019;24:4329. doi: 10.3390/molecules24234329. PubMed DOI PMC

Sexton T.J., Jacobs L.A., McDaniel G.R. A new poultry semen extender. 4. Effect of antibacterials in control of bacterial contamination in chicken semen. Poult. Sci. 1980;59:274–281. doi: 10.3382/ps.0590274. PubMed DOI

Shafeeque C.M., Singh R.P., Sharma S.K., Mohan J., Sastry K.V., Kolluri G., Saxena V.K., Tyagi J.S., Kataria J.M., Azeez P.A. Development of a new method for sperm RNA purification in the chicken. Anim. Reprod. Sci. 2014;149:259–265. doi: 10.1016/j.anireprosci.2014.06.032. PubMed DOI

Slanina T., Miškeje M., Tirpák F., Błaszczyk M., Formicki G., Massányi P. Caffeine Strongly Improves Motility Parameters of Turkey Spermatozoa with No Effect on Cell Viability. Acta Vet. Hung. 2018;66:137–150. doi: 10.1556/004.2018.013. PubMed DOI

Boone M.A., Hughes B.L. Contamination of semen and its effect on avian fertility. Poult. Sci. 1970;49:402–404. doi: 10.3382/ps.0490402. PubMed DOI

Ahmed K. Bacterial Flora of Poultry Semen and Their Antibiotic Sensitivity Pattern. Int. J. Appl. Pure Sci. Agric. 2015;1:39–41.

Keller L.H., Benson C.E., Krotec K., Eckroade R.J. Salmonella enteritidis colonization of the reproductive tract and forming and freshly laid eggs of chickens. Infect. Immun. 1995;63:2443–2449. doi: 10.1128/iai.63.7.2443-2449.1995. PubMed DOI PMC

Vizzier-Thaxton Y., Cox N.A., Richardson L.J., Buhr R.J., McDaniel C.D., Cosby D.E., Wilson J.L., Bourassa D.V., Ard M.B. Apparent attachment of Campylobacter and Salmonella to broiler breeder rooster spermatozoa. Poult. Sci. 2006;85:619–624. doi: 10.1093/ps/85.4.619. PubMed DOI

Iaffaldano N., Reale A., Sorrentino E., Coppola R., Di Iorio M., Rosato M.P. Risk of Salmonella transmission via cryopreserved semen in turkey flocks. Poult. Sci. 2010;89:1975–1980. doi: 10.3382/ps.2009-00573. PubMed DOI

Perek M., Elian M., Heller E.D. Bacterial flora of semen and contamination of the reproductive organs of the hen following artificial insemination. Res. Vet. Sci. 1969;10:127–132. doi: 10.1016/S0034-5288(18)34460-6. PubMed DOI

Mezhoud H., Boyen F., Touazi L.H., Garmyn A., Moula N., Smet A., Haesbrouck F., Martel A., Iguer-Ouada M., Touati A. Extended spectrum β-lactamase producing Escherichia coli in broiler breeding roosters: Presence in the reproductive tract and effect on sperm motility. Anim. Reprod. Sci. 2015;159:205–211. doi: 10.1016/j.anireprosci.2015.06.021. PubMed DOI

Negi S., Vander H., Chauhan A., Rana K., Prabha V. Microbial Sperm Immobilization Factor from Pseudomonas aeruginosa as a Contraceptive Agent: An Experimental Study. Ann. Infert. Rep. Endocrin. 2018;1:1007.

Sepúlveda L., Bussalleu E., Yeste M., Bonet S. Effect of Pseudomonas aeruginosa on sperm capacitation and protein phosphorylation of boar spermatozoa. Theriogenology. 2016;85:1421–1431. doi: 10.1016/j.theriogenology.2015.12.025. PubMed DOI

Stones D.H., Krachler A.M. Against the tide: The role of bacterial adhesion in host colonization. Biochem. Soc. Trans. 2016;44:1571–1580. doi: 10.1042/BST20160186. PubMed DOI PMC

Benoff S., Cooper G.W., Centola G.M., Jacob A., Hershlag A., Hurley I.R. Metal ions and human sperm mannose receptors. Andrologia. 2000;32:317–329. doi: 10.1046/j.1439-0272.2000.00401.x. PubMed DOI

Wolff H., Panhans A., Stolz W., Meurer M. Adherence of Escherichia coli to sperm: A mannose mediated phenomenon leading to agglutination of sperm and E. coli. Fertil. Steril. 1993;60:154–158. doi: 10.1016/S0015-0282(16)56054-3. PubMed DOI

Fraczek M., Piasecka M., Gaczarzewicz D., Szumala-Kakol A., Kazienko A., Lenart S., Laszczynska M., Kurpisz M. Membrane stability and mitochondrial activity of human-ejaculated spermatozoa during in vitro experimental infection with Escherichia coli, Staphylococcus haemolyticus and Bacteroides ureolyticus. Andrologia. 2012;44:315–329. doi: 10.1111/j.1439-0272.2012.01283.x. PubMed DOI

Prabha V., Sandhu R., Kaur S., Kaur K., Sarwal A., Mavuduru R.S., Singh S.K. Mechanism of sperm immobilization by Escherichia coli. Adv. Urol. 2010;2010:240268. doi: 10.1155/2010/240268. PubMed DOI PMC

Berger G.K., Smith-Harrison L.I., Sandlow J.I. Sperm agglutination: Prevalence and contributory factors. Andrologia. 2019;51:e13254. doi: 10.1111/and.13254. PubMed DOI

He B., Guo H., Gong Y., Zhao R. Lipopolysaccharide-induced mitochondrial dysfunction in boar sperm is mediated by activation of oxidative phosphorylation. Theriogenology. 2017;87:1–8. doi: 10.1016/j.theriogenology.2016.07.030. PubMed DOI

Ristow L.C., Welch R.A. Hemolysin of uropathogenic Escherichia coli: A cloak or a dagger? Biochim. Biophys. Acta. 2016;1858:538–545. doi: 10.1016/j.bbamem.2015.08.015. PubMed DOI

Baronetti J.L., Villegas N.A., Aiassa V., Paraje M.G., Albesa I. Hemolysin from Escherichia coli induces oxidative stress in blood. Toxicon. 2013;70:15–20. doi: 10.1016/j.toxicon.2013.03.014. PubMed DOI

Kaur K., Kaur S., Rishi P., Singh S.K., Prabha V. Evidence for the occurrence of receptor in sperm for sperm agglutinating factor isolated from Escherichia coli. Gynecol. Endocrinol. 2012;34:207–209. doi: 10.1155/2013/548497. DOI

Vander H., Gupta S., Kaur S., Kaur K., Prabha V. Characterization of sperm immobilization factor from Escherichia coli and its receptor to study the underlying mechanism of sperm immobilization. Am. J. Biomed. Sci. 2013;5:25–33. doi: 10.5099/aj130100025. DOI

Ďuračka M., Khasanova N., Slanina T., Lukáč N., Tvrdá E. The in vitro effect of kanamycin on the behaviour of bovine spermatozoa. Arch. Ecotoxicol. 2019;1:36–40. doi: 10.36547/ae.2019.1.4.36-40. DOI

Belenky P., Ye J.D., Porter C.B., Cohen N.R., Lobritz M.A., Ferrante T., Jain S., Korry B.J., Schwarz E.G., Walker G.C., et al. Bactericidal Antibiotics Induce Toxic Metabolic Perturbations that Lead to Cellular Damage. Cell Rep. 2015;13:968–980. doi: 10.1016/j.celrep.2015.09.059. PubMed DOI PMC

Santonastaso M., Mottola F., Iovine C., Colacurci N., Rocco L. Protective Effects of Curcumin on the Outcome of Cryopreservation in Human Sperm. Reprod Sci. 2021;28:2895–2905. doi: 10.1007/s43032-021-00572-9. PubMed DOI PMC

Soleimanzadeh A., Saberivand A. Effect of curcumin on rat sperm morphology after the freeze-thawing process. Vet. Res. Forum. 2013;4:185–189. PubMed PMC

Omur A.D., Coyan K. Protective effects of the antioxidants curcumin, ellagic acid and methionine on motility, mitochondrial transmembrane potential, plasma membrane and acrosome integrity in freeze-thawed Merino ram sperm. Vet. Med. 2016;61:10–16. doi: 10.17221/8677-VETMED. DOI

Tvrdá E., Lovíšek D., Gálová E., Schwarzová M., Kováčiková E., Kunová S., Žiarovská J., Kačániová M. Possible Implications of Bacteriospermia on the Sperm Quality, Oxidative Characteristics, and Seminal Cytokine Network in Normozoospermic Men. Int. J. Mol. Sci. 2022;23:8678. doi: 10.3390/ijms23158678. PubMed DOI PMC

Kohanski M.A., Dwyer D.J., Hayete B., Lawrence C.A., Collins J.J. A common mechanism of cellular death induced by bactericidal antibiotics. Cell. 2007;130:797–810. doi: 10.1016/j.cell.2007.06.049. PubMed DOI

Sahebkar A., Cicero A.F.G., Simental-Mendía L.E., Aggarwal B.B., Gupta S.C. Curcumin downregulates human tumor necrosis factor-α levels: A systematic review and meta-analysis of randomized controlled trials. Pharmacol. Res. 2016;107:234–242. doi: 10.1016/j.phrs.2016.03.026. PubMed DOI

Fraczek M., Kurpisz M. Mechanisms of the harmful effects of bacterial semen infection on ejaculated human spermatozoa: Potential inflammatory markers in semen. Folia Histochem. Cyto. 2015;53:201–217. doi: 10.5603/fhc.a2015.0019. PubMed DOI

Zhao X., Drlica K. Reactive oxygen species and the bacterial response to lethal stress. Curr. Opin. Microbiol. 2014;21:1–6. doi: 10.1016/j.mib.2014.06.008. PubMed DOI PMC

Aparnak P., Saberivand A. Effects of curcumin on canine semen parameters and expression of NOX5 gene in cryopreserved spermatozoa. Vet. Res. Forum. 2019;10:221–226. doi: 10.30466/vrf.2019.76137.2015. PubMed DOI PMC

Tvrdá E., Tušimová E., Kováčik A., Paál D., Greifová H., Abdramanov A., Lukáč N. Curcumin has protective and antioxidant properties on bull spermatozoa subjected to induced oxidative stress. Anim. Reprod. Sci. 2016;172:10–20. doi: 10.1016/j.anireprosci.2016.06.008. PubMed DOI

Bucak M.N., Başpınar N., Tuncer P.B., Coyan K., Sarıözkan S., Akalın P.P., Büyükleblebici S., Küçükgünay S. Effects of curcumin and dithioerythritol on frozen-thawed bovine semen. Andrologia. 2012;44:102–109. doi: 10.1111/j.1439-0272.2010.01146.x. PubMed DOI

Eini F., Kutenaei M.A., Zareei F., Dastjerdi Z.S., Shirzeyli M.H., Salehi E. Effect of bacterial infection on sperm quality and DNA fragmentation in subfertile men with leukocytospermia. BMC Mol. Cell. Biol. 2021;22:42. doi: 10.1186/s12860-021-00380-8. PubMed DOI PMC

Tvrdá E., Benko F., Ďuračka M. Oxidative Stress as an Underlying Mechanism of Bacteria-Inflicted Damage to Male Gametes. Oxygen. 2022;2:547–569. doi: 10.3390/oxygen2040036. DOI

Fraczek M., Hryhorowicz M., Gaczarzewicz D., Szumala-Kakol A., Kolanowski T.J., Beutin L., Kurpisz M. Can apoptosis and necrosis coexist in ejaculated human spermatozoa during in vitro semen bacterial infection? J. Assist. Reprod. Genet. 2015;32:771–779. doi: 10.1007/s10815-015-0462-x. PubMed DOI PMC

Azawi I., Ismaeel M.A. Influence of addition of different antibiotics in semen diluent on viable bacterial count and spermatozoal viability of Awassi ram semen. Vet. World. 2012;5:75–79. doi: 10.5455/vetworld.2012.75-79. DOI

Khaki A. Assessment on the adverse effects of Aminoglycosides and Flouroquinolone on sperm parameters and male reproductive tissue: A systematic review. Iran. J. Reprod. Med. 2015;13:125–134. PubMed PMC

Di Iorio M., Marchisi A., Rocco M., Chrenek P., Iaffaldano N. Comparison of different extenders on the preservability of rabbit semen stored at 5 °C for 72 hours. Ital. J. Anim. Sci. 2014;13:710–714. doi: 10.4081/ijas.2014.3444. DOI

Acharya M., Burke J., Rorie R. Effect of Semen Extender and Storage Temperature on Motility of Ram Spermatozoa. Adv. Reprod. Sci. 2020;8:14–30. doi: 10.4236/arsci.2020.81002. DOI

Zaghloul A.A. Relevance of Honey Bee in Semen Extender on the Quality of Chilled-Stored Ram Semen. J. Anim. Poultry Prod. Mansoura Univ. 2017;8:1–5. doi: 10.21608/jappmu.2017.45740. DOI

Back D.G., Pickett B.W., Voss J.L., Seidel G.E. Effect of antibacterial agents on the motility of stallion spermatozoa at various storage times, temperatures and dilution ratios. J. Anim. Sci. 1975;41:137–143. doi: 10.2527/jas1975.411137x. PubMed DOI

Gross S., Seinige D., Kehrenberg C., Oliveira M., Siebert U. Occurrence of Antimicrobial-Resistant Escherichia coli in Marine Animals in the North and Baltic Sea: Preliminary Results; Proceedings of the from the 50th Annual IAAAM Conference; Durban, South Africa. 18–22 May 2019.

McMillan E.A., Nguyen L.-H.T., Hiott L.M., Sharma P., Jackson C.R., Frye J.G., Chen C.-Y. Genomic Comparison of Conjugative Plasmids from Salmonella enterica and Escherichia coli Encoding Beta-Lactamases and Capable of Mobilizing Kanamycin Resistance Col-like Plasmids. Microorganisms. 2021;9:2205. doi: 10.3390/microorganisms9112205. PubMed DOI PMC

Poole K. Pseudomonas aeruginosa: Resistance to the max. Front. Microbiol. 2011;2:65. doi: 10.3389/fmicb.2011.00065. PubMed DOI PMC

Faisal A.J., Salman H.A. Determination of Semen Quality and Antibacterial Susceptibility Pattern of Bacteria Isolated from Semen of Iraqi Subjects. Microbiol. Biotechnol. Lett. 2021;49:587–593. doi: 10.48022/mbl.2108.08006. DOI

Salman H.A., Abdulmohsen A.M., Falih M.N., Romi Z.M. Detection of multidrug-resistant Salmonella enterica subsp. enterica serovar Typhi isolated from Iraqi subjects. Vet. World. 2021;14:1922–1928. doi: 10.14202/vetworld.2021.1922-1928. PubMed DOI PMC

Goularte K.L., Voloski F.L.S., Redú J.F.M., Ferreira C.E.R., Vieira A.D., Duval E.H., Mondadori R.G., Lucia T., Jr. Antibiotic resistance in microorganisms isolated in a bull semen stud. Reprod. Domest. Anim. 2020;55:318–324. doi: 10.1111/rda.13621. PubMed DOI

Bresciani C., Cabassi C.S., Morini G., Taddei S., Bigliardi E., Di Lanni F., Sabboni A., Parmigiani E. Boar semen bacterial contamination in Italy and antibiotic efficacy in a modified extender. Ital. J. Anim. Sci. 2014;13:3082. doi: 10.4081/ijas.2014.3082. DOI

Kaur A., Sharma P., Capalash N. Curcumin alleviates persistence of Acinetobacter baumannii against colistin. Sci. Rep. 2018;8:11029. doi: 10.1038/s41598-018-29291-z. PubMed DOI PMC

Gülen D., Şafak B., Erdal B., Günaydın B. Curcumin-meropenem synergy in carbapenem resistant Klebsiella pneumoniae curcumin-meropenem synergy. Iran. J. Microbiol. 2021;13:345–351. doi: 10.18502/ijm.v13i3.6397. PubMed DOI PMC

Yuan Y., Liu Q., Huang Y., Qi M., Yan H., Li W., Zhuang H. Antibacterial Efficacy and Mechanisms of Curcumin-Based Photodynamic Treatment against Staphylococcus aureus and Its Application in Juices. Molecules. 2022;27:7136. doi: 10.3390/molecules27207136. PubMed DOI PMC

Tyagi P., Singh M., Kumari H., Kumari A., Mukhopadhyay K. Bactericidal activity of curcumin I is associated with damaging of bacterial membrane. PLoS ONE. 2015;10:e0121313. doi: 10.1371/journal.pone.0121313. PubMed DOI PMC

Dai C., Lin J., Li H., Shen Z., Wang Y., Velkov T., Shen J. The Natural Product Curcumin as an Antibacterial Agent: Current Achievements and Problems. Antioxidants. 2022;11:459. doi: 10.3390/antiox11030459. PubMed DOI PMC

Gholami M., Zeighami H., Bikas R., Heidari A., Rafiee F., Haghi F. Inhibitory activity of metal-curcumin complexes on quorum sensing related virulence factors of Pseudomonas aeruginosa PAO1. AMB Express. 2020;10:111. doi: 10.1186/s13568-020-01045-z. PubMed DOI PMC

Haukvik T., Bruzell E., Kristensen S., Tønnesen H.H. Photokilling of bacteria by curcumin in different aqueous preparations. Studies on curcumin and curcuminoids XXXVII. Die Pharmazie. 2009;64:666–673. PubMed

Moghaddam K., Iranshahi M., Yazdi M., Shahverdi A. The combination effect of curcumin with different antibiotics against Staphylococcus aureus. Int. J. Green Pharm. 2009;3:141–143.

Mun S.H., Kim S.B., Kong R., Choi J.G., Kim Y.C., Shin D.W., Kang O.H., Kwon D.Y. Curcumin reverse methicillin resistance in Staphylococcus aureus. Molecules. 2014;19:18283–18295. doi: 10.3390/molecules191118283. PubMed DOI PMC

Ďuračka M., Halenár M., Tvrdá E. In vitro effects of selected biologically active compounds on rabbit spermatozoa motility behaviour. J. Microbiol. Biotech. Food Sci. 2017;6:1290–1294. doi: 10.15414/jmbfs.2017.6.6.1290-1294. DOI

Marathe S.A., Ray S., Chakravortty D. Curcumin increases the pathogenicity of Salmonella enterica serovar Typhimurium in murine model. PLoS ONE. 2010;5:e11511. doi: 10.1371/journal.pone.0011511. PubMed DOI PMC

Short-Term Storage of Rooster Ejaculates: Sperm Quality and Bacterial Profile Differences in Selected Commercial Extenders

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