78株鸡关节炎源金黄色葡萄球菌毒力基因与耐药基因分析

doi:10.11843/j.issn.0366-6964.2025.11.026

摘要/Abstract

摘要：

金黄色葡萄球菌是禽养殖业常见的病原菌，因其携带多种毒力因子及多重耐药性，对禽养殖业造成严重的经济损失。为探究辽宁沈阳地区鸡关节炎源金黄色葡萄球菌的流行特征，对2023—2024年分离的78株鸡关节炎性金黄色葡萄球菌进行毒力基因与耐药基因的分析。通过聚合酶链式反应(PCR)对毒力基因分布、耐药基因进行检测，采用K-B法检测其耐药性，通过结晶紫染色法对生物被膜形成能力进行检测。通过对15种毒力基因进行检测，黏附基因clfA检出率最高为100%，随后依次为黏附基因clfB(98.7%)和溶血素基因hlA(82%)，而中毒性休克综合征毒素基因tssT(12.8%)、肠毒素基因seA(3.8%)和剥脱毒素基因etA(1.3%)的检出率低。对10种抗生素耐药性检测显示，78株金黄色葡萄球菌均呈现不同程度的耐药，对四环素(100%)、青霉素G(98.7%)、诺氟沙星(96.2%)、克林霉素(89.7%)、复方新诺明(84.6%)、庆大霉素(82.1%)、红霉素(79.5%)的耐药率较高，但对头孢西丁和利福平(97.4%)敏感。对15种耐药基因进行检测，显示分离菌携带多种耐药基因，氨基糖苷类耐药基因aac(6')/aph(2')和ant(4')的检出率分别为92.3%和80.8%，大环内酯类耐药基因ermC和ermB检出率分别为53.8%和50.0%，但四环素类耐药基因tetM检出率仅为19.2%。对分离菌株生物被膜形成能力检测表明，有73株金黄色葡萄球菌具有生物被膜形成能力，占比为93.6%。对耐药基因与耐药表型的相关性分析结果显示，氨基糖苷类耐药基因aac(6')/aph(2″)和ant(4')、大环内酯类耐药基因ermB和ermC及多重耐药基因cfr分别与庆大霉素耐药菌株、红霉素耐药菌株、红霉素和青霉素G耐药菌株有显著相关性(P < 0.05)。对生物被膜表型与耐药表型进行相关性分析，结果显示红霉素及氯霉素耐药株的产生与生物被膜的形成具有显著相关性(P < 0.05)。78株鸡关节炎源金黄色葡萄球菌的耐药性强，易形成生物被膜，可为该地区金黄色葡萄球菌引起的鸡关节炎防控提供了参考。

关键词: 鸡关节炎源性金黄色葡萄球菌, 毒力基因, 生物被膜, 耐药性

Abstract:

Staphylococcus aureus is a common pathogen in the poultry industry, causing significant economic losses due to its multiple virulence factors and multidrug resistance. To investigate the epidemiological characteristics of Staphylococcus aureus from chicken arthritis sources in Shenyang, Liaoning, a total of 78 strains of Staphylococcus aureus isolated from chicken arthritis sources between 2023 and 2024 were analyzed for virulence and resistance genes. The distribution of virulence genes and antibiotic resistance genes was detected using polymerase chain reaction (PCR). Antibiotic susceptibility was determined by the Kirby-Bauer (K-B) method, and biofilm formation capacity was assessed via crystal violet staining. Among the 15 virulence genes tested, the adhesion gene clfA had the highest detection rate (100%), followed by the adhesion gene clfB (98.7%) and the hemolysin gene hlA (82%). In contrast, the toxic shock syndrome toxin gene tssT (12.8%), enterotoxin gene seA (3.8%), and exfoliative toxin gene etA (1.3%) showed low detection rates. Antibiotic resistance testing against 10 antibiotics revealed that all 78 strains exhibited varying degrees of resistance. High resistance rates were observed for tetracycline (100%), penicillin G (98.7%), norfloxacin (96.2%), clindamycin (89.7%), trimethoprim-sulfamethoxazole (84.6%), gentamicin (82.1%), and erythromycin (79.5%). However, the strains were highly susceptible to cefoxitin and rifampicin (97.4%). Among the 15 antibiotic resistance genes tested, the aminoglycoside resistance genes aac(6') /aph(2″) and ant(4') were detected at rates of 92.3% and 80.8%, respectively. The macrolide resistance genes ermC and ermB were detected at 53.8% and 50.0%, respectively, while the tetracycline resistance gene tetM was only detected in 19.2% of strains. Biofilm formation assays demonstrated that 73 strains (93.6%) exhibited biofilm-forming capacity. Correlation analysis revealed significant associations between aminoglycoside resistance genes (aac(6') /aph(2″) and ant(4')), macrolide resistance genes (ermB and ermC), and the multidrug resistance gene cfr with resistance to gentamicin, erythromycin, and penicillin G, respectively (P < 0.05). For the correlation between biofilm phenotype and antibiotic resistance phenotypes, the results indicated that the development of erythromycin- and chloramphenicol-resistant strains was significantly correlated with biofilm formation (P < 0.05). The 78 strains of Staphylococcus aureus isolated from chicken arthritis exhibited strong drug resistance and a high propensity for biofilm formation, providing valuable insights for the prevention and control of chicken arthritis caused by Staphylococcus aureus in this region.

Key words: Staphylococcus aureus, virulence genes, biofilm, drug resistance

中图分类号:

S852.611

聂莲花, 樊文燕, 李梦雅, 丁纯海, 吴自豪, 王志豪, 李芳芳, 蒋蔚, 韩先干, 王海东. 78株鸡关节炎源金黄色葡萄球菌毒力基因与耐药基因分析[J]. 畜牧兽医学报, 2025, 56(11): 5670-5682.

NIE Lianhua, FAN Wenyan, LI Mengya, DING Chunhai, WU Zihao, WANG Zhihao, LI Fangfang, JIANG Wei, HAN Xiangan, WANG Haidong. Analysis of Virulence and Antibiotic Resistance Genes in 78 Strains of Staphylococcus aureus from Chicken Arthritis Sources[J]. Acta Veterinaria et Zootechnica Sinica, 2025, 56(11): 5670-5682.

图/表 13

表 1

本研究所用引物"

分类 Classification	基因名称 Gene name	引物序列(5′→3′) Primer sequence	产物大小/bp Length
特异性基因 Specific gene	nuc	GCGATTGATGGTGATACGGTT	279
特异性基因 Specific gene	nuc	AGCCAAGCCTTGACGAACTAAAGC	279
肠毒素 Enterotoxin	seA	GCA GGG AAC AGC TTT AGG C	521
	seA	GTT CTG TAG AAG TAT GAAACA CG	521
	seC	CTT GTA TGT ATG GAG GAA TAA CAA	284
	seC	TGC AGG CAT CAT ATC ATA CCAA	284
	seH	CAA CTG CTG ATT TAG CTC AG	359
	seH	GTC GAA TGA GTAATC TCT AGG	359
	seJ	CAT CAG AAC TGT TGT TCC GCT AG	142
	seJ	CTG AAT TTT ACC ATC AAA GGT AC	142
中毒性休克综合征毒素 Toxic shock syndrome toxin	tssT	GCT TGC GAC AAC TGC TAC AG	559
中毒性休克综合征毒素 Toxic shock syndrome toxin	tssT	TGG ATC CGT CAT TCA TTG TTA	559
剥脱毒素 Exfoliative toxin	pvL	ATC ATT AGG TAAAAT GTC TGG ACAT GAT CCA	433
	pvL	GCA TCA AST GTA TTG GAT AGC AAAAGC	433
	etA	CGC TGC GGA CAT TCC TAC ATG G	676
	etA	TAC ATG CCC GCC ACT TGC TTG T	676
	etB	CAG ATAAAG AGC TTT ATA CAC ACA TTA	612
	etB	AGT GAA CTT ATC TTT CTA TTG AAA AAC ACT C	612
溶血素 Hemolysin	hlA	CTG ATT ACT ATC CAA GAA ATT CGA TTG	209
	hlA	CTT TCC AGC CTA CTT TTT TAT CAG T	209
	hlB	GTG CAC TTA CTG ACA ATA GTG C	309
	hlB	GTT GAT GAG TAG CTA CCT TCA GT	309
纤连蛋白结合蛋白 Fibronectin-binding protein	fnbA	GTG AAG TTT TAG AAG GTG GAAAGA TTA G	634
	fnbA	GCT CTT GTAAGA CCA TTT TTC TTC AC	634
	fnbB	GTAACA GCT AAT GGT CGA ATT GAT ACT	524
	fnbB	CAA GTT CGA TAG GAG TAC TAT GTT C	524
黏附因子 Adhesion factor	clfA	ATT GGC GTG GCT TCA GTG CT	292
	clfA	CGT TTC TTC CGT AGT TGC ATT TG	292
	clfB	TGC AAG TGC AGA TTC CGA AAA AAA C	194
	clfB	CCG TCG GTT GAG GTG TTT CAT TTG	194
胶原蛋白黏附素 Collagen adhesin	cnA	AAA GCG TTG CCT AGT GGA GAC	228
胶原蛋白黏附素 Collagen adhesin	cnA	AGT GCC TTC CCA AAC CTT TT	228
多重耐药基因 Multidrug-resistant gene	Cfr	TGAAGTATAAAGCAGGTTGGGAGTCA	746
多重耐药基因 Multidrug-resistant gene	Cfr	ACCATATAATTGACCACAAGCAGC	746
氨基糖苷类 Aminoglycoside	aac(6′)/aph(2′)	CCAAGAGCAATAAGGGCATA	220
	aac(6′)/aph(2′)	CACTATCATAACCACTACCG	220
	aph(3′)-Ⅲa	CACTATCATAACCACTACCG	523
	aph(3′)-Ⅲa	GCCGATGTGGATTGCGAAAA	523
	ant(4′)	GCAAGGACCGACAACATTTC	294
	ant(4′)	TGGCACAGATGGTCATAACC	294
	ant(6′)	ACTGCTTAATCAATTGG	597
	ant(6′)	GCCTTTCCGCCACCTCACCG	597
	ant(3′)	TGATTTGCTGGTTACGGTGAC	284
	ant(3′)	CGCTATGTTCTCTTGCTTTTG	284
大环内酯类 Macrolide	ermA	TCAGGAAAAGGACATTTTACC	423
	ermA	ATACTTTTTGTAGTCCTTCTT	423
	ermB	TGGTATTCCAAATGCGTAATG	745
	ermB	CTGTGGTATGGCGGGTAAGT	745
	ermC	CGTAACTGCCATTGAAATAGACC	246
	ermC	AATAATCTTTTAGCAAACCCGTA	246
四环素类 Tetracycline	tetM	GTGGACAAAGGTACAACGAG	406
	tetM	CGGTAAAGTTCGTCACACAC	406
	tetO	AACTTAGGCATTCTGGCTCAC	515
	tetO	TCCCACTGTTCCATATCGTCA	515
万古霉素 Vancomycin	vanA	GCTATTCAGCTGTACTC	783
	vanA	CAGCGGCCATCATACGG	783
	vanB	CATCGCCGTCCCCGAATTTCAAA	297
	vanB	GATGCGGAAGATACCGTGGCT	297
	vanC	GGTATCAAGGAAACCTC	822
	vanC	CTTCCGCCATCATAGCT	822
β-内酰胺类 β-lactam	femA	TTACTACGCTGGTGGAACTTCA	191
β-内酰胺类 β-lactam	femA	CATCGGCATCATAGCCCTTT	191

表 1

表 2

图 1

图 2

图 3

表 3

表 4

图 4

图 5

图 6

图 7

表 5

表 6

生物被膜表型与耐药表型相关性分析结果"

抗生素 Antibiotics	分类 Classification	生物被膜/% Biofilm				总计 Total	χ²	P
抗生素 Antibiotics	分类 Classification	无 None	弱 Weak	中 Moderate	强 Strong	总计 Total	χ²	P
克林霉素 Clindamycin	敏感Sensitivity	0(0.00)	0(0.00)	0(0.00)	1(4.00)	1(1.28)	4.343	0.227
	中介Intermediary	0(0.00)	1(3.85)	2(9.09)	5(20.00)	8(10.26)
	耐药Resistance	5(100.00)	25(96.15)	20(90.91)	20(80.00)	70(89.74)
	总计Total	5	26	22	25	78
庆大霉素 Gentamicin	敏感Sensitivity	1(20.00)	4(15.38)	5(22.73)	1(4.00)	11(14.10)	6.967	0.324
	中介Intermediary	0(0.00)	1(3.85)	2(9.09)	0(0.00)	3(3.85)
	耐药Resistance	4(80.00)	21(80.77)	15(68.18)	24(96.00)	64(82.05)
	总计Total	5	26	22	25	78
青霉素G Penicillin G	敏感Sensitivity	0(0.00)	0(0.00)	0(0.00)	1(4.00)	1(1.28)	2.148	0.542
	中介Intermediary	0(0.00)	0(0.00)	0(0.00)	1(4.00)	1(1.28)
	耐药Resistance	5(100.00)	26(100.00)	22(100.00)	24(96.00)	77(98.72)
	总计Total	5	26	22	25	78
红霉素 Erythromycin	敏感Sensitivity	0(0.00)	1(3.85)	2(9.09)	11(44.00)	14(17.95)	23.086	0.001^**
	中介Intermediary	0(0.00)	0(0.00)	0(0.00)	2(8.00)	2(2.56)
	耐药Resistance	5(100.00)	25(96.15)	20(90.91)	12(48.00)	62(79.49)
	总计Total	5	26	22	25	78
诺氟沙星 Norfloxacin	敏感Sensitivity	0(0.00)	0(0.00)	1(4.55)	1(4.00)	2(2.56)	3.546	0.738
	中介Intermediary	0(0.00)	0(0.00)	0(0.00)	1(4.00)	1(1.28)
	耐药Resistance	5(100.00)	26(100.00)	21(95.45)	23(92.00)	75(96.15)
	总计Total	5	26	22	25	78
利福平 Rifampicin	敏感Sensitivity	5(100.00)	26(100.00)	21(95.45)	24(96.00)	76(97.44)	1.368	0.713
	中介Intermediary	0(0.00)	0(0.00)	0(0.00)	1(4.00)	1(1.28)
	耐药Resistance	0(0.00)	0(0.00)	1(4.55)	1(4.00)	2(2.56)
	总计Total	5	26	22	25	78
复方新诺明 Compound sulfamethoxazole	敏感Sensitivity	1(20.00)	4(15.38)	5(22.73)	1(4.00)	11(14.10)	6.432	0.377
	中介Intermediary	0(0.00)	0(0.00)	1(4.55)	0(0.00)	1(1.28)
	耐药Resistance	4(80.00)	22(84.62)	16(72.73)	24(96.00)	66(84.62)
	总计Total	5	26	22	25	78
氯霉素 Chloramphenicol	敏感Sensitivity	1(20.00)	6(23.08)	8(36.36)	9(36.00)	24(30.77)	26.915	0.000^**
	中介Intermediary	2(40.00)	2(7.69)	1(4.55)	13(52.00)	18(23.08)
	耐药Resistance	2(40.00)	18(69.23)	13(59.09)	3(12.00)	36(46.15)
	总计Total	5	26	22	25	78

表 6

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抗菌药物 Antibacterial drug	抑菌圈直径/mm Inhibition circle diameter
抗菌药物 Antibacterial drug	敏感(S) Sensitivity	中介(I) Intermediary	耐药(R) Resistance
克林霉素 Clindamycin	≥21	15~20	≤14
庆大霉素 Gentamicin	≥15	13~14	≤12
四环素 Tetracycline	≥19	15~18	≤14
青霉素G Penicillin G	≥29	—	≤28
红霉素 Erythromycin	≥23	14~22	≤13
诺氟沙星 Norfloxacin	≥17	13~16	≤12
利福平 Rifampicin	≥20	17~19	≤16
复方新诺明 Compound sulfamethoxazole	≥17	13~16	≤12
氯霉素 Chloramphenicol	≥18	13~17	≤12
头孢西丁 Cefoxitin	≥22	—	≤21

抗生素分类 Classification of antibiotics	药物名称 Drug name	敏感菌株比例/% Percentage of sensitivity (%)(n/n)	中介菌株比例/% Percentage of intermediate (%)(n/n)	耐药菌株比例/% Percentage of resistance(%)(n/n)
林可霉素类 Lincomamides	克林霉素	0.0(0/78)	10.3(8/78)	89.7(70/78)
氨基糖苷类 Aminoglycosides	庆大霉素	14.1(11/78)	3.8(3/78)	82.1(64/78)
四环素类 Tetracyclines	四环素	0.0(0/78)	0.0(0/78)	100.0(78/78)
β-内酰胺类 β-lactam class	青霉素G	1.3(1/78)	0.0(0/78)	98.7(77/78)
β-内酰胺类 β-lactam class	头孢西丁	100.0(78/78)	0.0(0/78)	0.0(0/78)
大环内酯类 Macrolides	红霉素	17.9(14/78)	2.6(2/78)	79.5(62/78)
氟喹诺酮类 Fluoroquinolones	诺氟沙星	2.6(2/78)	1.3(1/78)	96.2(75/78)
安莎霉素类 Ansamycins	利福平	97.4(76/78)	0.0(0/78)	2.6(2/78)
叶酸途径拮抗剂 Folic acid antagonists	复方新诺明	14.1(11/78)	1.3(1/78)	84.6(66/78)
氯霉素类 Chloramphenicols	氯霉素	30.8(24/78)	23.1(18/78)	46.2(36/78)

耐药菌株号 Resistant strain number	耐药重数 Multiple	耐药菌株数 Number of resistance	耐药菌株比例/% Percentage of resistant strains
LN-68	9	1	1.3
LN-1，4，7，9，13，14，15，18，21，26，29，31，33，34，35，45，46，47，49，52，53，55，57，60，63，65，66，70，71，72	8	30	38.5
LN-3，8，16，17，20，22，25，28，32，39，44，56，69，73，74，75，76	7	17	21.8
LN-10，19，24，36，38，41，43，51，54，58，61，62，67	6	13	16.7
LN-2，5，6，11，12，23，27，30，37，40，42，50，59，64，77，78	5	16	20.5
LN-48	4	1	1.3

基因类别 Gene category	基因名称 Gene name	药物名称 Drug name	敏感/% Sensitive	中介/% Intermediate resistance	耐药/% Resistant	χ²	P
氨基糖苷类 Aminoglycosides	aac(6′)/aph(2′)	庆大霉素	5/11(45.45)	3/3(100.00)	64/64(100.00)	39.591	0.000^**
氨基糖苷类 Aminoglycosides	ant(4′)	庆大霉素	11/11(100.00)	1/3(33.33)	51/64(79.69)	7.013	0.030^*
大环内酯类 Macrolides	ermB	红霉素	1/14(7.14)	0/2(0.00)	38/62(61.29)	15.447	0.000^**
大环内酯类 Macrolides	ermC	红霉素	1/14(7.14)	1/2(50.00)	40/62(64.52)	15.14	0.001^**
多重耐药类 Multi drug resistance class	cfr	氯霉素	0/24(0.00)	0/18(0.00)	1/36(2.78)	1.182	0.554
		复方新诺明	0/11(0.00)	0/11(0.00)	1/66(1.52)	0.184	0.912
		利福平	1/76(1.32)	0/0(0.00)	0/2(0.00)	0.027	0.87
		诺氟沙星	0/2(0.00)	0/1(0.00)	1/75(1.33)	0.041	0.98
		红霉素	0/14(0.00)	1/2(50.00)	0/62(0.00)	38.494	0.000^**
		庆大霉素	0/11(0.00)	0/3(0.00)	1/64(1.56)	0.222	0.895
		克林霉素	0/0(0.00)	0/8(0.00)	1/70(1.43)	0.116	0.734
		青霉素G	1/1(100.00)	0/0(0.00)	0/77(0.00)	78	0.000^**

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