微生物学报

Antimicrobials	Resistance rate in Kunshan (%)	Resistance rate in Danyang (%)	Overall resistance rate (%)
The bold is the class of antimicrobials.
β-lactam antibiotics	45.16 (28/62)	16.88 (13/77)	29.50 (41/139)
Penicillin	45.16 (28/62)	16.88 (13/77)	29.50 (41/139)
Amoxicillin	27.42 (17/62)	3.90 (3/77)	14.39 (20/139)
Cefotaxime	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
Rifamycins	4.84 (3/62)	2.60 (2/77)	3.60 (5/139)
Rifampicin	4.84 (3/62)	2.60 (2/77)	3.60 (5/139)
Glycopeptides	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
Vancomycin	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
Qxazolidinones	27.42 (17/62)	15.58 (12/77)	20.86 (29/139)
Linezolid	27.42 (17/62)	15.58 (12/77)	20.86 (29/139)
Quinolones	67.74 (42/62)	29.87 (23/77)	46.76 (65/139)
enrofloxacin	64.52 (40/62)	29.87 (23/77)	45.32 (63/139)
Marbofloxacin	67.74 (42/62)	29.87 (23/77)	46.76 (65/139)
Amphenicols	53.23 (33/62)	53.25 (41/77)	53.24 (74/139)
Chloramphenicol	30.65 (19/62)	22.08 (17/77)	25.90 (36/139)
Florfenicol	53.23 (33/62)	50.65 (39/77)	51.80 (72/139)
Lincosamides	96.77 (60/62)	100.00 (77/77)	98.56 (137/139)
Licomycin	96.77 (60/62)	53.25 (41/77)	72.66 (101/139)
Clindamycin	95.16 (59/62)	100.00 (77/77)	97.84 (136/139)
Pleuromutilin	54.84 (34/62)	53.25 (41/77)	53.96 (75/139)
Tiamulin	54.84 (34/62)	45.45 (35/77)	49.64 (69/139)
Valnemulin	33.87 (21/62)	40.26 (31/77)	37.41 (52/139)
Aminoglycosides	79.03 (49/62)	75.32 (58/77)	76.98 (107/139)
Gentamicin	53.23 (33/62)	58.44 (45/77)	56.12 (78/139)
Kanamycin	61.29 (38/62)	61.04 (47/77)	61.15 (85/139)
Streptomycin	45.16 (28/62)	36.36 (28/77)	40.29 (56/139)
Spectinomycin	46.77 (29/62)	33.77 (26/77)	39.57 (55/139)
Macrolides	91.94 (57/62)	98.70 (76/77)	95.68 (133/139)
Tilmicosin	88.71 (55/62)	98.70 (76/77)	95.68 (133/139)
Erythromycin	90.32 (56/62)	98.70 (76/77)	94.96 (132/139)
Azithromycin	90.32 (56/62)	97.40 (75/77)	94.24 (131/139)
Tetracyclines	93.55 (58/62)	98.70 (76/77)	96.40 (134/139)
Doxycycline	93.55 (58/62)	98.70 (76/77)	96.40 (134/139)
Tetracycline	91.94 (57/62)	98.70 (76/77)	95.68 (133/139)

Antimicrobials	Resistance rate in Kunshan (%)	Resistance rate in Danyang (%)	Overall resistance rate (%)
The bold is the class of antimicrobials.
β-lactam antibiotics	45.16 (28/62)	16.88 (13/77)	29.50 (41/139)
Penicillin	45.16 (28/62)	16.88 (13/77)	29.50 (41/139)
Amoxicillin	27.42 (17/62)	3.90 (3/77)	14.39 (20/139)
Cefotaxime	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
Rifamycins	4.84 (3/62)	2.60 (2/77)	3.60 (5/139)
Rifampicin	4.84 (3/62)	2.60 (2/77)	3.60 (5/139)
Glycopeptides	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
Vancomycin	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
Qxazolidinones	27.42 (17/62)	15.58 (12/77)	20.86 (29/139)
Linezolid	27.42 (17/62)	15.58 (12/77)	20.86 (29/139)
Quinolones	67.74 (42/62)	29.87 (23/77)	46.76 (65/139)
enrofloxacin	64.52 (40/62)	29.87 (23/77)	45.32 (63/139)
Marbofloxacin	67.74 (42/62)	29.87 (23/77)	46.76 (65/139)
Amphenicols	53.23 (33/62)	53.25 (41/77)	53.24 (74/139)
Chloramphenicol	30.65 (19/62)	22.08 (17/77)	25.90 (36/139)
Florfenicol	53.23 (33/62)	50.65 (39/77)	51.80 (72/139)
Lincosamides	96.77 (60/62)	100.00 (77/77)	98.56 (137/139)
Licomycin	96.77 (60/62)	53.25 (41/77)	72.66 (101/139)
Clindamycin	95.16 (59/62)	100.00 (77/77)	97.84 (136/139)
Pleuromutilin	54.84 (34/62)	53.25 (41/77)	53.96 (75/139)
Tiamulin	54.84 (34/62)	45.45 (35/77)	49.64 (69/139)
Valnemulin	33.87 (21/62)	40.26 (31/77)	37.41 (52/139)
Aminoglycosides	79.03 (49/62)	75.32 (58/77)	76.98 (107/139)
Gentamicin	53.23 (33/62)	58.44 (45/77)	56.12 (78/139)
Kanamycin	61.29 (38/62)	61.04 (47/77)	61.15 (85/139)
Streptomycin	45.16 (28/62)	36.36 (28/77)	40.29 (56/139)
Spectinomycin	46.77 (29/62)	33.77 (26/77)	39.57 (55/139)
Macrolides	91.94 (57/62)	98.70 (76/77)	95.68 (133/139)
Tilmicosin	88.71 (55/62)	98.70 (76/77)	95.68 (133/139)
Erythromycin	90.32 (56/62)	98.70 (76/77)	94.96 (132/139)
Azithromycin	90.32 (56/62)	97.40 (75/77)	94.24 (131/139)
Tetracyclines	93.55 (58/62)	98.70 (76/77)	96.40 (134/139)
Doxycycline	93.55 (58/62)	98.70 (76/77)	96.40 (134/139)
Tetracycline	91.94 (57/62)	98.70 (76/77)	95.68 (133/139)

Resistance genes	Detection rate of resistance rate in Kunshan (%)	Detection rate of resistance rate in Danyang (%)	Overall detection rate (%)
The bold is the class of antimicrobials.
Macrolides	90.32 (56/62)	93.51 (72/77)	92.09 (128/139)
ermA	0.00 (0/62)	2.60 (2/77)	1.44 (2/139)
ermB	88.71 (55/62)	93.51 (72/77)	91.37 (127/139)
ermC	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
mefA	3.23 (2/62)	2.60 (2/77)	2.88 (4/139)
msr(D)	3.23 (2/62)	1.30 (1/77)	2.16 (3/139)
Lincosamides	9.68 (6/62)	20.78 (16/77)	15.83 (22/139)
lsa(E)	9.68 (6/62)	20.78 (16/77)	15.83 (22/139)
Tetracyclines	74.19 (46/62)	75.32 (58/77)	74.82 (104/139)
tetO	50.00 (31/62)	57.14 (44/77)	53.96 (75/139)
tetM	12.90 (8/62)	9.09 (7/77)	10.79 (15/139)
tet(O/W/32/O)	16.13 (10/62)	10.39 (8/77)	12.95 (18/139)
tetL	6.45 (4/62)	6.49 (5/77)	6.47 (9/139)
Amphenicols	9.68 (6/62)	7.79 (6/77)	8.63 (12/139)
fexA	6.45 (4/62)	7.79 (6/77)	7.19 (10/139)
fexB	3.23 (2/62)	0.00 (0/77)	1.44 (2/139)
Qxazolidinones	1.61 (1/62)	2.60 (2/77)	2.16 (3/139)
optrA	1.61 (1/62)	2.60 (2/77)	2.16 (3/139)
Aminoglycosides	53.23 (33/62)	49.35 (38/77)	51.08 (71/139)
aph(2')-Ib	0.00 (0/62)	1.30 (1/77)	0.72 (1/139)
aph(2')-Ic	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
aph(2')-Id	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
aph(3')-IIIa	19.35 (12/62)	11.69 (9/77)	15.11 (21/139)
ant(6')-Ia	9.68 (6/62)	7.79 (6/77)	8.63 (12/139)
aac(6')-aph(2'')	37.10 (23/62)	40.26 (31/77)	38.85 (54/139)

Resistance genes	Detection rate of resistance rate in Kunshan (%)	Detection rate of resistance rate in Danyang (%)	Overall detection rate (%)
The bold is the class of antimicrobials.
Macrolides	90.32 (56/62)	93.51 (72/77)	92.09 (128/139)
ermA	0.00 (0/62)	2.60 (2/77)	1.44 (2/139)
ermB	88.71 (55/62)	93.51 (72/77)	91.37 (127/139)
ermC	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
mefA	3.23 (2/62)	2.60 (2/77)	2.88 (4/139)
msr(D)	3.23 (2/62)	1.30 (1/77)	2.16 (3/139)
Lincosamides	9.68 (6/62)	20.78 (16/77)	15.83 (22/139)
lsa(E)	9.68 (6/62)	20.78 (16/77)	15.83 (22/139)
Tetracyclines	74.19 (46/62)	75.32 (58/77)	74.82 (104/139)
tetO	50.00 (31/62)	57.14 (44/77)	53.96 (75/139)
tetM	12.90 (8/62)	9.09 (7/77)	10.79 (15/139)
tet(O/W/32/O)	16.13 (10/62)	10.39 (8/77)	12.95 (18/139)
tetL	6.45 (4/62)	6.49 (5/77)	6.47 (9/139)
Amphenicols	9.68 (6/62)	7.79 (6/77)	8.63 (12/139)
fexA	6.45 (4/62)	7.79 (6/77)	7.19 (10/139)
fexB	3.23 (2/62)	0.00 (0/77)	1.44 (2/139)
Qxazolidinones	1.61 (1/62)	2.60 (2/77)	2.16 (3/139)
optrA	1.61 (1/62)	2.60 (2/77)	2.16 (3/139)
Aminoglycosides	53.23 (33/62)	49.35 (38/77)	51.08 (71/139)
aph(2')-Ib	0.00 (0/62)	1.30 (1/77)	0.72 (1/139)
aph(2')-Ic	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
aph(2')-Id	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
aph(3')-IIIa	19.35 (12/62)	11.69 (9/77)	15.11 (21/139)
ant(6')-Ia	9.68 (6/62)	7.79 (6/77)	8.63 (12/139)
aac(6')-aph(2'')	37.10 (23/62)	40.26 (31/77)	38.85 (54/139)

Strains	Mortality (%)	Serotype	Significance	P
The virulence of isolates was compared to the highly virulent strain SC070731 and subjected to statistical analysis using the Log-Rank (Mantel-Cox) test. The symbols , , , and ** correspond to P < 0.05, P < 0.01, P < 0.001, and P < 0.000 1, respectively, while “ns” signifies no significance.
SC070731	100.00	2	−	−
SH040917	0.00	9	****	< 0.000 1
2023WUSS142	86.67	1	ns	0.073 3
2023WUSS124	80.00	3	ns	0.098 0
2023WUSS014	46.67	4	***	0.000 2
2023WUSS016	73.33	5	**	0.006 1
2023WUSS048	73.33	5	ns	0.102 9
2023WUSS088	73.33	6	****	< 0.000 1
2023WUSS017	86.67	7	***	0.001 2
2023WUSS111	6.67	7	****	< 0.000 1
2023WUSS085	86.67	8	*	0.014 6
2023WUSS126	13.33	8	****	< 0.000 1
2023WUSS001	6.67	9	****	< 0.000 1
2023WUSS094	46.67	9	****	< 0.000 1
2023WUSS128	73.33	10	***	0.000 5
2023WUSS083	6.67	12	****	< 0.000 1
2023WUSS019	80.00	15	***	0.000 8
2023WUSS052	46.67	15	***	0.002 0
2023WUSS012	26.67	16	****	< 0.000 1
2023WUSS047	66.67	16	***	0.000 2
2023WUSS025	33.33	19	****	< 0.000 1
2023WUSS064	13.33	19	****	< 0.000 1
2023WUSS051	6.67	21	****	< 0.000 1
2023WUSS056	93.33	23	ns	0.315 2
2023WUSS082	0.00	24	****	< 0.000 1
2023WUSS021	6.67	29	****	< 0.000 1
2023WUSS053	33.33	29	****	< 0.000 1
2023WUSS058	26.67	30	****	< 0.000 1
2023WUSS007	66.67	31	****	< 0.000 1
2023WUSS043	53.33	31	***	0.000 7
2023WUSS045	0.00	1/2	****	< 0.000 1
2023WUSS087	66.67	1/2	*	0.010 7
2023WUSS029	26.67	NCL1	****	< 0.000 1
2023WUSS131	60.00	NCL1	**	0.006 1
2023WUSS036	6.67	NCL11	****	< 0.000 1
2023WUSS033	13.33	NCL2	****	< 0.000 1
2023WUSS063	20.00	NCL20	****	< 0.000 1
2023WUSS035	86.67	NCL3	ns	0.198 3
2023WUSS061	66.67	NCL3	****	< 0.000 1
2023WUSS132	73.33	NCL4	ns	0.126 5
2023WUSS133	80.00	NCL5	**	0.009 4
2023WUSS062	0.00	NCL7	****	< 0.000 1
2023WUSS134	13.33	NCL9	****	< 0.000 1
2023WUSS073	6.67	Unknown	****	< 0.000 1
2023WUSS076	40.00	Unknown	****	< 0.000 1

Strains	Mortality (%)	Serotype	Significance	P
The virulence of isolates was compared to the highly virulent strain SC070731 and subjected to statistical analysis using the Log-Rank (Mantel-Cox) test. The symbols , , , and ** correspond to P < 0.05, P < 0.01, P < 0.001, and P < 0.000 1, respectively, while “ns” signifies no significance.
SC070731	100.00	2	−	−
SH040917	0.00	9	****	< 0.000 1
2023WUSS142	86.67	1	ns	0.073 3
2023WUSS124	80.00	3	ns	0.098 0
2023WUSS014	46.67	4	***	0.000 2
2023WUSS016	73.33	5	**	0.006 1
2023WUSS048	73.33	5	ns	0.102 9
2023WUSS088	73.33	6	****	< 0.000 1
2023WUSS017	86.67	7	***	0.001 2
2023WUSS111	6.67	7	****	< 0.000 1
2023WUSS085	86.67	8	*	0.014 6
2023WUSS126	13.33	8	****	< 0.000 1
2023WUSS001	6.67	9	****	< 0.000 1
2023WUSS094	46.67	9	****	< 0.000 1
2023WUSS128	73.33	10	***	0.000 5
2023WUSS083	6.67	12	****	< 0.000 1
2023WUSS019	80.00	15	***	0.000 8
2023WUSS052	46.67	15	***	0.002 0
2023WUSS012	26.67	16	****	< 0.000 1
2023WUSS047	66.67	16	***	0.000 2
2023WUSS025	33.33	19	****	< 0.000 1
2023WUSS064	13.33	19	****	< 0.000 1
2023WUSS051	6.67	21	****	< 0.000 1
2023WUSS056	93.33	23	ns	0.315 2
2023WUSS082	0.00	24	****	< 0.000 1
2023WUSS021	6.67	29	****	< 0.000 1
2023WUSS053	33.33	29	****	< 0.000 1
2023WUSS058	26.67	30	****	< 0.000 1
2023WUSS007	66.67	31	****	< 0.000 1
2023WUSS043	53.33	31	***	0.000 7
2023WUSS045	0.00	1/2	****	< 0.000 1
2023WUSS087	66.67	1/2	*	0.010 7
2023WUSS029	26.67	NCL1	****	< 0.000 1
2023WUSS131	60.00	NCL1	**	0.006 1
2023WUSS036	6.67	NCL11	****	< 0.000 1
2023WUSS033	13.33	NCL2	****	< 0.000 1
2023WUSS063	20.00	NCL20	****	< 0.000 1
2023WUSS035	86.67	NCL3	ns	0.198 3
2023WUSS061	66.67	NCL3	****	< 0.000 1
2023WUSS132	73.33	NCL4	ns	0.126 5
2023WUSS133	80.00	NCL5	**	0.009 4
2023WUSS062	0.00	NCL7	****	< 0.000 1
2023WUSS134	13.33	NCL9	****	< 0.000 1
2023WUSS073	6.67	Unknown	****	< 0.000 1
2023WUSS076	40.00	Unknown	****	< 0.000 1

Strains	Mortality (%)	Serotype	Significance	P
The virulence of isolates was compared to the highly virulent strain SC070731 and subjected to statistical analysis using the Log-Rank (Mantel-Cox) test. The symbols * and **** correspond to P < 0.05 and P < 0.000 1, respectively, while “ns” signifies no significance.
SH040917	0.00	9	****	< 0.000 1
SC070731	100.00	2	−	−
2023WUSS056	90.00	23	ns	0.860 0
2023WUSS124	90.00	3	ns	0.061 7
2023WUSS142	80.00	1	*	0.010 1

Strains	Mortality (%)	Serotype	Significance	P
The virulence of isolates was compared to the highly virulent strain SC070731 and subjected to statistical analysis using the Log-Rank (Mantel-Cox) test. The symbols * and **** correspond to P < 0.05 and P < 0.000 1, respectively, while “ns” signifies no significance.
SH040917	0.00	9	****	< 0.000 1
SC070731	100.00	2	−	−
2023WUSS056	90.00	23	ns	0.860 0
2023WUSS124	90.00	3	ns	0.061 7
2023WUSS142	80.00	1	*	0.010 1

2023年江苏地区屠宰场健康猪源猪链球菌致病与耐药特征

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许杨 ¹^,²^,³ , 王瑞光 ¹^,²^,³ , 彭泽仁 ¹^,²^,³ , 吴宗福 ¹^,²^,³^,⁴^,^*

微生物学报 | 研究报告 2025,65(1): 211-224

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微生物学报 | 研究报告 2025, 65(1): 211-224

2023年江苏地区屠宰场健康猪源猪链球菌致病与耐药特征

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许杨¹^,²^,³, 王瑞光¹^,²^,³, 彭泽仁¹^,²^,³, 吴宗福¹^,²^,³^,⁴^,^*

作者信息

1 南京农业大学动物医学院, 江苏南京 210014

2 农业农村部动物细菌学重点实验室, 江苏南京 210014

3 世界动物卫生组织猪链球菌病参考实验室, 江苏南京 210014

4 广东省养猪与猪病防控技术研究企业重点实验室, 广东海大畜牧兽医研究院, 广东广州 511400

The pathogenic and antimicrobial resistance characteristics of Streptococcus suis isolates from healthy pigs at slaughterhouses in Jiangsu Province, 2023

Yang XU¹^,²^,³, Ruiguang WANG¹^,²^,³, Zeren PENG¹^,²^,³, Zongfu WU¹^,²^,³^,⁴^,^*

Affiliations

1 College of Veterinary Medicine, Nanjing Agricultural University, Nanjing 210014, Jiangsu, China

2 Key Laboratory of Animal Bacteriology, Ministry of Agriculture and Rural Affairs, Nanjing 210014, Jiangsu, China

3 WOAH Reference Laboratory for Swine Streptococcosis, Nanjing 210014, Jiangsu, China

4 Guangdong Haid Institute of Animal Husbandry & Veterinary, Guangdong Provincial Key Laboratory of Research on the Technology of Pig-breeding and Pig-disease Prevention, Guangzhou 511400, Guangdong, China

出版时间: 2025-01-04 doi: 10.13343/j.cnki.wsxb.20240369

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摘要

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【目的】猪链球菌(Streptococcus suis, SS)是猪的常见致病菌，也是一种人畜共患病原。江苏曾于1998年暴发猪链球菌疫情，大量生猪死亡的同时，也导致14人感染死亡。因此，对江苏地区屠宰场健康猪进行猪链球菌感染调查，具有公共卫生意义。【方法】于2023年采集江苏两地屠宰场健康猪扁桃体，进行猪链球菌分离鉴定和血清分型，通过所分离菌株对斑马鱼和小鼠毒力测定、药敏试验及耐药基因检测，探究猪链球菌分离菌株的致病和耐药特征。【结果】2023年7月采集江苏昆山地区扁桃体样本，阳性率为50.85% (30/59)，分离鉴定出62株猪链球菌，其中分离率最高为31型(12.90%，8/62)，其次为19型(11.29%，7/62)、NCL2型(8.06%，5/62)等；2023年7月、11月采集江苏丹阳地区扁桃体样本，阳性率为60.71% (34/56)，分离鉴定出77株猪链球菌，其中分离率最高为16型(11.69%，9/77)，其次为9型(10.39%，8/77)、21型(10.39%，8/77)、31型(10.39%，8/77)等。两地分离株对林可酰胺类(98.56%，137/139)、大环内酯类(95.68%，133/139)、四环素类(96.40%，134/139)抗生素耐药率较高；97.84% (136/139)的菌株属于多重耐药菌株。所有菌株对头孢噻肟、万古霉素敏感。根据分离株来源及血清型选择42株(昆山市18株，丹阳市24株)代表菌株进行斑马鱼毒力测定，攻毒剂量为3×10⁶ CFU/尾时，有7株菌对斑马鱼致病力强，致死率≥80.00%。选择致死率≥80.00%且死亡趋势与强度对照无显著差异的3株代表菌株(分别为血清1型、3型、23型)进行小鼠试验，致死率均≥80.00%。【结论】江苏地区健康猪扁桃体的猪链球菌携带率较高(55.65%，64/115)，97.84% (136/139)的分离株为多重耐药菌株，血清1型、3型、23型分离株致病力强，值得关注。

关键词

猪链球菌 / 屠宰场 / 江苏 / 耐药特征 / 致病特征

Abstract

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[Objective] Streptococcus suis is a prevalent pathogen attacking pigs and a zoonotic agent. In 1998, an outbreak of S. suis infection in Jiangsu caused numerous pig deaths and 14 human deaths. Therefore, investigating S. suis infections in healthy pigs from slaughterhouses in Jiangsu is crucial for public health. [Methods] Tonsils were collected from healthy pigs in slaughterhouses of Jiangsu in 2023, and S. suis was isolated, identified, and serotyped. The pathogenicity of S. suis isolates to zebrafish and mouse models was examined. Furthermore, the antibiotic resistance characteristics and genes and the antimicrobial susceptibility of the isolates were identified and evaluated. [Results] The positive rate of S. suis in the samples collected from Kunshan in July 2023 was 50.85% (30/59). A total of 62 strains were isolated from the samples collected from Kunshan, and serotype 31 (12.90%, 8/62) had the highest isolation rate, followed by serotype 19 (11.29%, 7/62) and serotype NCL2 (8.06%, 5/62). In the samples collected from Danyang in July and November 2023, the positive rate of S. suis was 60.71% (34/56), and 77 strains were isolated. Serotype 16 had the highest isolation rate of 11.69% (9/77), followed by serotype 9 (10.39%, 8/77), serotype 21 (10.39%, 8/77), and serotype 31 (10.39%, 8/77). The isolates from both regions exhibited high resistance to lincosamides (98.56%, 137/139), macrolides (95.68%, 133/139), and tetracyclines (96.40%, 134/139). Furthermore, 97.84% (136/139) of strains were multi-drug resistant. All the strains were sensitive to cefotaxime and vancomycin. According to the sources and serotypes, we selected 42 representative strains (18 from Kunshan and 24 from Danyang) to perform zebrafish infection experiments. At a dose of 3×10⁶ CFU/fish, seven strains exhibited high pathogenicity to zebrafish, causing the mortality rates ≥80.00%. Three strains (serotypes 1, 3, and 23) causing mortality rates ≥80.00% in zebrafish and comparable to the virulent strain SC070731 were selected for mouse infection experiments. All the three strains led to the mortality rates ≥80.00% in mice. [Conclusion] The healthy pigs in Jiangsu have a high carrying rate of S. suis (55.65%, 64/115), and 97.84% (136/139) of the isolates are multi-drug resistant. Strains of serotypes 1, 3, and 23 exhibited strong pathogenicity.

Key words

Streptococcus suis / slaughterhouse / Jiangsu / antimicrobial resistance / pathogenic characteristics

引用本文

许杨, 王瑞光, 彭泽仁, 吴宗福. 2023年江苏地区屠宰场健康猪源猪链球菌致病与耐药特征. 微生物学报, 2025 , 65 (1) : 211 -224 . DOI: 10.13343/j.cnki.wsxb.20240369

Yang XU, Ruiguang WANG, Zeren PENG, Zongfu WU. The pathogenic and antimicrobial resistance characteristics of Streptococcus suis isolates from healthy pigs at slaughterhouses in Jiangsu Province, 2023[J]. Acta Microbiologica Sinica, 2025 , 65 (1) : 211 -224 . DOI: 10.13343/j.cnki.wsxb.20240369

正文

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猪链球菌(Streptococcus suis, SS)是猪的常见病原菌，可导致猪败血症、脑膜炎等，同时也是一种重要人畜共患病原。该菌在危害养猪业发展的同时，也给公共卫生安全带来威胁^[1]。猪链球菌感染人类的报道遍及全球。中国于1998年江苏、2005年四川两次暴发猪链球菌感染人疫情，分别导致25例感染和14例死亡，以及215例感染和38例死亡^[2-3]。2006年之后，人感染猪链球菌病例主要散发于广西等地区，主要为ST1与ST7菌株^[4]。按荚膜多糖抗原不同，猪链球菌分为传统血清型29种(1−19、21、23−25、27−31、1/2)^[5]和Chz血清型^[6]；近年来，基于荚膜基因簇的序列差异，在未分类的菌株中发现了新荚膜基因簇血清型27种(NCL1–20, 21a, 21b, 22–26)^[7-10]。如今，已有包括1、2、4、5、7、9、14、16、21、24、31型在内的11种血清型能感染人^[11-12]。

屠宰场健康猪携带猪链球菌的比例较高，是易感猪和人的重要传染源^[13]。近年来，由于养殖过程中抗生素的大量使用，猪链球菌在药物的选择压力下产生了耐药性。不同地区的猪链球菌，其分离率、血清型、致病及耐药特征均存在差异。考虑到江苏曾暴发过人感染疫情，因此对该地区屠宰场健康猪进行猪链球菌感染调查，明确其耐药、致病特征，具有公共卫生意义。本研究于2023年采集江苏两地屠宰场健康猪扁桃体，分离猪链球菌并鉴定血清型，通过斑马鱼和小鼠测定分离株毒力，并进行药敏试验及耐药基因检测，以分析其致病和耐药特征。研究结果有利于深入剖析猪链球菌在江苏地区的感染情况及其耐药、致病特征，为设计合理的防控措施奠定基础。

1 材料与方法

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1.1 菌株

本研究中的菌株于2023年分离于江苏昆山、丹阳两地屠宰场采集的健康猪扁桃体中。分离菌株对斑马鱼毒力测定的对照菌株(血清2型强毒菌株SC070731、血清9型弱毒菌株SH040917)及药敏试验质控菌株金黄色葡萄球菌(Staphylococcus aureus) ATCC 29213，均保存于本课题组。

1.2 主要试剂

Mueller-Hinton肉汤(Mueller-Hinton Broth, MHB)、Todd-Hewitt肉汤(Todd-Hewitt Broth, THB)培养基均购自青岛高科技工业园海博生物技术有限公司；PBS磷缓冲液(片剂)购自北京索莱宝科技有限公司；抗生素购自上海麦克林生化科技股份有限公司；限制性核酸内切酶FastDigest BstN I购自赛默飞世尔科技公司；2×Rapid Taq Master Mix、FastPure DNA Extraction Mini Kit、DL2000 DNA Marker均购自南京诺唯赞生物科技股份有限公司；PCR引物由南京擎科生物科技有限公司合成。

1.3 培养基及抗生素的配制

MHB、THB培养基的配制参考产品说明书；猪链球菌筛选培养基是在THB培养基的基础上加入结晶紫(终浓度1.2 mg/L)，121 ℃灭菌20 min后，冷却至55 ℃时加入庆大霉素(终浓度1.2 mg/L)和萘啶酮酸(终浓度30 mg/L)配制而成，具体方法参考文献[14]。药敏试验所需抗生素溶液配制方法参照美国临床和实验室标准协会(Clinical and Laboratory Standards Institute, CLSI) M31-A3标准^[15]。母液浓度为2 560 μg/mL，滤器(0.22 μm)过滤分装后保存于−20 ℃。

1.4 样品处理及猪链球菌的分离鉴定

扁桃体样品运送到实验室后，用无菌PBS反复冲洗扁桃体并用乙醇消毒后，取0.1 g扁桃体内部组织，置于匀浆管中配平并充分研磨。

匀浆液1:25转接至猪链球菌液体筛选培养基中静置培养8 h后，以菌液为模板，PCR检测谷氨酸脱氢酶(gdh)、DNA修复酶(recN)基因，双阳性则鉴定为猪链球菌阳性。阳性菌液接种固体筛选培养基进行纯化鉴定，gdh、recN双阳性则鉴定为猪链球菌，并于−80 ℃冰箱冻存保存^[16]。引物信息及具体步骤参考文献[17]。

1.5 猪链球菌血清型分型

将复苏后的菌株，通过血清型鉴定引物进行PCR扩增鉴定，引物信息及具体步骤参考文献[17]。由于普通PCR无法区分2型或1/2型、1型或14型菌株，对属于这4种血清型的猪链球菌，参考Matiasovic等^[18]的方法，使用cpsK特异性引物扩增，并采用PCR产物纯化试剂盒纯化回收，用BstNⅠ限制性内切酶进行酶切，琼脂糖凝胶电泳鉴定。2型、14型菌株的cpsK基因可被BstN I酶切成2个片段，大小分别为139 bp和347 bp；1型、1/2型cpsK基因无法被切割，产物大小为完整的486 bp。同一扁桃体分离的同一血清型菌株只保存一株。

1.6 分离菌株的耐药特性

以金黄色葡萄球菌ATCC 29213为质控菌株，用CLSI推荐的肉汤稀释法测定最小抑菌浓度(minimum inhibitory concentration, MIC)，选用的抗生素共11类23种。其耐药折点参考文献[16]。

1.7 分离菌株的耐药基因检测

PCR检测猪链球菌19个常见耐药基因，引物信息及步骤参考文献[17]。

1.8 动物毒力试验

1.8.1 分离菌株对斑马鱼的毒力测定

参考文献[14]，根据猪链球菌来源及血清型分布选择代表菌株进行斑马鱼毒力测定。挑选规格大小相近的成年斑马鱼进行试验。正式攻毒前需复壮菌株，将5 mL菌液培养至对数期(OD₆₀₀为0.6)，随后5 000 r/min离心10 min，PBS洗涤3次，最后用1 mL PBS重悬。每株菌感染2尾斑马鱼，每尾泄殖腔注射20 μL重悬菌液。每隔4 h对斑马鱼进行观察，观察到濒死后从其脑部分离猪链球菌：1 mL注射器抽取斑马鱼脑脊液，将其接种血平板，37 ℃温箱培养8−12 h后挑取疑似单菌落培养至浑浊。用gdh、recN及血清型引物进行鉴定。阳性菌液1:50转接至5 mL THB培养基后培养至OD₆₀₀为0.6。菌液经过5 000 r/min离心10 min，洗涤后用无菌PBS重悬，调整OD₆₀₀为0.6。攻毒菌量为3×10⁶ CFU/尾，每株菌攻毒15尾，每尾20 μL。攻毒完成后置于28 ℃专用温箱，每12 h观察并记录斑马鱼死亡尾数，持续观察96 h。攻毒菌液稀释后取10⁻³、10⁻⁴、10⁻⁵这3个浓度梯度进行菌落计数，确定攻毒剂量。以血清2型强毒株SC070731、血清9型弱毒株SH040917作为对照，PBS作为空白对照。结果均与强毒SC070731比较并用Log-Rank检验进行统计分析。

1.8.2 分离菌株对小鼠的毒力测定

4周龄SPF级雌性BALB/c小鼠购自上海斯莱克实验动物有限责任公司，生产许可证编号：SCXK (沪) 2022-0004。分离菌株对小鼠毒力测定经南京农业大学动物管理与伦理委员会批准(审核编号：NJAU.No20240306035)，在南京农业大学实验动物中心进行(许可证：SYXK (Su) 2021-0086)。参考文献[14]，选择对斑马鱼致死率≥80.00%且与强毒株SC070731攻毒组差异不显著的菌株进行小鼠试验。正式攻毒前将冻存菌液进行复苏，将5 mL菌液培养至对数期后5 000 r/min离心10 min，清洗2−3次后，用1 mL PBS进行重悬。将重悬菌液按200 μL/只腹腔注射小鼠复壮，每隔4 h进行观察，观察到小鼠濒死后，采集其心血接种至血平板，37 ℃温箱培养12 h。挑取疑似单菌落培养至浑浊，用gdh、recN及血清型引物进行鉴定。根据菌株的CFU计算所需菌液量，将阳性菌液1:50转接至THB培养基后培养至对数期(OD₆₀₀为0.6)。菌液5 000 r/min离心10 min，清洗2−3次后重悬，将重悬菌液浓度控制OD₆₀₀为0.6。攻毒剂量为3×10⁸ CFU/只，每组10只，每只200 μL。以血清2型强毒株SC070731、血清9型弱毒株SH040917为对照，PBS为空白对照。用PBS稀释攻毒菌液，取10⁻³、10⁻⁴、10⁻⁵、10⁻⁶这4个浓度梯度进行菌落计数确定攻毒菌量。每12 h观察小鼠死亡情况，持续1周。结果均和强毒对照SC070731比较，并用Log-Rank检验进行统计分析。

2 结果与分析

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2.1 猪链球菌分离鉴定

2023年7月，在江苏昆山市的屠宰场共采集59份健康猪扁桃体，其中30份为阳性，阳性率50.85%。分离鉴定出62株猪链球菌，分属于18种血清型，其中分离率最高的血清型为31型(12.90%，8/62)，其次为19型(11.29%，7/62)、NCL2型(8.06%，5/62)、4型(4.84%，3/62)、9型(4.84%，3/62)、12型(4.84%，3/62)、16型(4.84%，3/62)等，结果见图1。11种感染人的血清型共分离出7种，分别为4、5、7、9、16、24、31型，占比35.48% (22/62)，存在于16个扁桃体中(16/30)，占比53.33%。40.00% (12/30)的扁桃体存在2种及以上不同血清型的菌株。

2023年7月、11月在江苏丹阳市屠宰场采集了56份健康猪扁桃体，其中34份为阳性，阳性率60.71%。分离鉴定出77株猪链球菌，分属于23种血清型，其中占比最高的是16型(11.69%，9/77)，其次为9型(10.39%，8/77)、21型(10.39%，8/77)、31型(10.39%，8/77)、7型(9.09%，7/77)、1/2型(5.19%，4/77)、30型(3.90%，3/77)等，结果见图2。共分离7种感染人的血清型，分别为1、5、7、9、16、21、31型，占比54.55% (42/77)，存在于30个扁桃体中(30/34)，占比88.24%。64.71% (22/34)的扁桃体存在2种及以上不同血清型菌株。

两地血清型分布均多而较复杂，总分离率最高的为31型(11.51%，16/139)，其次为16型(8.63%，12/139)、9型(7.91%，11/139)、7型(6.47%，9/139)、19型和21型(5.76%，8/139)。两地存在感染人的血清型的阳性扁桃体比例均大于50.00%。

2.2 分离菌株的耐药特性

对139株猪链球菌(昆山市62株，丹阳市77株)进行11类23种抗生素的药敏试验。两地分离株对大环内酯类、林可酰胺类、四环素类药物的耐药率较高，分别为95.68% (133/139)、98.56% (137/139)、96.40% (134/139)。

昆山市分离株对β-内酰胺类、喹诺酮类、噁唑烷酮类、利福平类抗生素的耐药率均显著高于丹阳市。45.16% (28/62)的昆山分离株对β-内酰胺类抗生素耐药，16.88% (13/77)的丹阳分离株对β-内酰胺类抗生素耐药。两地共有21株分离株对青霉素高度耐药(MIC≥8 μg/mL)，其中20株分离自昆山地区。根据多重耐药的标准(对≥3类的抗生素耐药)^[19]，昆山市62株猪链球菌菌株中有59株属于多重耐药菌株，而丹阳市77株则都属于多重耐药菌株(图3)。所有菌株对头孢噻肟、万古霉素敏感，两地区分离株耐药率见表1。

2.3 分离菌株的耐药基因检测

对139株猪链球菌(昆山市62株，丹阳市77株)检测常见的19种耐药基因，结果见表2。两地区菌株抗生素耐药基因携带率较为相似。两地区92.09% (128/139)的菌株检测出大环内酯类抗性基因，其中有6株菌耐药而未检测出耐药基因，1株菌存在耐药基因但不耐药。74.82% (104/139)的菌株检测出四环素类耐药基因，其中1株无耐药表型，31株菌耐药但未检测出四环素类耐药基因。仅有15.83% (22/139)的菌株存在林可酰胺类相关耐药基因，其中117株菌耐药而未检出林可酰胺类耐药基因；51.08% (71/139)的菌株存在氨基糖苷类耐药基因，其中2株菌无耐药表型，38株菌耐药而未检出氨基糖苷类耐药基因；8.63% (12/139)的菌株存在酰胺醇类耐药基因，其中2株菌无耐药表型，64株菌耐药而未检出酰胺醇类耐药基因。

2.4 分离菌株对斑马鱼的毒力测定

根据猪链球菌分离株来源及血清型分布选择代表菌株42株(昆山市18株，丹阳市24株)进行斑马鱼毒力测定，结果见表3。攻毒量为3×10⁶ CFU/尾时，菌株2023WUSS017、2023WUSS019、2023WUSS056、2023WUSS085、2023WUSS124、2023WUSS133、2023WUSS142对斑马鱼的致病力较强，致死率为80.00%−100.00%，与强毒对照毒力相当；15株菌对斑马鱼毒力中等，致死率40.00%−73.30%；其余菌株致病力较弱，低于33.30%。

2.5 分离菌株对小鼠的毒力测定

选择斑马鱼致死率≥80.00%且与强毒对照SC070731死亡情况较为相符的菌株2023WUSS056、2023WUSS124、2023WUSS142用小鼠模型进一步验证其毒力，结果见表4。血清23型菌株2023WUSS056、血清3型菌株2023WUSS124、血清1型菌株2023WUSS142对小鼠致病力强，致死率分别为90.00%、90.00%、80.00%，与斑马鱼毒力测定结果相符。

3 讨论与结论

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Ma等^[20]发现在中国香港经常接触猪或生猪肉的养殖户、屠宰场工人猪链球菌年发病率是普通人群的350倍以上。荷兰养殖户、屠宰场工人感染猪链球菌的风险比普通人高约1 500倍^[21]。欧洲、美洲等地区感染人的病例集中在与屠宰场相关的人群中^[22]。越南屠宰场健康猪来源的猪链球菌是感染人的重要来源^[23]。因此，对屠宰场健康猪进行猪链球菌感染调查，确定其致病、耐药特征，具有公共卫生意义。

Thongkamkoon等^[24]检测了泰国帕尧省屠宰场180头健康猪，分离鉴定出196株猪链球菌，优势血清型为血清23型(10.2%)。Zheng等^[25] 2011−2012年采集北京、江苏、四川、贵州四地屠宰场健康猪咽拭子，分离率最高的是血清29型和血清11型。在印度采集健康猪扁桃体563个，分离出87株猪链球菌，其中血清7型(24.13%)、血清5型(18.39%)是优势分离血清型^[26]。本研究中昆山、丹阳两地猪链球菌阳性率分别为50.85%和60.71%，感染人的血清型分别占比35.48%、54.55%，与沈艳玲^[27] 2017−2019年分离的江苏屠宰场猪链球菌阳性率相似。两地区猪链球菌的优势血清型分布不同，昆山市分离率最高为31型，其次为19型；与沈艳玲^[27] 2017−2019年在江苏地区进行感染调查的情况相符。然而两地均未分离到血清2型，这与卞晨^[28] 2020年对江苏地区屠宰场感染调查的结果一致。近年来，血清2型菌株从健康猪中分离率较低：刘召颖等^[17] 2020−2021年采集了浙江屠宰场内健康猪扁桃体，2型分离率为2.94%；彭泽仁等^[14] 2022年采集了四川、广西的屠宰场健康猪扁桃体，2型分离率为0.02%；杨振波等^[29] 2022年采集广东地区健康猪扁桃体，血清2型分离率仅为0.88%；Sedano等^[30]在菲律宾9个省采集了119个样品，分离出269株猪链球菌，并未分离到血清2型菌株。两地无法定型菌株占比14.39%，这可能是因为这些菌株存在新的荚膜基因簇，今后还需进一步分析其荚膜基因簇序列，明确是否存在新的荚膜基因簇菌株。上述结果显示，昆山、丹阳两地屠宰场来源的健康猪携带猪链球菌的比例较高，血清型复杂且多样，存在9种感染人的血清型。本研究采集样品的地点、时间和样品量有限，今后应持续对该地区进行检测，从而有助于为该地区量身定制有效的猪链球菌病预防与控制措施。

猪链球菌对常用抗生素，如林可酰胺类、大环内酯类及四环素类普遍耐药^[31]。刘召颖等^[17] 2020−2021年在浙江地区分离的猪链球菌，68株均多重耐药，对林可酰胺类、大环内酯类及四环素类药物耐药均超过98%；都玉等^[32] 2021年在重庆分离的87株猪链球菌中多重耐药菌株占比96.55%，对四环素类、林可酰胺类、大环内酯类抗生素耐药均超过90%；Liu等^[11]对26株血清8型菌株的研究发现，这些菌株均为多重耐药菌株，对四环素类、林可酰胺类、大环内酯类抗生素的耐药均超过90%；杜凡姝等^[33] 2016年在江苏苏北分离的107株猪链球菌中95.33%为多重耐药菌株，对四环素、克林霉素、红霉素的耐药率均超过90%；Zhang等^[34] 2016−2018年在中国6个省份分离223株猪链球菌98.65%为多重耐药菌株，对克林霉素、四环素、红霉素的耐药率均超过96%。本研究中97.84%的菌株为多重耐药，对大环内酯类、四环素类、林可酰胺类抗生素的耐药率均超过95.00%。耐药基因erm(B)广泛存在，是导致菌株对林可酰胺类及大环内酯类药物耐药的主要原因，与之前的研究结果相符^[17]。链球菌属对氨基糖苷类药物表现低水平耐药，但氨基糖苷类相关耐药基因的存在则可引发高水平耐药^[31]；本研究有51.08%的菌株存在氨基糖苷类相关耐药基因，耐药水平较高。两地区共有20.86%的菌株对噁唑烷酮类抗生素耐药，但仅有2.16%的菌株含有噁唑烷酮类抗生素利奈唑胺耐药基因optrA。这与之前的研究不同，Huang等^[35]对江苏地区107株猪链球菌进行了利奈唑胺耐药性检测，38%的菌株耐药，optrA基因存在于所有耐药菌株。部分菌株存在耐药表型但无相关耐药基因，可能是由于耐药基因引物处存在突变，导致PCR不能检出，或存在其他与耐药相关的基因；部分菌株携带耐药相关基因(如噁唑烷酮类、四环素类、酰胺醇类等)，但未展现相应耐药表型，可能是由耐药基因发生突变、无法表达或表达水平低等原因造成的。

β-内酰胺类药物是治疗猪链球菌的主要抗生素之一。近年来，在药物的选择压力下，猪链球菌的青霉素耐药率也有攀升趋势，其耐药机制主要是青霉素结合蛋白(PBPs)的突变^[36]。Vela等^[37]发现1999−2001年西班牙病猪中分离株的青霉素耐药率 < 1%，而Petrocchi-Rilo等^[38]发现2021年西班牙发病猪来源分离株的青霉素耐药率升至26.2%。Lunha等^[36]发现2023年泰国病猪分离的猪链球菌对青霉素耐药率为50.2%。刘召颖等^[17]于2020−2021年在浙江分离的猪链球菌对β-内酰胺类抗生素的耐药率为26.47%。杜凡姝等^[33] 2016年在江苏苏北分离的猪链球菌中青霉素耐药率为27.68%。值得注意的是，本研究中昆山市分离株对β-内酰胺类抗生素的耐药率为45.16%，显著高于丹阳市。这可能是由于昆山屠宰场来源猪在养殖过程中使用较多的β-内酰胺类抗生素。目前，对猪链球菌利福平耐药的报道较少，但两地均有几株菌对利福平耐药，与之前的研究相似^[17]。本研究中所有菌株对头孢噻肟、万古霉素敏感，提示这些抗生素可用于两地的猪链球菌病防控。

斑马鱼和小鼠毒力测定均表明，血清1型菌株2023WUSS142、血清3型菌株2023WUSS124、血清23型菌株2023WUSS056致病力强。目前血清1、3^[38]、23型^[39]均可从发病猪中分离获得，血清1型菌株可分离于猪关节、脑、肺部，血清3型菌株可分离于猪肺部^[38]。Zouharová等^[39]对分离自捷克的528株发病猪来源菌株进行分型，血清3型(26株，4.92%)、1型(22株，4.17%)、23型(3株，0.57%)均存在；王娟^[40]对2011−2014年分离自广东发病猪的40株分离株进行检测发现，血清3型(13.79%)为优势血清型；北美发病猪中血清型2型和3型为优势血清型，分别为24.3%和21%^[41]；肖琦等^[42]在江苏和广东病死猪分离获得2株猪链球菌均为血清3型，且毒力强；Wisselink等^[43]从7个欧洲国家病猪中分离的411株菌株中，血清1型(12%)为优势血清型；Petrocchi-Rilo等^[38]研究了西班牙的10个自治社区的207株发病猪来源的分离株，1型(21.3%)、3型(6.3%)和23型(1.0%)均存在。而且，血清1型还属于感染人的血清型，2011年从泰国东部的败血症患者血液中分离出1株血清1型菌株^[12]。

综上所述，江苏两地屠宰场健康猪群猪链球菌感染率较高，血清型多而复杂，存在血清1型、3型、23型等强毒株，97.84%的菌株为多重耐药菌，研究结果为江苏地区该类疫病防控提供了参考。

基金

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国家自然科学基金(32172859)

参考文献

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文献

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参考文献引证文献

排序方式：

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2025年第65卷第1期

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doi: 10.13343/j.cnki.wsxb.20240369

接收时间：2024-06-17
首发时间：2026-03-21
出版时间：2025-01-04

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出版历史

收稿日期：2024-06-17
录用日期：2024-10-08

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National Natural Science Foundation of China(32172859)

国家自然科学基金(32172859)

作者信息

1 南京农业大学动物医学院, 江苏南京 210014

2 农业农村部动物细菌学重点实验室, 江苏南京 210014

3 世界动物卫生组织猪链球菌病参考实验室, 江苏南京 210014

4 广东省养猪与猪病防控技术研究企业重点实验室, 广东海大畜牧兽医研究院, 广东广州 511400

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2种不同金属材料的力学参数

科 Family	属数 Number of genus	种数 Number of species	占总种数比例 Percentage of total species (%)	属 Genus	种数 Number of species	占总种数比例 Percentage of total species (%)
鹅膏菌科Amanitaceae	2	11	5.26	鹅膏菌属 Amanita	10	4.78
小菇科 Mycenaceae	2	12	5.74	丝盖伞属 Inocybe	5	2.39
多孔菌科 Polyporaceae	8	14	6.70	蜡蘑属 Laccaria	5	2.39
红菇科 Russulaceae	3	23	11.00	小皮伞属 Marasmius	6	2.87
				小菇属 Mycena	11	5.26
				光柄菇属 Pluteus	5	2.39
				红菇属 Russula	17	8.13
				栓菌属 Trametes	5	2.39

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Antimicrobials	Resistance rate in Kunshan (%)	Resistance rate in Danyang (%)	Overall resistance rate (%)
The bold is the class of antimicrobials.
β-lactam antibiotics	45.16 (28/62)	16.88 (13/77)	29.50 (41/139)
Penicillin	45.16 (28/62)	16.88 (13/77)	29.50 (41/139)
Amoxicillin	27.42 (17/62)	3.90 (3/77)	14.39 (20/139)
Cefotaxime	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
Rifamycins	4.84 (3/62)	2.60 (2/77)	3.60 (5/139)
Rifampicin	4.84 (3/62)	2.60 (2/77)	3.60 (5/139)
Glycopeptides	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
Vancomycin	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
Qxazolidinones	27.42 (17/62)	15.58 (12/77)	20.86 (29/139)
Linezolid	27.42 (17/62)	15.58 (12/77)	20.86 (29/139)
Quinolones	67.74 (42/62)	29.87 (23/77)	46.76 (65/139)
enrofloxacin	64.52 (40/62)	29.87 (23/77)	45.32 (63/139)
Marbofloxacin	67.74 (42/62)	29.87 (23/77)	46.76 (65/139)
Amphenicols	53.23 (33/62)	53.25 (41/77)	53.24 (74/139)
Chloramphenicol	30.65 (19/62)	22.08 (17/77)	25.90 (36/139)
Florfenicol	53.23 (33/62)	50.65 (39/77)	51.80 (72/139)
Lincosamides	96.77 (60/62)	100.00 (77/77)	98.56 (137/139)
Licomycin	96.77 (60/62)	53.25 (41/77)	72.66 (101/139)
Clindamycin	95.16 (59/62)	100.00 (77/77)	97.84 (136/139)
Pleuromutilin	54.84 (34/62)	53.25 (41/77)	53.96 (75/139)
Tiamulin	54.84 (34/62)	45.45 (35/77)	49.64 (69/139)
Valnemulin	33.87 (21/62)	40.26 (31/77)	37.41 (52/139)
Aminoglycosides	79.03 (49/62)	75.32 (58/77)	76.98 (107/139)
Gentamicin	53.23 (33/62)	58.44 (45/77)	56.12 (78/139)
Kanamycin	61.29 (38/62)	61.04 (47/77)	61.15 (85/139)
Streptomycin	45.16 (28/62)	36.36 (28/77)	40.29 (56/139)
Spectinomycin	46.77 (29/62)	33.77 (26/77)	39.57 (55/139)
Macrolides	91.94 (57/62)	98.70 (76/77)	95.68 (133/139)
Tilmicosin	88.71 (55/62)	98.70 (76/77)	95.68 (133/139)
Erythromycin	90.32 (56/62)	98.70 (76/77)	94.96 (132/139)
Azithromycin	90.32 (56/62)	97.40 (75/77)	94.24 (131/139)
Tetracyclines	93.55 (58/62)	98.70 (76/77)	96.40 (134/139)
Doxycycline	93.55 (58/62)	98.70 (76/77)	96.40 (134/139)
Tetracycline	91.94 (57/62)	98.70 (76/77)	95.68 (133/139)

Antimicrobials

Resistance rate in Kunshan (%)

Resistance rate in Danyang (%)

Overall resistance rate (%)

The bold is the class of antimicrobials.

β-lactam antibiotics

45.16 (28/62)

16.88 (13/77)

29.50 (41/139)

Penicillin

45.16 (28/62)

16.88 (13/77)

29.50 (41/139)

Amoxicillin

27.42 (17/62)

3.90 (3/77)

14.39 (20/139)

Cefotaxime

0.00 (0/62)

0.00 (0/77)

0.00 (0/139)

Rifamycins

4.84 (3/62)

2.60 (2/77)

3.60 (5/139)

Rifampicin

4.84 (3/62)

2.60 (2/77)

3.60 (5/139)

Glycopeptides

0.00 (0/62)

0.00 (0/77)

0.00 (0/139)

Vancomycin

0.00 (0/62)

0.00 (0/77)

0.00 (0/139)

Qxazolidinones

27.42 (17/62)

15.58 (12/77)

20.86 (29/139)

Linezolid

27.42 (17/62)

15.58 (12/77)

20.86 (29/139)

Quinolones

67.74 (42/62)

29.87 (23/77)

46.76 (65/139)

enrofloxacin

64.52 (40/62)

29.87 (23/77)

45.32 (63/139)

Marbofloxacin

67.74 (42/62)

29.87 (23/77)

46.76 (65/139)

Amphenicols

53.23 (33/62)

53.25 (41/77)

53.24 (74/139)

Chloramphenicol

30.65 (19/62)

22.08 (17/77)

25.90 (36/139)

Florfenicol

53.23 (33/62)

50.65 (39/77)

51.80 (72/139)

Lincosamides

96.77 (60/62)

100.00 (77/77)

98.56 (137/139)

Licomycin

96.77 (60/62)

53.25 (41/77)

72.66 (101/139)

Clindamycin

95.16 (59/62)

100.00 (77/77)

97.84 (136/139)

Pleuromutilin

54.84 (34/62)

53.25 (41/77)

53.96 (75/139)

Tiamulin

54.84 (34/62)

45.45 (35/77)

49.64 (69/139)

Valnemulin

33.87 (21/62)

40.26 (31/77)

37.41 (52/139)

Aminoglycosides

79.03 (49/62)

75.32 (58/77)

76.98 (107/139)

Gentamicin

53.23 (33/62)

58.44 (45/77)

56.12 (78/139)

Kanamycin

61.29 (38/62)

61.04 (47/77)

61.15 (85/139)

Streptomycin

45.16 (28/62)

36.36 (28/77)

40.29 (56/139)

Spectinomycin

46.77 (29/62)

33.77 (26/77)

39.57 (55/139)

Macrolides

91.94 (57/62)

98.70 (76/77)

95.68 (133/139)

Tilmicosin

88.71 (55/62)

98.70 (76/77)

95.68 (133/139)

Erythromycin

90.32 (56/62)

98.70 (76/77)

94.96 (132/139)

Azithromycin

90.32 (56/62)

97.40 (75/77)

94.24 (131/139)

Tetracyclines

93.55 (58/62)

98.70 (76/77)

96.40 (134/139)

Doxycycline

93.55 (58/62)

98.70 (76/77)

96.40 (134/139)

Tetracycline

91.94 (57/62)

98.70 (76/77)

95.68 (133/139)

Resistance genes	Detection rate of resistance rate in Kunshan (%)	Detection rate of resistance rate in Danyang (%)	Overall detection rate (%)
The bold is the class of antimicrobials.
Macrolides	90.32 (56/62)	93.51 (72/77)	92.09 (128/139)
ermA	0.00 (0/62)	2.60 (2/77)	1.44 (2/139)
ermB	88.71 (55/62)	93.51 (72/77)	91.37 (127/139)
ermC	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
mefA	3.23 (2/62)	2.60 (2/77)	2.88 (4/139)
msr(D)	3.23 (2/62)	1.30 (1/77)	2.16 (3/139)
Lincosamides	9.68 (6/62)	20.78 (16/77)	15.83 (22/139)
lsa(E)	9.68 (6/62)	20.78 (16/77)	15.83 (22/139)
Tetracyclines	74.19 (46/62)	75.32 (58/77)	74.82 (104/139)
tetO	50.00 (31/62)	57.14 (44/77)	53.96 (75/139)
tetM	12.90 (8/62)	9.09 (7/77)	10.79 (15/139)
tet(O/W/32/O)	16.13 (10/62)	10.39 (8/77)	12.95 (18/139)
tetL	6.45 (4/62)	6.49 (5/77)	6.47 (9/139)
Amphenicols	9.68 (6/62)	7.79 (6/77)	8.63 (12/139)
fexA	6.45 (4/62)	7.79 (6/77)	7.19 (10/139)
fexB	3.23 (2/62)	0.00 (0/77)	1.44 (2/139)
Qxazolidinones	1.61 (1/62)	2.60 (2/77)	2.16 (3/139)
optrA	1.61 (1/62)	2.60 (2/77)	2.16 (3/139)
Aminoglycosides	53.23 (33/62)	49.35 (38/77)	51.08 (71/139)
aph(2')-Ib	0.00 (0/62)	1.30 (1/77)	0.72 (1/139)
aph(2')-Ic	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
aph(2')-Id	0.00 (0/62)	0.00 (0/77)	0.00 (0/139)
aph(3')-IIIa	19.35 (12/62)	11.69 (9/77)	15.11 (21/139)
ant(6')-Ia	9.68 (6/62)	7.79 (6/77)	8.63 (12/139)
aac(6')-aph(2'')	37.10 (23/62)	40.26 (31/77)	38.85 (54/139)

Resistance genes

Detection rate of resistance
rate in Kunshan (%)

Detection rate of resistance
rate in Danyang (%)

Overall detection rate (%)

The bold is the class of antimicrobials.

Macrolides

90.32 (56/62)

93.51 (72/77)

92.09 (128/139)

ermA

0.00 (0/62)

2.60 (2/77)

1.44 (2/139)

ermB

88.71 (55/62)

93.51 (72/77)

91.37 (127/139)

ermC

0.00 (0/62)

0.00 (0/77)

0.00 (0/139)

mefA

3.23 (2/62)

2.60 (2/77)

2.88 (4/139)

msr(D)

3.23 (2/62)

1.30 (1/77)

2.16 (3/139)

Lincosamides

9.68 (6/62)

20.78 (16/77)

15.83 (22/139)

lsa(E)

9.68 (6/62)

20.78 (16/77)

15.83 (22/139)

Tetracyclines

74.19 (46/62)

75.32 (58/77)

74.82 (104/139)

tetO

50.00 (31/62)

57.14 (44/77)

53.96 (75/139)

tetM

12.90 (8/62)

9.09 (7/77)

10.79 (15/139)

tet(O/W/32/O)

16.13 (10/62)

10.39 (8/77)

12.95 (18/139)

tetL

6.45 (4/62)

6.49 (5/77)

6.47 (9/139)

Amphenicols

9.68 (6/62)

7.79 (6/77)

8.63 (12/139)

fexA

6.45 (4/62)

7.79 (6/77)

7.19 (10/139)

fexB

3.23 (2/62)

0.00 (0/77)

1.44 (2/139)

Qxazolidinones

1.61 (1/62)

2.60 (2/77)

2.16 (3/139)

optrA

1.61 (1/62)

2.60 (2/77)

2.16 (3/139)

Aminoglycosides

53.23 (33/62)

49.35 (38/77)

51.08 (71/139)

aph(2')-Ib

0.00 (0/62)

1.30 (1/77)

0.72 (1/139)

aph(2')-Ic

0.00 (0/62)

0.00 (0/77)

0.00 (0/139)

aph(2')-Id

0.00 (0/62)

0.00 (0/77)

0.00 (0/139)

aph(3')-IIIa

19.35 (12/62)

11.69 (9/77)

15.11 (21/139)

ant(6')-Ia

9.68 (6/62)

7.79 (6/77)

8.63 (12/139)

aac(6')-aph(2'')

37.10 (23/62)

40.26 (31/77)

38.85 (54/139)

Strains	Mortality (%)	Serotype	Significance	P
The virulence of isolates was compared to the highly virulent strain SC070731 and subjected to statistical analysis using the Log-Rank (Mantel-Cox) test. The symbols , , , and ** correspond to P < 0.05, P < 0.01, P < 0.001, and P < 0.000 1, respectively, while “ns” signifies no significance.
SC070731	100.00	2	−	−
SH040917	0.00	9	****	< 0.000 1
2023WUSS142	86.67	1	ns	0.073 3
2023WUSS124	80.00	3	ns	0.098 0
2023WUSS014	46.67	4	***	0.000 2
2023WUSS016	73.33	5	**	0.006 1
2023WUSS048	73.33	5	ns	0.102 9
2023WUSS088	73.33	6	****	< 0.000 1
2023WUSS017	86.67	7	***	0.001 2
2023WUSS111	6.67	7	****	< 0.000 1
2023WUSS085	86.67	8	*	0.014 6
2023WUSS126	13.33	8	****	< 0.000 1
2023WUSS001	6.67	9	****	< 0.000 1
2023WUSS094	46.67	9	****	< 0.000 1
2023WUSS128	73.33	10	***	0.000 5
2023WUSS083	6.67	12	****	< 0.000 1
2023WUSS019	80.00	15	***	0.000 8
2023WUSS052	46.67	15	***	0.002 0
2023WUSS012	26.67	16	****	< 0.000 1
2023WUSS047	66.67	16	***	0.000 2
2023WUSS025	33.33	19	****	< 0.000 1
2023WUSS064	13.33	19	****	< 0.000 1
2023WUSS051	6.67	21	****	< 0.000 1
2023WUSS056	93.33	23	ns	0.315 2
2023WUSS082	0.00	24	****	< 0.000 1
2023WUSS021	6.67	29	****	< 0.000 1
2023WUSS053	33.33	29	****	< 0.000 1
2023WUSS058	26.67	30	****	< 0.000 1
2023WUSS007	66.67	31	****	< 0.000 1
2023WUSS043	53.33	31	***	0.000 7
2023WUSS045	0.00	1/2	****	< 0.000 1
2023WUSS087	66.67	1/2	*	0.010 7
2023WUSS029	26.67	NCL1	****	< 0.000 1
2023WUSS131	60.00	NCL1	**	0.006 1
2023WUSS036	6.67	NCL11	****	< 0.000 1
2023WUSS033	13.33	NCL2	****	< 0.000 1
2023WUSS063	20.00	NCL20	****	< 0.000 1
2023WUSS035	86.67	NCL3	ns	0.198 3
2023WUSS061	66.67	NCL3	****	< 0.000 1
2023WUSS132	73.33	NCL4	ns	0.126 5
2023WUSS133	80.00	NCL5	**	0.009 4
2023WUSS062	0.00	NCL7	****	< 0.000 1
2023WUSS134	13.33	NCL9	****	< 0.000 1
2023WUSS073	6.67	Unknown	****	< 0.000 1
2023WUSS076	40.00	Unknown	****	< 0.000 1

Strains

Mortality (%)

Serotype

Significance

The virulence of isolates was compared to the highly virulent strain SC070731 and subjected to statistical analysis using the Log-Rank (Mantel-Cox) test. The symbols *, **, ***, and **** correspond to P < 0.05, P < 0.01, P < 0.001, and P < 0.000 1, respectively, while “ns” signifies no significance.

SC070731

100.00

−

SH040917

0.00

****

< 0.000 1

2023WUSS142

86.67

0.073 3

2023WUSS124

80.00

0.098 0

2023WUSS014

46.67

***

0.000 2

2023WUSS016

73.33

0.006 1

2023WUSS048

73.33

0.102 9

2023WUSS088

73.33

****

< 0.000 1

2023WUSS017

86.67

***

0.001 2

2023WUSS111

6.67

****

< 0.000 1

2023WUSS085

86.67

0.014 6

2023WUSS126

13.33

****

< 0.000 1

2023WUSS001

6.67

****

< 0.000 1

2023WUSS094

46.67

****

< 0.000 1

2023WUSS128

73.33

***

0.000 5

2023WUSS083

6.67

****

< 0.000 1

2023WUSS019

80.00

***

0.000 8

2023WUSS052

46.67

***

0.002 0

2023WUSS012

26.67

****

< 0.000 1

2023WUSS047

66.67

***

0.000 2

2023WUSS025

33.33

****

< 0.000 1

2023WUSS064

13.33

****

< 0.000 1

2023WUSS051

6.67

****

< 0.000 1

2023WUSS056

93.33

0.315 2

2023WUSS082

0.00

****

< 0.000 1

2023WUSS021

6.67

****

< 0.000 1

2023WUSS053

33.33

****

< 0.000 1

2023WUSS058

26.67

****

< 0.000 1

2023WUSS007

66.67

****

< 0.000 1

2023WUSS043

53.33

***

0.000 7

2023WUSS045

0.00

1/2

****

< 0.000 1

2023WUSS087

66.67

1/2

0.010 7

2023WUSS029

26.67

NCL1

****

< 0.000 1

2023WUSS131

60.00

NCL1

0.006 1

2023WUSS036

6.67

NCL11

****

< 0.000 1

2023WUSS033

13.33

NCL2

****

< 0.000 1

2023WUSS063

20.00

NCL20

****

< 0.000 1

2023WUSS035

86.67

NCL3

0.198 3

2023WUSS061

66.67

NCL3

****

< 0.000 1

2023WUSS132

73.33

NCL4

0.126 5

2023WUSS133

80.00

NCL5

0.009 4

2023WUSS062

0.00

NCL7

****

< 0.000 1

2023WUSS134

13.33

NCL9

****

< 0.000 1

2023WUSS073

6.67

Unknown

****

< 0.000 1

2023WUSS076

40.00

Unknown

****

< 0.000 1

Strains	Mortality (%)	Serotype	Significance	P
The virulence of isolates was compared to the highly virulent strain SC070731 and subjected to statistical analysis using the Log-Rank (Mantel-Cox) test. The symbols * and **** correspond to P < 0.05 and P < 0.000 1, respectively, while “ns” signifies no significance.
SH040917	0.00	9	****	< 0.000 1
SC070731	100.00	2	−	−
2023WUSS056	90.00	23	ns	0.860 0
2023WUSS124	90.00	3	ns	0.061 7
2023WUSS142	80.00	1	*	0.010 1

Strains

Mortality (%)

Serotype

Significance

The virulence of isolates was compared to the highly virulent strain SC070731 and subjected to statistical analysis using the Log-Rank (Mantel-Cox) test. The symbols * and **** correspond to P < 0.05 and P < 0.000 1, respectively, while “ns” signifies no significance.

SH040917

0.00

****

< 0.000 1

SC070731

100.00

−

2023WUSS056

90.00

0.860 0

2023WUSS124

90.00

0.061 7

2023WUSS142

80.00

0.010 1