新疆阿克苏地区猪场optrA/lsa(E)阳性粪肠球菌的耐药情况及传播特点分析

doi:10.3864/j.issn.0578-1752.2023.16.013

摘要/Abstract

摘要：

【目的】了解新疆阿克苏地区猪源粪肠球菌中optrA和lsa(E)的流行及传播特点，并探明optrA和lsa(E)阳性粪肠球菌的耐药情况，为评估两个耐药基因对公共卫生的影响和危害提供科学依据。【方法】对新疆农业大学兽医药理学实验室分离保存的322株粪肠球菌采用PCR的方法进行optrA和lsa(E)筛查，根据CLSI推荐药物及方法采用琼脂稀释法测定optrA和lsa(E)阳性菌株对氨苄西林、红霉素、泰乐菌素、四环素、多西环素、利奈唑胺、氟苯尼考、万古霉素、左氧氟沙星、恩诺沙星、庆大霉素和沃尼妙林的最小抑菌浓度（MIC）并进行耐药判定，利用PCR方法筛查相应的耐药基因，包括ermA、ermB、ermC、fexA、fexB、tet(K)、tet(L)、tet(M)、aac(6')-le-aph(2")-Ia和cfr。选取31株不同来源的optrA和lsa(E)阳性粪肠球菌进行MLST分子分型和接合转移试验。【结果】共193株粪肠球菌检出optrA和/或lsa(E)，其中38株optrA和lsa(E)共存，9株仅携带optrA，146株仅携带lsa(E)。这193株粪肠球菌对红霉素、泰乐菌素、四环素、多西环素、庆大霉素和沃尼妙林的耐药率均达到100%，虽然optrA检出率远低于lsa(E)，但optrA阳性菌株总体耐药程度明显高于仅携带lsa(E)的菌株以及optrA、lsa(E)双阴性的菌株，其耐药基因的检出结果也呈现相同趋势。optrA和lsa(E)共存和仅携带optrA菌株的多重耐药谱集中在8耐和10耐，占比分别为84.6%和100.0%，而仅携带lsa(E)的菌株和optrA、lsa(E)双阴性菌株的多重耐药谱主要集中在6—8耐，占比为89.4%和90.7%。进一步分析optrA、lsa(E)与耐药性之间的关系发现，耐药较为严重的猪场optrA和lsa(E)的检出率也相对较高。耐药基因检出结果显示：193株菌均不同程度地携带ermB、ermC、tet(K)、tet(L)、tet(M)、aac(6')-Ie-aph(2")-Ia、fex(A)，并且optrA、lsa(E)共存的菌株及仅携带optrA菌株的耐药基因检出率总体上也高于仅携带lsa(E)的菌株和optrA、lsa(E)双阴性菌株。MLST和接合转移试验结果提示，optrA/lsa(E)菌株遗传环境复杂、可能既存在克隆传播又存在水平转移的现象。【结论】新疆阿克苏地区猪源粪肠球菌中optrA和lsa(E)的高携带率以及高耐药水平表明该地区耐药形势严峻，对当地生猪养殖业甚至于公共卫生安全都造成威胁，应及时采取措施以防控耐药性的进一步发展。

关键词: 阿克苏地区, 猪场, 粪肠球菌, optrA基因, lsa(E)基因, 耐药

Abstract:

【Objective】 The purpose of this study was to investigate the prevalence of optrA and lsa(E) genes in Enterococcus faecalis isolates from pig farms in Aksu region of Xinjiang and the resistance profiles of these optrA/lsa(E)-carrying isolates, which would provide scientific data for evaluating the impact and hazard of these two important resistance genes. 【Method】PCR screening of optrA and lsa(E) genes were conducted for the collected 322 E. faecalis isolates in laboratory of veterinary pharmacology from Xinjiang Agricultural University. The minimum inhibitory concentrations (MICs) of doxycycline, linezolid, florfenicol, vancomycin, levofloxacin, enrofloxacin, gentamicin and valnemulin were determined by agar dilution method recommended by CLSI documents. Corresponding resistance genes, including ermA, ermB, ermC, fexA, fexB, tet(K), tet(L), tet(M), aac(6')-le- aph(2")-Ia, and cfr, were detected by PCR method. 31 strains with different backgrounds were selected to determine the MLST types and subjected to conjugation transfer experiments. 【Result】A total of 193 E. faecalis isolates were positive for optrA and/or lsa(E), of which 38 strains co-harbored optrA and lsa(E), 9 strains produced only optrA gene, and 146 strains contained only lsa(E) gene. The 193 E. faecalis strains showed 100% resistance to erythromycin, tylosin, tetracycline, doxycycline, gentamicin and valnemulin. Although the detection rate of optrA gene was much lower than that of lsa(E), the bacterial resistance degree in optrA-carrying isolates was significantly higher than that in strains carrying only lsa(E) gene and optrA and lsa(E)-negative strains. The detection rates of resistance genes also showed similar trend. E. faecalis strains carrying both optrA and lsa(E) and strains carrying only optrA showed multiresistance to 8 and 10 antibiotics, accounting for 84.6% and 100.0%, respectively. E. faecalis strains carrying only lsa(E) and optrA and lsa(E)-negative strains were mainly resistant to 6-8 antibitoics, accounting for 84.6% and 100.0%, respectively. Further analysis showed that detection rates of optrA and lsa(E) genes were higher in the pig farms with high resistance degree. Screening of resistance genes showed that ermB, ermC, tet(K), tet(L), tet(M), aac(6')-Ie-aph(2")-Ia, and fex(A) genes were presented in the 193 E. faecalis strains. In general, the detection rates of resistance genes in E. faecalis strains carrying both optrA and lsa(E) and single optrA genes were higher than that in strains carrying single lsa(E) and optrA and lsa(E)-negative strains. The results of MLST and conjugation transfer experiments indicated that optrA/lsa(E)-producing E. faecalis strains were genetically complex and clonal and horizontal transfer co-existed in these pig farms. 【Conclusion】The high carriage rate of optrA and lsa(E) genes and the high level of drug resistance in E. faecalis in pig farms in Aksu region of Xinjiang indicated that antibiotic resistance was serious in this region, which could threaten not only pig industry, but also public health. Preventive and control actions should be taken immediately to prevent further deterioration of antibiotic resistance.

Key words: Aksu area, pig farms, Enterococcus faecalis, OptrA gene, Lsa(E) gene, drug resistance

王东, 陈万昭, 李宏博, 秦蕾, 徐琦琦, 刘泽鹏, 夏利宁. 新疆阿克苏地区猪场optrA/lsa(E)阳性粪肠球菌的耐药情况及传播特点分析[J]. 中国农业科学, 2023, 56(16): 3213-3225.

WANG Dong, CHEN WanZhao, LI HongBo, QIN Lei, XU QiQi, LIU ZePeng, XIA LiNing. Analysis of Drug Resistance and Epidemic Characteristics of optrA/lsa(E) in Enterococcus faecalis from Pig Farms in Aksu Area of Xinjiang[J]. Scientia Agricultura Sinica, 2023, 56(16): 3213-3225.

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引物名称 Primer	引物序列 Sequence (5'-3')	片段大小 Products (bp)	退火温度 Annealing temperature (℃)
optrA-F	AGGTGGTCAGCGAACTAA	1466	54
optrA-R	ATCAACTGTTCCCATTCA	1466	54
lsa(E)-F	TTGTACGGAATGTATGG	675	52
lsa(E)-R	TTCGCTTCTATTAAGCACTCTT	675	52

引物名称 Primer	引物序列 Sequences (5'-3')	片段大小 Products (bp)	退火温度 Annealing temperature (℃)
ermA-F	TCTAAAAAGCATGTAAAAGAA	645	53.0
ermA-R	CTTCGATAGTTTATTAATATTAGT	645	53.0
ermB-F	GAAAAAGTACTCAACCAAATA	639	50.0
ermB-R	AGTAACGGTACTTAAATTGTTTAC	639	50.0
ermC-F	TCGAAACGTAATATAGATAAA	642	47.5
ermC-R	GCTAATATTGTTTAAATCGTCAAT	642	47.5
tet(L)-F	GTTGCGCGCTATATTCCAAA	788	51.7
tet(L)-R	TTAAGCAAACTCATTCCAGC	788	51.7
tet(K)-F	TTAGGTGAAGGGTTAGGTCC	718	49.9
tet(K)-R	GCAAACTCATTCCAGAAGCA	718	49.9
tet(M)-F	ACAGAAAGCTTATTATATAAC	171	48.5
tet(M)-R	TGGCGTGTCTATGATGTTCAC	171	48.5
fexA-F	GTACTTGTAGGTGCAATTACGGCTGA	1272	57.0
fexA-R	CGCATCTGAGTAGGACATAGCGTC	1272	57.0
fexB-F	TTCCCACTATTGGTGAAAGGAT	750	51.9
fexB-R	GCAATTCCCTTTTATGGACGTT	750	51.9
cfr-F	TGAAGTATAAAGCAGGTTGGGAGT	746	53.2
cfr-R	ACCATATAATTGACCACAAGCAGC	746	53.2
aac(6')-aph(2")-F	CCAAGAGCAATAAGGGATACC	672	58.0
aac(6')-aph(2")-R	ACCCTCAAAAACTGTTGTTGC	672	58.0

基因携带情况 Gene carriage status	检出率（检出数/菌株总数）Detectable rate (Number of detections/ total number of strains)
基因携带情况 Gene carriage status	A猪场 A farm	B猪场 B farm	C猪场 C farm	D猪场 D farm	合计 Total
共存菌株 Coexistence of two genes	4.5%（2/44）	27.2%（22/81）	0（0/35）	8.6%（14/162）	11.8%（38/322）
仅检出optrA的菌株 Strains with only the optrA detected	4.5%（2/44）	8.6%（7/81）	0（0/35）	0（0/162）	2.8%（9/322）
仅检出lsa(E)的菌株 Strains with only the lsa(E) detected	11.4%（5/44）	33.3%（27/81）	22.8%（8/35）	63.0%（102/162）	45.3%（146/322）

抗菌药物 Antibacterial drug	猪场（耐药数/菌株数）Swine farm (Number of drug resistance/ Number of strains)
抗菌药物 Antibacterial drug	A猪场 A farm	B猪场 B farm	C猪场C farm	D猪场 D farm	合计 Total
AMP	0.0% a（0/44）	0.0% a（0/81）	0.0% a（0/146）	0.0% a（0/162）	0.0%（0/322）
ERY	97.7% a（43//44）	100.0% a（81/81）	94.3% a（33/35）	100.0% a（162/162）	99.1%（319/322）
TYL	97.7% a（43/44）	100.0% a（81/81）	91.4% a（32/35）	100.0% a（162/162）	98.8%（318/322）
LZD	11.4% a（5/44）	35.8% b（29/81）	0.0% c（0/35）	7.4% ac（12/162）	14.3%（46/322）
TET	100.0% a（44/44）	100.0% a（81/81）	97.1% a（34/35）	100.0% a（162/162）	99.7%（321/322）
DOX	100.0% a（44/44）	100.0% a（81/81）	100.0% a（35/35）	100.0% a（162/162）	100.0%（322/322）
VAN	0.0% a（0/44）	0.0% a（0/81）	0.0% a（0/35）	0.0% a（0/162）	0.0%（0/322）
FFC	29.5% a（13/44）	54.3% b（44/81）	0.0% c（0/35）	17.9% a（29/162）	26.7%（86/322）
LEV	11.4% ab（5/44）	96.3% c（78/81）	8.6% b（3/35）	23.5% a（38/162）	38.5%（124/322）
ENR	27.3% a（12/44）	96.3% b（78/81）	5.7% c（2/35）	27.8% a（45/162）	42.5%（137/322）
GEN	100.0% a（44/44）	100.0% a（81/81）	100.0% a（35/35）	96.3% a（156/162）	98.1%（316/322）
VAL	100.0% a（44/44）	100.0% a(81/81)	100.0% a(35/35)	96.3% a(156/162)	98.1%(316/322)

抗菌药物 Antibacterial drug	耐药率（耐药菌株数/菌株总数）Drug resistance rate (number of drug-resistant strains/total number of strains)
抗菌药物 Antibacterial drug	共存菌株 Strain with coexistence of two genes	仅检出optrA的菌株 Strains with only the optrA detected	仅检出lsa(E)的菌株 Only lsa(E) positive strains	optrA、lsa(E)阴性菌株 optrA, lsa(E) negative strains
AMP	0 a（0/38）	0 a（0/9）	0 a（0/146）	0.0% a（0/129）
ERY	100.0% a（38/38）	100.0% a（9/9）	100.0% a（146/146）	97.7% a（126/129）
TYL	100.0% a（38/38）	100.0% a（9/9）	100.0% a（146/146）	96.9% a（125/129）
LZD	100.0% a（38/38）	100.0% a（9/9）	0% b（0/146）	0.0% b（0/129）
VAL	100.0% a（38/38）	100.0% a（9/9）	100.0% a（146/146）	99.2% a（128/129）
TET	100.0% a（38/38）	100.0% a（9/9）	100.0% a（146/146）	99.2% a（128/129）
DOX	100.0% a（38/38）	100.0% a（9/9）	100.0% a（146/146）	100.0% a（129/129）
VAN	0 a（0/38）	0 a（0/9）	0 a（0/146）	0 a（0/129）
FFC	100.0% a（38/38）	100.0% a（9/9）	13.7% b（20/146）	17.8% b（23/129）
LEV	52.6% a（20/38）	77.0% a（7/9）	40.4% a（59/146）	29.5% b（38/129）
ENR	55.3% a（21/38）	77.0% a（7/9）	45.9% a（67/146）	29.5% b（38/129）
GEN	100.0% a（38/38）	100.0% a（9/9）	95.9% a（140/146）	100.0% a（129/129）