Ingham Anna Cäcilia, Urth Tinna Ravnholt, Sieber Raphael Niklaus, Stegger Marc, Edslev Sofie Marie, Angen Øystein, Larsen Anders Rhod
Department of Bacteria, Parasites and Fungi, Statens Serum Institutgrid.6203.7, Copenhagen, Denmark.
Department of Infectious Disease Epidemiology and Prevention, Statens Serum Institutgrid.6203.7, Copenhagen, Denmark.
Appl Environ Microbiol. 2021 Aug 26;87(18):e0122521. doi: 10.1128/AEM.01225-21.
Drivers of pig trucks constitute a potential route of human transmission of livestock-associated methicillin-resistant Staphylococcus aureus clonal complex 398 (LA-MRSA CC398). In this study, we determined MRSA prevalence in pig truck drivers ( = 47) and monitored the nasal microbiota of 9 drivers 3 times daily throughout 1 workweek ( = 113 samples) and compared it to that of their spouses ( = 25 samples from 6 spouses) and 89 nonexposed subjects. S. aureus isolates ( = 232) derived from a subset of nasal and truck samples were whole-genome sequenced. The nasal alpha diversity of drivers in the beginning of the workday was lower than that of nonexposed subjects. During the workday, it increased significantly. Similarly, the drivers' nasal composition shifted during the workday, becoming increasingly different from that of their spouses and nonexposed individuals. Clustering into community state types (CSTs) revealed frequent switches from either S. aureus- or -dominated CSTs in the mornings to a dominated CST during the workday. Six intermittent MRSA carriers were mostly MRSA negative in the mornings, and their nasal microbiota resembled that of nonexposed subjects. When acquiring MRSA during the workday, they switched to the dominated CST. In contrast, the nasal microbiota of two persistent MRSA carriers was dominated by staphylococci. In conclusion, we show that the nasal microbiota of pig truck drivers is very dynamic, undergoes drastic changes during workdays, and differs from that of nonexposed subjects even before pig contact. MRSA-carrying drivers may eventually introduce MRSA into the community and health care facilities. Carriage dynamics, however, showed that for most drivers, CC398 MRSA is rapidly lost and only rarely causes transmission to spouses. In Denmark, the number of human methicillin-resistant Staphylococcus aureus (MRSA) cases has increased dramatically since the early 2000s, starting from imported cases and spreading in the community. However, today, approximately one-third of all new cases are attributed to livestock-associated MRSA clonal complex 398 (LA-MRSA CC398). This mirrors the increase in pig farms, of which 95% are now positive for LA-MRSA, and this has been caused mainly by three dominant lineages enriched for a number of key antimicrobial resistance genes. Although most human LA-MRSA CC398 infections in Denmark are linked to livestock contact, still up to one-third are not. Pig truck drivers constitute a previously understudied occupation group which may transmit LA-MRSA CC398 to household members, the community, and hospitals. In this study, we demonstrate dramatic work-related changes in the nasal microbiota of pig truck drivers, as well as in their carriage of LA-MRSA CC398. However, they likely do not constitute an important reservoir for LA-MRSA CC398 dissemination.
运猪车司机构成了与家畜相关的耐甲氧西林金黄色葡萄球菌克隆复合体398(LA-MRSA CC398)人际传播的潜在途径。在本研究中,我们测定了运猪车司机(n = 47)的耐甲氧西林金黄色葡萄球菌(MRSA)流行率,并在1个工作周内每天3次监测9名司机的鼻腔微生物群(n = 113份样本),并将其与他们配偶的鼻腔微生物群(来自6名配偶的25份样本)以及89名未接触者进行比较。对从一部分鼻腔和车辆样本中分离出的金黄色葡萄球菌菌株(n = 232)进行全基因组测序。工作日开始时,司机的鼻腔α多样性低于未接触者。在工作日期间,其显著增加。同样,司机的鼻腔菌群在工作日期间发生了变化,与他们的配偶和未接触者的菌群差异越来越大。聚类为社区状态类型(CSTs)显示,从早上以金黄色葡萄球菌或其他菌为主导的CSTs频繁转变为工作日期间以其他菌为主导的CSTs。6名间歇性MRSA携带者早上大多为MRSA阴性,其鼻腔微生物群与未接触者相似。当在工作日期间感染MRSA时,他们转变为以其他菌为主导的CSTs。相比之下,两名持续性MRSA携带者的鼻腔微生物群以葡萄球菌为主导。总之,我们表明运猪车司机的鼻腔微生物群非常动态,在工作日期间会发生剧烈变化,甚至在接触猪之前就与未接触者不同。携带MRSA的司机最终可能会将MRSA引入社区和医疗保健机构。然而,携带情况动态显示,对于大多数司机来说,CC398 MRSA会迅速消失,很少传播给配偶。在丹麦,自21世纪初以来,人类耐甲氧西林金黄色葡萄球菌(MRSA)病例数量急剧增加,从输入性病例开始并在社区传播。然而,如今,所有新病例中约三分之一归因于与家畜相关的MRSA克隆复合体398(LA-MRSA CC398)。这反映了养猪场数量的增加,其中95%现在对LA-MRSA呈阳性,这主要是由富含一些关键抗菌耐药基因的三个优势谱系引起的。尽管丹麦大多数人类LA-MRSA CC398感染与家畜接触有关,但仍有多达三分之一并非如此。运猪车司机构成了一个此前未被充分研究的职业群体,可能会将LA-MRSA CC398传播给家庭成员、社区和医院。在本研究中,我们证明了运猪车司机鼻腔微生物群以及他们携带LA-MRSA CC398的情况与工作相关的显著变化。然而,他们可能不是LA-MRSA CC398传播的重要储存宿主。