Outbreaks of Salmonella enterica infections linked to animal contact: Demographic and outbreak characteristics and comparison to foodborne outbreaks—United States, 2009–2014

In the United States, multistate Salmonella outbreaks are most commonly linked to a food source; however, contact with live animals can also result in outbreaks of human illness. To characterize Salmonella outbreaks linked to animal contact and examine differences compared to foodborne outbreaks, we analysed data reported to the Centers for Disease Control and Prevention through the National Outbreak Reporting System (NORS) from 2009 to 2014 with a primary mode of transmission listed as “animal contact” or “food.” Four hundred and eighty‐four outbreaks with animal contact or foodborne transmission were reported through NORS; of these outbreaks, 99 (20.5%) resulted from Salmonella transmission through animal contact and 385 (79.5%) resulted from foodborne transmission, which resulted in 3,604 (19.8%) and 13,568 (80.2%) illnesses, respectively. A higher proportion of illnesses among children aged <1 year and children aged 1–4 years were linked to animal contact outbreaks compared to foodborne outbreaks (15.2% vs. 1.4%, p < 0.01 and 24.5% vs. 5.6%, p < 0.01, respectively). Illnesses resulting in hospitalizations (OR: 1.81, 95% CI: 1.62, 2.02) were more likely to be associated with animal contact compared to food. Animal contact outbreaks reported to NORS were more likely to be multistate compared to foodborne outbreaks (OR: 5.43, 95% CI: 3.37, 8.76) and had a longer median duration (99.0 days vs. 9.0 days, p < 0.01). Characterizing the differences between outbreaks of illness linked to animal contact and outbreaks linked to food provides useful information to investigators to improve public health response.     

噬菌体对鸡肠炎沙门氏菌的防治研究

肠炎沙门氏菌是全球食源性疾病暴发的主要病原菌之一,可引起禽类发病死亡,造成巨大的经济损失.噬菌体是一种细菌病毒,具有严格的宿主特异性.在耐药菌日益增长、抗生素使用受限的情况下,可考虑将噬菌体作为消除病原体的替抗药物.因此,文章就噬菌体对肠炎沙门氏菌的防控及其应用前景展开综述,同时为其他耐药菌的治疗防控提供新的策略.     

禽肠炎沙门菌外膜蛋白OMPX基因的克隆及其在乳酸乳球菌中的表达

以禽肠炎沙门菌基因组DNA为模板,采用PCR技术扩增得到外膜蛋白OMPX基因片段,并将其克隆到乳酸乳球菌表达载体pMG36e中,构建重组质粒pMG36e-OMPX。将重组质粒电转入乳酸乳球菌MG1614,得到重组基因工程乳酸乳球菌,在GM17培养基中培养12h后,经SDS-PAGE分析显示表达的蛋白约为16 000,与预期相符,经Western-blot检测表明,表达的蛋白具有良好的反应特异性。     

Changes in the prevalence,genotypes and antimicrobial resistance phenotypes of non‐typhoidal Salmonella recovered from mail‐order hatchling poultry sold at US feed stores, 2013–2015

Every year, multiple outbreaks of salmonellosis in humans are linked to contact with mail‐order chicks and ducks. The objective of this study was to describe the temporal changes in the prevalence of serovars, genotypes and antimicrobial resistance (AMR) phenotypes of non‐typhoidal Salmonella (NTS) recovered from shipped boxes of mail‐order hatchling poultry in the United States during 2013 to 2015. In each year, a sample of feed stores belonging to a single national chain participated in the study. The store employees submitted swabs or hatchling pads from hatchling boxes and shipment tracking information of the arriving boxes to the investigators. NTS was cultured from the samples and isolates were sent to the National Veterinary Services Laboratories (Ames, IA) for serotyping, pulsed‐field gel electrophoresis (PFGE) and AMR phenotyping. The PFGE patterns of Salmonella serovars isolated from hatchling boxes were compared with those from human outbreaks of salmonellosis linked to live poultry contact. The box‐level prevalence of NTS was significantly higher in 2015 compared to 2014. Also, the population of Salmonella serovars recovered in 2015 was more diverse and substantially different from those recovered in the previous two years. Of PFGE patterns recovered from hatchling boxes, seven distinct patterns in 2015, three in 2014 and four in 2013 were indistinguishable from the PFGE patterns of human outbreaks‐associated strains in the respective years. Importantly, a significant positive correlation was found between the box‐level prevalence of PFGE patterns and the number of human illnesses associated with the same patterns. Also, the proportion of multidrug‐resistant isolates was higher in 2014 and 2015 compared to that in 2013. The results demonstrate that shipments of mail‐order hatchling poultry are frequently contaminated with Salmonella genotypes indistinguishable from human outbreaks‐associated strains each year, and control efforts at hatchery level are likely to have an important public health impact.     

畜禽及环境中沙门氏菌的PCR快速检测与控制

本文运用PCR技术检测家畜及环境中的沙门氏菌,25种沙门氏菌均获得特异性扩增,3种非沙门氏菌检测结果为阴性。表明PCR技术具有快速简便、敏感高和特异性强等优点,值得在沙门氏菌的快速检测中推广应用。并简要介绍了沙门氏菌的相关控制措施。     

广西畜禽产品中沙门氏菌血清型、耐药性及耐药基因调查

试验旨在了解广西部分地区畜禽产品中沙门氏菌血清型分布和耐药状况,以及β-内酰胺酶bla_TEM、bla_CTX-M基因和氟喹诺酮类抗生素耐药基因qnrA、oqxA、oqxB、aac（6'）-Ⅰ b-cr的流行情况。对沙门氏菌进行分离鉴定与血清型分型,采用K-B纸片法对其中随机挑选的80株分离株进行24种抗菌药物敏感性试验,并采用PCR方法进行耐药基因检测。结果显示,从零售生鲜畜禽肉中分离的176株沙门氏菌分属5个血清群,共26种血清型,主要优势血清群为B群60.23%（106/176）、E群18.75%（33/176）和C群15.91%（28/176）,主要优势血清型为德尔卑沙门氏菌35.23%（62/176）、鼠伤寒沙门氏菌11.93%（21/176）和伦敦沙门氏菌9.66%（17/176）。80株分离株对24种抗菌药物均产生不同程度的耐药,其中对复方新诺明、林可霉素、利福平的耐药率最高,均高于90.00%,对青霉素、氨苄西林、阿莫西林、强力霉素、头孢拉啶、头孢氨苄、头孢曲松、头孢他啶、头孢噻肟、阿奇霉素的耐药率介于50.00%~90.00%之间,对环丙沙星、氧氟沙星、氟苯尼考的耐药率小于10.00%;所有分离株均为多重耐药株,其中最少为2重耐药,最多为17重耐药,多重耐药性主要集中在10~16重耐药,共占总数的78.75%（63/80）。PCR结果显示,80株分离株各基因的检出率分别为：bla_TEM 98.75%（79/80）、bla_CTX-M 26.25%（21/80）、oqxA 26.25%（21/80）、oqxB 21.25%（17/80）、qnrA 16.25%（13/80）、aac（6'）-Ⅰb-cr 50.00%（40/80）。结果表明,广西畜禽产品源沙门氏菌血清型呈多样性分布,分离株的耐药情况严重,临床日益严重的耐药现象与耐药基因的普遍存在有很大的关系。     

Serological and Virological Surveillance of Avian Influenza A Virus H9N2 Subtype in Humans and Poultry in Shanghai,China, Between 2008 and 2010

We report the serological evidence of low‐pathogenic avian influenza (LPAI) H9N2 infection in an occupational poultry‐exposed population and a general population. A serological survey of an occupational poultry‐exposed population and a general population was conducted using a haemagglutinin‐inhibiting (HI) assay in Shanghai, China, from January 2008 to December 2010. Evidence of higher anti‐H9 antibodies was found in serum samples collected from poultry workers. During this period, 239 H9N2 avian influenza viruses (AIVs) were isolated from 9297 tracheal and cloacal paired specimens collected from the poultry in live poultry markets. In addition, a total of 733 influenza viruses were isolated from 1569 nasal and throat swabs collected from patients with influenza‐like symptoms in a sentinel hospital, which include H3N2, H1N1, pandemic H1N1 and B, but no H9N2 virus was detected. These findings highlight the need for long‐term surveillance of avian influenza viruses in occupational poultry‐exposed workers.     

Non‐Typhoidal Salmonella Colonization in Chickens and Humans in the Mekong Delta of Vietnam

Salmonellosis is a public health concern in both the developed and developing countries. Although the majority of human non‐typhoidal Salmonella enterica (NTS) cases are the result of foodborne infections or person‐to‐person transmission, NTS infections may also be acquired by environmental and occupational exposure to animals. While a considerable number of studies have investigated the presence of NTS in farm animals and meat/carcasses, very few studies have investigated the risk of NTS colonization in humans as a result of direct animal exposure. We investigated asymptomatic NTS colonization in 204 backyard chicken farms, 204 farmers and 306 matched individuals not exposed to chicken farming, in southern Vietnam. Pooled chicken faeces, collected using boot or handheld swabs on backyard chicken farms, and rectal swabs from human participants were tested. NTS colonization prevalence was 45.6%, 4.4% and 2.6% for chicken farms, farmers and unexposed individuals, respectively. Our study observed a higher prevalence of NTS colonization among chicken farmers (4.4%) compared with age‐, sex‐ and location‐ matched rural and urban individuals not exposed to chickens (2.9% and 2.0%). A total of 164 chicken NTS strains and 17 human NTS strains were isolated, and 28 serovars were identified. Salmonella Weltevreden was the predominant serovar in both chickens and humans. NTS isolates showed resistance (20–40%) against tetracycline, chloramphenicol, sulfamethoxazole‐trimethoprim and ampicillin. Our study reflects the epidemiology of NTS colonization in chickens and humans in the Mekong delta of Vietnam and emphasizes the need of larger, preferably longitudinal studies to study the transmission dynamics of NTS between and within animal and human host populations.     

A case–case study comparing the individual risk factors and symptomatology of Salmonella Heidelberg and Salmonella Typhimurium in Ontario in 2015, following implementation of the Ontario Investigation Tools

Salmonella Heidelberg and Salmonella Typhimurium are among the most common serotypes responsible for human salmonellosis in Ontario. Introduction of the Ontario Investigation Tools (OIT) in 2014 allowed for standardized case investigation and reporting. This study compared the risk factors and symptomatology for sporadic S. Heidelberg and S. Typhimurium cases reported in Ontario in 2015, following implementation of the OIT. Multilevel logistic regression models were applied to assess associations between serotype and individual‐level demographic characteristics, exposures and symptoms for sporadic confirmed cases of S. Heidelberg and S. Typhimurium in Ontario in 2015. There were 476 sporadic cases of S. Typhimurium (n = 278) and S. Heidelberg (n = 198) reported in Ontario in 2015. There were significant associations between the odds of the isolate from a case being one of these serotypes, and travel, consumption of sprouts (any type), contact with reptiles and development of malaise, fever or bloody diarrhoea. The S. Typhimurium and S. Heidelberg cases differed in both symptom presentation and risk factors for illness. Case–case comparisons of Salmonella serotypes have some advantages over case–control studies in that these are less susceptible to selection and recall bias while allowing for rapid comparison of cases to identify potential high‐risk exposures that are unique to one of the serotypes when compared to the other. Comparing cases of two different Salmonella serotypes can help to highlight risk factors that may be uniquely associated with one serotype, or more strongly associated with one serotype compared to another. This information may be useful for understanding relative source attribution between common serotypes of Salmonella.     

Phage and MLVA Typing of Salmonella Enteritidis Isolated from Layers and Humans in Belgium from 2000–2010, A Period in which Vaccination of Laying Hens was Introduced

The aim of the study was to characterize isolates of Salmonella enterica serovar Enteritidis (S. Enteritidis) obtained from humans and layer farms in Belgium collected during 2000–2010. Three periods were compared, namely (i) before implementation of vaccination (2000–2004), (ii) during voluntary vaccination (2005–2006) and (iii) during implementation of the national control program (NCP) for Salmonella including mandatory vaccination against S. Enteritidis (2007–2010). The characteristics compared across time periods were distributions of phage type and multiple‐locus variable number tandem‐repeat assay (MLVA). While PT4 and PT21 were predominantly isolated in Belgium in layers and humans before 2007, a significant reduction of those PTs was observed in both populations in the period 2007–2010. The relative proportion of PT4b, PT21c and PT6c was found to have increased considerably in the layer population since 2007. In the human population, PT8, PT1 and the group of ‘other’ PTs were more frequently isolated compared to the previous periods. When comparing the proportion of the predominant MLVA types Q2 and U2, no significant difference was found between the layer and human population in the three periods and between periods within each category (layer and human). A significant difference in isolate distribution among MLVA clusters I and II was found between human and layer isolates recovered during Period 3 and in the human population between Period 1 and 3. Results suggest that the association between S. Enteritidis in layers and the occurrence of the pathogen in humans changed since implementation of the NCP in 2007.     

Distribution and Diversity of Salmonella Strains in Shipments of Hatchling Poultry,United States, 2013

Multistate outbreaks of salmonellosis associated with live poultry contact have been occurring with increasing frequency. In 2013, multistate outbreaks of salmonellosis were traced back to exposure to live poultry, some of which were purchased at a national chain of farm stores (Farm store chain Y). This study was conducted at 36 stores of Farm store chain Y and was concurrent with the timing of exposure for the human outbreaks of salmonellosis in 2013. We used environmental swabs of arriving shipment boxes of hatchling poultry and shipment tracking information to examine the distribution, diversity and anti‐microbial resistance of non‐typhoidal Salmonella (NTS) across farm stores and hatcheries. Isolates recovered from shipment boxes underwent serotyping, anti‐microbial resistance (AMR) testing and pulsed‐field gel electrophoresis (PFGE). Postal service tracking codes from the shipment boxes were used to determine the hatchery of origin. The PFGE patterns were compared with the PFGE patterns of NTS causing outbreaks of salmonellosis in 2013. A total of 219 hatchling boxes from 36 stores in 13 states were swabbed between 15 March 2013 and 18 April 2013. NTS were recovered from 59 (27%) of 219 hatchling boxes. Recovery was not significantly associated with species of hatchlings, number of birds in the shipment box, or the presence of dead, injured or sick birds. Four of the 23 PFGE patterns and 23 of 50 isolates were indistinguishable from strains causing human outbreaks in 2013. For serotypes associated with human illnesses, PFGE patterns most frequently recovered from shipment boxes were also more frequent causes of human illness. Boxes positive for the same PFGE pattern most frequently originated from the same mail‐order hatchery. Only one of 59 isolates was resistant to anti‐microbials used to treat Salmonella infections in people. This study provides critical information to address recurrent human outbreaks of salmonellosis associated with mail‐order hatchling poultry.     

生鲜禽蛋中兽药使用现状及药物残留有关规定的概述

从国内外禽蛋贸易、蛋禽的安全用药、禽蛋中的食品安全标准、我国禽蛋中兽药残留现状以及相关问题的分析和建议进行综述,以期为养殖企业规范用药、监管部门政策制定和调整、科研机构针对禽蛋食品安全相关研究的开展提供参考。     

乌鲁木齐某农场沙门氏菌的分离鉴定

新疆乌鲁木齐某养鸡场近期发生一起临床表现为实验结果可为精神萎顿、食欲减少、腹泻、有的出现眼盲或肢关节呈跛行等症状的疫情。对送检病料进行病原分离和生化鉴定,结合分子生物学方法、动物回归及药敏试验,确认该鸡场疫情病原为鸡白痢沙门氏菌。建议加强饲养管理、改善环境卫生、做好隔离消毒。本实验可为该病的防控提供参考。     

Antimicrobial Resistance Profiles and Diversity in Salmonella from Humans and Cattle, 2004–2011

Analysis of long‐term anti‐microbial resistance (AMR) data is useful to understand source and transmission dynamics of AMR. We analysed 5124 human clinical isolates from Washington State Department of Health, 391 cattle clinical isolates from the Washington Animal Disease Diagnostic Laboratory and 1864 non‐clinical isolates from foodborne disease research on dairies in the Pacific Northwest. Isolates were assigned profiles based on phenotypic resistance to 11 anti‐microbials belonging to eight classes. Salmonella Typhimurium (ST), Salmonella Newport (SN) and Salmonella Montevideo (SM) were the most common serovars in both humans and cattle. Multinomial logistic regression showed ST and SN from cattle had greater probability of resistance to multiple classes of anti‐microbials than ST and SN from humans (P < 0.0001). While these findings could be consistent with the belief that cattle are a source of resistant ST and SN for people, occurrence of profiles unique to cattle and not observed in temporally related human isolates indicates these profiles are circulating in cattle only. We used various measures to assess AMR diversity, conditional on the weighting of rare versus abundant profiles. AMR profile richness was greater in the common serovars from humans, although both source data sets were dominated by relatively few profiles. The greater profile richness in human Salmonella may be due to greater diversity of sources entering the human population compared to cattle or due to continuous evolution in the human environment. Also, AMR diversity was greater in clinical compared to non‐clinical cattle Salmonella, and this could be due to anti‐microbial selection pressure in diseased cattle that received treatment. The use of bootstrapping techniques showed that although there were shared profiles between humans and cattle, the expected and observed number of profiles was different, suggesting Salmonella and associated resistance from humans and cattle may not be wholly derived from a common population.     

Identification of a Plasmid‐Mediated Quinolone Resistance Gene in Salmonella Isolates from Texas Dairy Farm Environmental Samples

A recent increase in plasmid‐mediated quinolone resistance (PMQR) has been detected among Salmonella isolated from humans in the United States, and it is necessary to determine the sources of human infection. We had previously isolated Salmonella from dairy farm environmental samples collected in Texas, and isolates were tested for anti‐microbial susceptibility. Two isolates, serotyped as Salmonella Muenster, showed the discordant pattern of nalidixic acid susceptibility and intermediate susceptibility to ciprofloxacin. For this project, whole‐genome sequencing of both isolates was performed to detect genes associated with quinolone resistance. The plasmid‐mediated qnrB19 gene and IncR plasmid type were identified in both isolates. To our knowledge, this is the first report of PMQR in Salmonella isolated from food animals or agricultural environments in the United States.     

Serotypes of Salmonella Isolated from Faeces of Patients with Acute Diarrhoea in Gwangju Area,Korea, During 2000–2009

The purpose of this study was to determine the changing pattern of Salmonella serotypes causing acute diarrhoea in humans in Gwangju area, Korea, during 2000–2009. A total of 596 Salmonella isolated from culture of 29 896 faecal samples of patients with acute diarrhoea were included in this study. Faecal samples were collected from local hospitals and clinics in Gwangju area during January 2000–December 2009. The mean annual frequency of isolates for the 10 years was 2.0% (range, 0.9–6.0). The isolates were serologically classified into 43 different serotypes. The 10 most common serotypes were Salmonella Enteritidis (47.9%), S. Typhimurium (20.4%), S. Braenderup (3.2%), S. Montevideo (2.9%), S. Paratyphi B (2.9%), S. London (2.3%), S. Bardo (1.7%), S. Virchow (1.7%), S. Infantis (1.5%) and S. Typhi (1.5%), accounting for 86% of all the isolates. Temporal variations were observed in the distribution of different Salmonella serotypes over the years, and only S. Enteritidis and S. Typhimurium were persistent throughout the study period. Although age specificity varied with serotypes, Salmonella was isolated most frequently from children below 5 years of age (179/596, 30.0%). A seasonal trend was apparent, and the highest rates were found in the summer months. This is the first report of the annual frequency of isolation of Salmonella serotypes, and seasonal and age‐specific patterns of salmonellosis in humans in Gwangju area, Korea, over a decade‐long period.     

Prevalence and risk factors for Salmonella spp. and Campylobacter spp. caecal colonization in broiler chicken and turkey flocks slaughtered in Quebec, Canada

We conducted an observational study to estimate prevalence and risk factors for Salmonella spp. and Campylobacter spp. caecal colonization in poultry. Eighty-one broiler chicken and 59 turkey flocks selected among flocks slaughtered in the province of Quebec, Canada, were included in the study. Flock status was evaluated by culturing pooled caecal contents from about 30 birds per flock. Exposure to potential risk factors was evaluated with a questionnaire. Odds ratios were computed using multivariable logistic regression.

The prevalence of Salmonella-positive flocks was 50% (95% CI: 37, 64) for chickens and 54% (95% CI: 39, 70) for turkeys, respectively. Odds of Salmonella colonization were 2.6 times greater for chicken flocks which failed to lock the chicken house permanently. In turkeys, odds of Salmonella colonization were 4.8–7.7 times greater for flocks which failed to be raised by ≤2 producers with no other visitors allowed onto the premises, or origin from a hatchery.

The prevalence of Campylobacter-positive flocks was 35% (95% CI: 22, 49) for chickens and 46% (95% CI: 30, 62) for turkeys. Odds of colonization were 4.1 times higher for chicken flocks raised on farms with professional rodent control and 5.2 times higher for flocks with manure heap >200 m from the poultry house, and also increased with the number of birds raised per year on the farm and with the age at slaughter. For turkeys, odds of Campylobacter flock colonization were 3.2 times greater in flocks having a manure heap at ≤200 m from poultry house and 4.2 times greater in flocks drinking unchlorinated water.     

Prevalence and Antimicrobial Resistance of Salmonella enterica Serovar Indiana in China (1984–2016)

Salmonella enterica serovar Indiana, first described in 1955, is generally regarded as having a low frequency worldwide with outbreaks of gastroenteritis and abortions described in North America and Europe. In China, S. Indiana was first reported in 1984 and in the subsequent 71 surveys in 35 cities/municipalities from 18 provinces, 70% of which were after 2012, S. Indiana has been shown to have become widely prevalent in people, animals, food and the environment around abattoirs and meat processing facilities. The organism is now one of the most common serovars found in livestock and raw meat in China with S. Indiana isolates having high levels of drug resistance, especially against tetracyclines, quinolones, folate pathway inhibitors, phenicols, penicillins, monobactams and nitrofurans. Further, S. Indiana isolates that are concurrently resistant to ciprofloxacin and ceftriaxone/cefotaxime have emerged. Studies have suggested the high levels of multidrug resistance of S. Indiana might be associated with the presence of class 1 integrons and plasmids. Unfortunately, information on the high prevalence of S. Indiana and its extensive drug resistance in China has largely escaped international recognition as it largely appears in local reports written in Chinese. To address this situation, we reviewed all the available local Chinese and international publications on the organism in China and report our findings in this review.