Highly Drug-Resistant Salmonella enterica Serovar Indiana Clinical Isolates Recovered from Broilers and Poultry Workers with Diarrhea in China

Gong, Jicheng; Wang, Chengming; Shi, Shourong; Bao, Hongduo; Zhu, Chunhong; Kelly, Patrick J.; Zhuang, Liying; Lu, Guangyu; Dou, Xiaowei; Wang, Ran; Xu, Bo; Zou, Jianmin

doi:10.1128/aac.03009-15

Cited by 52 publications

(56 citation statements)

References 21 publications

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“…In addition, there are reports of non-typhoidal serovars causing salmonellosis in chickens (Ogunleye and Carlson 2012; Gong et al., 2016). Therefore, identifying mitigation strategies is of paramount importance to the poultry industry.…”

Section: Discussionmentioning

confidence: 99%

Inhibition of the virulence, antibiotic resistance, and fecal shedding of multiple antibiotic-resistant Salmonella Typhimurium in broilers fed Original XPC™

et al. 2016

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Salmonella carriage is an insidious problem for the poultry industry. While most Salmonella serotypes are avirulent in poultry, these bacteria can contaminate chicken meat during processing, leading to one of the most important food safety hazards. In this study, we examined the anti-Salmonella effects of Diamond V Original XPC™ (XPC) included in the finisher diet fed to commercial broilers. On 3 occasions between day one (D1) and D20, broilers were experimentally infected with multiple antibiotic-resistant Salmonella Typhimurium. After confirming that the chicks were shedding Salmonella in the feces on D21, broiler chicks were fed a diet containing XPC (n = 57 birds; 1.25 kg/MT) or an XPC-free control diet (CON) (n = 57 birds) to D49. Fecal samples were obtained weekly and subjected to selective culture for enumerating and determining the antibiotic resistance of the Salmonella. Salmonella isolates were then subjected to an in vitro virulence assay, which predicts the ability of Salmonella to cause illness in a mammalian host. Broilers were euthanized on D49 and a segment of the large intestine was removed and subjected to the same assays used for the fecal samples. When compared to the birds fed the CON diet, Salmonella fecal shedding, virulence (invasion and invasion gene expression), and antibiotic resistance were significantly decreased in birds fed XPC (5-fold, 7.5-fold, 6-fold, and 5.3-fold decreases, respectively). Birds fed XPC exhibited heavier body weight (BW) and greater BW gains than those fed the CON diet. The decrease in virulence was associated with a decreased expression of a genetic regulator of Salmonella invasion into cells (hilA), while the decrease in antibiotic resistance was due to a loss of an integron (SGI1) from the input strain. This study revealed that Original XPC™ inhibits the shedding, downstream virulence, and antibiotic resistance of Salmonella residing in broilers.

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Section: Discussionmentioning

confidence: 99%

Inhibition of the virulence, antibiotic resistance, and fecal shedding of multiple antibiotic-resistant Salmonella Typhimurium in broilers fed Original XPC™

et al. 2016

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“…In reports on sick or dead animals including ducks (Xu et al., ), geese (Yu et al., ), pigs (Jiang et al., ) and chickens (Gong et al., ; Zhang et al., ), S . Indiana was always the most common, or second most common serovar isolated, with S .…”

Section: Overview Of S Indiana In Chinamentioning

confidence: 99%

“…It is noteworthy that S . Indiana was found to have replaced the traditional dominant Salmonella serotypes isolated from broilers with diarrhoea in a large‐scale study covering the major broiler breeding areas in China (Gong et al., ).…”

Section: Overview Of S Indiana In Chinamentioning

confidence: 99%

“…Further, numerous S . Indiana isolates from multiple sources have been shown to be highly drug resistant with concurrent resistance to ciprofloxacin and ceftriaxone/cefotaxime (Jiang et al., ; Bai et al., , ; Gong et al., ). With the difficulties associated with treating multi‐drug‐resistant strains of Salmonella , there has thus been increasing concern about S .…”

Section: Introductionmentioning

confidence: 99%

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

Gong

Kelly

Wang

2016

Zoonoses and Public Health

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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.

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“…Indiana, and S . Typhimurium are the most common Salmonella serovars in Chinese food‐producing animals and meat products (Gong et al, ; Wang et al, ; Yang et al, ; Zhang et al, ). Salmonella serovars, Enteritidis, Indiana, and Typhimurium, not only result in serious economic losses in livestock husbandry but also cause serious public health problems through contaminated meat products (Antunes, Mourão, Campos, & Peixe, ; Gong, Kelly, & Wang, ).…”

Section: Introductionmentioning

confidence: 99%

Multiplex polymerase chain reaction to detect Salmonella serovars Indiana, Enteritidis, and Typhimurium in raw meat

Zhang

Zhuang

et al. 2019

Journal of Food Safety

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Salmonella‐contaminated raw food is an important source of human food poisoning. Traditional methods for detecting Salmonella in meat involve many time‐consuming and laborious steps, preventing timely and effective control of the pathogen. In this study, a multiplex polymerase chain reaction (PCR) assay that targets serovar‐specific genes such as A7P63_0910 (Salmonella Indiana), sdfI (Salmonella Enteritidis), and STM4497 (Salmonella Typhimurium) for three meat‐associated Salmonella serovars was established. This multiplex PCR has been validated by extensive testing on reference strains and clinical isolates belonging to different Salmonella serovars (n = 348) and non‐Salmonella bacteria (n = 12). The detection limit is 100 CFU per reaction for bacterial culture, being equivalent to 10 pg per reaction for bacterial genomic DNA. Detection of Salmonella in raw meat samples by this multiplex PCR revealed that the prevalence of S. Indiana, S. Enteritidis, and S. Typhimurium is 7.7%, 5.7%, and 2.0%, respectively. The multiplex PCR established in this study can be used as a novel and convenient tool for simultaneous detection of three major meat‐associated Salmonella serovars, including the newly emerging and highly drug‐resistant S. Indiana. Practical applications In this study, a multiplex polymerase chain reaction (PCR) assay that targets serovar‐specific genes such as A7P63_0910 (Salmonella Indiana), sdfI (Salmonella Enteritidis), and STM4497 (Salmonella Typhimurium) for three meat‐associated Salmonella serovars was established. This multiplex PCR is suitable for the simultaneous detection and differentiation of three major meat‐associated Salmonella serovars, and has been validated by extensive testing of reference strains and clinical isolates. The multiplex PCR assay can provide rapid and specific screening for top three Salmonella serovars in meat samples.

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Highly Drug-Resistant Salmonella enterica Serovar Indiana Clinical Isolates Recovered from Broilers and Poultry Workers with Diarrhea in China

Cited by 52 publications

References 21 publications

Inhibition of the virulence, antibiotic resistance, and fecal shedding of multiple antibiotic-resistant Salmonella Typhimurium in broilers fed Original XPC™

Inhibition of the virulence, antibiotic resistance, and fecal shedding of multiple antibiotic-resistant Salmonella Typhimurium in broilers fed Original XPC™

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

Multiplex polymerase chain reaction to detect Salmonella serovars Indiana, Enteritidis, and Typhimurium in raw meat

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