Abstract

Poultry and poultry-derived products such as meat and eggs are among the main sources of non-typhoidal Salmonella (NTS) transmission to the human. Therefore, we performed a systematic review and used random-effects meta-analyses to 1) estimate the prevalence of NTS in poultry samples from birds, products and subproducts, and environmental samples, 2) examine the diversity and frequency of their serovars, and 3) estimate the prevalence and profiles of antimicrobial resistance (AMR) in NTS isolates reported in studies from the Americas. We included 157 studies from 15 countries comprising 261,408 poultry samples and estimated an overall pooled prevalence of 17.9% (95% CI: 10.8–26.3) in birds, 21.8% (17.7–26.1) in products and subproducts, and 29.5% (24.2–35.1) in environmental samples. At the national level, the prevalence of NTS was heterogenous across countries with the highest values in Mexico, the USA, and Canada. In total, 131 serovars were identified from 13,388 isolates, Heidelberg, Kentucky, Enteritidis, and Typhimurium were the most prevalent in the overall top 10 ranking (range 6.5–20.8%). At the national level, Enteritidis and Typhimurium were identified in most of the countries, though with national differences in their ranks. The prevalence of AMR increased from 24.1% for 1 antibiotic, to 36.2% for 2-3 antibiotics, and 49.6% for ≥ 4 antibiotics. Kentucky, Heidelberg, Typhimurium, and Enteritidis were the serovars with the highest prevalence of AMR and tetracycline, ampicillin, streptomycin, ceftiofur, and amoxicillin-clavulanic acid were the top five antibiotics to which NTS isolates were resistant. In conclusion, NTS was distributed through the avian production chain with high and heterogenous values of prevalence in poultry samples. Besides, there were distinctive patterns of serovars distribution across countries and an alarming prevalence of AMR among zoonotic serovars.
Keywords: Infectious diseases, Foodborne disease, Food safety, Multi-drug resistance, Salmonellosis, Zoonosis.
1. INTRODUCTION
Salmonella are Gram negative rod-shaped bacilli that belongs to the family Enterobactericeae . The Salmonella genus includes only two species, one of which is Salmonellaenterica that is divided into six subspecies that includesS. enterica subsp. enterica (Popoff, Bockemühl, & Gheesling, 2004). According to the Kauffmann-White scheme,Salmonella strains are serologically classified into more than 2,610 serovars based on their specific antigenic reaction (Guibourdenche et al., 2010). S. enterica subsp. enterica is of medical interest because causes an infectious disease that can be classified into: enteric fever (typhoidal) that affects only humans and non-typhoidal Salmonella (NTS) that affects both humans and animals (Barrow & Methner, 2013). Indeed, NTS is considered among the main pathogen bacteria that cause foodborne disease (FBD), which causes a significant public health, economic and social burden worldwide, particularly in low- and middle-income countries (World Health Organization, 2021).
Non-typhoidal salmonellosis is commonly manifested as mild to moderate gastroenteritis characterized by vomiting, nausea, diarrhea, and abdominal pain (Foley & Lynne, 2008). Usually, these symptoms developed 6-72 h after ingestion of the bacteria (Centers for Disease Control and Prevention, 2004) and are resolved within 2-7 days because they are self-limiting and thus do not require treatment. However, NTS can develop into a more severe illness that invade normally sterile sites that results in bacteremia, meningitis, and other focal infections, which are denominated invasive NTS (Crump, Sjölund-Karlsson, Gordon, & Parry, 2015). Only in 2017, there were 535,000 cases of invasive NTS worldwide that caused 77,500 deaths worldwide that affected mostly children under five years of age, elderly people, and people with HIV infection (Stanaway et al., 2019).
In the human, NTS is acquired mainly through contaminated food of animal origin such as poultry products and poultry-derived products, which are recognized as common sources of transmission (Gonçalves-Tenório, Silva, Rodrigues, Cadavez, & Gonzales-Barron, 2018). In poultry, this pathogen bacteria can be found in the carcasses, raw meat, and eggs (eggshell, salk, and yolk) (Foley, Lynne, & Nayak, 2008), as well as in live birds from poultry farms (El-Sharkawy et al., 2017), and in the environment related to poultry production and slaughter (Manoj & Singh, 2015). Thus, NTS is widely distributed in the poultry production chain and serves as an important reservoir for the dissemination of the pathogen to the humans (Howard, O’Bryan, Crandall, & Ricke, 2012).
From the perspective of public health, the subspecies entericaconcentrates the most important zoonotic serovars of NTS that include Typhimurium and Enteritidis, which are frequently reported as a cause of FBD associated to the consumption of poultry products (Park et al., 2014). Previous studies have reported contrasting patterns of serovars predominance across the regions of the world: in poultry from Asia, Latin America, Europe, and Africa, Enteritis was predominant, and Kentucky and Sofia were most prevalent in North America and Oceania (Ferrari et al., 2019), whereas in poultry samples from Europe, Enteritidis, Infantis, and Typhimurium were the most frequent serovars (Antonelli, Belluco, Mancin, Losasso, & Ricci, 2019). Nevertheless, the pattern of predominance and distribution of the serovars might be prone to change due to the increase in the international trading of poultry and poultry-derived products (Manoj & Singh, 2015) in conjunction with the implementation of control measures that have induced the expansion of previously less common serovars (Antunes, Mourão, Campos, & Peixe, 2016). Besides, the emergence and spread of NTS serovars with antimicrobial resistance (AMR) is a major public health concern given that the abusive use of antibiotics in intensive livestock systems increase the rate of appearance of AMR (Antunes et al., 2016) and because antibiotics are crucial for successful treatment of invasive infections.
In consequence, it is necessary to implement effective intervention strategies focused on reducing and controlling the dissemination of NTS from poultry to humans. Besides, estimating the burden of the most important FBD, such as NTS that cause a great impact on public health, is an essential component in the effort to reduce its negative effect (World Health Organization, 2021). In this context, identifying and estimating the magnitude of Salmonella serovars with AMR in poultry and their products capable of causing FBD in humans might provide an initial step in the identification of sources of exposure for the dissemination of NTS because these products are recognized as the main source of foodborne salmonellosis (Antunes et al., 2016) . This is particularly important in regions of the world with a high level of poultry production and consumption, such is the case of the Americas that concentrates 42.3% of the poultry meat production at the global level (FAO, 2019). Therefore, we conducted a systematic review and meta-analysis to 1) estimate the prevalence of NTS in poultry samples from birds, products and subproducts, and environmental samples, 2) determine the diversity and frequency of their serovars, and 3) estimate the prevalence and profiles of AMR in NTS isolates reported in studies from the Americas.
2. METHODS