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