3.4 What is the prevalence of NTS in samples of poultry from the
Americas?
As summarized in Table 2 , the prevalence of NTS varied both
according to the type of the sample assessed and the country. The pooled
overall prevalence of NTS was 17.9% (95% CI: 10.8 to 26.3) in 43
studies that reported 24,113 samples of birds from 11 countries with a
significant test of effect size (Z=7.5, p =0.00) and substantial
heterogeneity as judged by the I 2 (99.5%,p =0.00). For these samples, the subgroup analysis revealed a
lower prevalence of 9.8% of NTS in individual data (3.8 to 18.2, n=25)
in comparison to the value of 33.8% (16.6 to 53.3, n=18) estimated in
flock data (Supplementary Figure 1 ). At the national level, the
prevalence of NTS ranged from 23.2 to 50% in samples of birds reported
in studies from Mexico, the USA, Uruguay, and Venezuela. In contrast,
the prevalence of NTS was lower in studies from Brazil, Chile, Paraguay,
and Trinidad and Tobago where the estimations varied between 0.8 and
3.7% (Table 2 ).
In 90 studies that reported 173,354 samples of products and subproducts
from 10 countries, the overall pooled prevalence of NTS was 21.8% (17.7
to 26.1) with a significant test of effect size (Z=16.8, p =0.00)
and a significant variation attributable to heterogeneity
(I 2=99.6%, p =0.00). According to
subgroup analysis, the prevalence estimations were consistent between
the individual (21.2%, 17.7 to 26.1, n=78) and collective data (28.1%,
12.6 to 46.4, n=12) of these samples (Supplementary Figure 2 ).
The studies from Canada showed the highest pooled prevalence of NTS in
samples from products and subproducts, while prevalence values ranging
from 31.2 to 34.4% were estimated in studies from Guatemala, Mexico,
and Puerto Rico. Finally, Argentina, Brazil, Costa Rica, and Trinidad
and Tobago had prevalence values below-average (Table 2 ).
Regarding the environmental samples, the pooled prevalence of NTS was
29.5% (24.2 to 35.1) in 61 studies that comprised 63,941 samples from
eight countries. There was a significant test of effect size (Z=17.1,p =0.00) and substantial heterogeneity across studies
(I 2=94.4%, p =0.00), and the subgroup
analysis showed a contrasting difference of 21.9 and 52.4% at the
individual (17.6 to 26.6, n=43) and collective (41.7 to 62.9, n=18)
level, respectively (Supplementary Figure 3 ). At the national
level, the studies from Canada and the USA had prevalence values above
the overall estimation, whereas with estimations varying 3.3 to 9.0%,
the studies from Argentina and Costa Rica showed the lowest prevalence
of NTS in environmental samples (Table 2 ).
Which are the main serovars of NTS identified in each type of
sample?
In total, 131 NTS serovars were identified from 13,388 isolates from
poultry samples reported in 94 publications from 13 countries
(Fig. 3 ). The USA and Canada contributed both with the highest
percentage of isolates (84.0%) and the greatest diversity of NTS
serovars (68 and 57, respectively). Likewise, Brazil and Colombia
provided a great diversity of serovars (53 and 40, respectively),
whereas the remaining countries reported a lower diversity of NTS
serovars (range 1-19). A detailed list of the distribution of the 131
NTS serovars per country is provided in Supplementary Table 5 .
Overall, 84.3% of the isolates were distributed among 10 NTS serovars,
Heidelberg, Kentucky, and Enteritidis were the most prevalent (20.8,
20.6, and 17.6%, respectively), whereas Mbandaka, Schwarzengrund, and
Montevideo were less prevalent with values ranging from 2.2 to 2.4%.
Outside the top 10 serovars, the category “Others” comprised the
remaining 121 serovars that were found in 2,103 isolates. As shown inFigure 3 , there was a heterogenous pattern in the top 10
ranking of the NTS serovars across countries, which additionally had
several serovars not included in the overall top 10 ranking.
Additionally, in Costa Rica, Ecuador, Mexico, and Trinidad and Tobago
their 1st top serovar was not included in the overall
top 10 ranking list. Even though the serovars Heidelberg and Kentucky
were ranked as 1st and 2nd overall,
these serovars were reported only in 5 and 6 countries, respectively,
where their ranks varied across countries. In contrast, serovars
Enteritidis and Typhimurium (3rd and
4th overall) were identified in most of the countries
(10 and 8 respectively); thus, these two serovars had the broadest
distribution in poultry samples across countries from the Americas.
Furthermore, Enteritidis was the 1st top-ranked
serovar in the USA, Brazil, Colombia, Paraguay, and Uruguay where its
prevalence ranged from 23.4 to 100% and the 2ndtop-ranked serovar in Argentina, Chile, and Ecuador. Similarly,
Typhimurium was the 1st top-ranked serovar in Chile
and the 3rd ranked in Colombia. Despite the serovars
Hadar, Thompson, and Montevideo were ranked in the top 10 overall, they
were reported only in two countries each and thus showed a narrow
geographical distribution.
We constructed Sankey diagrams to examine and compare the distribution
of the top five NTS serovars according to the type of poultry sample
(Fig. 4 ). Laying hens, broilers, and a mixture category that
grouped chicks and hens were the main sources of NTS isolates in animal
samples, whereas carcasses, eggs, and subproducts for consumption (such
as meat and processed products) provided most of the isolates for the
products and subproducts group. Finally, among environmental samples,
most of the isolates were obtained from production wastes (such as
litter and feces), breeding facilities, and production supplies (such as
water, feed, and litter). Serovars Enteritidis and Heidelberg were
identified in all the poultry samples, whereas the samples from products
and subproducts and environmental shared 4 out of 5 serovars
(Enteritidis, Kentucky, Heidelberg, and Typhimurium). Among the samples
from birds and products and subproducts, Enteritidis was the most
prevalent serovar with 32.4 and 22.8%, respectively, followed by
Senftenberg and Kentucky (10.6% for birds and 21.5% for products and
subproducts). Heidelberg and Kentucky were the most prevalent serovars
in environmental samples (32.1 and 28.8%, respectively).
What is the prevalence and the profile of antimicrobial
resistance in NTS isolates of poultry?
Of the 46 publications that assessed the AMR of the NTS isolates, 38/46
reported the prevalence in 3,078 isolates of which 2,223 were resistant
to at least one antibiotic. As depicted in Figure 5a , the
prevalence of AMR tended to be higher according to the increase in the
number of antibiotics to which the NTS isolates were resistant: 1
antibiotic, 24.1% (14.7 to 34.9%, n=440); 2-3 antibiotics, 36.2%
(24.5 to 48.6%, n=758); and ≥ 4 antibiotics, 49.6% (36.9 to 62.2%,
n=1,025). Besides, there was a heterogenous pattern of prevalence to AMR
among the three types of samples because in samples from birds and
products and subproducts, resistance to ≥ 4 antibiotics was highly
prevalent (61.2 and 48.7%), whereas resistance to 2-3 antibiotics was
highly prevalent in environmental samples (47.1%)
(Supplementary Figure 4 ).
A total of 26/46 publications reported 50 serovars from 1,688 NTS
isolates that were resistant to at least one antibiotic. As shown inFigure 5b , 10 serovars contributed with 79.2% of the total,
among which Kentucky (29.5%), Heidelberg (16.7%), Typhimurium (9.8%),
and Enteritidis (7.1%) were the top four serovars most frequently
reported as resistant to at least one antibiotic. Outside the top 10
ranking, the category “Others” comprised 40 serovars from 331 NTS
isolates of which Typhimurium var. 5-, 4,5, 12:1:, Pullorum, Anatum,
Lithfield, Montevideo, Hadar, Ohio, Newport, and Senftenberg were
reported in 10 to 33 isolates each. In contrast, serovars such as
Havana, Idikan, Ouakam, Bredeney, Alachua, Corvallis, Istambul,
Livingstone, Worthington, and I 4,5, 12: - were reported only once
across the publications.
In total, 40/46 publications reported 15 groups of antibiotics that
included 57 antibiotics to which 8,911 NTS isolates were resistant. Each
group included between 1 and 11 antibiotics that varied in the frequency
of report (Supplementary Table 6 ). In Figure 5c are
depicted the main six groups of drugs and their corresponding
antibiotics to which 90.6% of the isolates were resistant.
Cephalosporins, penicillins, tetracyclines, and aminoglycosides were the
top four groups, which concentrated 71.9% of the resistant isolates of
NTS. As shown in Figure 5d , with a prevalence that ranged from
5.8 to 16.2%, tetracycline, ampicillin, streptomycin, ceftiofur, and
amoxicillin-clavulanic acid were among the top 10 antibiotics with the
highest overall prevalence of resistance in Salmonella isolates.
In the bottom rank, gentamicin and trimethoprim-sulfamethoxazole were
the antibiotics with the lowest prevalence of resistance in NTS.
Regarding the three poultry samples, the profile of antimicrobial
resistant was heterogenous. Except for tetracycline, which was the
1st top-ranked antibiotic among resistant isolates,
the remaining antibiotics varied in their position within the rank. For
instance, streptomycin that was the second most prevalent in birds,
ranked 4th and 5th in environmental
samples and products and subproducts. Likewise, ampicillin ranked
5th in environmental samples, whereas in the two other
samples this antibiotic was among the top three, nalidixic acid that was
the third to last most prevalent overall, in environmental samples was
ranked 3rd. Besides, in the three samples of poultry
there were 1-2 antibiotics that were not included in the overall top 10
ranking.