1. Introduction
According to the latest scientific report of the European Food Safety Authority (EFSA) and the European Centre for Disease Prevention and Control (ECDC) on the trends and sources of zoonoses and foodborne outbreaks in the European Union (EU), campylobacteriosis is the most commonly reported foodborne gastrointestinal infection in humans in the EU and has been so since 2007 [
1]. Estimates of the overall human health impact of bacterial agents transmitted commonly through food, place
Campylobacter as the first or second most common agent after nontyphoidal
Salmonella in Europe, North America, Australia, and Japan [
2,
3,
4]. The notable absence of notified
Campylobacter outbreaks in China and some other populous countries, like India, could be attributed to the lack of mandatory surveillance by the established foodborne disease surveillance system or to the underreporting (e.g., mild symptoms and a smaller number of cases seeking health care) and/or underdiagnosis (e.g., lack of testing and diagnostic accuracy) of the disease, the lack of epidemiological surveillance data connecting causative agents of outbreaks, and the different dietary habits on those countries [
5,
6,
7].
Major food categories of interest for
Campylobacter occurrence include mostly meat and meat products (i.e., animal carcasses and fresh/ready-to-eat (RTE), cooked and fermented products), as well as milk and milk products (i.e., raw and pasteurized milk and dairy products including cheese) [
1], although the prevalence of the disease-causing
Campylobacter spp. is significantly increased in poultry meat samples compared to other types of meat or compared with milk and dairy products [
8,
9,
10,
11]. The strong-evidence foodborne association of campylobacteriosis outbreaks with the consumption of raw or incompletely thermally processed poultry meat is already well known and has been emphatically documented nowadays [
8,
10,
12], while the foodborne illness due to the presence of
Campylobacter spp. in poultry has been classified as the costliest pathogen-meat combination from an economic perspective [
13]. Regardless the fact today poultry is considered the main reservoir for
Campylobacter spp. (source of infection), latest epidemiological evidence suggests pathogen transmission to humans through a pathway implicating cattle as the primary reservoir of
Campylobacter (source of contamination), infecting people via the fecal-oral route and the consumption of contaminated chickens [
14].
World poultry meat consumption refers to the consumption of meat from chickens (broilers), turkey, and other avian species (e.g., ducks, geese). Available data compiled from the Food and Agriculture Organization (FAO) of the United Nations (UN) reveal an increase in worldwide annual poultry meat consumption per capita by more than 5.0 kg in the past 20 years; from 10.8 kg in 2000 to 16.2 kg in 2020 [
15]. Chickens are by far the main protein source of animal origin for humans in terms of livestock animals reared and slaughtered for their meat [
15], so the previous rates represent roughly the chicken meat being consumed on a global basis.
The different thermotolerant campylobacters validly described to date are summarized in
Supplementary Table S1. Of these,
Campylobacter jejuni and
C. coli are the two most important species mainly detected in foods of animal origin [
55], [
56] (p. 1670). These two species account for almost 90% of the reported human campylobacteriosis cases, with over 80% of the occurring gastrointestinal infections being attributable to
C. jejuni and the rest about 10% of infections attributed to
C. coli [
56] (pp. 1669–1670), [
57]. Therefore, until recently it was well established and beyond any reasonable question that
C. jejuni is the dominant species among all other
Campylobacter spp. isolated from chicken meat samples. Lately, however,
C. coli has been increasingly recovered from chicken samples to such an extent that it is now obvious it many times comprises the dominant species among the identified campylobacters in the meat samples [
58,
59,
60,
61,
62]. To this end, in studies pertaining to the metropolitan area of Athens, Greece, and its suburbs in the Attica region, Andritsos et al. [
63] reported isolation rates of 6% and 27% for
C. jejuni and
C. coli, respectively, during
Campylobacter spp. detection in chicken meat samples, whereas the strict majority (87.5%) of the recovered campylobacters (16) from 830 fecal samples collected from five poultry farms by Marinou et al. [
64] were identified as
C. coli, without any of the strains being identified as
C. jejuni whatsoever. Taking into account that in the latter case of
Campylobacter presence in broilers’ litter, the positive predictive value in terms of microorganism’s occurrence in carcass skin samples is much greater, unless the pathogen cannot be detected in the intestinal content of the bird [
65],
C. coli dominance in the chicken flocks should be taken for granted.
Considering all the above, the present work attempts for the first time, to the best of the authors’ knowledge, a detailed review in the literature in order to elucidate the underlying epidemiological transition from
C. jejuni to
C. coli in chicken meat, along with the distribution of campylobacters in poultry.
Figure 1 outlines the factors affecting the occurrence of
Campylobacter spp. in poultry meat samples, while those factors are thoroughly being discussed below.
5. Biofilm-forming ability of Campylobacter spp.
The survival of campylobacter in the food chain remains a paradox since the bacterium is a fastidious organism with characteristic special growth requirements for successful subculturing in the laboratory (e.g., heat-resistant, microaerophilic organism requiring the presence of blood in its culture medium). Recently, biofilm formation has been proposed as the main mechanism of maintenance and transmission for the pathogen from animals to humans [
156]. In general, the biofilm-forming ability of
Campylobacter is strain-dependent and varies among organism’s isolated strains [
157,
158], as well as between different
Campylobacter spp. [
159,
160,
161], while it is also affected by the presence of other bacterial species [
162,
163,
164,
165,
166,
167]. Regarding the biofilm-forming ability of
C. jejuni and
C. coli, the latter isolates seem able to form biofilms significantly better compared to
C. jejuni isolates (
p < 0.05) [
157,
160] and that could be another reason for the increased prevalence of
C. coli against
C. jejuni in the chicken meat samples.
The ability of
C. jejuni to form a biofilm is highly dependent on the strain and the type of abiotic surface on which it is found [
159]. Teh et al. [
165] concluded that
C. jejuni exhibits a much weaker biofilm-forming ability compared to other bacteria, such as
Pseudomonas spp.,
Staphylococcus aureus,
Salmonella spp., and
E. coli. However, in controlled mixed-microbial populations of a specific
C. jejuni strain (sequence type; ST-474) with
Enterococcus faecalis and/or
Staphylococcus sp., optical intense biofilms for the two species were developed when they were grown with
C. jejuni, while
C. jejuni cells were recovered from most of the biofilms containing
E. faecalis and/or
Staphylococcus sp. [
165]. That was the case and in the studies of Ica et al. [
166] and Sterniša et al. [
167], where the co-cultivation of
C. jejuni with
P.aeruginosa and
P. fragi, respectively, resulted in the increased determined number of culturable biofilm
C. jejuni cells. In contrast to monoculture biofilms, the mixed-culture biofilms of
C. jejuni with pseudomonads had significantly enhanced mechanical strength [
166]. Enhanced biofilm formation was also observed for
C. jejuni and
C. coli in the presence of
S. aureus, with increased aerotolerance and survivability in parallel for the
Campylobacter strains [
162].
Author Contributions
Conceptualization, N.D.A.; methodology, N.D.A. and M.M.; X.X.; validation, N.D.A., N.T. and M.M.; formal analysis, N.D.A. and M.M.; investigation, N.D.A. and N.T.; resources, N.D.A. and M.M.; data curation, N.D.A. and M.M.; writing—original draft preparation, N.D.A.; writing—review and editing, N.D.A., N.T. and M.M.; visualization, N.D.A.; supervision, N.T.; project administration, N.D.A. All authors have read and agreed to the published version of the manuscript.