Heliyon 10 (2024) e26356

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Heliyon
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Research article

Prevalence and risk factors of Campylobacter jejuni and

Campylobacter coli in fresh chicken carcasses from retail sites in
Bogotá, Colombia
Brigithe Tatiana Ortiz a, *, Deyci Rodríguez b, Silvia Restrepo a
a
Laboratory of Mycology and Phytopathology (LAMFU), Department of Chemical and Food Engineering, Universidad de los Andes, Bogotá D.C.,
Colombia
b
Laboratory of Food Microbiology, Faculty of Sciences, Pontificia Universidad Javeriana, Bogotá D.C., Colombia

A R T I C L E I N F O A B S T R A C T

Keywords: Campylobacter is one of the most common causes of foodborne gastroenteritis. The objective of
Campylobacter jejuni this study was to estimate the prevalence and risk factors associated with Campylobacter jejuni and
Campylobacter coli Campylobacter coli species in fresh chicken carcasses for human consumption from farmers’
Colombia
markets and small food stores in seven localities of Bogotá, Colombia. Ninety-one samples of fresh
Risk factors
chicken carcasses were collected from farmers’ markets and small food stores at seven localities in
Chicken carcass
Bogotá. Samples were tested for Campylobacter using the real-time polymerase chain reaction
(real time PCR) and isolation by plating. To analyze possible risk factors associated with
Campylobacter spp. contamination in retail chicken carcasses, information was collected using a
structured questionnaire and a univariate logistic regression analysis (α = 0.05) was used. Forty-
two positive samples were obtained for Campylobacter spp., given a prevalence of 46.2%, of which
54.8% were to C. jejuni, 9.52% to C. coli and 35.7% to joint contaminations. C. jejuni was the most
prevalent species. Risk factors found included poor cleanliness, in frequency of disinfection, type
of establishment, and direct contact of chickens with other food. This study is the first report in
the country on the prevalence and risk factors of Campylobacter in retail chicken.

1. Introduction

Foodborne diseases are a significant public health problem worldwide. One of the most important foodborne diseases is
Campylobacter spp. a bacterial genus considered by the World Health Organization to be on the top four leading global causes of acute
diarrheal disease (ADE) and the most frequent gastroenteritis-causing bacterium in the world [1]. Campylobacter causes campylo­
bacteriosis in humans and animals and is recognized as a zoonosis of worldwide distribution [2]. Campylobacter jejuni and Campylo­
bacter coli are the species commonly implicated in human cases, and most infections present as mild or asymptomatic gastroenteritis
[1]. However, the infection may lead to severe complications, such as reactive arthritis, Miller-Fisher syndrome (MFS) and Guillain
Barré syndrome (GBS) [3]. Campylobacter is a Gram-negative bacterium that does not form spores, has a curved or spiral morphology,
usually has a slow growth (up to 96 h), and presents a rapid and characteristic dart-like or corkscrew-like movement, as its members

* Corresponding author.
E-mail addresses: bt.ortiz@uniandes.edu.co (B.T. Ortiz), deyci.rodriguez@javeriana.edu.co (D. Rodríguez), srestrep@uniandes.edu.co
(S. Restrepo).

https://doi.org/10.1016/j.heliyon.2024.e26356
Received 26 August 2023; Received in revised form 8 December 2023; Accepted 12 February 2024
Available online 17 February 2024
2405-8440/© 2024 The Authors. Published by Elsevier Ltd. This is an open access article under the CC BY license
(http://creativecommons.org/licenses/by/4.0/).
B.T. Ortiz et al. Heliyon 10 (2024) e26356

possess a polar flagellum at one or both ends of the cell. This microorganism is sensitive to oxygen and free radicals, so they are
considered microaerophiles [4,5]. Most Campylobacter species are thermotolerant, growing between 37 and 42 ◦ C, with an optimum
temperature of 41.5 ◦ C– 42 ◦ C. However, They have shown that they can resist low temperatures <4 ◦ C [6]. In addition, under
environmental stress, Campylobacter can enter a viable but non-culturable cell state (VBNC), a state in which the bacterium stop
growing on commonly used culture media but remains viable with minimal metabolic activity [7,8].
The prevalence of Campylobacter worldwide is variable but is usually higher in products whose sources are broiler chicken [9,10].
Poultry is the main reservoir of Campylobacter spp. since their intestines provide a favorable environment as a supply of nutrients that
support their growth and colonization [11,12]. Once a bird is infected, Campylobacter can be transmitted horizontally to most of the
other birds in the flock in just a few days, reaching between 10 and 108 CFU/g in the intestinal tract, and remaining colonizing the
animal until slaughter [13]. Based on the above, it is considered that one of the main routes of transmission of Campylobacter spp. to
humans is the consumption of contaminated poultry products, especially by the C. jejuni species, which is usually the predominant
colonizer, followed by C. coli [13,14]. However, these species can also be transmitted through other contaminated foods, such as
unpasteurized milk and untreated water [14,15].
Contamination of chicken carcasses can lead to the survival of Campylobacter in raw poultry products during their shelf life and
generate a risk of possible infection in humans who consume these contaminated products [15]. Likewise, other risk factors such as
cross-contamination phenomena through contact with contaminated handlers, surfaces, utensils and food, infected pets, and farm
animals, especially in developing countries, are a high risk of transmission to humans [16].
Studies on the percentage prevalence of this pathogen in chicken have been conducted in different parts of the world and variability
has been found. For example, in China, 29 chicken carcass samples were analyzed, and a prevalence of 79.5% was detected [17]. In
Croatia, 241 fresh chicken samples were analyzed, and 73.9% prevalence for Campylobacter spp. was found [18]. However, in countries
in the Americas such as Mexico, Argentina and Colombia, there are not many studies and prevalence information available. In a study
conducted in Mexico, a prevalence of 89% was found in the analysis of 76 fresh chicken samples [19] and another study in Peru showed
a prevalence of 97.5% in the analysis of 120 fresh chicken samples [20].
There exist a European Union Regulation 2017/1495 published in 2017, which incorporates methods for testing of poultry car­
casses for Campylobacter and establishes a process hygiene criterion for Campylobacter in broiler carcasses [21]. Likewise, regulations
on campylobacteriosis place it under surveillance in several countries, including in North America, Europe and Asia. For example,
human campylobacteriosis is a notifiable disease in Europe [22]. It has been nationally notifiable in Canada since 1986 and in the
United States since 2015, it became notifiable at the national level [22,23]. However, in some developing countries, such as Brazil,
Mexico, Thailand and the Central African Republic, the lack of routine regulation and diagnosis, there is a problem in analyzing and
understanding the importance of campylobacteriosis [24,25]. Some reviews on the global epidemiology of Campylobacter spp. show
that usually in developing countries, there is no routine diagnosis of this pathogen and no adequate epidemiological surveillance [26].
The poultry industry in Colombia is one of the most dynamic fields in the agricultural sector, especially in broiler production.
Colombia ranks 11th in the world in chicken production and 5th in the Americas after the United States, Brazil, Mexico, and Argentina
[27]. In terms of per capita consumption, Colombia ranks 14th in the world, with a significant increase over the last 22 years from 14 to
36.3 kg/inhabitant [28]. Among the few studies conducted in Colombia, one developed by the National Institute of Health, known in
Colombia as Instituto Nacional de Salud (INS) in 2012, found a prevalence of 10.9% for Campylobacter in 19 chicken carcass processing

Fig. 1. Geographical distribution of the sampled localities of Bogotá: Antonio Nariño, Barrios Unidos, Kennedy, Los Mártires, San Cristóbal, Santa
Fe and Usaquén.

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plants [29]. Another study conducted in 2016 found a prevalence of 10% [30]. In addition, the Colombian Integrated Surveillance
Program for Antimicrobial Resistance (COIPARS) has identified Salmonella spp. and Campylobacter spp. as two of the most important
foodborne pathogens for public health in the country [31–33]. Despite this, above, there are no studies on Campylobacter spp. in
chicken carcasses in retail markets and possible risk factors associated with contamination by this pathogen. This may be due to
difficulties in its detection in the absence of epidemiological surveillance and mandatory reporting of Campylobacter spp. in com­
mercial establishments [29,31,34]. Therefore, the objective of this study was to estimate the prevalence and risk factors associated
with Campylobacter jejuni and Campylobacter coli species in fresh chicken carcasses for human consumption from farmers’ markets and
small food stores in seven localities of Bogotá, Colombia.

2. Methods

2.1. Sample collection

Ninety-one samples of fresh chicken carcasses were collected from farmers’ markets and retail small food stores located in seven
localities of the city of Bogotá through convenience sampling (Fig. 1). The following localities were selected: Antonio Nariño (South),
Barrios Unidos (North), Kennedy (Southwest), Los Mártires (East), San Cristóbal (Southeast), Santa Fe (Downtown) and Usaquén
(North). For each location, 13 chicken carcass samples (approximately eight from farmers’ markets and five from small food stores)
were collected between June and November 2021. The chicken carcasses were purchased, therefore, no approval from the Committee
on Investigation and Use of Laboratory Animals (CICUAL) was required. At each point of purchase, the internal temperature of the
samples was measured with a digital punch thermometer to determine the storage conditions for sale. Each sample was kept in plastic
bags, labeled and transported under refrigerated conditions to the Food Microbiology laboratory of the Pontificia Universidad Jav­
eriana where it’s were processed on same day.

2.2. Questionnaire

At each sampling site, a structured questionnaire approved by the Ethics Committee of the School of Engineering of the Universidad
de los Andes was administered to vendors to obtain information on handling, storage, and hygiene conditions to evaluate possible risk
factors associated with Campylobacter contamination of chicken. Surveyed persons were informed about the procedure on the basis of
an informed consent form. The questionnaire included closed-ended questions to collecting data on the following elements: type and
location of the site, product storage conditions, cleaning practices and frequency, personal protection elements, and worktop material.
Some questions were verified by direct observation by the interviewer (Table S1, Supplementary Material).

2.3. Statistical analysis

To analyze risk factors, a descriptive univariate logistic regression analysis was performed using the RStudio program version
February 1, 5033 (R Core Team, 2020). However, four variables: i) use of work clothing, ii) type of countertop, iii) use of sanitizers, and
iv) how the food was displayed did not elicit different responses among respondents, so they were omitted from the analysis. A
conditional logistic model was used for univariate analysis, and exposures with p < 0.05 were considered significant. Variables were
constructed by combining multiple items from the questionnaire. Additionally, the Chi-square test using RStudio software was used to
test associations with significance between the prevalence of Campylobacter spp. in fresh chicken carcasses and sample origin: place/
stores and localities. The results were considered statistically significant for p-values < 0.05. In addition, a generalized linear model
(GLM) with binomial distribution was performed to show the differences between localities given the prevalence of Campylobacter in
each one. The GLM used, the bias-reduced logistic regression from the brglm2 package of the RStudio program was used; the results
were statistically significant with p-values < 0.1.

2.4. Sample processing

Sample processing was performed according to the MLG 41.04 USDA-FSIS protocol "Isolation and identification of Campylobacter
jejuni/lari/coli from poultry, sponge and raw product rinse samples" [35]. Each sample was aseptically removed and placed in a
pre-labeled WhirlPak® NASCO plastic bag (37.5 × 50 cm) and rinsed with 400 ml of buffered peptonized water (BPW) (Britania SA,
CABA, Argentina), manually massaging for 3–5 min to ensure complete contact with the BPW. Then, 30 ml of the rinse was removed,
and a selective enrichment was performed in 30 ml of Bolton broth supplemented with antibiotics and 5% horse blood (2X BF-BEB)
(Oxoid cat no. SR0117, England) in 100 ml WhirlPak® bags. Enrichments were incubated at 42 ◦ C for 24 h under microaerobiosis
conditions using a CampyGen Oxoid™ envelope (CN0025A, Oxoid Ltd, Wade Road, Basingstok, UK) inside a 2.5 L OXOID® vessel.

2.5. Detection and identification

Detection and identification Campylobacter species was performed according to the recommendations of the MLG 41.04 USDA-FSIS
protocol, and samples were analyzed by the real-time polymerase chain reaction assay (real time PCR) using the BAX® System
(Hygiena, BAXQ7) kit for Campylobacter spp. Described in MLG 41A.00 [35]. Lysis was performed using a ratio of 150 μl of protease per
12,000 μl of lysis buffer and five μl of the previously incubated enrichment. Lysis was performed in a heating block with the following

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conditions: preheating at 37 ◦ C for 20 min, 95 ◦ C for 10 min. At the end of lysis, the tubes were cooled to 8 ◦ C. Afterwards subsequently
30 μl was taken to hydrate, the PCR tablets in the kit and the real time PCR process was performed in the BAX® equipment for 70 min.
C. jejuni ATCC® 33560 and C. coli ATCC®43478 strains were used for quality control.

2.6. Isolation

Isolations were performed in two ways and in parallel to achieve better isolate colonies that met the expected morphology of
C. jejuni and C. coli. For both species, translucent or mucoid colonies were expected, shiny and generally with a faint pink color in the
medium, flat, or slightly elevated, which can vary significantly in size [35]. The two plating procedures were performed by filtration
and depletion seeding. Filtration with sterile 0.45 μm cellulose membrane filter (Sartorius Stedim Biotech, Germany) was performed
by taking 100 μl of the enriched sample in Bolton broth. The filters were placed in small petri dishes (60 × 15 mm) containing 10 ml of
Campy-Cefex medium supplemented with 5% horse blood in small 60 × 15 mm petri dishes containing 10 ml of this medium. The
samples were passively filtered for 15–20 min at room temperature. Initially, tests were performed withthe filter left in place during
incubation and in other cases removing it at 15–20 min. However, it was decided to remove the filter after 15–20 min, because that
better results were obtained by finding more isolated colonies of Campylobacter spp. The use of filters was performed to increase the
recovery of bacterial isolates from the enrichment broth and to reduce competing bacteria [36,37]. The second procedure consisted of
taking 10 μl of the enrichment in Bolton broth with a sterile plastic loop and plating by depletion in Campy-Cefex culture medium. The
boxes of both procedures were incubated under microaerobiosis conditions using the CampyGen Oxoid® envelope at 42 ◦ C for 24 ± 2
h. Then, passages were made on Campy-Cefex and Karmali media (Liofilchem®, Italy) to obtain pure cultures of presumptive
Campylobacter colonies (Fig. S1, Supplementary Material). Colonies were subjected to Gram staining, a motility test in 0.85% saline,
and oxidase and catalase tests were performed. Confirmed isolates were stored at − 20 ◦ C in 10% Skim Milk broth (Merck, Darmstadt
Germany).

3. Results

3.1. Prevalence

Of the 91 samples processed, 42 were positive for Campylobacter spp., and the prevalence was 46.2% (42/91). Of the 42 positive
samples, C. jejuni was the most prevalent species with 54.8% (23/42) positive samples, followed by co-contamination of C. jejuni and
C. coli in the same sample, 35.7% (15/42) and a small percentage of samples were contaminated only with C. coli 9.5% (4/42). The
associations between the prevalence of Campylobacter in retail chicken carcasses and the place of origin (farmers’ markets/small food
stores) were statistically significant (p < 0.05) and it was evident that the prevalence was higher in small food stores than in farmers’
markets. We also observed that,the species C. jejuni was the most common in both farmers’ markets and small food stores (Table 1).
Regarding the localities, Usaquén had the highest prevalence (100%), followed by Barrios Unidos (76.9%), San Cristóbal (53.9%),
and Antonio Nariño (38.5%). The lowest prevalence of Campylobacter was recorded in Santa Fe (23.1%), Kennedy (15.4%), and Los
Mártires (15.4% each). The association between the prevalence of Campylobacter spp. In retail chicken carcasses and the locality of
origin was significant (p < 0.001). To show the differences in Campylobacter prevalence among the localities, data were analyzed using
the GLM model and it was found that the locality of Usaquén presented significant differences (p < 0.1) with the localities of Santa Fe,
Kennedy and Los Mártires (Fig. 2). On the other hand, Table 2 shows the prevalence of the species found by locality, where the Barrios
Unidos locality was significantly different from Kennedy and Los Mártires (p < 0.1). In addition, the Barrios Unidos locality was the
only one that presented a prevalence for C. jejuni (50%), C. coli (20%) and simultaneous C. jejuni/C. coli contamination (30%).
In addition, the localities of Antonio Nariño, Los Mártires, Usaquén and San Cristóbal presented contamination with samples
containing C. jejuni and others with simultaneous C. jejuni/C. coli contamination, but none presented only positive samples with C. coli.
On the contrary, samples from the Santa Fe locality did not present simultaneous contamination with C. jejuni/C. coli, but separately
with C. coli, and samples from the Kennedy locality were the only ones that showed contamination with C. jejuni only (Table 2). It was
also shown that C. jejuni was the species with the highest prevalence compared to C. coli in each locality and that the samples from the
Kennedy locality were the only ones that presented contamination only with C. jejuni compared to the other localities that presented
contamination with the both species of Campylobacter spp. It also shows an important prevalence of the co-occurrence presence of
C. jejuni/C. coli in the Usaquén locality.
Regarding the results obtained in each locality according to the place of origin (farmers’ markets/small food stores), it was found
that in most cases the highest percentage of contaminated samples came from small food stores in most cases and again we found that
C. jejuni was the most common species in both farmers’ markets and small food stores in each of the localities (Table 3).

Table 1
Prevalence of C. jejuni and C. coli in retail chicken carcasses of farmers’ markets y small food stores.
Location C+ (%)a C. jejuni (%) C. coli (%) C. jejuni + C. coli (%)b

Farmers’ markets 18/53 (34%) 10/18 (55.5%) 1/18 (5.6%) 7/18 (38.9%)
Small food stores 24/38 (63.2%) 13/24 (54.2%) 3/24 (12.5%) 8/324 (33.3%)
a
Number of positive samples for Campylobacter spp. in farmers’ markets was 18 and in small food stores was 24.
b
Percentage of positive samples with the joint presence of C. jejuni/C. coli.

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Fig. 2. Percentage of positive samples for Campylobacter in seven localities of the city of Bogotá. Different letters indicate statistically significant
differences between localities (p < 0.1). Bars indicate ± standard error (n: 13 per locality).

Table 2
Prevalence of C. jejuni and C. coli species in retail chicken carcasses in the different localities sampled in the city of Bogotá.
Localities C+ (%)a C. jejuni (%) C. coli (%) C. jejuni + C. coli (%)b

Antonio Nariño 5/13 (38.5%) 4 (80%) 0 (0%) 1 (20%)

Barrios Unidos 10/13 (76.9%) 5 (50%) 2 (20%) 3 (30%)
Kennedy 2/13 (15.4%) 2 (100%) 0 (0%) 0 (0%)
Los Mártires 2/13 (15.4%) 1 (50%) 0 (0%) 1 (50%)
Usaquén 13/13 (100%) 3 (23.1%) 0 (0%) 10 (76.9%)
Santa Fe 3/13 (23.1%) 2 (66.7%) 1 (33.3%) 0 (0%)
San Cristóbal 7/13 (53.9%) 6 (85.7%) 1 (14.3%) 0 (0%)
a
The total number of samples positive for Campylobacter spp.
b
Percentage of positive samples with the joint presence of C. jejuni/C. coli.

3.2. Risk factors

This study identified four (4) possible risk factors associated with Campylobacter contamination in chicken meat marketed in retail
outlets in the city of Bogotá. It is important to note that taking these factors together could explain most of the contamination. The
significant factors that were poor cleaning of the scales (OR: 41.42, 95% CI: 7.57–226.6, p = < 0.001), low frequency of disinfection of
in food handling utensils (OR: 45.94, 95% CI: 5.4–392.9, p = < 0.001), type of place (farmers’ markets/small food stores) (OR: 4.24,
95% CI: 1.29–13.9, p = 0.0169), direct contact of chicken carcasses with other poultry meat food or prey (OR: 20.59, 95% CI: 4.03105,
p = 0.001) (Table 4). The above indicates that the probability of cross-contamination with Campylobacter due to poor scale cleaning
and low frequency of disinfection higher as result of contact of chicken carcasses with other food and originating from small food
higher than the probability of contamination as stores/farmers’ markets.

4. Discussion

In Colombia, there have been no studies to compare the prevalence of Campylobacter in chicken carcasses sold at retail in the
country or Bogotá, so this is the first study with this objective. Bogotá is the largest market city in the country, contributing more than a
third of the gross domestic product (GDP) (31%) and is considered an engine of the national economy due to the size of its population,
being the most populated city in the country, with 7.8 million according to the latest census conducted by the National Administrative

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Table 3
Prevalence of Campylobacter spp. in chicken carcasses from farmers’ markets and small food stores in different localities.
Localities Location na C. jejuni (%) C. coli (%) C. jejuni + C. coli (%)b

Antonio Nariño Farmers’ markets 1 100 0 0

Small food stores 4 75 0 25
Barrios Unidos Farmers’ markets 5 80 0 20
Small food stores 5 20 40 40
Kennedy Farmers’ markets 0 0 0 0
Small food stores 2 100 0 0
Los Mártires Farmers’ markets 1 100 0 0
Small food stores 1 0 0 100
Usaquén Farmers’ markets 8 25 0 75
Small food stores 2 0 0 100
Santa Fe Farmers’ markets 0 0 0 0
Small food stores 2 50 50 0
San Cristóbal Farmers’ markets 2 50 50 0
Small food stores 5 100 0 0
a
The total number of samples positive for Campylobacter spp.
b
Percentage of positive samples with the joint presence of C. jejuni/C. coli.

Table 4
Conditional logistic regression analysis for possible risk factors related to the prevalence of Campylobacter in retail chicken carcasses in farmers’
markets and small food stores in the different localities sampled in the city of Bogotá.
Risk Factor Variables Category % (No. positives/observationsa) P value OR CI 95%
positives

Use personal protective equipment Good 47.1% (16/34) REF NA NA NA

Regular 70.6% (12/17) 0.12 2.64 0.77 9.05
Frequency of utensil disinfection Each time they are used 6.3% (1/16) REF NA NA NA
Twice a day 77.1% (27/35) <0.001b 45.94 5.37 392.9
Sample temperature at the time of Within cooling range 0–4 ◦ C 50% (16/32) REF NA NA NA
purchase Greater than cooling range 63.2% (12/19) 0.368 1.69 0.53 5.35
0–4 ◦ C
Type of location Farmers’ markets 39.3% (11/28) REF NA NA NA
Small food stores 73.9% (17/23) 0.0169b 4.24 1.29 13.9
Origin of chicken Food plant 56.1% (23/41) REF NA NA NA
Farm 50% (5/10) 0.731 0.78 0.19 3.09
Contact of chicken carcasses with other No 30% (9/30) REF NA NA NA
food Yes 90.5% (19/21) 0.001b 20.59 4.03 105
The scale is for the exclusive use of the Yes 50% (18/36) REF NA NA NA
chicken No 66.7% (10/15) 1.973 0.50 0.56 6.84
The scale is cleaned each time it is used Yes 10% (2/20) REF NA NA NA
No 83.9% (26/31) <0.001b 41.42 7.57 226.6
a
The total number of observations analyzed for each risk factor variable was 5.
b
Significance (p < 0.05), NA: Not Applicable, REF: Reference Category.

Department of Statistics (DANE) in 2018 [38]. Its inhabitants represent approximately 15.4% of the national population [39,40]. In
terms of chicken production, the department of Cundinamarca (of which Bogotá is part) ranks second among the departments with the
largest share in the country’s poultry sector with 20.2% of GDP [39].
The overall prevalence of Campylobacter obtained in this study was 46.2% in chicken carcasses sold in retail establishments in
Bogotá. Since we do not have data on the epidemiology of this bacterium in Colombia, we do not know whether this scenario is recent
or long-standing. However, when comparing the results of this study with data from other international investigations, it is evident that
the prevalence of Campylobacter in raw chickens sold at retail was higher (46.2%) but close to those reported in American countries
such as Argentina 32% [41], Brazil 35.8% [42], Ecuador 44% [43], Mexico 43% [36] and then in European countries such as Spain
39.4% [44], Italy 34.1% [45], or Asian countries such as China 45.1% [17] and Pakistan 35.2% [46]. Nevertheless, higher prevalence
values close to those reported in this study are found in other countries: such as the United States 59.2% [47], Thailand 57% [48] and
Western Australia 58.7% [49] Haz clic o pulse aquí para escribir texto.The reported differences in prevalence among these studies may
be due to possible differences in the sampling scheme or design, the number of samples analyzed, the type of sample (fresh versus
frozen chicken), the detection protocol, chicken production systems, among others.
Furthermore, C. jejuni was found to be the most frequent species compared to C. coli and a significant proportion of contamination
by both species (C. jejuni/C. coli) was evident. In addition, interesting results of joint contamination by both species (C. jejuni/C. coli)
were found. The above is consistent with what has been observed in several studies showing that C. jejuni is more prevalent than C. coli
in the contamination of chicken carcasses at retail level [15,41,42,48,50,51]. The high prevalence of C. jejuni in chicken carcasses may
be due the fact that this bacterial species usually has a higher survival rates at low temperatures compared to C. coli [48,52]. However,
further studies are needed to compare the prevalence and survival kinetics of these bacterial species in chickens.

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There were differences in the proportion of chicken carcasses contaminated with Campylobacter spp. in farmers’ markets vs. small
food stores. A higher prevalence of the bacterium was found in the latter and C. jejuni was found to be the most common species in both
establishments. Although in Colombia there is no information on Campylobacter spp. in these places, some international studies have
obtained similar results regarding a higher prevalence in small food stores than in farmers’ markets [48,53]However, other studies
have shown a higher prevalence in farmers’ markets than in small food stores [54–56], and these differences may be due to the level of
sanitation, when handling, processing and performing storage operations in these stores [57]. Therefore, more studies on the
contamination of chicken carcasses with Campylobacter spp. in this type of retail locations need to be conducted in Colombia for a
better comparison.
Regarding the co-contamination of C. jejuni and C. coli in chicken carcasses, it is emphasized that these results are important
because, although C. jejuni and C. coli have very similar phenotypic and genotypic characteristics, it has been shown that C. jejuni has
an advantage over C. coli in the process of infection in humans because it carries important virulence determinants that are essential to
cause its pathogenesis in comparison to C. coli [58]. Nevertheless, it has also been shown that C. coli infection was found in older people
compared to C. jejuni and there is also evidence of greater resistance to various antibiotics such as erythromycin in C. coli than in
C. jejuni [59,60]. These two species are among the top four causes of diarrheal disease worldwide [61]. Therefore, it is important to
conduct studies to analyze the possible public health implications of finding foods, such as chicken, contaminated with both species at
the same time.
Moreover, this study’s shows notable differences in the prevalence percentages of the species of C. jejuni and C. coli in each locality.
In the locality of Usaquén, we observed that all the samples obtained were contaminated with Campylobacter spp. This is an important
finding since this locality has one of the three main food supply centers in Bogotá: the Codabas farmers’ market, which supplies part of
the northern part of the city. Approximately 70% of the food consumed by the inhabitants of the surrounding communities comes from
this food distribution center [62]. Likewise, the locality of Barrios Unidos presented a high prevalence (76.9%) of contamination with
Campylobacter spp. This locality borders the locality of Usaquén and possibly the chicken retail sites such as the small food stores in this
locality may be supplied by the Codabas farmers’ markets, so there may be a flow in the contamination of chicken carcasses in this
locality when purchased in places that present presumptive contamination with Campylobacter, such as Codabas.
However, the other sampled localities showed low prevalence percentages, with exception of the locality of San Cristóbal. These
localities are apparently supplied with poultry products by the farmers’ markets supply corporation (Corabastos) of the locality of
Kennedy, a farmers’ markets where all the products from the different regions of Colombia arrive [39,40,63]. In the locality of
Kennedy, two positive samples were obtained that came from small food stores and not from the farmers’ markets, which leads us to
consider that possibly, in this central supply center, adequate control and hygiene practices are being maintained with respect to this
pathogen. However, it is necessary to carry out further studies with a larger number of samples and locations to obtain more infor­
mation on the prevalence of Campylobacter in these localities.
The percentage prevalence of Campylobacter evidenced in this study in retail chicken channels in Bogotá contributes to having more
information about this pathogen in order to generate improvements in hygienic practices and strengthen training programs for retail
establishments to reduce the presence of Campylobacter in foods such as raw chicken [48]. The risk factors found in this study are
consistent with those of other studies [64–66], which evidence that poor utensil and equipment hygiene are associated with a high
incidence of Campylobacter species isolated from chicken meat. A possible reason for these findings is the poor use of disinfection
protocols and, the use of disinfectant concentrations below the recommended level, inadequate exposure time, among other variables
that may influence the efficacy of disinfectants against Campylobacter [67,68]. Some disinfectants, such as chlorine and iodine
releasers, are microbicidal halogens that are widely used for disinfectant purposes on bacteria such as Campylobacter [67]. One of the
most used according to the respondents is sodium hypochlorite, but in the study by Gutiérrez-Martín et al., 2011 [67] they evidenced
that this disinfectant may be ineffective against C. jejuni. However, other studies have obtained good results against Campylobacter
when using 0.63% sodium hypochlorite, is used and left on for 5 min [69]. Considering these studies, a longer exposure time and/or a
higher concentration might make the disinfectant more effective. Therefore, it is advisable to develop studies to evaluate the effec­
tiveness of the cleaning and disinfection protocols against Campylobacter spp. being used in the poultry industry and in places where
chicken is sold at retail.
These results can be helpful for the surveillance of Campylobacter spp. in Bogotá and to promote the initiative to carry out more
studies in other cities of the country. They are also important data for the formulation of policies to further strengthen the food safety
system along the chain of production, processing, and mainly commercialization of retail poultry. Therefore, it is important to establish
strategies to reduce the prevalence of Campylobacter in raw chicken and reduce the risk of a possible disease or condition such as
campylobacteriosis. Implementation of good agricultural and management practices improved hygienic conditions and consumer
education on food safety when handling raw poultry can help reduce the contamination of poultry products with this bacterium.
Likewise, the creation and implementation a manual of good hygienic practices for the sale of poultry at farmers’ markets and small
food stores can be a strategy to educate and raise awareness among vendors and consumers regarding the proper handling of poultry
carcasses. Most of the risk factors were associated with poor hygienic and disinfection practices, so, to improve these conditions in
retail outlets, personnel should be informed and sensitized about the risk of this pathogen, especially regarding food safety and its
relevance mainly in chicken meat.

5. Conclusions

This study is the first report on the prevalence of Campylobacter in fresh chicken carcasses for human consumption in small food
stores and farmers’ markets in Bogotá. The results obtained indicate that C. jejuni is the most predominant species, followed by C. coli.

7
B.T. Ortiz et al. Heliyon 10 (2024) e26356

Furthermore, inadequate cleaning of equipment and utensils; and reduced frequency of cleaning and disinfection are possible potential
risk factors for the presence of Campylobacter in chicken carcasses marketed in the city, highlights the importance of strengthening
cleaning and disinfection systems in retail outlets such as farmers’ markets and small food stores. Therefore, these results can be helpful
for the surveillance of Campylobacter spp. in Colombia and for implementation surveillance programs for Campylobacter spp. to control
its presence in products offered to consumers. Likewise, the proposal of quality assurance strategies and the creation and imple­
mentation of a manual of good hygiene practices for the sale of chicken in farmers’ markets and small food stores at retail level can be
way to educate and raise awareness among sellers and consumers regarding the proper handling of chicken. It is important to highlight
the need to carry out more studies to determine the general prevalence of Campylobacter spp. in chicken meat intended for human
consumption in the country, thus having an approach to the actual situation of this pathogen in Colombia, which will allow the
regulatory authorities to establish the necessary measures to reduce a possible impact of this pathogen on public health and also to
generate education among consumers for the proper handling and preparation of this food at home.

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Ethical considerations

This study was reviewed and approved by Ethics Committee Faculty of Engineering, Universidad de los Andes, with the approval
number: 241. All participants provided informed consent to participate in the study and for the publication of their anonymized case
details.

Data availability statement

The original contributions presented in the study are included in the article/supplementary materials, further inquiries can be
directed to the corresponding author/s.

CRediT authorship contribution statement

Brigithe Tatiana Ortiz: Conceptualization, Data curation, Formal analysis, Investigation, Methodology, Writing – original draft,
Writing – review & editing. Deyci Rodríguez: Conceptualization, Investigation, Supervision, Validation, Writing – original draft,
Writing – review & editing. Silvia Restrepo: Conceptualization, Investigation, Supervision, Validation, Writing – original draft,
Writing – review & editing, Resources.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to
influence the work reported in this paper.

Acknowledgements

We are grateful to the Laboratory of Food Microbiology of the Pontificia Universidad Javeriana in Bogotá; the Large Animal Clinic
of the Universidad Nacional in Bogotá; the Department of Biological Sciences, the Laboratory of Mycology and Phytopathology
(LAMFU) and the Vice-Presidency of Research and Creation of the Universidad de los Andes in Bogotá.

Appendix A. Supplementary data

Supplementary data to this article can be found online at https://doi.org/10.1016/j.heliyon.2024.e26356.

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