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Characterization of Salmonella species from pork meat in Tolima, Colombia¤


Caracterización de las especies de Salmonella en carne porcina en Tolima, Colombia


Caracterização de espécies de Salmonella a partir de carne de porco em Tolima, Colômbia



Iang S Rondón-Barragán1,2*, MV, MSc; Evelyn C Arcos1, MV; Leandro Mora-Cardona1, MV; Clemencia Fandiño1,2, Lic Bacteriology.


1Grupo de Investigación en Inmunobiología y Patogénesis (GIP), Departamento de Sanidad Animal, Facultad de Medicina Veterinaria y Zootecnia, Universidad del Tolima, Tolima, Colombia.

22Laboratorio de Diagnóstico Veterinario, Tolima, Colombia.

*Corresponding author: Iang S Rondón-Barragán. Laboratorio de Diagnóstico Veterinario, Bloque 33 L105, Universidad del Tolima, Ibagué-Tolima, Colombia AA 456. Email:


Received: March 17, 2014; accepted: May 12, 2014



Background: Salmonella is a Gram-negative bacterium and the principal cause of human gastroenteritis that originates from the consumption of animal products.Objective: to determine serotype and antibiotic resistance of Salmonella spp. isolated from pork meat and environmental samples in 6 slaughterhouses and 14 butcheries in Tolima, Colombia. Methods: slaughterhouses and butcheries were selected depending on their slaughter capacity and compliance with good manufacturing practices. Samples (n = 507) were taken from carcasses, the environment, and fomites (i.e., surfaces of knives, hooks, floor, siphons, work surfaces, and transport trucks), then cultured in Salmonella selective media. Following this, the isolated Salmonella spp. was identified using a conventional biochemical test and genus antiserum (Poli A + Vi). The Kauffman-Whyte scheme was used for serotyping and the agar diffusion method (Kirby-Bauer) was used to determine antibiotic sensitivity. Results:Manhattan, Derby, Typhimurium, Javiana, Muenster, Hvittingfoss, Sinsfort, Kattbus, and Saint Paul serotypes of Salmonella were isolated from both pork meat and environmental samples, being Derby the most common serotype. Salmonella isolates showed antibiotic multiresistance mainly to tetracycline, lincomycin and nalidixic acid. Conclusion: several Salmonella serotypes are present in slaughterhouses and meat samples from butcheries, and they show similar antibiotic resistance patterns. This work represents the first report on Salmonella serotypes in slaughterhouses and pork meat from butcheries in Tolima, Colombia.

Keywords: antibiotic resistance, enterobacteria, isolates, serotyping.


Antecedentes: Salmonella es una bacteria Gram-negativa y la principal causa de gastroenteritis en humanos transmitida por consumo de alimentos de origen animal.Objective: determinar el serotipo y la resistencia antibiótica de Salmonella spp. aisladas de carne porcina y muestras ambientales en 6 plantas de beneficio y 14 expendios en Tolima, Colombia. Métodos:las plantas de beneficio y los expendios fueron seleccionados dependiendo del volumen de animales sacrificados y el establecimiento de las buenas prácticas de manufactura. Las muestras (n = 507) fueron tomadas de las carcasas, ambiente y fómites (i.e. superficie de cuchillos, ganchos, piso, sifones, mesones y camiones de transporte), cultivadas en medios de cultivo selectivos para Salmonella. Las Salmonella spp., aisladas fueron identificadas mediante purnas bioquímicas convencionales y antisuero de género (Poli A + Vi). La sero-tipificación fue llevada a cabo a través del esquema Kauffman-Whyte y la sensibilidad antibiótica a través del método de difusión en agar (Kirby-Bauer).. Resultados: fueron aislados los serotipos de Salmonella Manhattan, Derby, Typhimurium, Javiana, Muenster, Hvittingfoss, Sinsfort, Kattbus y Saint Paul tanto de carne porcina como muestras ambientales, siendo el serotipo Derby el más frecuente. Los aislamientos mostraron patrones de multi-resistencia antibiótica, principalmente a tetraciclina, lincomicina y ácido nalidíxico. Conclusión: diversos serotipos de Salmonella fueron aislados de muestras de plantas de beneficio y expendios de carne porcina y estos demostraron patrones similares de resistencia antibiótica. Este trabajo representa el primer reporte de serotipos de Salmonella en plantas de beneficio y expendios de carne porcina en Tolima, Colombia.

Palabras clave: aislamientos, enterobacterias, resistencia a antibióticos, serotipificación.


Antecedentes: a Salmonella é uma bactéria Gram-negativa e causa principal de gastroenterite humana transmitida por consumo de produtos de origem animal. Objetivo: determinar o serotipo e de resistência a antibióticos de Salmonella spp. isolada a partir de carne de porco e amostras ambientais em 6 frigoríficos e lojas 14 açougues em Tolima, Colômbia. Métodos: abatedouros e açougues foram selecionados de acordo com o volume de animais sacrificados eo estabelecimento de boas práticas de manufatura. As amostras (n = 507) foram retirados de cadáveres, meio ambiente e fômites (ou seja, superfícies de facas, ganchos, piso, sifões, mésons e caminhões de transporte), cultivadas em meios de cultura de Salmonella seletiva e a isolada Salmonella spp., foram identificados usando e anti-soro de teste género bioquímica convencional (Poli A + Vi). A sorotipagem foi realizada utilizando esquema de Kauffman-Whyte e teste de sensibilidade aos antibióticos foi feito pelo método de difusão em ágar (Kirby-Bauer). Resultados: ''o'' sorotipos de Salmonella de Manhattan,= o surotipos de Salmonella Derby, Typhimurium, Javiana, Muenster, Hvittingfoss, Sinsfort, Kattbus e Saint Paul foram isolados de ambas as carnes de porco e amostras ambientais, sendo o sorotipo Derby o mais frequente. Os isolados de Salmonella apresentaram padrões de multirresistência aos antibióticos, principalmente para tetraciclina, lincomicina e ácido nalidíxico. Conclusão: vários sorotipos de Salmonella estão presentes em matadouros e lojas amostras de carne de porco de talho e mostram padrões similares de resistência a antibióticos. Este trabalho representa o primeiro relato de sorotipos de Salmonella em abatedouros e açougues de carne de porco em Tolima, Colômbia.

Palavras chave: enterobacteria, isolamentos, resistência aos antibióticos, sorotipagem..




Salmonellosis is the principal gastroenteritis etiology in humans associated with consumption of food from animal origin, where the most frequently isolated serovar in ill humans and pigs is S. Typhimurium (Torpdahl et al., 2006). This pathogen is the most common cause of acute infectious gastroenteritis in Colombia (Bustos et al., 2008).

In spite of the well-known role of Samonella as a foodborne disease (FBD), it is difficult to estimate FBD incidence due to the lack of a strict link with food (Flint et al., 2005) and a number of limitations including: 1) people do not always seek medical aid when they become infected; 2) physicians do not always request a stool culture in suspicious cases; 3) not all positive cases are reported and shared in databases; and 4) there are differences in healthcare seeking behaviors among differing age groups (Kumar et al., 2009; Meneses, 2010). To address these difficulties, the world health organization (WHO) developed surveillance programs for FBD such as Salm-Surv for salmonellosis (Petersen et al., 2002) as well as sentinel sites for other bacteria including Salmonella, Shigella, and Brucella (Flint et al., 2005).

Salmonellosis is considered a major health concern worldwide; it is estimated that 95% of these particular infections are FBDs (Xia et al., 2009).

Human infections by Salmonella serovars have been reported in several countries, including Colombia (Ashbolt et al., 2004; Durango et al., 2004; Voetsch et al., 2004; Vaillant et al., 2005). In the United States, an estimated 56.8% of salmonellosis cases in humans might be attributable to pigs (BIOHAZ, 2012). Arguello et al. (2013b) demonstrated a 40.9% Salmonella prevalence in Danish pig herds, measured at the slaughterhouse. However, overall prevalence in Danish pork was reported to be as low as 1.2% (Alban et al., 2012). Similarly, Arguello et al. (2012) showed 39% Salmonella prevalence in pig carcasses in Spain. Bolton et al. (2013) reported 36.8% prevalence in the UK, and Methner et al. (2011) reported 13.8% in Germany. Arcos et al. (2013) demonstrated 4.3% Salmonella prevalence at slaughterhouses and retail market in Tolima, Colombia.

Although Salmonella species have been isolated from commercial pig farms (Fierro et al., unpublished data) and pork meat at slaughterhouses and butcheries in Tolima (Arcos et al., 2013) limited information is available to establish a clear picture of pig health status in this region. Currently, the main risk factors associated with Salmonella incidence in pig farms are the lack of pest controls and sow replacement programs (Henao et al., 2012). Few studies have addressed antibiotic resistance of Salmonella isolates from pig farms in Tolima (Fierro et al., 2011).

The aim of this study was to conduct a preliminary characterization of Salmonella species isolated from pig carcasses and environmental samples at slaughterhouses and butcheries in Tolima.


Materials and methods

Ethical considerations

The Ethics Committee of the Research Center of Universidad del Tolima approved this study in January 16, 2011.


Six slaughterhouses and 14 pork butcheries of the 32 present in Tolima were included in the study based on their routine slaughter volume and use of good manufacturing practices (GMP). The Colombian institute for drug and food surveillance (INVIMA) supported the study. Carcasses and environmental samples were collected at the slaughterhouse after slaughter and again after delivery to the butcheries. Trucks and shop environments were also sampled. Collected samples were submitted to the Laboratorio de Diagnóstico Veterinario at Universidad del Tolima.

Sample size

Six Tolima municipalities (Chaparral, Fresno, Guamo, Ibagué, Líbano and Mariquita) were selected taking into account the number of slaughtered pigs per week (>80). Based on 0% Salmonella prevalence in Ibagué slaughterhouses, with a 95% confidence level and 5% expected prevalence (Pabón, 1978), sample size was calculated using the following equation (Thrusfield, 2007):


z2: prefixed confidence coefficient (1,962 for a 95% confidence).

p: expected prevalence (in this study, 5% = 0.05).

q: 1- p.

d: Accuracy (in this study, 5%).

The calculated minimum number of samples was 73. A total of 507 samples were taken in this study.

Sample collection

Destructive and non-destructive sampling methods were used on the surface of pig carcasses at slaughterhouses and butcher shops. A non-destructive method was used for carcass skin with sterile swabs (3M Manufacturing Company, Saint Paul, MN, USA), which were hydrated with buffered peptone water for initial dilution and pre-enrichment step. A 10x10 cm area was calculated in each carcass and three vertical and horizontal smears were made from cheeks, abdomen and leg. In addition, 100 g of pork meat was sampled from the abdomen and throat of each carcass. These were cut with sterile scalpels (destructive method) and placed in individual sterile and hermetic bags. Environmental samples were collected from knives, work surfaces, floors, siphons and trucks using commercial swab sponges (EnviroSpongeTM / HydroSpongeTM, Biotrace International®, South Africa). All samples were kept refrigerated until analysis.

Salmonella isolation

Salmonella species were isolated following standard international guidelines (ISO 6579, 2002). Briefly, samples were incubated in buffered peptone water as a pre-enrichment step at 37 °C for 24 hours, followed by a selective enrichment step in two media: tetrathionate broth at 37 °C (Müller-Kauffmann) and Rappaport Vassiliadis at 42 °C. Bacterial samples were cultured in SS agar (Salmonella-Shigella, Oxoid, Germany), XLT4 agar (Xylose Lysine Tergitol-4, Oxoid, Germany), and XLD agar (Xylosa Lysine Desoxycholate, Oxoid, Germany). Suspected bacterial colonies were cultured in McConkey agar and Trypticase soy agar (TSA) and confirmed as Salmonella spp. by using Poli A-I + Vi antiserum (Difco® 222641, USA). In addition, Salmonella isolates were confirmed by typical biochemical tests through an API ® 20E test (Biomereux, France).


Salmonella isolates were serotyped using the Kauffman-White scheme (Brenner, 1998) for O and H antigens with commercial antiserum (Difco, Becton, Dickinson and Company, Sparks, MD). Serotyping was done based on the antigenic description by Grimont & Weill (2007) as well as nomenclature described by Tindal et al. (2005) and the judicial commission of the international committee on systematics of prokaryotes (JCICSP, 2005).

Antibiotic resistance

Antibiotic resistance was assessed with the Kirby- Bauer method (agar diffusion) to determine sensitivity against several antimicrobials (ampicillin, amoxicillin, apramycin, ciprofloxacin, chloramphenicol, cephalexin, enrofloxacin, gentamicin, kanamycin, lincomycin, nalidixic acid, neomycin, nitrofuranoine, tetracycline, and sulfametoxazole/trimethoprim). A bacterial suspension in Mueller-Hinton agar (Oxoid, Germany) was calibrated according to 0.5 McFarland scale of turbidity. The 2005 protocol of the national committee for clinical laboratory standards (NCCLS) was used to interpret bacterial growth inhibition on plate at 37 °C for 24 h.



Isolation of Salmonella species

Salmonella spp. was isolated from 25 out of 507 samples (4.9%) including 421 from carcasses and 86 from environments. Salmonella prevalence in carcasses was 3.32% (14/421) whereas prevalence in environmental samples was 12.79% (11/86). Salmonella isolated from carcasses included 10 from meat (71.4%) and 4 from smears of carcass surfaces (28.6%). Salmonella isolated from environmental samples included 3 from knives (27.2%), 3 from hooks (27.2%), 3 from siphons (27.2%), and 2 from floors (18.4%). In summary, Salmonella isolates were found in meat (40%), carcass smears (16%), knives (12%), hooks (12%), siphons (12%) and floors (8%).


The identified Salmonella serotypes were Samonella ser. Manhattan (2/25; 8%), Salmonella ser. Derby (9/25; 36%), Salmonella ser. Typhimurium (3/25; 12%), Salmonella ser. Javiana (1/25; 4%), Salmonella ser. Muenster (5/25; 20%), Salmonella ser. Hvittingfoss (2/25; 8%), Salmonella ser. Sinsfort (1/25; 4%), Salmonella ser. Kattbus (1/25; 4%), and Salmonella ser. Saint Paul (1/25; 4%; Table 1).

Antibiotic resistance

The majority of Salmonella species isolated in this study were resistant to more than 2 antibiotics (60%). Regardless of its origin, Salmonella isolates showed antibiotic multi-resistance to lincomycin (25/25; 100%), tetracycline (19/25; 76%), nalidixic acid, and neomycin (Table 1). Only one Salmonella isolate showed resistance to both amoxicillin and ampicillin.



Salmonella serotypes Derby, Typhimurium, Heidelberg, Worthington, and Mbandaka are the most common serotypes in swine worldwide (Davies et al., 1997; Mueller-Doblies et al., 2013). S. Typhimurium and S. Derby are the main serotypes isolated from pigs at slaughterhouses in the European Union and the United States (Anonymous, 2008). In this study, S. Derby was the main isolated serotype (36%) from pork. Similar results were reported in Italy (Piras et al., 2011; 47%) and France (40.5%; Bouvet et al., 2003), where S. Typhimurium (27%) was the second serotype in this country—it was slightly higher (36.9%) in Germany (Methner et al., 2011). In contrast, studies by Yang et al. (2013) in China reported S. Enteritidis as the main serotype isolated from pork origin and they isolated only one S. Derby out of 31 Salmonella serotypes. De Busser et al. (2011) also reported S. Typhimurium as the main isolate (58.7%), whereas S. Derby had a prevalence of 8.3% in Belgium. Recently, Arguello et al. (2013b) reported 64.4% and 4.9% S. Typhimurium and S. Derby prevalence in Denmark, respectively.

Salmonella Muenster and S. Typhimurium were the second and third more frequent serotypes isolated in this study, respectively, which is in agreement with Prendergast et al. (2012) who reported several serotypes in Ireland, including S. Typhimurium, S. Infantis, S. Derby, S. Virchow, and S. Livingstone (two strains isolated from porcine carcass swabs could not be fully typed and therefore were referred to as S. Unnamed). Similarly, Botteldoorn et al. (2003), Bolton et al. (2013), Delhalle et al. (2009), McDowell et al. (2007), Meneses (2010), Arguello et al. (2012), Arguello et al. (2013a), and Mueller-Doblies et al. (2013) found S. Typhimurium, S. Derby, S. Rissen, S. Muenster, and S. Javiana in pork samples from other countries. In this study, S. Saint Paul was isolated in 4% of the samples (1/25), in contrast with reports by Kikuvi et al. (2010) indicating this serotype was predominant (64.2%) in Kenya. Other serotypes such as S. Manhattan, S. Javiana, S. Hvittingfoss, S. Sinsfort, and S. Kattbus, have been previously reported in Germany (Methner et al., 2011). Our results indicate that the main Salmonella serotypes isolated from pork meat and environmental samples have similarities to those from North America and European countries, and differ from those originating in Africa.

Although some studies have shown that serotypes isolated from pig farms, slaughterhouses and those detected in infected animals are unrelated or completely different (Hurd et al., 2001), there is an emerging concern that the transport method and carcass reception at butcheries could increase the contamination rate or bacterial isolation from carcasses or environmental samples. In this regard, our study found two Salmonella isolates in carcasses at slaughterhouses, whereas 10 Salmonella isolates were detected at butcheries (Table 1), thus, although we cannot exclude the possibility of contamination during transport or carcass handling, contamination of pork carcasses seems to be more probable during handling at butcher shops given that transport trucks were negative to Salmonella.

Antibiotic, multi-resistant pattern by Salmonella isolates has been reported from pig samples worldwide (Herrera-León et al., 2007; Nwachukwu et al., 2010; Liu et al., 2011; Yang et al., 2013). In this study, tetracycline resistance was high, similar to reports of Salmonella isolates from pork in another countries (Aragaw et al., 2007; Meneses, 2010; Nwachukwu et al., 2010; Mueller-Doblies et al., 2013; Xia et al., 2013; Yang et al., 2013). In contrast, resistance to this antibiotic was lower than 10% in other studies (Kikuvi et al., 2010). Similarly, all Salmonella isolates showed resistance to lincomycin, despite few reports describe resistance to this antibiotic (Arroyo and Arroyo 1995; Fierro et al., 2011). De Geeter et al., (1976) reported that the use of lincomycin in pig diets did not affect the spread of S. Typhimurium through the feces. In addition, high resistance to clindamycin—a lincosamide antibiotic—has been reported in Salmonella spp. strains (Harakeh et al., 2005; Thakur and Bajaj, 2006). Crossed resistance has been demonstrated through linF gene expression (Achard et al., 2005), which could partially explain the high resistance observed by the strains in the present study.

Antibiotic resistance by Salmonella isolates to nalidixic acid was also high (32%). Other researchers have reported similar results (35.8%; McDowell et al., 2007). Our results appear to be higher than values reported by Mueller-Doblies et al. (2013), who found less than 9% Salmonella isolates resistant to this antibiotic in Great Britain and 2.1% in Ireland (McDowell et al., 2007). In contrast, Nwachukwu et al. (2010) reported 87.5% resistance in Nigeria, and Yang et al. (2013) found 77.6% resistance to nalidixic acid in China.

Differences were also found for chloramphenicol, gentamycin, and ampicillin resistance. Values were lower (4%) in the present study compared to those reported by Nwachukwu et al. (2010), Piras et al. (2011), Mueller-Doblies et al. (2013), and Yang et al. (2013).

Salmonella isolates were resi stant to sulfamethoxazole/trimethoprim (12%). Mueller- Doblies et al. (2013) and Yang et al. (2013) reported higher resistance to both antibiotics (47.6% and 83.6%, respectively). On the other hand, Salmonella showed no resistance to ciprofloxacin, kanamycin, and apramycin, in contrast to what has been reported by Yang et al. (2003; 24.3%) and McDowell et al. (2007; 1.6%).

In conclusion, Derby, Muenster, and Typhimurium serotypes are the predominant Salmonella isolates from slaughterhouses and butcher's shops in Tolima. These serotypes were isolated from carcasses as well as from equipment used at pork butcheries. Salmonella isolates showed multi-resistance to various antibiotics and this finding constitutes an alert signal and an important issue that needs to be addressed by the national institute of surveillance of drugs and foods (INVIMA) which regulates the use of antimicrobial agents in the pig production chain.



This manuscript is based on the project ''Determinación de la prevalencia de Salmonella spp. y cuantificación de factores de riesgo asociados a su presencia en carne porcina del departamento del Tolima'' (2008W4497-3594), funded by contract 054/2008 CIAT/MADR, Ministerio de Agricultura y Desarrollo Rural de Colombia. The authors wish to thank the Asociación Colombiana de Porcicultores (ACP), Comité Central de Investigación and Laboratorio de Diagnóstico Veterinario, with special thanks to Luis Hernando Ortiz.


Conflicts of interest

The authors declare they have no conflicts of interest with regard to the work presented in this report.



¤ To cite this article: Rondón-Barragán IS, Arcos EC, Mora-Cardona L, Fandiño C. Characterization of Salmonella species from pork meat in Tolima, Colombia. Rev Colomb Cienc Pecu 2015; 28:74-82.



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