Universidad de Sonora

ISSN: 1665-1456

Volume XXV, Issue 2

Journal of biological and health sciences

http://biotecnia.unison.mx

*Correspondence author: Gildardo Rivera

e-mail: gildardors@hotmail.com

Received: October 9, 2022

Accepted: February 2, 2023

Enterobacteriaceae in Pork Meat:

Causal Agents of Public Health Problems

Enterobacterias en Carne de Cerdo: Agentes Causales de Problemas de Salud Pública

Alma D. Paz-González,, Karina Vázquez, Ana V. Martínez-Vázquez, Carlos Ramírez- Martínez, Gildardo Rivera*

 Facultad de Medicina Veterinaria y Zootecnia, Universidad Autónoma de Nuevo León, General Escobedo, ZC , México

 Laboratorio de Biotecnología Farmacéutica, Centro de Biotecnología Genómica, Instituto Politécnico Nacional, Reynosa,

ZC , México.

SUMMARY

Pork meat is one of the most consumed products worldwide,

and pathogenic microorganisms in pork, such as Enterobac-

teriaceae, represent a public health risk, causing foodborne

diseases. Enterobacteriaceae in pork meat processing is an

indicator of poor sanitation management. Escherichia coli

(E. coli) and Salmonella spp. are the most prevalent bacteria.

Dierent studies report that their high percentage and the

multidrug resistance found are an alarming risk to consu-

mers´ health.

Keywords: Enterobacteriaceae, Pork, Public health.

RESUMEN

La carne de cerdo es uno de los productos más consumidos a

nivel mundial, y los microorganismos patógenos en la carne

de cerdo, como las Enterobacterias, representan un riesgo

para la salud pública, provocando enfermedades de transmi-

sión alimentaria. Las Enterobacterias en el procesamiento de

la carne de cerdo son un indicador de una gestión sanitaria

deciente. Escherichia coli (E. coli) y Salmonella spp. son las

bacterias más prevalentes. Diferentes estudios indican que

su porcentaje alto y la multifarmaco-resistencia son un riesgo

alarmante para la salud de los consumidores.

Palabras clave: Enterobacterias, Carne de cerdo, Salud pú-

blica.

INTRODUCTION

Meat is one of the main food sources for the human popula-

tion worldwide. It is an important source of protein, essential

amino acids, zinc, iron, phosphorus, and vitamin B, providing

benets to adults (cell repair and regeneration) and children

and adolescents (growth and development) (Bohrer, 2017).

The consumption of meat is in high demand globally. Howe-

ver, consumption varies depending on the region due to the

inuence of various factors such as gender, rural or urban

origin, educational level, and age of consumers (Estevez-

Moreno et al., 2021). Another important factor is income,

which in the case of the Mexican population, is a determining

aspect inuencing the selection of chicken, pork, or beef

meat (Huerta-Sanabria et al., 2018).

The production and consumption of chicken, pork,

beef, lamb, and mutton have grown, reaching record highs

in 2021, with an annual meat production and consumption

of 335,275 and 334,975, respectively. Mexico is among the

countries with the highest meat protein production and

consumption. Chicken meat is the most consumed (4,166

tons), followed by pork (2,217 tons) and beef (1,723 tons)

(OECD-FAO, 2022).

On the other hand, one of the world’s biggest problems

facing meat production and distribution is its susceptibi-

lity to bacterial contamination. This situation is related to

deciencies in hygiene and poor handling practices during

processing and distribution, which cause public health pro-

blems such as gastroenteritis and diarrhea, among others.

The Center for Disease Control and Prevention (CDC) reports

more than 250 foodborne diseases (FBD), mainly caused by

bacteria (CDC, 2021). Microbial spread in meat occurs during

the slaughtering process, mainly Enterobacteriaceae, a large

family of gram-negative bacteria, such as Salmonella, Esche-

richia coli (E. coli), Klebsiella pneumoniae (K. pneumoniae), and

Yersinia, among others (Rönnqvist et al., 2018; Peruzy et al.,

2021). Bacteria, such as Staphylococcus aureus (S. aureus),

Pseudomonas, Brochothrix, Carnobacterium photobacterium

(C. photobacterium), Listeria, among others, have also been

frequently detected in meat processing (Peruzy et al., 2019).

Enterobacteriaceae cause FBD (Mladenović et al., 2021),

mainly gastrointestinal illnesses (Guzmán et al., 2017). In

recent years there has been infections with strains resistant

to one or more antibiotics, which has complicated treatment,

aggravating the disease, and even leading to the death of pa-

tients. For this reason, the World Health Organization (WHO)

considers bacterial or multidrug resistance as one of the ten

main health problems worldwide (WHO, 2019).

Dierent techniques have been established to detect

Enterobacteriaceae, such as traditional microbiological

methods involving bacterial colony counting and molecular

techniques, such as the polymerase chain reaction (PCR),

for rapid and more accurate detection (Cauchie et al., 2020).

Several studies have shown that Enterobacteriaceae are a

recurrent problem in the production and commercialization

of meat products, representing an important public health

risk. Therefore, this study analyzed the presence of Entero-

bacteriaceae in pork meat and its potential risk as a causal

agent of diseases.

DOI: 10.18633/biotecnia.v25i2.1846

74 Volume XXV, Issue 2

Paz-González et al: Biotecnia / XXV (2): 73-78 (2023)

We searched scientic articles in the PubMed, Science-

Direct, and Google Scholar databases for information and

data on food safety issues in pork meat, regarding their

production and consumption, bacterial pathogens presence,

the prevalence of Enterobacteriaceae, and their impact on

public health. The search was restricted to publications in

English and Spanish. The literature review was carried out

from March to July of 2022. The literature search was under-

taken using the keywords: Enterobacteriaceae, meat, pork,

antimicrobial resistance, and public health.

Prevalence of Enterobacteriaceae in pork meat

Several studies have demonstrated the presence of Entero-

bacteriaceae in pork meat samples (Table 1). In the United

States, E. coli was detected with a prevalence of 12 % and Sal-

monella spp. with almost 6 % (Mollenkopf et al., 2011); years

later, E. coli was reported with a value of 18 % (Scheinberg et

al., 2017). While, in the northeast from Mexico, in the state of

Tamaulipas, an investigation reported E. coli contamination

in pork meat with a high prevalence (50 %) (Martínez et al.,

2018).

Salmonella spp. had a prevalence of 32 % in Romania

(Mihaiu et al., 2014), and 56 % (Arcos-Ávila et al., 2013), and

71.4 % in Colombia (Rondón-Barragán et al., 2015). Salmone-

lla has been detected with a prevalence of 22 % in samples of

ground pork in the central region from Mexico (Villalpando-

Guzmán et al., 2016). A recent study in southern Brazil detec-

ted Salmonella enterica (S. enterica) in this same type of meat

with a prevalence of 17 % (Kich et al., 2020). In contrast to

these results, in Mexico city reported Salmonella spp. with a

prevalence of only 2 % (Gutiérrez et al., 2020).

Antimicrobial resistance in pork meat

Due to the high manufacture and administration of antibio-

tics in the production process of livestock animals (in 2010,

more than 63,000 tons were used, and by 2030, more than

105,000 tons is estimated), antimicrobial resistance has

rapidly increased and become a global public health threat

(Van Boeckel et al., 2015; Elshamy and Aboshanab, 2020).

The presence of antibiotic-resistant bacteria in pork

meat is a serious problem. Bacterial strains with resistance to

dierent groups of antibiotics are shown in Table 2. In Europe,

E. coli and Salmonella strains multiresistant to β-lactams were

detected in samples from a processing company in Germany,

that was supplied by slaughterhouses from Poland, Belgium,

and Spain. Therefore, the authors suggested that the cause

of such resistance is due to a very extensive processing and

distribution chain (Schill et al., 2017). In Latin America, E. coli

strains resistant to ve antibiotics (ampicillin, tetracycline,

nalidixic acid, chloramphenicol, and cotrimoxazole) were

isolated in pork samples from markets in Lima, Peru (Ruiz-

Roldán et al., 2018).

Impact on public health

According to WHO estimates, in 2015, FBD (caused by

bacteria, viruses, parasites, toxins, and chemicals) triggered

various outbreaks worldwide, sickening more than 600

million people annually and killing around 420,000. On the

American continent, more than 77 million people fall ill

annually, and around 9,000 die from consuming contamina-

ted food. Among the food pathogens that endanger health,

the Enterobacteriaceae responsible for diseases are mainly

Salmonella (salmonellosis) and E. coli, which cause gastroin-

testinal problems such as nausea, vomiting, abdominal pain,

and diarrhea. Other signs are fever and headache (WHO,

2018; Nastasijevic et al., 2020).

Enterobacteriaceae infections from pork meat con-

sumption represent a serious worldwide health problem

for consumers. In the United States, chicken and pork meat

consumption cause most salmonellosis infections (Bonardi,

Tabla 1. Prevalencia de Enterobacterias en carne de cerdo de diferentes países.

Table 1. Prevalence of Enterobacteriaceae in pork from dierent countries.

Bacteria Prevalence (%) Type of

sample Place of origin Country

E. coli

Salmonella spp.

12.2

5.8

Meat Retail markets

United States

(Mollenkopf et al., 2011)

Salmonella spp. 32.21 Meat Production and retail

markets

Romania

(Mihaiu et al., 2014)

Salmonella spp. 56.0 Meat Slaughter Colombia

(Arcos-Ávila et al., 2013)

Salmonella spp. 71.4 Meat Slaughter Colombia

(Rondón-Barragán et al., 2015)

Salmonella spp. 22.5 Ground beef Retail markets Mexico

(Villalpando-Guzmán et al., 2016)

E. coli 18 Meat Slaughter United States

(Scheinberg, 2017)

E. coli 50.8 Ground beef Retail markets Mexico

(Martínez et al., 2018)

Salmonella spp. 2.7 Tenderloin Retail markets Mexico

(Gutiérrez et al., 2020)

Salmonella enterica 17.2 Meat Slaughter Brazil

(Kich et al., 2020)

Volume XXV, Issue 2 75

Paz-González et al: Enterobacteriaceae in Pork Meat: Causal Agents of Public / XXV (2): 73-78 (2023)

Tabla 2. Resistencia antimicrobiana de Enterobacterias provenientes de carne de cerdo.

Table 2. Antimicrobial resistance of Enterobacteriaceae from pork.

Bacteria Resistant to Country

E. coli GEN,GEN, TGCTGC,, OFXOFX,, LEV.LEV. Slovakia

(Gajdošová et al., 2011)

E. coli AMC, AMP, PIP, CEC, COX, CXM, IMP,AMC, AMP, PIP, CEC, COX, CXM, IMP, APR, GEN, NEO, SPT, STR, APR, GEN, NEO, SPT, STR,

TOB, TOB, CMP,CMP, CIP, ENR, COL, DOX, CIP, ENR, COL, DOX, CXT.CXT.

Germania

(Schwaiger et al., 2012)

E. coli

Proteus vulgaris

Klebsiella pneumoniae

Enterobacter cloacae

AMP, PIPAMP, PIP,, CAZCAZ, , CXMCXM,, CTX.CTX. Spain

(Ojer-Usoz et al., 2013)

Salmonella spp. TET,TET, FFC, FFC, AMPAMP,, CMP, CMP, AMCAMC,, EFTEFT, , STX, TMP, STX, TMP, GENGEN, , CIP.CIP. Colombia

(Bermúdez & Rincón 2014)

Salmonella spp. SXT, SXT, STRSTR, , SPTSPT, , TETTET, , AMPAMP, TMP, TMP Thailand

(Sinwat et al., 2015)

E. coli AMP, AMC, CXT,AMP, AMC, CXT, CMP,CMP,

STR, KAN, GEN,STR, KAN, GEN, SXT, TMP, SXT, TMP, TET, TET, CIP.CIP.

Czech Republic

(Skočková et al., 2015)

E. coli CXTCXT Cuba

(Marrero-Moreno et al., 2017)

E. coli GENGEN, , CEP, CEP, CTXCTX,, CIP,CIP, AMPAMP,, CAZCAZ,, CMP.CMP.

Germany

(Schill et al., 2017)

Escherichia fergusonii AMPAMP

E. cloacae CTXCTX,, CAZCAZ,, AMP.AMP.

Proteus mirabalis CEP, CEP, CTXCTX, , TGC,TGC, AMPAMP, , CMP,CMP, COL.COL.

P. vulgaris CEP,CEP, TGC,TGC, AMPAMP,, CMP, CMP, COL.COL.

E. coli AMPAMP, , TETTET, , NALNAL, , CIP,CIP, CMP.CMP. Peru

(Ruiz-Roldán et al., 2018)

E. coli AMP, AMC, PIP, EPF, AMP, AMC, PIP, EPF, TET, TET, GEN, TOB.GEN, TOB. Thailand

(Lugsomya et al., 2018)

β-lactamicos: amoxicilina (AMC), ampicilina (AMP), piperacilina (PIP), cefaclor (CEC), cefoxitina (COX), cefuroxima (CXM), imipenem (IMP), cefotaxima (CXT),

ceftiofur (EFT), cefalosporina (CEP). Cloranfenicol: cloranfenicol (CMP) Aminoglicosidos: apramicina (APR), gentamicina (GEN), neomicina (NEO), especti-

nomicina (SPT), estreptomicina (STR), tobramicina (TOB), kanamicina (KAN), orfenicol (FFC). Fluoroquinolones: ciprooxacina (CIP), enrooxacina (ENR),

doxiciclina (DOX). Antimetabolitos: sulfametoxazol (SXT), trimetoprima (TMP). Tetracliclinas: tetracliclina (TET). Quinolonas: lovofoxacina (LEV), ooxacina

(OFX), ácido nalidíxico (NAL). Glicilciclina: tigeciclina (TGC). Ureidopenicilinas: ceftazidime (CAZ). Polimixina: colistina (COL).

β-lactams: amoxicillin (AMC), ampicillin (AMP), piperacillin (PIP), cefaclor (CEC), cefoxitin (COX), cefuroxime (CXM), imipenem (IMP), cefotaxime (CXT),

ceftiofur (EFT), cephalosporin (CEP). Chloramphenicol: chloramphenicol (CMP). Aminoglycosides: apramycin (APR), gentamicin (GEN), neomycin (NEO),

spectinomycin (SPT), streptomycin (STR), tobramycin (TOB), kanamycin (KAN), orfenicol (FFC). Fluoroquinolones: ciprooxacin (CIP), enrooxacin (ENR),

doxycycline (DOX). Antimetabolites: sulfamethoxazole (SXT), trimethoprim (TMP). Tetracycliclines: tetracyclicline (TET). Quinolones: lovofoxacin (LEV),

ooxacin (OFX), nalidixic acid (NAL). Glycylcycline: tigecycline (TGC). Ureidopenicillins: ceftazidime (CAZ). Polymyxin: colistin (COL).

2017). According to Tran et al. (2018), Salmonella enterica (S.

enterica) and some E. coli strains from pigs are major intesti-

nal pathogens. In Germany, public health authorities investi-

gated salmonellosis outbreaks in 2013 and 2014. Based on a

trace-back analysis, they detected Salmonella muenchen (S.

muenchen) in a pig breeding farm and considered it a pro-

bable source of contamination. The investigation suggested

that intoxications were caused by consuming raw pork and

pork products, traditional foods in some regions of Germany

(Schielke et al., 2017).

In The Netherlands, a study reported a strong asso-

ciation between salmonellosis and pork, considering that

consuming pork contaminated with Salmonella increases

the risk of intoxication in people treated with medications

such as antibiotics or antacids. Additionally, salmonellosis

contamination can also occur in workers from pig farms and

slaughterhouses (Berends et al., 1998).

An investigation by Hernandez et al. (2011) showed data

on salmonellosis cases (paratyphoid and other salmonella-

derived diseases) in Mexico from 2000-2008. In 2000, 10,000

cases were reported, although, in the same year, they began

to decrease; however, from 2002 to 2007, the cases increa-

sed to 12,000 and slightly decreased in 2008. In the case of

shigellosis, by the end of 1999, there were 40,000 cases, with

a signicant decrease in the 2000-2008 period, reaching

10,000 cases; however, this number was still considered high

according to those reported in the epidemiology bulletin of

the Mexican Republic.

Good handling practices

Good handling practices and sanitary surveillance are im-

portant during the dierent stages of the production and

distribution chain, to avoid pork meat contamination with

bacterial pathogens harmful to humans (Tang et al., 2017).

Meat can be contaminated from its origin due to animal

diseases, medication residues, or when the microbial ora of

the slaughtered animal comes into contact with the meat. It

can also be contaminated by surfaces, equipment, utensils,

water, and even the hands of workers (Nerin et al., 2016).

Slaughterhouses represent a strategic control point for

achieving meat product safety (COFEPRIS, 2017, in Spanish).

In the case of Mexico, the National Health, Safety and Food

76 Volume XXV, Issue 2

Paz-González et al: Biotecnia / XXV (2): 73-78 (2023)

Quality Service (SENASICA, in Spanish) and the Agriculture

and Rural Development Secretariat (SADER, in Spanish), have

as their objective the reduction in agricultural and livestock

risks, among others, and to keep the surveillance of food

contamination and agri-food quality of import and export

products under strict control.

Breeding and animal care stage: At the start of pig bree-

ding, feeding plays an important role in avoiding risks to

animal and human health. In Mexico, the Ocial Mexican

Standard, NOM-061-ZOO-1999, which states the “Animal

health specications of food products for human consump-

tion”, indicates which nished food products should be used

for animal consumption. In the care of animals intended for

human consumption, overexposure to antibiotics has poten-

tial adverse eects through direct toxicity to consumers and

the generation of microbial resistance (Chen et al., 2019). Due

to the presence of antimicrobial-resistant bacteria, the use of

antimicrobials for animal growth promotion was banned in

Europe and the United States, particularly those classied as

critically important for treating human infections (Iriti et al.,

2020). In Mexico, the specications for the use of antibiotics

in animals are described in the Ocial Mexican Standard

NOM-064-ZOO-2000, “Guidelines for the classication and

prescription of veterinary pharmaceutical products by the

level of risk of their active ingredients.” It establishes the te-

chnical and scientic criteria for the active ingredients used

in the formulation of veterinary pharmaceutical products to

avoid toxic eects on animals.

Slaughter and distribution stage: The pig slaughter pro-

cess is commonly carried out in Federal Inspection Type (TIF,

in Spanish) slaughterhouses, Health Secretariat Type (TSS, in

Spanish) municipal slaughterhouses, or private slaughter-

houses. TIF slaughterhouses are subject to stricter standards

of hygiene regulation and cold chain integrity and are mainly

used by large meat companies (OECD, 2018). However, the

three slaughter sites must comply with the sanitary regula-

tions for handling animal products stipulated in the NOM-

194-SSA1-2004 standard, which has as its main objective the

denition of the sanitary specications that establishments

must comply with if engaged in the slaughter and prepara-

tion of animals for supply, storage, transport, and sale of their

products. In addition, meat product transportation and dis-

tribution chains must comply with NOM-024-ZOO-1995. This

standard mentions the specications and zoosanitary charac-

teristics for the transportation of animals, their products, and

by-products, and chemical, pharmaceutical, biological, and

food products for use in animals or consumption by them. To

this end, the Federal Commission for the Protection against

Sanitary Risks (COFEPRIS, in Spanish) monitors the strategy

for evaluating sanitary risks and management actions in

slaughterhouses to reduce risks in meat products.

CONCLUSION

The increase in the worldwide production and consumption

of pork meat in recent years have acquired greater relevance

for the food industry because the industry must provide food

free of pathogenic microorganisms. Enterobacteriaceae are

important because they spread easily and contaminate pork

meat, causing gastrointestinal diseases. In this study, about

the prevalence of Enterobacteriaceae in pork meat shown

that Salmonella and Escherichia are frequently reported in

slaughterhouses and retail markets. Unfortunately, both ge-

nerous of strains are reported with antimicrobial resistance

to several groups of antibiotics, such as β-lactams, aminogl-

ycosides, uoroquinolones, and chloramphenicol. Therefore,

the responsible use of antibiotics in veterinary swine care

practices should adhere to the provisions of good manage-

ment practices manuals and current regulations aimed at

the proper use of antibiotics during the raising of animals for

human consumption.

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