**3. Overview of resistant pathogens isolated from food**

Fruits, vegetables, and foods from animal origin can be contaminated with antibiotic-resistant bacteria at any time in the food chain FAO [2]. There has been an increase in drug resistance in pathogens isolated from food for human consumption since 2000. *Salmonella enterica* and *Escherichia coli* isolates have been considered among the most important pathogens, because they can make zoonotic transfer of resistant genes [44]. However other pathogens, such as *Vibrio* spp., some species of *Aeromonas*, spores of *Clostridium botulinum* type F, or enteric bacteria such as *Campylobacter*, have been linked to gastrointestinal diseases in humans who have consumed foods of animal and marine origin. It has been reported that multidrug-resistant plasmids are easily transferred to *Aeromonas salmonicida* by *E. coli* [45, 46].

*Salmonella* is a pathogenic bacterium that cause a gastrointestinal disease called salmonellosis. In Latin America, Asia, and Africa, 200–500 cases of salmonellosis per 100,000 inhabitants per year have been documented, where the 95% of the infections come from the consumption of contaminated foods [47]. Worldwide, it was estimated that the infections caused by *Salmonella enterica* are above 93.8 million cases with 155,000 deaths per year [48].

*Salmonella enterica* is one of the most frequently isolated foodborne pathogens from different kinds of food. In the United States, between 11 and 20% of strains

**177**

*Multidrug-Resistant Bacterial Foodborne Pathogens: Impact on Human Health and Economy*

isolated from animals destined to human consumption were resistant to more than five different antibiotics [49]. Other studies mention that 82% of the isolates in strains from food are resistant to at least one antibiotic, associated with high resistance levels to tetracycline, streptomycin, sulfamethoxazole, and ampicillin [49]. In Latin American countries, the average of *Salmonella* resistant isolates is dependent on the region and analyzed food. In Brazil in a study conducted in a salami processing line, a 3.7% resistance to 1 antibiotic and 11.1% resistance to 3 or more antibiotics out of a total of 54 isolates have been reported [50]. In contrast, in a study conducted in pork carcasses, 147 out of 155 *Salmonella* strains isolated

*Escherichia coli* is one of the most widespread microorganisms in nature, and it is a member of the normal intestinal flora of many organisms, including humans. In a study conducted in Havana, Cuba, 74 *E. coli*-resistant strains were isolated from foods involved in foodborne diseases (ETA). Among foods with the highest CFU of *E. coli* serogroups identified, there were soy yogurt (14.3% of isolates), pork steak (11.9%), chicken hash (11.9%), cheese (9.5%), ham (9.5%), and beef hash (7.1%). Resistance to ampicillin was present in 36.4% of the isolates, and some isolates were also resistant to streptomycin, sulfamethoxazole, and tetracycline [52]. In America, Eastern Mediterranean, Africa, Southeast Asia, and the Western Pacific regions, an increased resistance to third-generation cephalosporins and fluoroquinolones into

On the other hand, studies conducted in dairy products have shown that 73.3% (33/45) of the *E. coli* strains isolated were susceptible to all antibiotics tested and 24.4% (11/45) showed resistance to ampicillin. The phylogenetic analysis of the *E. coli* isolates resulted in grouping into two phylogroups, A and B1, which have a higher frequency of resistance genes than those that were grouped in B2 and D. It is worth to notice that *E. coli* isolates in this study that belonged to phylogroup A and B1 were commensal strains with few or no virulence factors [54]. These results suggest that the food chain is the vehicle for the transfer of resistant genes, and it has been suggested that *E. coli* strains present in food are the original carrier of many mechanisms of antibiotic resistance in the intestinal microbiota of humans.

Studies conducted in different food classes have isolated other bacterial genera different to *Salmonella enterica* and *E. coli*. One of the most studied is *Staphylococcus aureus*, which causes staphylococcal poisoning. Strains of *S. aureus* have been studied in the last decades because they show resistance to methicillin. The analyses done in 282 *S. aureus* strains isolated from food and manipulators showed that 56.1%

Another bacterial genus of health importance is *Mycobacterium bovis*. In the United States, outbreaks by *M. bovis* have been associated with the consumption of contaminated food. In 2007, 203 samples of cheese imported from Mexico were collected at the California customs office. Of the samples collected, 4.9% tested positive for *Mycobacterium* genus, with drug susceptibility test to streptomycin, isoniazid, rifampicin, ethambutol, and pyrazinamide, showing that they were susceptible to all the antibiotics tested except pyrazinamide [56]. In contrast, in Japan, 58 *M. bovis* strain isolates from dairy cattle reported 7 strains resistant to the fluoroquinolones enrofloxacin, orbifloxacin, and danofloxacin. The fluoroquinolone resistance was associated with the mutation to quinolone resistance-determining regions of *gyrA* and *parC* genes (QRDR). The strains that showed no fluoroquino-

*Listeria*, *Shigella*, and *Campylobacter* are other bacterial genera that have been isolated from foods and have shown antibiotic resistance. *Listeria monocytogenes* strains isolated from cheese have shown resistance to streptomycin, kanamycin, cephalothin, and tetracycline [58]. The analysis of 152 *Shigella* strains isolated

of the strains were resistant to one or more antimicrobials [55].

lone resistance phenotype did not present mutations [57].

(94.85%) were resistant to at least one or more antibiotics [51].

*DOI: http://dx.doi.org/10.5772/intechopen.88789*

*E. coli* isolates has been reported [53].

#### *Multidrug-Resistant Bacterial Foodborne Pathogens: Impact on Human Health and Economy DOI: http://dx.doi.org/10.5772/intechopen.88789*

isolated from animals destined to human consumption were resistant to more than five different antibiotics [49]. Other studies mention that 82% of the isolates in strains from food are resistant to at least one antibiotic, associated with high resistance levels to tetracycline, streptomycin, sulfamethoxazole, and ampicillin [49]. In Latin American countries, the average of *Salmonella* resistant isolates is dependent on the region and analyzed food. In Brazil in a study conducted in a salami processing line, a 3.7% resistance to 1 antibiotic and 11.1% resistance to 3 or more antibiotics out of a total of 54 isolates have been reported [50]. In contrast, in a study conducted in pork carcasses, 147 out of 155 *Salmonella* strains isolated (94.85%) were resistant to at least one or more antibiotics [51].

*Escherichia coli* is one of the most widespread microorganisms in nature, and it is a member of the normal intestinal flora of many organisms, including humans. In a study conducted in Havana, Cuba, 74 *E. coli*-resistant strains were isolated from foods involved in foodborne diseases (ETA). Among foods with the highest CFU of *E. coli* serogroups identified, there were soy yogurt (14.3% of isolates), pork steak (11.9%), chicken hash (11.9%), cheese (9.5%), ham (9.5%), and beef hash (7.1%). Resistance to ampicillin was present in 36.4% of the isolates, and some isolates were also resistant to streptomycin, sulfamethoxazole, and tetracycline [52]. In America, Eastern Mediterranean, Africa, Southeast Asia, and the Western Pacific regions, an increased resistance to third-generation cephalosporins and fluoroquinolones into *E. coli* isolates has been reported [53].

On the other hand, studies conducted in dairy products have shown that 73.3% (33/45) of the *E. coli* strains isolated were susceptible to all antibiotics tested and 24.4% (11/45) showed resistance to ampicillin. The phylogenetic analysis of the *E. coli* isolates resulted in grouping into two phylogroups, A and B1, which have a higher frequency of resistance genes than those that were grouped in B2 and D. It is worth to notice that *E. coli* isolates in this study that belonged to phylogroup A and B1 were commensal strains with few or no virulence factors [54]. These results suggest that the food chain is the vehicle for the transfer of resistant genes, and it has been suggested that *E. coli* strains present in food are the original carrier of many mechanisms of antibiotic resistance in the intestinal microbiota of humans.

Studies conducted in different food classes have isolated other bacterial genera different to *Salmonella enterica* and *E. coli*. One of the most studied is *Staphylococcus aureus*, which causes staphylococcal poisoning. Strains of *S. aureus* have been studied in the last decades because they show resistance to methicillin. The analyses done in 282 *S. aureus* strains isolated from food and manipulators showed that 56.1% of the strains were resistant to one or more antimicrobials [55].

Another bacterial genus of health importance is *Mycobacterium bovis*. In the United States, outbreaks by *M. bovis* have been associated with the consumption of contaminated food. In 2007, 203 samples of cheese imported from Mexico were collected at the California customs office. Of the samples collected, 4.9% tested positive for *Mycobacterium* genus, with drug susceptibility test to streptomycin, isoniazid, rifampicin, ethambutol, and pyrazinamide, showing that they were susceptible to all the antibiotics tested except pyrazinamide [56]. In contrast, in Japan, 58 *M. bovis* strain isolates from dairy cattle reported 7 strains resistant to the fluoroquinolones enrofloxacin, orbifloxacin, and danofloxacin. The fluoroquinolone resistance was associated with the mutation to quinolone resistance-determining regions of *gyrA* and *parC* genes (QRDR). The strains that showed no fluoroquinolone resistance phenotype did not present mutations [57].

*Listeria*, *Shigella*, and *Campylobacter* are other bacterial genera that have been isolated from foods and have shown antibiotic resistance. *Listeria monocytogenes* strains isolated from cheese have shown resistance to streptomycin, kanamycin, cephalothin, and tetracycline [58]. The analysis of 152 *Shigella* strains isolated

*Pathogenic Bacteria*

**Antibiotic class/ antibiotics**

**Peptides** [41] Polymyxin B Colistin

**Rifamycins** [42] Rifampicin

**Sulfonamides** [36] Sulfanilamide Sulfadiazine Sulfatiazole

**Tetracyclines** [43] Doxycycline Minocycline Oxytetracycline

**Table 1.**

*\*The subclasses of the class of beta-lactam*

**176**

*E. coli* [45, 46].

**3. Overview of resistant pathogens isolated from food**

*Modes of action to different classes of antibiotics and their mechanisms of resistance.*

million cases with 155,000 deaths per year [48].

Fruits, vegetables, and foods from animal origin can be contaminated with antibiotic-resistant bacteria at any time in the food chain FAO [2]. There has been an increase in drug resistance in pathogens isolated from food for human consumption since 2000. *Salmonella enterica* and *Escherichia coli* isolates have been considered among the most important pathogens, because they can make zoonotic transfer of resistant genes [44]. However other pathogens, such as *Vibrio* spp., some species of *Aeromonas*, spores of *Clostridium botulinum* type F, or enteric bacteria such as *Campylobacter*, have been linked to gastrointestinal diseases in humans who have consumed foods of animal and marine origin. It has been reported that multidrug-resistant plasmids are easily transferred to *Aeromonas salmonicida* by

**Mode of action Mechanism of resistance**

*Intrinsic*

LPS

*Intrinsic*

[33]

*Acquired*

*Intrinsic*

transporter)

• Ribosomal modification • Enzyme inhibition

• Integrons (*sul1* gene)

• Plasmids (*IncQ* class*: sul2* gene)

• Bacterial flow pumps (SMR, RND, or ABC

(coded by different classes of *tet*, *otr*, *and tcr* genes)

• Lipid modifications

• Reduction of specific proteins of the membrane and

• Point mutations in the rifampicin-binding region of

• Bacterial flow pumps (VceB and Acr transporter)

the β subunit of RNAP (*rpoB* gene)

They displace the Mg+2 and Ca+2 ions and interact electrostatically with the

lipopolysaccharides (LPS) of the external Gram-negative cell membranes

They stop transcription by interacting with the β subunit of RNA polymerase (RNAP)

They act as competitive inhibitors of DHPS; they block the folate biosynthesis in the bacterial cell

subunit

They block the access of the tRNA to the ribosome by binding to the 30S ribosomal

*Salmonella* is a pathogenic bacterium that cause a gastrointestinal disease called salmonellosis. In Latin America, Asia, and Africa, 200–500 cases of salmonellosis per 100,000 inhabitants per year have been documented, where the 95% of the infections come from the consumption of contaminated foods [47]. Worldwide, it was estimated that the infections caused by *Salmonella enterica* are above 93.8

*Salmonella enterica* is one of the most frequently isolated foodborne pathogens from different kinds of food. In the United States, between 11 and 20% of strains

from various foods that caused outbreaks of shigellosis in Brazil showed that several strains were resistant to streptomycin (88.6%), followed by ampicillin (84.6%) and sulfamethoxazole/trimethoprim (80.5%). The resistant strains were grouped into 73 patterns, where pattern A (resistance to ampicillin, sulfamethoxazole/trimethoprim, tetracycline, streptomycin, and chloramphenicol and intermediate resistance to kanamycin) grouped the highest number of isolates (*n* = 36) [59]. In Malaysia, *Campylobacter* spp. was reported with a prevalence of 17.4%, from a total of 340 cattle samples. *Campylobacter* isolates showed resistant to tetracycline (76.9%) and ampicillin (69.2%), while resistance to chloramphenicol was low (7.6%) [60].

Even in farms of goldfish (*Carassius auratus*), 70 strains of bacterial genera such as *Aeromonas hydrophila*, *Vibrio fluvialis*, and *V. furnissii* have been identified, with 45% of the isolates being resistant to 6 of the 14 antibiotics tested; 100% of the strains were resistant to cephalothin, 94% to ampicillin, 89% to chloramphenicol, 88% to tetracycline, 85.3% to nitrofurantoin, 61.3% to carbenicillin, and 65.3% to kanamycin. Twenty three percent of the isolates presented sensitivity to amikacin, trimethoprim, cefotaxime, netilmicin, pefloxacin, and gentamicin. Only one strain, *A. hydrophila*, showed resistance to all antibiotics tested. Twenty strains generated resistance to 7 different antibiotics, and 67 of the 70 strains generated resistance to more than 1 antibiotic [46].

As we can see in this overview, the resistance of the different bacterial genera isolated in a great diversity of foods is alarming, since many of these bacterial genera are the cause of many foodborne diseases. The diseases produced by these resistant pathogenic bacteria are difficult to treat, being able to provoke death in some patients.
