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Listeria monocytogenes strains isolated from dry milk samples in Mexico: occurrence and antibiotic sensitivity.


Listeria monocytogenes was first described as a human pathogen by Nyfeldt in 1929, and is a relevant cause of morbidity and mortality (Yang, Yeh, Tsai, & Yu, 2006). It is a frequent causal agent of meningitis, and may cause severe septicemia, particularly in pregnant women and immunocompromised patients (ILSI Research Foundation & Risk Science Institute Expert Panel on Listeria monocytogenes in Foods, 2005). Although L. monocyto genes has been known as a human and animal pathogen for over 50 years, listeriosis was not acknowledged as a public health problem until recently (Vazquez-Boland et al., 2001). Mortality from listeriosis ranges from 13% to 34% (Teo, Ziegler, & Knabel, 2001).

L. monocytogenes is widely distributed in nature and can be isolated from several natural sources, such as soil and vegetables as well as river, channel, estuarine, and residual waters (El-Shenawy & El-Shenawy, 2006; Erdenlig et al., 2000). More than 40 species of domestic animals, including cows and sheep, as well as 17 wild and domestic bird species are known reservoirs, and Listeria spp. can be isolated from feces, nasal, and genitourinary secretion of apparently healthy specimens. Listeria spp. can be transmitted among animals by the fecal-oral route (Hellstrom, Kiviniemi, Autio, & Korkeala, 2008), or by foods handled by asymptomatic carriers (Kathariou, 2002). Well-documented foodborne listeriosis outbreaks have been associated with cheese, coleslaw, meat, vegetables, and fish (Thimothe, Nightingale, Gall, Scott, & Wiedmann, 2004; Vazquez-Boland et al., 2001), as well as with several dairy products, such as raw and pasteurized milk, fresh Swiss- and Mexican-style cheese, chocolate milk, and butter (Waak, Tham, & Danielsson-Tham, 2002). Most L. monocytogenes isolates and other Listeria species are sensitive to a wide range of antibiotics active against gram-positive bacteria, with the exception of cephalosporins and fosfomycin (Antunes, Reu, Sousa, Pestana, & Peixe, 2002; Charpentier & Courvalin, 1999; Vitas, Sanchez, Aguado, & Garcia-Jalon, 2007). Since the first multiresistant L. monocytogenes strain was observed in France in 1988 (Poyart-Salmeron, Carlier, Trieu-Cout, Courtien, & Courvalin, 1990), different patterns of antibiotic resistance have been reported in environmental, food, and clinical sources (Aureli et al., 2003; Hansen, Gerner-Smidt, & Bruun, 2005; MacGowan, Reeves, & McLauchlin, 1990; Paciorek, 2004; Walsh, Duffy, Sheridan, Blair, & McDowell, 2001).

Information on the presence of L. monocytogenes in Mexico is scarce and the frequency of listeriosis is unknown. Vazquez-Salinas and co-authors (2001) reported the presence of serotypes 1 and 4b in raw milk in the outskirts of Mexico City, while Heredia and coauthors (2001) found L. monocytogenes in 16% of the ground meat samples collected from retail stores in the metropolitan area of Monterrey, Mexico. In addition, Rodas-Suarez and co-authors (2006) detected the presence of Listeria spp. in oyster, fish, and seawater samples and found L. monocytogenes in 4.5% of fish samples and 8.3% of seawater samples, but not in oysters. Multiresistant environmental strains were found in the aforementioned work, representing a potential threat to human health. Moreno-Enriquez and coauthors (2007) described the prevalence of L. monocytogenes in fresh cheese, cheese processing plants, and dairy farms in Sonora, in northern Mexico.

Dry milk is a particular concern in Mexico, as approximately 150,000 metric tons of dry milk are imported every year (Food and Agriculture Organization of the United Nations, 2007), at a cost of around $250 million (Secretaria de Agricultura, Ganaderia, Desarrollo Rural, Pesca y Alimentacion, 2007). It is used to make fluid milk, cheese, cream, yogurt, ice cream, and milk formulas, and it is used by the pharmaceutical and cosmetology industries. More importantly, most of this dry milk is used to make dairy products widely distributed among the population covered by welfare programs. Although powdered milk has historically been a source of Salmonella spp., no research has been done related to Listeria in dry milk. Because of the aforementioned prevalence in Mexico of the dry milk market, the purpose of our study was to determine the presence of Listeria spp. in imported dry milk samples and to determine the sensitivity of the L. monocytogenes isolates to different antimicrobial agents.

Materials and Methods Sampling

Dry milk samples (100 whole and 110 skimmed) obtained in bulk from La Merced market (Mexico City) between December 2005 and May 2006 were analyzed. A total of 500 g of representative dry milk samples from different countries were processed according to Military Standard 105E (ANSI/ASQ Z1.4, ISO 2859, BS6001, DIN40.080, NFX06022, UN148-42, KS A 3109). Samples were obtained by mixing uniform weight subsamples of each of three bulk samples drawn in aseptic conditions and transported to the laboratory in ethylene oxide-sterilized polyethylene bags (Nasco Wirp Pak) for analysis.

Isolation of Listeria and Bacteria Identification

A single 25-g portion of each dry milk sample was added to 225 mL pre-enrichment broth and incubated for 48 hours at 30[degrees]C. Then a 0.1-mL sample was streaked on Oxford agar and incubated at 30[degrees]C for 24-48 hours. Presumptive identification was based on characteristic Listeria spp. colony morphology: 0.1-0.2 mm diameter, shiny, humid, convex, whole black edges surrounded by an esculin hydrolysis halo. Five colonies per plate were selected to observe "in fresh" motility and were then seeded in SIM tubes.

Gram staining, catalase production, hemolytic activity on sheep blood agar, and oxidase tests were performed. Colonies of Listeria and also of Staphylococcus, Streptococcus, and Lactobacillus were identified using the API microbiological identification system.

Serotyping and Mouse Pathogenicity

L. monocytogenes isolates were serotyped using polyvalent "O," somatic 1 and 4, and antiflagellar AB antisera according to the Bacteriological Analytical Manual (U.S. Food and Drug Administration) method (Hitchins, 2002).

To determine mean lethal dose ([LD.sub.50]), batches of five National Institutes of Healthstrain mice per L. monocytogenes isolate who were 8-12 weeks old, weighed approximately 21 g, and were parasite free were used. Twenty-three L. monocytogenes isolates were cultivated in brain-heart infusion (BHI) broth at 37[degrees]C and 150 rpm for 18-21 hours. Cells were harvested, concentrated by centrifugation at 3000 x g for 30 minutes, and then washed with phosphate buffered saline. The suspension was adjusted to an [OD.sub.595] of 0.3, to reach a cellular concentration between 108 and 109 CFU/mg/L. Decimal serial dilutions were made to obtain concentrations of 1 x [10.sup.4] , 1 x [10.sup.5], 1 x [10.sup.6], and 1 x [10.sup.7] CFU/ mg/L; 0.1 mL of each suspension was inoculated intraperitoneally to each mouse, and the number of injected viable cells was confirmed by culturing in BHI agar. The number of live and dead mice was recorded every 24 hours until completion of 15 experimental days. Finally, bacteria were recovered from mice through necropsy, viscerectomy, maceration of the affected organs, and seeding in gelose-blood medium.

Antibiotic Sensitivity

Antibiotic sensitivity was assessed using the Bauer-Kirby disk diffusion assay performed in triplicates. Test and control strains were seeded in Mueller-Hinton agar supplemented with 0.5% defibrinated sheep blood and 0.1% esculin (Soriano, Fernandez Roblas, Calvo, & Garcia Calvo, 1998), previously adjusted to the 0.5 McFarland nephelometer tube. The disks contained the following antibiotics: 10 [micro]g ampicillin, 30 [micro]g cephalothin, 30 [micro]g cefotaxime, 30 ug ceftazidime, 30 [micro]g cefuroxime, 1 [micro]g dicloxacillin, 15 [micro]g erythromycin, 10 [micro]g gentamicin, 5 [micro]g pefloxacin, 10 IU penicillin, 30 [micro]g tetracycline, and 25 [micro]g trimethoprimsulfamethoxazole. Serial dilutions of each antibiotic were made in Todd-Hewitt broth (5120 to 0.031 [micro]g mg/L) to determine the minimum inhibitory concentrations ([MIC.sub.50] and [MIC.sub.90]) following the Clinical and Laboratory Standards Institute (formerly National Committee on Clinical Laboratory Standards [NCCLS]) guidelines (NCCLS, 1998). For this purpose, test and control strains were seeded in Mueller-Hinton agar and adjusted to the 0.5 McFarland nephelometer tube and diluted (1:10) before inoculation. Adjusted strains were inoculated in 100 [micro]L to Todd-Hewitt broth containing different antibiotic dilutions. The tubes were incubated at 30[degrees]C for 48 hours and then tested to estimate the [MIC.sub.50] and [MIC.sub.90]. The samples were reseeded in Todd-Hewitt broth without antibiotic to determine whether the MIC had a bactericidal or bacteriostatic effect. L. monocytogenes American Type Culture Collection (ATCC) 19114, E. coli ATCC 29922, Pseudomonas aeruginosa ATCC 27853, and Staphylococcus aureus ATCC 25923 strains were used as references for testing of antibiotic activity.

S. aureus and E. coli strains were used as sensitive controls and P. aeruginosa strain was used as a resistant control. L. monocytogenes strain was used to evaluate the behavior of a commercial Listeria species towards the tested antibiotics.

Statistical Analysis

Analysis of variance was used to determine the statistical significance of antibiotic sensitivity variations of Listeria isolates (Crawley, 1993; McCullagh & Nelder, 1983). Tukey's test (p < .05) was used to measure the difference.


Isolation of Listeria From Dry Milk Samples

L. monocytogenes was isolated from dry skim milk samples, but was not found in whole milk samples. Of 550 isolates, Staphylococcus spp. were identified (60.2%); and also Streptococcus spp. (28%), Listeria spp. (7.8%), and Lactobacillus spp. (4%). This recovery rate could be underestimated as sporal germination and the growth of thermo-resistant Bacillus and Lactobacillus may mask the presence of Listeria spp. in dry milk samples (Teo et al., 2001). Several studies suggest that the presence of other microorganisms mask the development of sublethally damaged Listeria spp. (Vlaemynck & Moermans, 1996), even when selective media are used to isolate and recover this pathogen.

Analysis of variance revealed no significant difference with a 95% confidence interval (p < .05) among the 23 isolates of L. monocytogenes regarding antimicrobial activity (sensitivity to antibiotics).

Serotyping and Mouse Pathogenicity

All isolates confirmed as L. monocytogenes agglutinated with serum type 1 and 4. Of 23 L. monocytogenes isolates, 17 (73.9%) belonged to serotype 4b, and 6 (26.1%) to serotype 1. Of the Listeria species, only L. monocytogenes is considered to be a significant human and animal pathogen, even though occasional human infections caused by L. welshimrei, L. innocua, and L. seeligeri have been reported. L. monocytogenes serotypes (1/2a, 1/2b, and 4b) are associated with most cases of human listeriosis (Perrin, Berner, & Delamare, 2003).

Eight of the 115 L. monocytogenes-inoculated mice (7%) died after four days of inoculation, and 17.3% died after five days of inoculation. Mortality increased sharply on day 6 (34.7%, 40 mice) and on day 7 (56.5%, 65 mice). Serotype 1 isolates were more virulent (100% of mortality rate at 48 hours) than serotype 4 isolates. For serotype 4 isolates, only by increasing bacterial concentration was mice mortality achieved. The number of viable cells required to cause death (LD50) with all the isolates ranged from 1.4 x [10.sup.6] to 3.3 x [10.sup.7] CFU/mg/L.

Antibiotic Sensitivity

Human listeriosis is considered a public health problem of low incidence but high mortality, requiring prompt diagnosis and adequate antibiotic therapy (Aureli et al., 2003). Over the last two decades, a high number of foodborne listeriosis outbreaks have occurred, some with high mortality rates. Antibiotic resistance and inefficient empirical treatment of Listeria infections could be responsible for this increased mortality.

Because human listeriosis can be foodborne, sensitivity and resistance of food isolates to antibiotics should be assessed. All L. monocytogenes isolates analyzed were sensitive to the [beta]-lactam antibiotic cefotaxime and 91.30% were sensitive to gentamicin.

We found diverse sensitivity frequencies, however, to other antibiotics: 86.96% to dicloxacillin, 82.61% to cefuroxime, 82.61% to tetracycline, 69.56% to erythromycin, 69.56% to trimethoprim-sulfamethoxazole, 52.17% to ceftazidime, 39.13% to ampicillin, 30.43% to penicillin, 26.09% to pefloxacin, and 17.39% to cephalothin (Table 1); 9%-14% of the isolates showed multiresistance to one or more of the following antibiotics: ampicillin, erythromycin, tetracycline, dicloxacillin, and trimethoprimsulfamethoxazole, which are the basic antibiotics used in Mexico for the treatment of listeriosis (Table 2).


Isolation of Listeria From Dry Milk Samples

Listeria strains were isolated only from skim milk samples. The presence of fat and the interface formed between the fat (cream) and the aqueous phase was possibly the reason for the lack of isolation from whole milk samples. Isolation of L. monocytogenes from whole milk could be more difficult owing to the fast growth of accompanying microbiota, which could mask or inhibit the development of L. monocytogenes. Additionally, the presence of Listeria only in skim milk could be due to the further manipulation it undergoes during its production process.

Listeria isolates were identified as L. monocytogenes (23 isolates), L. innocua (13 isolates), L. ivanovii (1 isolate), and L. seeligeri (6 isolates). The presence of Listeria in these samples may be due to postprocessing cross contamination, frequently caused by improper sanitation conditions or postproduction exposure during packaging (Tompkin, 2002). Moreover, Listeria is able to survive under environmental and metabolic stress (Brown, 1991), and is relatively less sensitive to pasteurization temperatures compared with vegetative forms of other microbial foodborne pathogens. It is known to survive refrigeration, dry environments, and the presence of certain inhibitory agents (Doyle, Mozzota, Wang, Wiseman, & Scott, 2001; Farber, Daley, Coates, Emmons, & McKellar, 1992). It is also able to survive in milk processing plants for up to seven years (Waak et al., 2002). Cow infections are more frequent during winter and spring, when the animals are hoarded (Abou-Eleinin, Ryser, Donnelly, 2000). Listeriosis in cows has been associated with the consumption of contaminated silage, a well-identified source of Listeria (Kathariou, 2002; Perry & Donnelly, 1990; Schlech, 1992).

The high frequency of isolation for Staphylococcus spp. in our work can be explained because this bacterium survives pasteurization. In addition, the survival of these bacteria in milk powder has been previously reported (Soejima et al., 2007).

Antibiotic Sensitivity

Although as stated above, most of L. monocytogenes isolates and other Listeria species are not sensitive to cephalosporins, cefotaxime is a third-generation cephalosporin and this can explain the lack of resistance to this antibiotic.

The resistance profile shown in the results was found in O:1 serotype isolates from milk samples and includes antibiotics commonly used to treat listeriosis. Multiresistant L. monocytogenes strains associated with mobile gene elements from Enterococcus, Streptococcus, and Staphylococcus (Antunes et al., 2002; Charpentier, Gerbaud, & Courvalin, 1994) have been isolated from clinical (Yucel, Citak, & Onder, 2005) and other sources (Aureli et al., 2003). Although it was previously thought that multiresistant strains of Listeria spp. were not commonly found in nature, some studies have reported evidence of the emergence of multiresistant L. monocytogenes strains from sources such as dairy farms (Moreno-Enriquez et al., 2007; Srinivasan et al., 2005), bulk milk samples (Schlegelova et al., 2002), cabbage farms, and packing sheds (Prazak, Murano, Mercado, & Acuff, 2002), while earlier work done in our laboratory showed their presence in fish and seawater samples (Rodas-Suarez et al., 2006).


Our study provides additional evidence of the emergence of multiresistant strains of Listeria spp. in a widely consumed dairy product (powdered milk is a ready-to-eat food), representing a considerable threat to human health that should be taken into account. Finding trimethoprim-sulfamethoxazole-resistant strains isolated from milk is relevant because this antibiotic is frequently used to treat listeriosis in patients who are allergic to penicil lin (Aureli et al., 2003). Indiscriminate, widespread use of sulfonamides to treat cow mastitis probably favors the prevalence of resistant strains and consequently affects the treatment of listeriosis (Gitter, Bradley, Blampied, 1980).

Imports of skim milk powder have risen in Mexico in recent years to nearly 54% as compared to previous years (Bovine Milk Product System, 2012), thereby also increasing the risk to consumers. Moreover, the skim milk powder is used in the formulation of animal feed (Animal Health Specifications of Food Products for Animal Consumption, 2000), hence posing a potential risk to animals and indirectly to humans.

The lack of Listeria isolation from whole milk samples does not necessarily indicate the absence of this bacterium; hence, techniques beyond the traditional microbiological culture methods must be reinforced to reliably track these bacteria.

Acknowledgement: We thank Ingrid Mascher for English improvement of the manuscript.


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O.R. Rodas-Suarez, PhD

E.I. Quinones-Ramirez, PhD

Escuela Nacional de Ciencias Biologicas

Instituto Politecnico Nacional

F.J. Fernandez, PhD

C. Vazquez-Salinas, PhD

Division de Ciencias Biologicas y de la Salud

Universidad Autonoma Metropolitana

Corresponding Author: E.I. Quinones-Ramirez, Departamento de Microbiologia, Escuela Nacional de Ciencias Biologicas, Instituto Politecnico Nacional, Carpio y Plan de Ayala s/n. Col. Casco de Santo Tomas, C.P 11340, Mexico City, Mexico. E-mail:

Resistance Profile of Listeria Isolates

Species # Isolates Resistant Isolates


L. monocytogenes 23 14 19 0 11
L. innocua 13 12 9 0 7
L. ivanovii 1 0 0 0 0
L. seeligeri 6 0 0 0 0

Species Resistant Isolates


L. monocytogenes 4 3 7 2 17
L. innocua 4 2 4 2 7
L. ivanovii 0 0 0 0 0
L. seeligeri 0 0 0 0 0

Species Resistant Isolates


L. monocytogenes 16 4 7
L. innocua 9 2 4
L. ivanovii 0 0 0
L. seeligeri 0 0 0

Note. AM = ampicillin; CF = cephalothin; CTX = cefotaxime; CAZ =
ceftazidime; CXM = cefuroxime; DC = dicloxacillin; E =
erythromycin; GE = gentamicin; PEF = pefloxacin; PE = penicillin;
TE = tetracycline; SXT = trimethoprim-sulfamethoxazole. Tests were
done in triplicate.


Number of Listeria monocytogenes Isolates Growing at Different
Concentrations, [MIC.sub.50] and [MIC.sub.90] (a) Estimated for
Five Antibiotics

 Antibiotic Concentration
Antibiotic ([micro]g/mg/L)

 0.031 0.062 0.125 0.25 0.5

Ampicillin 7 2 4 3 3
Erythromycin 6 3 3 3 3
Tetracycline 6 2 3 3 3
Dicloxacillin 4 3 4 3 3
Trimethoprim- 4 3 5 3 4

 Antibiotic Concentration
Antibiotic ([micro]g/mg/L)

 1 2 4 8 16 32

Ampicillin 0 0 2 1 0 0
Erythromycin 0 0 1 0 0 0
Tetracycline 2 1 1 0 0 0
Dicloxacillin 3 1 2 0 1 0
Trimethoprim- 2 1 1 1 0 0

Antibiotic [MIC.sub.50] [MIC.sub.90]

Ampicillin 1.15 16.19
Erythromycin 4.04 11.98
Tetracycline 0.1654 17.67
Dicloxacillin 8.28 30.68
Trimethoprim- 2.62 21.90

Note. Isolates (n = 23) from dry skim milk samples were tested in
triplicate. Antibiotic concentration and microorganism viability
showed a negative correlation (r = -.88; p < .0001).
(a) MIC = minimum inhibitory concentrations.
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Author:Rodas-Suarez, O.R.; Quinones-Ramirez, E.I.; Fernandez, F.J.; Vazquez-Salinas, C.
Publication:Journal of Environmental Health
Article Type:Report
Geographic Code:1MEX
Date:Aug 30, 2013
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