Prevalence and antimicrobial resistance of Campylobacter spp. isolated from retail chicken and duck meat in South Korea

Food Control 62 (2016) 63–68

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Short communication

Prevalence and antimicrobial resistance of Campylobacter spp. isolated from retail chicken and duck meat in South Korea Bai Wei1, Se-Yeoun Cha1, Ran-Hee Yoon, Min Kang, Jae-Hee Roh, Hye-Suk Seo, Jin-A. Lee, Hyung-Kwan Jang∗ Departments of Infectious Diseases & Avian Diseases, College of Veterinary Medicine and Korea Zoonosis Research Institute, Chonbuk National University, 79 Gobong-ro, Iksan, Jeollabuk-do 570-752, Republic of Korea

a r t i c l e

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Article history: Received 4 July 2015 Received in revised form 6 October 2015 Accepted 13 October 2015 Available online 19 October 2015 Keywords: Campylobacter Prevalence Chicken and duck meat Antimicrobial resistance

a b s t r a c t This study was conducted to determine the prevalence and antimicrobial resistance of Campylobacter isolates from chicken and duck meat in South Korea. A total of 149 Campylobacter spp. was isolated and 124 (66.7%) isolates were identified as Campylobacter jejuni, 24 (12.9%) isolates as Campylobacter coli, and one was unidentified. There were 102 isolates from retail duck meat with the isolation rate of 96.2%, which was significant higher (p < 0.05) than 47 isolates from 80 of chicken meat with the isolation rate of 58.8%. Campylobacter isolation rates ranged from 83.3% to 100.0% among traditional markets, wholesale markets and supermarkets; whereas the isolation rate from online store (50.0%) was significantly lower (p < 0.01) than the traditional markets, wholesale markets and supermarkets. Resistance to nalidixic acid, tetracycline and ciprofloxacin was most common both for chicken and duck Campylobacter isolates. All 24 C. coli isolates were resistant to tetracycline. Campylobacter isolates from duck had higher antibiotics resistant rates to ampicillin, ciprofloxacin, gentamicin, nalidixic acid and tetracycline, than chickens. The majority of the Campylobacter isolates were classified as multi-drug resistant, 57.1% of the C. jejuni isolates and 70.9% C. coli isolates were resistant to at least four antibiotics tested in this study. One C. jejuni isolate showed resistance to all eight antibiotics tested in this study. Our results show that retail chicken and duck meat has a high prevalence of Campylobacter, and the high prevalence of resistant and multidrug resistant Campylobacter in retail chicken and duck meat is a potential campylobacteriosis risk for humans living in South Korea. © 2015 Elsevier Ltd. All rights reserved.

1. Introduction Campylobacter is one of the most common causes of foodborne illness in humans and is the most common bacterium causing gastroenteritis worldwide. There were 212,064 confirmed cases of campylobacteriosis reported in Europe in 2010, and it has continued to be the most commonly reported gastrointestinal bacterial pathogen (EFSA, 2012). Campylobacter jejuni is the most common species isolated from humans, whereas Campylobacter coli is less frequent in causing human acute gastroenteritis

∗

Corresponding author. E-mail addresses: [email protected] (B. Wei), [email protected] (S.-Y. Cha), [email protected] (R.-H. Yoon), [email protected] (M. Kang), [email protected] (J.-H. Roh), [email protected] (H.-S. Seo), [email protected] (Jin-A. Lee), [email protected] (H.-K. Jang). 1 These authors contributed equally to this study. http://dx.doi.org/10.1016/j.foodcont.2015.10.013 0956-7135/© 2015 Elsevier Ltd. All rights reserved.

(EFSA, 2012). Enteritis is the most common clinical syndrome caused by Campylobacter, but other extra-intestinal complications include bacteremia, reactive arthritis, and Guillain–Barre syndrome (Yuki, 2007). Infections caused by Campylobacter are well known and are generally transmitted through water, milk, and wild and domestic food animals, whereas poultry and poultry meat products are considered the main source of human infection (Sheppard et al., 2009). Chickens are generally considered the most common source, but there is little information concerning contamination of duck worldwide. A high prevalence of Campylobacter has been reported in domestic South Korean duck farms recently (Wei, Cha, et al., 2014; Wei, Huang, Liao, Liu, & Chiou, 2014). While there is little information concerning the contamination of Campylobacter in duck at the retail level worldwide. Fewer such studies have been performed in Asian countries, which have more than 80% of the duck meat consumption. The majority of human infections are sporadic and self-limiting.

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Antimicrobials are not usually recommended for treatment except in severe cases and fluoroquinolones and macrolides are the preferred treatment options. Nonetheless, fluoroquinolone-resistant Campylobacter spp. has been reported in human infections since the 1990s and the frequency is increasing rapidly (Nachamkin, Ung, & Li, 2002). Although use of antibiotics as growth promoters has been banned in food animals in several countries including South Korea, resistant bacteria are still detected in raw meat (Ku et al., 2011). Antibiotics are used in veterinary medicine to treat sick animals or for prophylactic purposes. These antibiotics are often identical to those used in human medicine and are often of high clinical importance. The objective of this study was to elucidate the prevalence of foodborne pathogen-Campylobacter in retail duck and chicken meat, and to analyze the level of antimicrobial resistance in these bacterial isolates.

2.2. Isolation and identification of Campylobacter For isolation of Campylobacter, 25 g of each poultry meat samples including skin were aseptically weighted and homogenized for 2 min in a stomacher with 225 ml buffered peptone water (Difco, Sparks, MD, USA) in sterile plastic bags. Each 25 g meat sample from whole body was included the neck, wing, breast and leg including skin sample. Next, 10 ml of the homogenate was added to 10 ml of 2 × Bolton broth (Oxoid Ltd., Basingstoke, England) with Laked Horse Blood (Oxoid) supplemented with cefoperazone, vancomycin, trimethoprim, and cycloheximide (Oxoid), and incubated for 4 h at 37 °C followed by 48 h at 42 °C in a microaerophilic environment of 10% CO2 , 5% O2 , and 85% N2 . Then the enrichment was plated onto modified charcoal–cefaperazon– desoxycholate agar (mCCDA, Oxoid) containing an antibiotic supplement of cefoperazone and amphotericin (Oxoid) at 42 °C for 48 h. After incubation, the plates were examined for the typical colonies, which are generally small, gray, drop-like, and shiny. Three to five presumptive Campylobacter colonies from each selective agar plate were further cultured on 5% sheep blood agar plates (Komed, Seongnam, South Korea) for 24–48 h at 42 °C under microaerophilic conditions. Presumptive Campylobacter isolates were confirmed by PCR assay as described previously (Wei, Cha, et al., 2014; Wei, Huang, et al., 2014). After identifying each isolate, the Campylobacter isolates were stored in brain heart infusion broth (Oxoid) with 20% glycerol at −80 °C.

2. Materials and methods 2.1. Sample collection A total of 186 retail poultry meat samples (106 duck meat and 80 chicken samples) were collected from January to March 2013 in Jeonlado areas in South Korea (Table 1). Chicken meat included the whole body (48) and the breast (32), while duck meat included the whole body (52) and sliced samples (54). Each brand was purchased from every market, as either 1 or 2 samples if the whole body and portion both existed, to ensure complete coverage of all brands of poultry meat sold in Jeonlado. Each sample was separately retailed in a closed Styrofoam box packaged by over-wrapping with polyvinylidene film. These samples were obtained from supermarkets, traditional markets, wholesale markets, and online stores. These markets are the major sources of poultry meat for the local community. All samples purchased from supermarkets, traditional markets, and wholesale markets (where they were stored in a refrigerator) were placed immediately in a plastic bag and transported in a cool box to the laboratory. Online food shopping was that poultry meat was directly purchased from the websites of company; the meat was delivered by another logistics company who then shipped the poultry meat directly to the customer from the company’ storage warehouse. All retail poultry meat purchased from online stores was kept in an airtight Styrofoam box containing ice packs and transported to the laboratory within 48 h. All meat products were kept at 0–5 °C in the warehouse for the online stores; the temperature in the airtight Styrofoam box was examined for every sample at the time of arriving in the laboratory, the sample with the temperature less than 0 °C and more than 10 °C was refused to count. Samples were stored at refrigerated temperatures (0–5 °C) until examination and Campylobacter isolation from all samples was commenced within 4 h of arrival in the laboratory.

2.3. Antimicrobial susceptibility testing The agar dilution method was used to determine susceptibility of the Campylobacter isolates to eight antimicrobial agents: ampicillin, azithromycin, ciprofloxacin, clindamycin, erythromycin, gentamicin, nalidixic acid, and tetracycline (all purchased from Sigma Chemical Co., St. Louis, Mo, USA). The minimum inhibitory concentrations (MICs) were determined as previously described (Wei, Cha, et al., 2014; Wei, Huang, et al., 2014). The final inoculum on the agar was approximately 1.0 × 104 CFU per spot. The breakpoints were determined according to National Antimicrobial Resistance Monitoring System (NARMS, 2010). As no ampicillin breakpoints are available for Campylobacter, we used the breakpoints for Enterobacteriaceae from the Clinical and Laboratory Standards Institute criteria (CLSI, 2011). The C. jejuni ATCC 33560 was used as the quality control strain. The MIC50 and MIC90 values represent the MIC value at which ≥50%/90% of the isolates in a test population are inhibited (De Melo, Figueiredo, & Ferreira-Carvalho, 2003). The multiple antibiotics resistance (MAR) index of each strain was calculated and interpreted according to the formula: a/b, a is the number of antibiotics to which a particular isolate was resistant and b is the total number of antibiotics tested (Paul, Bezbaruah, Roy, & Ghosh, 1997).

Table 1 Prevalence and distribution of Campylobacter species isolated from retail chicken and duck meat. Poultry meat

No. of samples

Source

Sample type

Chicken

Whole body Breast Subtotal Whole body Slice Subtotal

Duck

Total a

48 32 80 52 54 106 186

Numbers in parentheses indicate the percentages.

Positivea

31 16 47 52 50 102 149

(64.6) (50.0) (58.8) (100.0) (92.6) (96.2) (80.1)

Distribution of Campylobacter isolatesa C. jejuni

C. coli

Campylobacter. spp

27 15 42 39 43 82 124

4 1 5 13 6 19 24

0 0 0 0 1 (1.9) 1 (0.9) 1 (0.5)

(56.3) (46.9) (52.5) (75.0) (79.6) (77.4) (66.7)

(8.3) (3.1) (6.3) (25.0) (11.1) (17.9) (12.9)

B. Wei et al. / Food Control 62 (2016) 63–68

2.4. Statistical analysis

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from the super market (Table 2) were purchased to investigate. Thirty-three isolates (91.7%) of Campylobacter were isolated from traditional markets, 36 (100%) from wholesale markets, and 57 (83.8%) from supermarkets, whereas the isolation rate (50.0%) of online stores was significantly (p < 0.01) lower than that from the traditional markets, wholesale markets, and supermarkets. Our choice to collect chicken and duck meat samples in different sampling stores allowed us not only to increase the variability of meat origin, but also to obtain a more realistic picture of the level of exposure of the consumers. In this study, the retail meat from the company storage warehouse was delivered to the traditional markets, wholesale markets, and supermarkets by a refrigerated car, and the retail meat was directly got from refrigerated cabinet in these markets. The retail meat purchased online was directly delivered to the laboratory from the company storage. Our results showed the isolation rate of Campylobacter was lower from online stores than supermarkets, wholesale markets and traditional markets. Previous studies showed that the inappropriate handing, storage, processing would alter the recovery of Campylobacter from poultry meat (Humphrey, O’Brien, & Madsen, 2007). From our result might suggest that the post–slaughter process would affect the Campylobacter recovery. To ensure complete coverage of all brands of poultry meat sold in Jeonlado, the poultry meat was sourced from several companies. So the initial contamination level of poultry meat might be various from different companies post slaughter, and the temperature control and hygienic management in the company’ storage warehouse or during the processing might be various. Although our antecedent study showed the lower prevalence of Campylobacter in online shopping than the traditional stores (traditional market, wholesale market and super market), further investigation of poultry products from the same company and different market types or delivery system is required. Currently, purchasing through the internet is the most rapidly growing form of shopping due to the advantages of convenience and time-saving, low search costs, better product selection and lower prices (Jones & Vijayasarathy, 1998). Online shopping has become a major shopping mode worldwide; particularly among younger generations who currently and will likely continue to comprise the main consumer group (Hernandez, Jimenez, & Martin, 2011). While the internet shopping with the property that not only could distribute contaminated products in a limit geographic area, but also to extensive areas within a short time. The first outbreak of a foodborne disease associated with online shopping was reported recently (Wei, Huang, et al., 2014). Food safety is the limiting factor to online shopping, with the challenging requirement of necessary information. This is the first time that the prevalence of Campylobacter has been investigated in poultry meat from online vendors.

Significant differences between the Campylobacter isolation rates were analyzed using the chi-Square test. A p < 0.05 was considered significant. 3. Results and discussion 3.1. Prevalence of Campylobacter in poultry meat Overall, a total of 149 Campylobacter spp was isolated from 186 samples. The result demonstrated a high prevalence of Campylobacter in retail poultry meat with the isolation rate of 80.1% (Table 1). There were 102 isolates from retail duck meat with an isolation rate of 96.2%, which was significantly higher (p < 0.05) than the isolation rate of 58.8% from chicken meat (47/80 isolates). The most prevalent Campylobacter species isolated from meat samples was C. jejuni (66.7%), following with C. coli (12.9%) and 1 isolate of unidentified species in poultry meat. Our results show a slightly lower isolation rate than the previous reports in South Korea may be the fact that our sampling period was on the cold season while the contamination rate of Campylobacter in chicken meat was low at this time (Boysen, Vigre, & Rosenquist, 2011; Kang et al., 2006). Unexpectedly, we found that the contamination rate was significantly higher in duck meat than chicken meat (p < 0.05), while the same or less contamination level than reported previously (Little, Richardson, Owen, de Pinna, & Threlfall, 2008; Whyte et al., 2004). Campylobacter contaminated in duck meat was less frequent in the US (12.5%), UK (50.7%) and Ireland (45.8%) (Little et al., 2008; McCrea et al., 2006; Whyte et al., 2004). The high prevalence of Campylobacter isolated from duck meat in this study may be due to the high prevalence in duck farm in South Korea (Wei, Cha, et al., 2014; Wei, Huang, et al., 2014), as well as the correlation between high intestinal concentration in the live birds and the carcasses (Rosenquist, Sommer, Nielsen, & Christensen, 2006). Another possible reason may be the effect of more careful attention dedicated in recent years to preserve retail chicken meat from further contamination from slaughter to consumers, while retail duck meat has not. Furthermore, Campylobacter cells located inside the feather follicles, while the thickness of duck skin was more than chicken and large number of live Campylobacter cells accessed and survived in the deeper layers of skin (Lee, Smith, & Coloe, 1998). Little et al. (2008) reported that the duck meat exhibited higher contamination level of Salmonella than chicken meat. In consequence, higher contamination level in duck highlighted the issue that more attention on the meat preparation in raising consumer awareness of the correct handling of duck meat to avoid cross-contamination in the kitchen. 3.2. Prevalence of Campylobacter in different sampling stores

3.3. Antibiotic resistance rates of Campylobacter isolates from poultry meat

Forty-six poultry meat samples including 29 samples of chicken and 17 retail duck meat from internet store, 36 samples from the traditional market, 36 samples from the wholesale store and 68

The antimicrobial resistance of Campylobacter isolates was determined in 148 of the 149 isolates obtained for C. jejuni and C. coli.

Table 2 Prevalence of Campylobacter isolated from the traditional stores and online stores. Source of samples

Traditional storea Traditional market

Chicken Duck Total a b

9/12 (75.0) 24/24 (100.0) 33/36 (91.7)

Number in parentheses indicate the percentages. –indicates no test.

Online storea Wholesale market b

– 36/36 (100.0) 36/36 (100.0)

Super market 28/39 (71.8) 29/29 (100.0) 57/68 (83.8)

10/29 (34.5) 13/17 (76.5) 23/46 (50.0)

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The results were presented in Table 3. Resistance to tetracycline was the most common (98.0%), followed by nalidixic acid (94.1%) and ciprofloxacin (90.1%) for Campylobacter isolates from duck, resistance to nalidixic (91.5%) acid and ciprofloxacin (83.0) was most common for chicken isolates. The MIC50 values of ciprofloxacin, nalidixic acid and tetracycline were higher than the limit for resistant criteria in both, the chicken and duck isolates. As reported from previous studies in South Korea and other countries, the majority of Campylobacter from poultry meat were resistant to fluoroquinolones and tetracycline (Engberg, Aarestrup, Taylor, GernerSmidt, & Nachamkin, 2001; Kim et al., 2010). The widespread use of antibiotics as supplements for disease prophylaxis and growth promotion has promoted the selection of antimicrobial-resistant bacterial strains at the farm level during poultry production. The resistance to fluoroquinolones and macrolides is alarming, as they are the drugs of choice for treating human campylobacteriosis (Luangtongkum et al., 2009). In addition the high resistance to tetracycline should be emphasized, as it represents a second-line therapeutic agent in human campylobacteriosis therapy. Our findings are of great concern considering that poultry are the major source of human Campylobacter infections and antimicrobial resistant strains can be easily transmitted to humans via the food chain, potentially increasing the campylobacteriosis burden. It is worth noting that the Campylobacter isolates from duck showed higher resistant rate than chicken isolates in ampicillin, ciprofloxacin, gentamicin, nalidixic acid and tetracycline. The longer feeding period in ducks (6–7 weeks) than chickens (4–5 weeks) would be a reason of the higher resistant rate of Campylobacter isolated from duck than chicken by prolonged selection pressure of antibiotics. And the long feeding period also increased the risk of the antibiotics resistant strain got the dominant status than the sensitive strain (Luangtongkum et al., 2008; Luo et al., 2005). Additionally, the earlier contaminated with Campylobacter in duck comparing with chicken would reinforce threaten of antibiotics resistant Campylobacter isolated from ducks (Kasrazadeh & Genigeorgis, 1987; Luangtongkum et al., 2008). In our study, the MIC90 values for gentamicin were same as the resistance criterion for the Campylobacter isolates from chicken, while it was higher than the resistance criterion from duck. This is different from previous reports that the prevalence of gentamicinresistant Campylobacter is generally low and that the MIC50 and MIC90 values are lower than the breakpoint (Bywater et al., 2004; Torralbo et al., 2015). However, recent studies suggested that the

prevalence of gentamicin-resistant Campylobacter is increasing and there is a high prevalence of gentamicin-resistant Campylobacter isolated in food-producing animals in China (Chen et al., 2010). Intravenous aminoglycoside (gentamicin) therapy is also considered to treat more serious cases of Campylobacter infections, such as bacteremia. Although cases of systemic campylobacteriosis are rare, the clinical consequences can be severe and lead to death. Therefore, assessing and monitoring aminoglycoside and other antimicrobial resistance of Campylobacter spp. in the main reservoir species is needed to protect public health. Drug resistance, especially multi-drug resistance, is a large and growing problem. The antimicrobial resistance profile and MAR index of C. jejuni and C. coli were showed in Table 4. All of the C. jejuni and C. coli isolates from poultry meat were resistant to at least one antimicrobial agent. The C. jejuni isolates had 23 different antimicrobial resistant profiles, while C. coli isolates exhibited 7 different profiles. The MAR index for isolated Campylobacter was very high in our research suggestive of public health implications. One C. jejuni isolate from duck meat showed the highest MAR index of 1 that resistant to all 8 antimicrobial agents. The most common resistant pattern both in C. jejuni and C. coli was Amp/Cip/Nal/Tet with MAR index of 0.5 for more than 40% of the isolates. The most frequent resistance pattern is similarly found in human origin Campylobacter in South Korea, suggestive that both chicken and duck Campylobacter could be an important source of human infection (Ku et al., 2011). Furthermore, resistant Campylobacter could enhance the invasiveness in human epithelium and manifest higher cytotoxicity than susceptible strains (Zeitouni, Guyard-Nicodeme, & Kempf, 2013). Our results update and provide novel data on the antimicrobial resistance of Campylobacter from chicken and duck meat in South Korea. We revealed the occurrence of high resistance to several antimicrobials, particularly key drugs for treating human campylobacteriosis, representing a potential public health risk. 4. Conclusion In conclusion, we report a high prevalence of contamination in chicken and duck meat. Our results also demonstrate that the contamination rates in food sold by online stores were lower than those of traditional stores. All tested strains expressed resistance to at least one of eight antimicrobials tested, and many isolates were multi-drug resistant. These results suggest the need to strengthen

Table 3 Numbers and percentages of antibiotic resistance in Campylobacter jejuni and C. coli isolated from duck and chicken meat. Antimicrobial agent

Range (μg/ml)

Source

C. jejuni

C. coli

Total

Breakpoint (μg/ml)

Ampicillin

0.03–256

32

Azithromycin

0.03–128

8

Ciprofloxacin

0.03–128

4

Clindamycin

0.03–128

8

Erythromycin

0.03–128

32

Gentamicin

0.03–128

8

Nalidixic acid

4–256

64

Tetracycline

0.03–256

16

Chicken Duck Chicken Duck Chicken Duck Chicken Duck Chicken Duck Chicken Duck Chicken Duck Chicken Duck

MIC50 /MIC90 (μg/ml)

Resistant no. (%)

MIC50 /MIC90 (μg/ml)

Resistant no. (%)

MIC50 /MIC90 (μg/ml)

Resistant no. (%)

32/128 64/128 0.25/16 0.06/1 16/32 16/32 0.13/0.5 0.13/0.5 1/64 0.5/8 1/8 0.25/8 128/>256 128/>256 64/>256 128/>256

22 57 8 5 35 72 2 1 7 4 5 11 39 76 22 80

256/256 128/256 0.06/0.13 0.13/2 32/64 8/32 0.13/0.25 0.13/2 4/4 0.25/16 0.25/8 0.5/64 >256/>256 128/>256 >256/>256 256/>256

5 (100.0) 13 (68.4) 0 1 (0.211) 4 (80.0) 19 (100.0) 0 0 0 2 (26.3) 0 4 (21.1) 4 (80.0) 19 (100.0) 5 (100.0) 19 (100.0)

32/256 64/128 0.25/16 0.06/1 16/32 16/32 0.13/5 0.13/0.5 1/64 0.5/8 0.5/8 0.25/32 256/>256 128/>256 128/>256 128/>256

27 70 8 6 39 91 2 1 7 6 5 15 43 95 27 99

(52.4) (69.5) (19.0) (0.061) (83.3) (87.8) (4.8) (1.2) (16.7) (4.9) (11.9) (13.4) (92.9) (92.7) (52.4) (97.6)

(57.4) (69.3) (17.0) (5.9) (83.0) (90.1) (4.3) (1.0) (14.9) (5.9) (10.6) (14.9) (91.5) (94.1) (57.4) (98.0)

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Table 4 Antimicrobial resistant profile and multiple antibiotic resistance (MAR) index of the Campylobacter jejuni and C. coli isolates. Species

Antimicrobial resistant profiles

MAR index

No. of isolates

Rate (%)

C. jejuni

Amp Nal Tet Azi/Nal Cip/Nal Nal/Tet Amp/Cip/Nal Amp/Cip/Tet Amp/Nal/Tet Cip//Nal/Tet Cip/Gen/Nal Cip/Gen/Tet Cip/Nal/Tet Amp/Cip/Nal/Tet Azi/Cip/Ery/Nal Cip/Gen/Nal/Tet Amp/Cip/Gen/Nal/Tet Azi/Cip/Ery/Gen/Nal Amp/Azi/Cip/Ery/Nal/Tet Amp/Azi/Cip/Gen/Nal/Tet Amp/Azi/Cip/Cli/Ery/Nal/Tet Amp/Azi/Cip/Ery/Gen/Nal/Tet Amp/Azi/Cip/Cli/Ery/Gen/Nal/Tet Amp/Tet Cip/Nal/Tet Amp/Cip/Nal/Tet Amp/Azi/Cip/Nal/Tet Amp/Cip/Ery/Nal/Tet Amp/Cip/Gen/Nal/Tet Amp/Cip/Ery/Gen/Nal/Tet

0.13 0.13 0.13 0.25 0.25 0.25 0.38 0.38 0.38 0.38 0.38 0.38 0.38 0.5 0.5 0.5 0.63 0.63 0.75 0.75 0.88 0.88 1 0.25 0.38 0.5 0.63 0.63 0.63 0.75

3 3 4 1 3 2 5 1 4 3 3 1 20 52 3 1 6 1 2 1 2 2 1 1 6 11 1 1 3 1

2.4 2.4 3.2 0.8 2.4 1.6 4.0 0.8 3.2 2.4 2.4 0.8 16.1 41.9 2.4 0.8 4.8 0.8 1.6 0.8 1.6 1.6 0.8 4.2 25.0 45.8 4.2 4.2 12.5 4.2

C. coli

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