Abstract
Campylobacter, Salmonella, and Listeria monocytogenes are important bacterial pathogens associated with gastroenteritis. The consumption of poultry meat and their products is considered as a major and leading source of human infection. While surveys of chicken meat and products, and its association with foodborne pathogens are widely available, such information on ducks is scarce. This survey examines the prevalence and antibiotic resistance of Campylobacter, Salmonella and L. monocytogenes isolated from ducks. Data obtained from key surveys are summarized. The observed prevalence of these pathogens and their resistance to various antibiotics varies from one study to the other. The mean prevalence (and range means from individual surveys) are duck 53.0% (0.0–83.3%), duck meat and parts 31.6% (12.5–45.8%), and duck rearing and processing environment 94.4% (92.0–96.7%) for Campylobacter spp. For Salmonella spp., the mean prevalence data are duck 19.9% (3.3–56.9%), duck meat and parts 28.4% (4.4–75.6%), duck egg, shell, and content 17.5% (0–4.17%), and duck rearing and processing environment 32.5% (10.5–82.6%). Studies on the prevalence and antibiotic resistance of L. monocytogenes in ducks are by far very rare compared to Campylobacter and Salmonella, although ducks have been noted to be a potential source for these foodborne pathogens. From our survey, ducks were more frequently contaminated with Campylobacter than Salmonella. Campylobacter and Salmonella spp. also exhibited varying resistance to multiple antibiotics.
Introduction
Continued development of resistance of these foodborne pathogens to multiple antibiotics aggravates the treating of patients infected with campylobacteriosis, salmonellosis, and listeriosis when treatment is warranted. Although numerous potential vehicles for transmission exist, the role of poultry is considered to be significant in the transmission of infections (Miller and Pegues, 2000; Adzitey and Huda, 2010; Adzitey and Nurul, 2011). The consumption of contaminated poultry meat and products, handling of contaminated raw poultry meat, and cross-contamination to other foods have been implicated in most cases (Frederick and Huda, 2011; Todd and Notermans, 2011).
Duck meat and eggs are comparable to that of chicken and can be an alternative source of protein and other nutrients for humans (Adzitey et al., 2012a). Duck is high in protein, iron, selenium, and niacin, and lower in calories compared to many cuts of beef (Anonymous, 2011a). Duck meat and products are relished and consumed by many, especially people from the Far East. With recommendations for the reduction of red meat intake due to its association with cardiovascular pathologies, the consumption of white meats, including duck meat, is gaining more attention (Witak, 2008). Nonetheless, the consumption of contaminated duck meat or products like chicken also pose a risk of contracting foodborne diseases, which has been given trivial attention in terms of epidemiological studies. For instance, the consumption of duck meat, eggs, and products has been implicated in outbreaks of Salmonellosis (MMWR, 2000; Clarke, 2010; FSA, 2010). An outbreak of Salmonella Typhimurium DT8 associated with duck eggs and products was responsible for the hospitalization of two people and the death of one (Clarke, 2010). Contact with young birds, including ducklings in a nursery school, has also been linked to outbreaks of Salmonella infection (CDR, 2010; Merritt and Herlihy, 2003). This review reports on the prevalence and antimicrobial resistance of Campylobacter, Salmonella, and L. monocytogenes in ducks.
Methods
We searched for articles that described the prevalence and antibiotic resistance of Campylobacter, Salmonella, and L. monocytogenes in ducks using the keywords ‘‘Campylobacter and duck,’’ ‘‘Salmonella and duck,’’ and ‘‘L. monocytogenes and ducks.’’ Databases including Scopus, Science Direct, Wiley, PudMed, and Springer provided by Universiti Sains Malaysia Library were used. We also used Google Scholar to search for the prevalence and antibiotic resistance of Campylobacter, Salmonella, and L. monocytogenes in ducks. The searches revealed that far less work has been published on the prevalence and antibiotic resistance of Campylobacter, Salmonella, and L. monocytogenes in ducks as compared to poultry. The articles used were publications from 1990 to date. Samples positive for Campylobacter and Salmonella spp. were grouped into duck (cloaca, caeca, feces, intestines, organs, hens, ducklings); duck meat and parts (carcass, carcass rinse, retail duck meat, heart, liver, gizzard, spleen); egg, shell, and content (egg shell, egg content, yolk sac, dead embryos); and rearing and processing environment (duck farm, hatchery, pond, wash water, soil, floor, transport crate, feed, drinking water, table). Samples positive for L. monocytogenes were discussed as published by individual articles due to the limited number of published data in this area.
Prevalence and Antibiotic Resistance of Campylobacter in Ducks
The prevalence of Campylobacter spp. (Table 1) among different surveys was highly variable. The prevalence ranged from 0.0% to as high as 96.7%. Higher prevalence of ≥80% was reported by countries such as the United Kingdom, Taiwan, and Tanzania. In the United Kingdom, a higher prevalence of Campylobacter spp. in chickens (83–83.3%) has been reported (Kramer et al., 2000; Jørgensen et al., 2002). Another study in the United Kingdom comparing the prevalence of Campylobacter in various poultry species indicated that chicken showed the highest contamination (60.9%), followed by duck (50.7%), turkey (33.7%), and other poultry meat (34.2%) (Little et al., 2008). In this survey, the rearing and processing environment (92%, 96.7%) was the most contaminated source, followed by duck. The high environmental contamination rates may contribute to meat contamination. Duck meat and parts were the least contaminated source. Duck meat and parts from the United Kingdom (45.4%) and Ireland (45.8%) had similar contamination rates. Campylobacter spp. were not isolated from duck samples examined in Ghana, although it was positive for other Africa countries such as Egypt (19.0%), Nigeria (63.5%), and Tanzania (80%). In Asia (Iran, Malaysia, and Taiwan), the prevalence of Campylobacter spp. ranged from 35.5% to 92%. The United States recorded lower a prevalence of 12.5% and 33.0% for ducks and duck meat and parts, respectively (McCrea et al., 2006).
Campylobacter jejuni was the predominant Campylobacter species in most of the studies, similar to what has been reported in humans, poultry, and other farm animals (Kramer et al., 2000; Jørgensen et al., 2002; Whyte et al., 2004). In one study, C. coli (87.5%) was predominant over C. jejuni (12.5%) (Little et al., 2008). Another study reported equal isolation of C. jejuni (30%) and C. coli (30%), but higher rates for C. upsaliensis (40%) (Ridsdale et al., 1999). The detection of Campylobacter spp. from duck meat and intestines using polymerase chain reaction (31%; 34 C. jejuni and 10 C. coli) was higher than the standard culture method (20%; 21 C. jejuni and seven C. coli) (Boonmar et al., 2007). Three C. jejuni and five C. coli strains were isolated from a total of 135 duck and chicken samples (Magistrado et al., 2001). Isolation of Campylobacters in ducklings (<2 weeks) is significantly lower (p<0.05) than other age groups (>2 weeks) (Tsai and Hsiang, 2004). Nonga and Muhaira (2000) also confirmed that the prevalence of Campylobacter in adult ducks (91.3%) was significantly (p<0.05) higher than ducklings (68.2%).
Antibiotic resistance of Campylobacter spp. isolated from ducks is shown in Table 2. Both C. jejuni and C. coli strains were susceptible (100%) to furazolidone. Similarly, 100% of C. jejuni isolates were susceptible to amikacin, doxycycline, and kanamycin, while C. coli isolates were susceptible to chloramphenicol, enrofloxacin, and gentamicin. Lower resistance (<10%) of C. jejuni isolates to gentamicin (7.8%), apramycin (7.6%), chloramphenicol (2.3%), and neomycin (2.2%) was observed. Campylobacter jejuni isolates were highly resistant to josamicin/trimethoprim (93.5%), ofloxacin (91.3%), sulfamethoxazole/trimethoprim (90.9%), polymyxin B (89.1%), and florfenicol (88%). All C. coli strains were resistant to norfloxacin (100%) and cephalothin (100%), while lower resistance (<10%) was observed for neomycin (9%), kanamycin (9%), cefotaxime (5%), and streptomycin (2.5%). Resistance to quinolones (nalidixic acid and ciprofloxacin) and macrolides (erythromycin) was more frequent in C. coli than in C. jejuni isolates (Little et al., 2008; Rahimi et al., 2011). Campylobacter isolates from ducks were more susceptible to macrolides than fluoroquinolones. Macrolides and fluoroquinolones are the drug of choice for treating campylobacteriosis when treatment is necessary (Clark, 2011). Therefore, resistance of duck Campylobacter isolates to these antimicrobial agents is a threat to public health. All studies examined the response of Campylobacter spp. to ciprofloxacin and tetracycline, indicating the importance of these antibiotics in the duck industry. Although multiple antibiotic resistance occurred, none of the isolates were 100% resistant to a particular antibiotic. We found from our survey that more studies reported on the antibiotic resistance of C. jejuni, compared to C. coli, probably because C. jejuni alone is responsible for about 90% of all cases of campylobacteriosis.
—, not done; Sxt, sSulfamethoxazole/trimethoprim; JT, jJosamicin/trimethoprim.
Prevalence and Antibiotic Resistance of Salmonella in Ducks
The average prevalence of Salmonella contamination was highest for duck rearing and processing environment (32.5%), followed by duck meat and parts (28.4%) and duck (19.9%) (Table 3). Duck egg, shell, and content (17.5%) recorded the lowest contamination rate. The high prevalence recorded for duck rearing and processing environment could be attributed to the fact that less attention is paid to biosecurity, standard and hygienic methods of rearing duck, and processing duck meat and products compared to poultry. This is probably reflected in the relatively high prevalence that occurred for duck meat and parts. Individual surveys also differed in the prevalence rate (Table 3). The highest prevalence rate of 82.6% was found in duck rearing and processing environment in Brazil. This was followed by duck meat and parts (75.6%), duck (56.9%), and duck egg, shell, and content (47.1%) from the same country. From this survey, it is quite obvious that ducks from Brazil were the most contaminated source of Salmonella, followed by ducks from the United Kingdom. Ducks from the United States recorded the lowest contamination rate. Different countries also reported different serovars to be the predominant Salmonella serovar. For instance, S. Typhimirium (26.7%), S. Potsdam (31.9%), and S. Saintpaul (29.8%) were reported to be the predominant Salmonella serovars by Pan et al. (2010) in China, by Tsai and Hsiang (2004) in Taiwan, and by Ribeiro et al. (2004) in Brazil, respectively. S. Typhimirium was commonly isolated from ducks from all the countries except Vietnam and Egypt. Three studies reported the presence of poultry host adapted Salmonella serovar S. Gallinarum and S. Pullorum in ducks (Hofer et al., 1997; Pan et al., 2010; Adzitey et al., 2012a). The isolation rate of Salmonella spp. in ducklings under 2 weeks of age was significantly higher (p<0.05) than the other age groups (>2 weeks old) (Tsai and Hsiang, 2004). Little et al. (2008) compared the prevalence of Salmonella spp. in some poultry species and found that duck had the highest contamination (29.9%), compared with chicken (5.6%), turkey (5.6%), and other poultry meat (8.6%).
The antibiotic resistance of Salmonella serovars obtained from five different surveys is presented in Table 4. The prevalence of resistance varied according to study, type of sample examined, and country involved. However, some findings were consistent with other studies. For example, no resistance to ceftriaxone was detected, while resistance to naladixic acid was 53.3% and 53.9% in two different studies, which was consistent with each other (Pan et al., 2010; Adzitey et al., 2012a). Resistance of Salmonella spp. to erythromycin (a macrolide) was 100%. Conversely, 100% susceptibility to ceftriaxone, kanamycin, ciprofloxacin (fluoroquinolone), ofloxacin, and polymyxin B was observed. According to this survey, these five antibiotics can be the drug of choice for treating Salmonella infections emanating from ducks. Lower resistance (≤5%) also occurred for norfloxacin, cephalexin, apramycin, florfenicol, oxolinic acid, cefotaxime, and cephalothin. Relatively high resistances occurred for augmentin (86.9%), tetracycline (70.6%), amoxicillin (43.5%), josamicin/trimethoprim (38.5%), nalidixic acid (38.3%), carbenicillin (33.3%), doxycycline (30.7%), sulfamethoxazole/trimethoprim (30.3%), sulphonamides (26.2%), streptomycin (24.0%), and sulfafurazole (20.0%). Pan et al. (2010) reported that Salmonella isolates from chickens displayed highest resistance, being resistant to at least one antimicrobial agent (100%), followed by those recovered from pigs (93.4%), goose (90.7%), and duck (80%). Salmonella isolates from turkey exhibited higher rates of multiple drug resistance (55.6%) than isolates from chicken (20.9%) and duck (13.6%) (Little et al., 2008).
—, not done.
Prevalence and Antibiotic Resistance of L. monocytogenes in Ducks
Previous studies of the association between L. monocytogenes and ducks are limited. In Bulgaria, Chipilev et al. (2010) examined duck breast and liver during gavaging, plant processing, and vacuum packing for Listeria spp. and reported a prevalence of 3.0%, 2.5%, 0.4%, and 0.0% for L. monocytogenes, L. innocua, L. grayi, and L. ivanovii, respectively. They also reported contamination of Listeria spp. for gavaged ducks was 6.8%, for feeds 17.6%, for positive swabs after slaughtering ducks 4.3%, and after vacuum packing 6.4%. The majority of the L. monocytogenes isolated from this study belonged to the serogroup II (12 duck and two feed samples), and two of the isolates belonged to serogroup I. In another study in Bulgaria, Karakolev et al. (2003) reported that 4.8% and 4.9% of frozen duck fillet and liver, respectively, were contaminated with L. monocytogenes. In Malaysia, a comparison of media for isolating Listeria spp. from naturally contaminated ducks indicated a prevalence of 39.8% (that is, of the 128 samples, 51 positives were observed on Palcam agar plates and 44 positives on Agar Listeria according to Ottaviani and Agosti (ALOA) plates) (Adzitey et al., 2011b). Nonetheless, a study by Njagi et al. (2003) in Kenya reported that no L. monocytogenes was isolated from cloacal and pharyngeal swabs taken from healthy indigenous ducks. Anonymous (2011b) reported that listeriosis in birds is rare, but chickens, turkeys, geese, ducks, canaries, and parrots appear to be the most commonly affected avian species. A study on the influence of different cooked meat juices—including beef, pork, lamb, chicken, and duck—to determine the ability of L. monocytogenes to attach or stick to stainless steel surfaces at different temperature indicated that cooked duck juices at 25°C promoted the highest levels of Listeria attachment (Anonymous, 2011c). They also reported that food poisoning bacteria prefer duck to beef on meat factory surfaces (Anonymous, 2011c). Unpublished data on the isolation of L. monocytogenes from ducks in Malaysia indicates the presence of this foodborne pathogen in duck intestines, feces, wash water (water used for washing carcasses), and soil samples collected from duck farms. These studies suggest that ducks are potential sources for this foodborne pathogen and that L. monocytogenes perhaps can persist longer in duck and duck-associated samples.
According to our survey, there is a very limited study on the prevalence of L. monocytogenes in ducks and no published literature on the response of duck L. monocytogenes isolates to antibiotics. We demonstrate interestingly that ducks and duck-related samples are potential sources for this foodborne pathogen, and studies to investigate this are warranted.
Conclusion
Few published studies have reported on the prevalence and antibiotic resistance of Campylobacter, Salmonella and Listeria spp. in ducks compared to poultry. The overall prevalence of Campylobacter and Salmonella spp. was 51.3% (range, 0.0–96.7%) and 24.3% (range, 0.0–82.6%), respectively. Risk factors for human Campylobacter, Salmonella, and L. monocytogenes infection therefore include the consumption of contaminated duck meat, and from handling of contaminated raw duck meat or products and cross-contamination to other ready-to-eat product. Duck farming and processing environments also pose the risk of Campylobacter, Salmonella, and L. monocytogenes infection. Adequate and proper cooking is recommended to kill all cells of these foodborne pathogens to reduce hazards in acquiring infections. Rapid increase in the incidence of antibiotic resistance and the emergence of multi-resistant strains of bacteria is an alarming problem worldwide. This has been attributed to the use of drugs and chemicals containing antibiotics in the treatment of humans, animals, or feed supplements and growth promoters in farm animals. The information obtained from this survey can serve as baseline information to monitor trends in the prevalence and resistance of Campylobacter, Salmonella, and Listeria spp. in ducks in the future. It also provides epidemiological data for duck producers, processers, and all stakeholders in public health and safety.
Footnotes
Acknowledgments
We are grateful to the Institute of Postgraduate Studies, Universti Sains Malaysia, for the support given in running research in the field of food safety. The first author is also a USM fellowship holder.
Disclosure Statement
No competing financial interests exist.
