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J APPL POULT RES 2008. 17:490-497. doi:10.3382/japr.2008-00051
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Research Reports

Antibacterial Effect of Trans-Cinnamaldehyde on Salmonella Enteritidis and Campylobacter jejuni in Chicken Drinking Water1,2

A. Kollanoor Johny*, M. J. Darre*, T. A. Hoagland*, D. T. Schreiber*, A. M. Donoghue{dagger}, D. J. Donoghue{ddagger} and K. Venkitanarayanan*,3

* Department of Animal Science, University of Connecticut, Storrs 06269; {dagger} PPPSRU, ARS, USDA, Fayetteville, AR 72701; and {ddagger} Center for Excellence in Poultry Science, University of Arkansas, Fayetteville 72701

3 Corresponding author: kumar.venkitanarayanan{at}uconn.edu


   SUMMARY
TOP
 SUMMARY
DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Salmonella Enteritidis and Campylobacter jejuni are 2 major foodborne pathogens in the United States, estimated to cause more than 3 million cases of human illness annually. Chickens are the natural hosts of these bacteria, and their drinking water can be a source of S. Enteritidis and C. jejuni, contributing to the colonization of birds. In this study, trans-cinnamaldehyde (TC), a natural, generally recognized as safe ingredient in cinnamon oil was evaluated for its efficacy to inactivate S. Enteritidis and C. jejuni in the drinking water of chickens. Well water containing 0, 0.016, 0.03, and 0.06% TC was inoculated with a 5-strain mixture of S. Enteritidis or C. jejuni (~6 log10 cells/mL). Water samples containing 1% chicken feces or feed were also included. The samples were incubated at 12.5 or 25°C for 7 d and analyzed for bacterial populations on d 0, 1, 3, 5, and 7. Duplicate samples of treatments and control were included, and the study was replicated 3 times. Trans-cinnamaldehyde at 0.06% inactivated Salmonella completely after 24 h in water with 1% feces at both temperatures. In water containing 1% feed, TC (0.06%) reduced S. Enteritidis to undetectable levels after 3 d at 12.5°C or 7 d at 25°C. Presence of feed or feces in water reduced the antibacterial effect (P < 0.001) of TC. The effect of TC on C. jejuni was more pronounced than that on S. Enteritidis. The TC at 0.06% completely inactivated the pathogen after 1 d of incubation at both temperatures. The presence of feces or feed did not have any effect (P > 0.001) on the antibacterial property of TC on C. jejuni. Results indicate that TC is effective in killing S. Enteritidis and C. jejuni in chicken drinking water and may decrease the likelihood that water will contribute to colonization of chickens by these pathogens.

Key Words: Salmonella • Campylobacter • chicken drinking water • trans-cinnamaldehyde


   DESCRIPTION OF PROBLEM
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Poultry meat and eggs constitute a vital part of the American diet, and their annual per capita consumption has steadily increased during the last decade [1]. The microbiological safety of these foods is a major concern to the government, poultry industry, and consumers because of the potential impact on public health and the economy. Among the foodborne pathogens transmitted through poultry products, Salmonella and Campylobacter are the most common infectious agents causing disease in humans [2, 3]. Annually more than 1.4 million cases of non-typhoid salmonellosis and 2.4 million cases of Campylobacter jejuni are estimated to occur in the United States [4]. The costs of poultry-associated cases of salmonellosis and campylobacteriosis in the country range from $64 million to 114.5 million, and $362 million to 699 million, respectively [5].

The primary colonization site of Salmonella Enteritidis and C. jejuni in chicken is the cecum and cecal carriage of these pathogens, resulting in horizontal transmission, contamination of eggshells with feces, and carcass contamination during slaughter [6]. It is also known that cecal colonization of birds with S. Enteritidis can result in the contamination of egg (yolk, albumen, shell membranes) by the transovarian route [7, 8]. Reducing the colonization of S. Enteritidis and C. jejuni in the chicken intestinal tract could reduce contamination of poultry meat and eggs with these pathogens. Therefore, practical and safe approaches for reducing colonization of birds with S. Enteritidis and C. jejuni are critical to improve the microbiological safety of poultry products.

Drinking water can be a major source of Salmonella for chickens [9–15]. Salmonellae were isolated from 12.3% of the water samples in poultry farms surveyed in Canada [16]. In another study, Sterski and coworkers [17] suggested that birds might be consuming about 105 salmonellae per mL of drinking water per day and reinfect themselves continually. Similarly, several researchers reported that drinking water serves as a source of C. jejuni for chickens [13, 18–22]. Zimmer and coworkers isolated C. jejuni from nipple waterer supply pipes [23]. Thus, proper disinfection of drinking water is an important on-farm intervention strategy for reducing the colonization of these pathogens in chickens. Although chlorination is commonly used for disinfection of chicken drinking water, it can result in the corrosion of the metal parts in nipple waterers. Additionally, in floor-reared management systems using bell drinkers chlorine is easily neutralized by organic matter [24] such as feed, litter, and feces that routinely get into the drinking water. It was also found that chlorination of chicken drinking water was not very effective in reducing colonization of birds with C. jejuni [13]. Treatment of drinking water with organic acids or acidic feed additives was reported to have minimal beneficial effect in controlling C. jejuni [3]. Therefore, an alternate antimicrobial to chlorine for disinfecting chicken drinking water is necessary.

The use of natural antimicrobial molecules for killing pathogenic microorganisms has received renewed attention due to concerns for toxicity of synthetic chemicals. Plant-derived essential oils represent a group of natural antimicrobials that have been traditionally used to preserve foods as well as enhance food flavor. The antimicrobial properties of several plant-derived essential oils have been demonstrated [25–27], and a variety of active components of these oils have been identified. Trans-cinnam-aldehyde (TC) is a chemical present as a major component of bark extract of cinnamon. It is classified as generally recognized as safe and is approved for use in foods (21 CFR 182.60) by the Food and Drug Administration. Trans-cinnamaldehyde has been reported to possess antimicrobial activity toward a wide range of foodborne pathogens, including gram-positive [28, 29] and gram-negative bacteria [30]. The objective of this study was to determine the potential of TC as an antimicrobial additive to kill S. Enteritidis and C. jejuni in chicken drinking water. Specifically, the antimicrobial effect of TC in water in the presence and absence of 1% chicken feces or 1% feed at 12.5 and 25°C was determined.


   MATERIALS AND METHODS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
Bacterial Cultures
A 5-strain mixture of S. Enteritidis; SE12 (chicken liver, phage type 14b), SE22 (chicken intestine, phage type 8), SE 28 (chicken ovary, phage type 13a), SE31 (chicken gut, phage type 13a), and SE90 (human, phage type 8) or C. jejuni (chicken carcass isolates) was used for the study. For S. Enteritidis, each strain preinduced for resistance to nalidixic acid (NA; 50 µ g/mL) [31] was cultured separately in 10 mL of tryptic soy broth (TSB) [32] supplemented with 50 µ g/mL of NA and incubated at 37°C for 24 h. After 3 successive transfers, equal volumes of the cultures were combined and sedimented by centrifugation (3,600 x g, 15 min at 4°C). The pellet was resuspended in sterile PBS (pH 7.3) and used as the inoculum. The bacterial population of the individual cultures and 5-strain cocktail was estimated by plating 0.1-mL portions of appropriate dilutions on xylose lysine desoxycholate agar (XLD) [32] plates containing NA and incubating at 37°C for 24 h. For culturing C. jejuni, each strain was cultured in 10 mL of Campylobacter enrichment broth [33] and incubated microaerobically (85% N, 10% CO2, 5% O2) at 42°C for 24 h. After 3 successive transfers, the cultures were sedimented by centrifugation (3,600 x g, 15 min at 4°C). The pellet was resuspended in Butterfield’s phosphate diluent (6.8% KH2PO4; pH 7.2) and used as the inoculum. The bacterial counts were estimated by surface plating 0.1-mL portions of appropriate dilutions on campy line agar (CLA) [34] and incubating the plates microaerobically at 42°C for 24 h.

Chicken Drinking Water, Inoculation, and Treatments
Well water was obtained from a local poultry farm, and aliquots of 100 mL each of water were dispensed in 250-mL wide-mouthed sterile plastic containers. Appropriate quantities of TC [31] were added to each water sample to obtain final concentrations of 0.016, 0.03, and 0.06% (wt/vol). Samples without TC (0%) served as controls. In addition, a set of water samples containing poultry feces (1% wt/vol) or feed (1% wt/ vol) were also included to determine the effect of feces/feed on the antimicrobial property of TC. Broiler starter feed and feces were obtained from the University Poultry Farm. Fresh semi-solid fecal samples collected from the battery cage-reared chickens were homogenized to form a composite mixture before use. Each treatment and control water sample was inoculated with 0.1 mL of the 5-strain mixture of S. Enteritidis or C. jejuni to obtain a final pathogen load of approximately 6.0 log10 cells/mL of water. The containers were loosely covered with a plastic lid to enable free passage of air and incubated at 12.5 or 25°C for 7 d. Water samples were analyzed for surviving pathogen populations on d 0, 1, 3, 5, and 7 of storage. Duplicate samples of each treatment and control were included at each of the specified temperatures, and the entire study was replicated 3 times (n = 12; 2 water samples x 2 plate counts x 3 trials).

Enumeration of Bacteria
For S. Enteritidis, the surviving population was enumerated in each water sample by plating 0.1-mL portions of the sample directly or after serial dilutions (1:10 in PBS) on duplicate XLD plates supplemented with 50 µ g/mL of NA (XLD-NA). The plates were incubated at 37°C for 48 h. When S. Enteritidis was not detected by direct plating, samples were tested for surviving cells by enrichment for 24 h at 37°C in 100 mL of TSB supplemented with NA, followed by streaking for isolation on XLD-NA plates. For C. jejuni, on each sampling day, 0.1-mL portions of undiluted or serially diluted water samples were surface plated on duplicate CLA plates, followed by microaerobic incubation at 42°C for 48 h. Enrichment of water for Campylobacter was done in 100 mL of Campylobacter enrichment broth at 42°C for 48 h under microaerophilic conditions followed by streaking on CLA plates.

Statistical Analysis
Each water container served as an experimental unit and a completely randomized 4 x 3 x 2 x 5 factorial design was followed for each pathogen. Factors included 4 treatments (0, 0.016, 0.03, and 0.06% TC), 3 groups (water, water with 1% feces and water with 1% feed), 2 temperatures (12.5 and 25°C), and 5 storage d (0, 1, 3, 5, and 7). Data were analyzed using the PROC MIXED version of the Statistical Analysis Software [35]. Differences among the means were detected at P ≤ 0.001 using the Fisher’s least significance difference test with appropriate corrections for multiple comparisons. Data are presented as means ± SE, where n = 12.


   RESULTS AND DISCUSSION
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 
In the current study, we evaluated the efficacy of TC as an antimicrobial additive for inactivating S. Enteritidis and C. jejuni in chicken drinking water at 12.5 and 25°C because these represent the average tap water temperatures during winter and summer months, respectively. Moreover, the lower and upper limits of the thermoneutral zone in poultry range from 12.7 to 23.8°C [36], and birds may refuse to drink when the water temperature is above 26.6°C [37].

Direct streaking and plating of well water and chicken feces on respective selective agar plates or enrichment in TSB followed by streaking on selective agar plates failed to yield any colonies of S. Enteritidis and C. jejuni, indicating that the water and feces were devoid of any inherent population of NA-sensitive/resistant S. Enteritidis and C. jejuni. The initial pH of the water samples was 6.7. There was negligible difference in the pH of water after the addition of TC.

The effect of TC on S. Enteritidis in chicken drinking water at 12.5°C is depicted in Figure 1Go. In water with no added feed or feces, all the tested concentrations of TC brought about greater than 5.0 log10 colony-forming units (cfu)/mL reduction in S. Enteritidis counts on d 1 of storage, with complete inactivation of the pathogen on d 3 of storage (Figure 1AGo). In control samples devoid of TC, the pathogen population gradually decreased, reaching approximately 2.0 log10 cfu/mL on d 7. In water containing 1% feces, the pathogen was reduced to undetectable levels (6.0 log10 cfu/mL reduction) by 0.06 and 0.03% TC on d 1 and 3, respectively (Figure 1BGo). The lowest concentration of 0.016% TC resulted in approximately 2.0 log10 cfu/mL reduction in pathogen counts on d 7. In control samples, the population of S. Enteritidis remained the same throughout the storage period. In water containing 1% feed, 0.06% TC completely inactivated the pathogen by d 3 of storage. In water samples containing 0.03% TC, there was >3.0 log10 cfu/mL reduction of S. Enteritidis in the 1% feed group on d 7 (Figure 1CGo). There was little change from the initial bacterial counts for the 0.016% TC group on d 7. In control water samples, the pathogen increased in its population by approximately 1.0 log10 cfu/mL by the last day of sampling (Figure 1CGo).


Figure 1
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  		Figure 1. Effect of trans-cinnamaldehyde on Salmonella Enteritidis in chicken drinking water at 12.5°C. A (water), B (water + 1% feces), C (water + 1% feed). Data are presented as means ± SE, n = 12. The error bars represent SE. cfu = colony-forming units.

 
Similar to the results observed at 12.5°C, TC was effective in killing S. Enteritidis in water at 25°C. All the tested TC concentrations completely killed the pathogen on d 1, whereas S. Enteritidis counts in control samples gradually decreased to approximately 1.0 log10 cfu/mL on d 7 (Figure 2Go). In water containing 1% feces, 0.06 and 0.03% TC reduced S. Enteritidis to undetectable levels on d 3, whereas only 1.0 log10 cfu/mL reduction in counts was observed in samples containing 0.016% TC on d 7. However, in control samples the pathogen grew by 2.0 log10 cfu/mL at the end of the storage period (Figure 2BGo). A significantly reduced killing effect of TC (P < 0.001) was observed in water samples containing 1% feed (Figure 2CGo). In all the samples except the 0.06% treatment, the population of S. Enteritidis increased during storage, although the increase in bacterial counts was minimal.


Figure 2
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  		Figure 2. Effect of trans-cinnamaldehyde on Salmonella Enteritidis in chicken drinking water at 25°C. A (water), B (water + 1% feces), C (water + 1% feed). Data are presented as means ± SE, n = 12. The error bars represent SE. cfu = colony-forming units.

 
As observed with S. Enteritidis, TC was effective in killing C. jejuni in chicken drinking water at both storage temperatures (Figures 3Go and 4Go). All the tested concentrations of TC reduced C. jejuni counts to undetectable levels within the first 3 d of storage. In control samples devoid of TC, the pathogen population decreased gradually and all the water samples yielded countable populations of C. jejuni until the last day of storage. The only exception to this was water stored at 25°C, where the bacterium was undetectable on d 7 (Figure 4AGo).


Figure 3
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  		Figure 3. Effect of trans-cinnamaldehyde on Campy-lobacter jejuni in chicken drinking at 12.5°C. A (water), B (water + 1% feces), C (water + 1% feed). Data are presented as means ± SE, n = 12. The error bars represent SE. cfu = colony-forming units.

 

Figure 4
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  		Figure 4. Effect of trans-cinnamaldehyde on Campy-lobacter jejuni in chicken drinking at 25°C. A (water), B (water + 1% feces), C (water + 1% feed). Data are presented as means ± SE, n = 12. The error bars represent SE. cfu = colony-forming units.

 
The extent of bacterial inactivation by TC in water was generally found to be dependent on its concentration at both storage temperatures. For example, at 12.5°C, the greatest concentration of TC (0.06%) reduced S. Enteritidis to undetectable levels on the first day of storage in all the samples (Figure 1AGo), whereas water containing the lesser concentrations of TC tested positive for the pathogen on the subsequent storage day (Figure 1AGo). A similar trend in bacterial reduction based on TC concentration was also observed in water samples containing C. jejuni.

Feed or feces exerted a significant effect (P ≤ 0.001) on the antibacterial property of TC on S. Enteritidis. For example, regardless of the storage temperature, all the concentrations of TC reduced S. Enteritidis to undetectable levels on the first day in water containing no feed or feces (Figure 1AGo and 2AGo). However, in water containing 1% feces or feed, only 0.6% TC resulted in complete inactivation of the pathogen on d 1, and samples containing 0.016% TC yielded approximately 4.0 to 5.0 log10 cfu/mL of the pathogen even on the last day of storage at 12.5°C (Figure 1B and 1CGo). Moreover, at 25°C, the number of S. Enteritidis increased in water samples containing the least concentration of 0.016% TC (Figure 2B and 2CGo). The reduced killing effect of TC observed in water samples containing feces or feed could be attributed to the binding of TC by the organic matter in these samples. It was also found that feed imparted a greater inhibitory effect (P = 0.001) on the antimicrobial property of TC than feces at both storage temperatures. This difference in the inhibitory effect between feed and feces could be attributed to the protective effect of fats [38, 39], carbohydrates [38, 40, 41], or proteins in the feed on bacteria. Previously, Gradel et al. [42] reported a greater relative survivability of Salmonella in dried feed than in dried feces.

The antibacterial effect of TC was more pronounced (P ≤ 0.001) on C. jejuni than S. Enteritidis, particularly in water samples containing 1% feces or feed (Figure 1B, 1CGo, 2B, 2CGo, 3B, 3CGo, 4B, and 4CGo) compared with Salmonella. Campylobacter jejuni is considered to be a fragile bacterium that is difficult to culture, especially when it is outside the host for longer periods of time. Campylobacter jejuni is also generally recognized as a poor competitor and a slow grower under 30°C [43], possibly explaining its decline in water samples containing feces or feed where background bacteria were present.

Results of this study indicate that TC has the potential as an antimicrobial additive for killing S. Enteritidis and C. jejuni in chicken drinking water. However, palatability studies on intake of TC-containing water by chickens are warranted before recommending its use as an antimicrobial additive in chicken drinking water.


   CONCLUSIONS AND APPLICATIONS
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
REFERENCES AND NOTES
 

  1. Trans-cinnamaldehyde has potential as a disinfectant/antimicrobial additive for killing S. Enteritidis and C. jejuni in chicken drinking water within the temperature range of 12.5 and 25°C.
  2. The antibacterial effect of TC was more pronounced on C. jejuni than S. Enteritidis.
  3. The antimicrobial effect of TC in water was suppressed more by the presence of feed than by feces.


   FOOTNOTES
 
1 Mention of a trade name, proprietary product, or specific equipment does not constitute a guarantee or warranty by the USDA and does not imply its approval to the exclusion of other products that are suitable. Back

2 Funded in part by USDA, CSREES National Integrated Food Safety Program no. 2006-02429 to Venkitanarayanan and Donoghue. Back


   REFERENCES AND NOTES
TOP
 SUMMARY
 DESCRIPTION OF PROBLEM
 MATERIALS AND METHODS
 RESULTS AND DISCUSSION
 CONCLUSIONS AND APPLICATIONS
 REFERENCES AND NOTES
 

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