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Poult Sci 2008. 87:1083-1088. doi:10.3382/ps.2008-00016
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ENVIRONMENT, WELL-BEING, AND BEHAVIOR

Influence of Exogenous Melatonin Administration on Salmonella Enteritidis Colonization in Molted Layers

D. J. Nisbet1, T. S. Edrington, J. L. McReynolds, T. R. Callaway and J. A. Byrd

Food and Feed Safety Research Unit, Southern Plains Agricultural Research Center, USDA-ARS, College Station, TX 77845

1 Corresponding author: d-nisbet{at}ffsru.tamu.edu


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Two studies were conducted to evaluate the effects of melatonin on Salmonella Enteritidis infection in experimentally challenged laying hens subjected to a forced molt. Leghorn hens (>50 wk of age) were randomly assigned to rooms, acclimated to a 16L:8D regimen, and provided ad libitum access to a nonmedicated mash layer diet and water. Birds in one room were molted (8L:16D; complete feed withdrawal), whereas birds in the second room served as nonmolted controls (CONT). Within each room, birds were randomly assigned to melatonin treatment (MEL; 12 birds/treatment), dosed orally commencing the same day as feed withdrawal for 10 d: (experiment I: 0 or 5 mg of melatonin; experiment II: 0, 10, or 20 mg of melatonin). Three days following feed withdrawal, all birds were experimentally infected with Salmonella Enteritidis, and after 10 d of feed withdrawal, all birds were killed and necropsied. In experiment I, concentrations of Salmonella Enteritidis in the cecal contents and the number of Salmonella Enteritidis-positive tissues from the crop, ceca, liver, spleen, and ovary were higher (P < 0.0001) in the MOLT compared with the CONT treatments. No differences (P > 0.10) were observed in any of the parameters examined due to MEL treatment. For experiment II, cecal concentrations of Salmonella Enteritidis were generally higher in the MOLT compared with the CONT treatment and within molted birds, cecal concentrations were higher in the MEL treatment (P < 0.05). Melatonin treatment in molted birds increased (P < 0.05) the percentage of positive crops in the MOLT+20 MEL treatment (P < 0.05). Salmonella-positive cecal tissue was increased (P < 0.001) in MOLT compared with CONT birds and was also higher in MOLT+10 MEL and MOLT+20 MEL birds compared with the MOLT-only treatment. Results from the current research suggest that dosage with high levels of melatonin may exacerbate Salmonella Enteritidis infection in layers subjected to forced molt.

Key Words: Salmonella Enteritidis • molting • laying hen • feed withdrawal • lighting


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
The induction of molt is a tool used by egg producers in the United States to increase egg yield and quality in older hens (Bell, 2003). The most effective method for forced molting involves feed withdrawal and a reduction of light exposure. However, this is a stressful situation for the hen resulting in immunodepression (Holt, 1992) and an increased susceptibility to Salmonella enterica serovar Enteritidis infection (Holt, 1993; Corrier et al., 1997; Ricke, 2003). Salmonella Enteritidis in poultry is invasive and can contaminate eggs via transovarian transmission following colonization of the intestinal tract and is therefore immune to egg washes and disinfectants of the whole egg (Gast and Beard, 1993; Thiagarajan et al., 1994). Table eggs are the primary source (when a source was identified) of Salmonella infection in humans (Patrick et al., 2004).

Previous research conducted by our laboratory attempted to explain the seasonal prevalence of another important foodborne pathogen, Escherichia coli O157:H7. Based on our hypothesis that physiological responses within the animal in response to decreasing day length are responsible for the seasonal shedding patterns of E. coli O157:H7, we initiated experimentation to examine the role of hormones and lighting on fecal shedding of E. coli O157:H7 in cattle. Administration of exogenous melatonin to feedlot cattle reduced the incidence of fecal shedding of E. coli O157:H7 compared with control animals (Edrington et al., 2008). In a second experiment, we provided artificial lighting to feedlot cattle during a period of decreasing day length and reported that fecal prevalence of E. coli O157 remained constant in cattle in the lighted pens, whereas prevalence was lower in control pens (Edrington et al., 2006). Taken together the results suggest that hormones secreted in response to decreasing day length reduce gastrointestinal populations, fecal shedding, or both of E. coli O157:H7 in cattle.

Continuing this thought process with layers and the gram-negative pathogen Salmonella, we might expect light reduction used in forced molting to increase melatonin concentrations and thereby decrease Salmonella Enteritidis populations and colonization. However, as mentioned above, hens in forced molt have an increased incidence of Salmonella Enteritidis colonization, indicating other factors may also be involved. In addition to the pineal gland, the gastrointestinal tract has been reported as producing significant quantities of melatonin, far exceeding pineal production (Bubenik, 2002; Kvetnoy et al., 2002). Furthermore, a relationship between feed intake and melatonin production in the gastrointestinal tract has been demonstrated in pigs, rats, mice, and monkeys (Huether, 1994; Bubenik et al., 1996, 2000). Bubenik (2002) concluded that a high proportion of melatonin produced by the pineal gland is secreted in response to darkness, whereas gastrointestinal melatonin is produced by enterochromaffin cells of the gastrointestinal tract, primarily in response to feeding. The practice of using feed withdrawal to initiate molting may result in a decrease in gastrointestinal melatonin, thereby facilitating Salmonella Enteritidis colonization in the hen, and may explain in part why the use of alternative molting diets have been successful in reducing Salmonella Enteritidis infection (Seo et al., 2001; Moore et al., 2004; Woodward et al., 2005). To determine if melatonin plays a role in Salmonella Enteritidis colonization in molted hens, we conducted 2 experiments in which exogenous melatonin was administered throughout a 10-d molt to layers experimentally inoculated with Salmonella Enteritidis.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
Test Birds
Single Comb White Leghorn hens (W-36) over 50 wk of age were obtained from a local commercial laying flock, transported to our laboratory, and individually housed in wire layer cages. Chickens were randomly placed in 1 of 2 rooms and allowed to acclimate for 2 wk before initiation of the experiment. During this acclimation period, birds were exposed to a 16L:8D regimen and provided ad libitum access to a nonmedicated corn-soybean meal based mash layer diet and water.

Molting Procedure and Treatments
Chickens in one room were subjected to molting (MOLT), whereas birds in the second room served as nonmolted controls (CONT). Standard molting procedures were used as described previously (McReynolds et al., 2005). To induce molt, lighting was reduced to 8L:16D for the remainder of the experiment, and 7 d following initiation of light restriction, feed was removed for the remaining 10 d of the experimental period. Within each room, birds were randomly assigned to melatonin treatment, commencing the same day as feed withdrawal [experiment I: 0 or 5 mg of melatonin (oral daily dosage for 10 d); experiment II: 0, 10, or 20 mg of melatonin dosed orally for 10 d]. Each treatment group (CONT, CONT+5, +10 or +20 MEL, MOLT, MOLT+5, +10 or +20 MEL) consisted of 12 birds each. The Animal Care and Use Committee of the Food and Feed Safety Research Laboratory, USDA preapproved the care, use, and handling of the experimental animals used in this research.

Salmonella Challenge, Sample Collection, and Bacterial Culture
Three days following feed withdrawal, chickens in all treatments were experimentally infected with a 1-mL dose of Salmonella Enteritidis [resistant to novobiocin (25 µg) and naladixic acid (20 µg)] via oral gavage (experiment I: 7.3 x 106/mL; experiment II: 4.1 x 106/mL). At the conclusion of each experiment, hens were killed and tissue samples from the crop, ceca, liver, spleen, and ovary aseptically collected. Additionally, 0.25 g of cecal contents were collected into 2.75 mL of Butterfield’s solution for serial dilution.

All tissue samples were enriched (24 h, 41°C) in Rappaport-Vassiliadis R10 broth before streaking onto brilliant green agar containing 25 and 20 µg of NO and NA, respectively. Plates were incubated for an additional 24 h (37°C) and examined for the presence of Salmonella colonies (qualitative determination). Cecal contents were serially diluted (10-fold increments) and plated as above for quantification of the challenge Salmonella Enteritidis strain. Plates were manually counted and Salmonella counts expressed as log10 Salmonella/g of cecal content. Unless otherwise noted, all media and agar were from Difco Laboratories (Detroit, MI).

Statistical Analysis
All data were analyzed using SAS Version 8.02 (SAS Inst. Inc., Cary, NC). The incidence of Salmonella Enteritidis-positive tissues were subjected to chi-square analysis using the Proc Freq procedure. Cecal concentrations of Salmonella Enteritidis were analyzed using ANOVA appropriate for a completely randomized design and treatment differences separated using Duncan’s multiple range tests. Differences among means were considered significant at a 5% level of significance.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Experiment I
Concentrations of Salmonella Enteritidis in the cecal contents were significantly greater in the MOLT compared with the CONT treatments. Likewise, the number of Salmonella Enteritidis-positive tissues (crop, ceca, liver, spleen, and ovary) were greater (P < 0.0001) in birds in the MOLT versus CONT treatments (Table 1Go). No differences (P > 0.10) were observed in any of the parameters examined due to MEL treatment.


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  		Table 1. Cecal content populations and percentage of tissue samples positive for Salmonella Enteritidis in experimentally infected laying hens molted (Molt) or not molted (Con) and receiving 5 mg of melatonin (Con+5; Molt+5) daily for 10 d
 
Experiment II
As in the first experiment, cecal concentrations of Salmonella Enteritidis were generally greater in the MOLT compared with the CON treatment; however, differences due to MEL treatment were observed. Administration of melatonin to the molted birds (MOLT+10 and MOLT+20) resulted in greater (P < 0.05) concentrations of Salmonella Enteritidis compared with no melatonin treatment (MOLT; Table 2Go). Additionally, Salmonella Enteritidis concentrations were similar in CONT+20 birds and MOLT birds not receiving melatonin. Granted, the concentrations in the MOLT treatment were numerically greater and would likely be statistically greater with an increase in experimental units and subsequently statistical power. Treatment differences were observed for the percentage of crop and cecal tissues that were Salmonella Enteritidis-positive. No crops from CONT birds were Salmonella Enteritidis-positive, whereas all MOLT treatments had at least one Salmonella Enteritidis-positive crop. Melatonin treatment in the molted birds increased (P < 0.05) the percentage of positive crops in the MOLT+20 treatment (P < 0.05) and was numerically greater in the MOLT+10 treatment. Salmonella-positive cecal tissue was increased (P < 0.001) in MOLT compared with CONT birds and was also greater in MOLT+10 and MOLT+20 birds compared with the MOLT-only treatment (Table 2Go). The percentage of liver (P = 0.09) and ovary (P = 0.12) tissues Salmonella Enteritidis-positive tended to be greater in MOLT compared with CONT treatments, whereas no differences were observed for Salmonella Enteritidis-positive spleen tissue (Table 2Go).


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  		Table 2. Cecal content populations and percentage of tissue samples positive for Salmonella Enteritidis in experimentally infected laying hens molted (Molt) or not molted (Con) and receiving 10 (Con+10, Molt+10) or 20 mg of melatonin (Con+20; Molt+20) daily for 10 d
 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The protective effects of melatonin in the gut are well documented. Gastrointestinal melatonin has been suggested as playing a protective role in disorders such as irritable bowel syndrome, gastroesophageal reflux disease, and intestinal colic in newborns (Talley, 1992; Weissbluth and Weissbluth, 1992). Others have reported relationships between melatonin and the digestive enzymes gastrin (Lewinski et al., 1991), cholecystokinin (Benouali et al., 1993; Jaworek et al., 2004), and pancreatic enzyme (Jaworek et al., 2004). Furthermore, melatonin is reported to protect against gastrointestinal mucosa ulceration via its antioxidant action, immune system stimulation, and by improving microcirculation and epithelial regeneration (Bubenik, 2001), and administration of melatonin reduced the incidence of gastric ulcers in rats (Cho et al., 1989; Khan et al., 1990) and pigs (Ayles et al., 1996). Additional research conducted by the authors reported that administration of exogenous melatonin decreased the incidence of fecal shedding of E. coli O157:H7 in feedlot cattle (Edrington et al., 2008). Taken together, we hypothesized that melatonin, administered to hens under stress due to feed and light restriction in a forced molt, would reduce the severity of Salmonella Enteritidis infection.

Results from the current research however, suggest just the opposite. The administration of a "high" level of melatonin utilized in the second experiment appeared to exacerbate Salmonella Enteritidis colonization in molted hens. The most plausible explanation may involve the role of melatonin on gut motility. Melatonin has been suggested as acting as a local regulator of gastrointestinal motility (Holloway et al., 1980) and has been shown to block the serotonin-induced contraction of smooth muscles in the gastrointestinal tract (Quastel and Rahamimoff, 1965; Bubenik, 1986; Harlow and Weekly, 1986) and reduced gastrointestinal muscle tone in vitro (Bubenik and Dhanvantari, 1989). Possibly, melatonin inhibition of gastrointestinal motility and subsequently food transit time is designed to allow for more efficient digestion of ingested food (Harlow and Weekly, 1986). Administration of the high dose of melatonin in the second experiment may have provided enough exogenous melatonin to affect gastrointestinal melatonin concentrations and thereby reduce gut motility. Additionally, caloric restriction as well as an acute food intake can elevate levels of gastrointestinal melatonin (Bubenik et al., 1992, 1996; Huether, 1994), and severe fasting almost doubled melatonin levels in the gastrointestinal tract of mice (Bubenik et al., 1992). A correlation was reported between local concentration of melatonin in the gastrointestinal tissues and the amount of passing food (Bubenik et al., 1996). Long-term elevation of peripheral melatonin levels induced by starvation may initiate an overall reduction in gastrointestinal activity, similar to that observed shortly before hibernation. In the case of fasted laying hens, the combined effect of fasting and melatonin administration may have substantially decreased gut motility and thereby allowed for greater Salmonella Enteritidis colonization and infection. This is supported by our observation that the high melatonin dose affected Salmonella Enteritidis in molted birds but not birds on full feed. Corn contains one of the highest melatonin concentrations of commonly used feedstuffs (1,366 pg/g), and therefore corn intake could theoretically influence melatonin concentrations (Hattori et al., 1995). However, based on the current results, it does not appear that melatonin derived from the high corn diet in the control birds was sufficient to produce effects similar to those observed in molted birds receiving the high melatonin dose.

The effects of melatonin on gut motility may explain in part the success of using alternative molting diets such as alfalfa meal or wheat middlings on reducing Salmonella Enteritidis colonization (Seo et al., 2001; McReynolds et al., 2005; Woodward et al., 2005). Providing a feed source, although limiting in nutrients compared with a normal diet, may provide enough bulk to keep gut motility functioning similar to that of birds on full feed.

A second explanation may involve the thyroid. Melatonin has been reported to have a general inhibitory affect on the thyroid and thyroid hormone production (Wright et al., 1996; Lewinski, 2002; Mogulkoc and Baltaci, 2002), and administration of high melatonin doses suppressed thyroid response to TSH, but not low doses (Wright et al., 1997). Perhaps the high dose of melatonin administered in the current research inhibited the thyroid in molted hens already stressed by feed restriction (but not control birds on full feed) and thereby increased their susceptibility to Salmonella Enteritidis infection.

In humans, some endocrine disorders are accompanied by zinc deficiency (Aihara et al., 1985; Kwan et al., 1995), supporting a relationship between zinc and the thyroid gland (Leblondel and Allain, 1989; Leblondel et al., 1992; Baltaci et al., 1999). In rats melatonin suppresses thyroid function, an effect that is diminished with zinc administration (Bediz et al., 2002; Baltaci et al., 2004). Zinc supplementation has been used successfully to induce molt in layers (Berry and Brake, 1985; Park et al., 2004) and has also been shown to effectively reduce the risk of Salmonella Enteritidis during induced molt (Moore et al., 2004). Taken together, this suggests that feed restriction in layers may increase gastrointestinal melatonin concentrations, inhibiting the thyroid and subsequently increasing Salmonella Enteritidis colonization in molted birds. Zinc administration, although not altering the increased melatonin levels associated with feed withdrawal, may counteract the thyroid-inhibiting action of melatonin, thereby reducing the incidence of Salmonella Enteritidis infection.

Melatonin increases the absorption of zinc from the digestive system (Mocchegiani et al., 1996; Fabris et al., 1997). Therefore, when full feed is provided, as in this research, or when alternative molting diets are fed, zinc is available for absorption in the gastrointestinal tract and counteracts the inhibitory effect of melatonin on the thyroid. Conversely, without any zinc-containing feed-stuff available to counteract the effects of melatonin, the thyroid is impaired and Salmonella Enteritidis colonization increases.

Granted, the majority of the available literature discussed above utilized experimental animals other than chickens, and species differences could negate the above proposed explanations for the melatonin treatment differences observed in this research. Because this was the initial stage of this research and because of the high cost associated with melatonin assay, we did not look at serum or gastrointestinal concentrations of melatonin. Additionally, we did not separate out the potential effects of light reduction and feed withdrawal, and the differences we observed could be a result of one or the other, or a combination of both. If primarily a result of feed withdrawal, then the success of experimental molting diets utilizing alfalfa meal, wheat middlings, or zinc supplementation may be explained in part by melatonin concentrations and possibly thyroid function. Research is currently underway to further investigate the findings reported herein.

Received for publication January 10, 2008. Accepted for publication February 20, 2008.


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