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ENVIRONMENT, WELL-BEING, AND BEHAVIOR |
Department of Animal Sciences, Purdue University, West Lafayette, IN 47907
2 Corresponding author: applegt{at}purdue.edu
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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0.05). Jejunal villus height increased as FW progressed. Jejunal crypt depths increased until 12 h of FW and then declined at 24 h. Mucus content decreased linearly and was reduced by 46% from 0 to 24 h FW (P < 0.05). The intestinal morphology alterations and the depletion of intestinal mucus that occur during a short-term FW may reduce the integrity of the intestine.
Key Words: broiler • feed withdrawal • intestine • morphology
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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As would be expected, the intestinal tract is remarkably affected by fasting. The GIT of chickens only constitutes roughly 1.5% of the chicken’s BW, yet consumes approximately 6 to 8% of the energy derived from the diet (Spratt et al., 1990) and thus responds very quickly and dramatically to changes in nutrient status and feed intake. In fact, during fasting in rats, the initial intestinal weight loss is far more pronounced relative to initial BW loss (Orr and Benet, 1975). Therefore, changes in nutrient status and particularly feed deprivation cause alterations in intestinal mucosal structure and function, which ultimately affect the integrity of the intestine (Ferraris and Carey, 2000; Dou et al., 2002).
Short-term fasting is known to alter the architecture of the chicken intestine by decreasing duodenal villi height and cell area as well as eliciting profound decreases in cell mitosis after a 1-d fast in White Leghorn roosters (Yamauchi and Tarachai, 2000). Additionally, Yamauchi et al. (1996) demonstrated that fasting White Leghorn hens for 12 h caused decreases in duodenal and jejunal villi heights but that ileal villi heights were not significantly decreased until 24 h of FW. Although these reports with White Leghorns are insightful, direct comparisons between laying hen and broiler intestinal morphology may not be definitive because of inherent differences in intestinal characteristics among strains (Yamauchi and Isshiki, 1991). However, few studies regarding the effects of FW on intestinal morphology have been conducted on broilers.
Long-term fasting (3 d) of broilers can lead to marked depression in the tips of the duodenal villi, separations in the epithelial cell cytoplasm, and the appearance of large vacuoles within the epithelial cells (Bayer et al., 1981). Though useful, this data does not address the effects of short-term FW (<24 h) on the intestinal ileal morphology and epithelial cell proliferation and migration. The ileal segment of the intestine is of particular interest due to its proximity to ceca, which are known to harbor large populations of microbiota and are also recognized as the portions of the intestine most often colonized by Salmonella (Fanelli et al., 1971). In fact, research has indicated that FW does not consistently evacuate cecal contents (Hinton et al., 2000) and may cause increases (Ramirez et al., 1997) or have no effect on cecal Salmonella colonization (Oyarzabal and Conner, 1996). Thus, the possibility arises that Salmonella is released into the ileum during FW, possibly increasing the potential for carcass contamination during processing if the ileum is ruptured. However, little is known regarding how the ileum is affected and how Salmonella might adapt to such situations.
Fasting also exerts marked effects upon the quantity of intestinal mucus found in the intestine. In a study on 28-d-old chicks, Smirnov et al. (2004) found that a 72-h fast caused decreases in the thickness of the mucus adherent layer that corresponded with increases in the size of goblet cells within all sections of the small intestine. Furthermore, although no increase in goblet cell numbers was observed in response to the 72-h fast, the researchers determined that amounts of duodenal and jejunal mucin mRNA and protein increased in response to a 72-h fast. They hypothesized that these changes might be due to greater mucus degradation, reduced rates of mucus secretion, or altered mucin turnover rates. The short-term effects of fasting on intestinal mucus layer thickness are not currently documented in adult broiler chickens.
A paucity of data exists regarding how incremental FW periods affect intestinal morphology, cell migration, and mucus content of the broiler intestine. With that in mind, 2 experiments were designed to determine how FW affects these characteristics in the market-age broiler intestine.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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All experiments were approved by the Purdue University Animal Care and Use Committee. For both experiments, male broilers were raised in floor pens with ad libitum access to standard industry corn–soybean meal diets (Applegate et al., 2003) and water. At 42 d of age [Experiment (Exp.) 1] and 39 d of age (Exp. 2), birds were randomly selected from 3 or 4 pens and placed into separate floor pens with 5 birds/pen (Exp. 1) or 8 birds/pen (Exp. 2). Feed was removed from the first pen 24 h before sampling and from the second and third pens 12 and 8 h before sampling, respectively, to simulate 8, 12, and 24 h of FW. Feed was not removed from the fourth pen, which was designated as the control or 0-h FW pen (Exp. 1). For Exp. 2, feed was removed in a similar fashion for 12 and 24 h. In both experiments, birds remained on litter with access to water for the first 4 h of the FW period and were then placed in crates. After the trial, birds were euthanized with CO2. For Exp. 1, BW and the weight of the left pectoralis major were also determined.
Intestinal Morphology
Exp. 1. Five birds per FW time were euthanized with an overdose of CO2, and intestinal sections were collected on 43 and 40 d of age for Exp. 1 and 2, respectively. A segment was collected from the distal jejunum and ileum and placed in 10% neutral buffered formalin (Sigma Chemical Co., St. Louis, MO) for 48 h, dehydrated with increasing concentrations of ethanol, cleared with SubX (Surgipath Medical Industries Inc., Richmond, IL), and placed into Polyfin paraffin (Polysciences Inc., Warrington, PA). Sections (5 µm) were stained with hematoxylin and eosin. Measurements for villi length and width were taken from the tip of the villus to the valley between individual villi, and measurements for crypt depth were taken from the valley between individual villi to the baso-lateral membrane. Ten villi were measured for each bird.
Exp. 2. At 39 d of age and 24 h before sampling, birds from each treatment received i.p. injections of 5-bromo-2'-deoxyuridine (BrdU; 10 mg/kg of BW; Sigma Chemical Co.) followed 180 min later by an injection of thymidine (500 mg/kg of BW), as previously described (Applegate et al., 1999) for determination of enterocyte migration rate. Sterile water was used as the vehicle for injection of both compounds. At 43 d of age, 8 birds/pen were euthanized, and ileal sections were collected for intestinal morphology and mucus. For the intestinal morphology samples, 2-cm sections of the ileum were sliced and placed in ice-cold Carnoy’s fixative (60% ethanol, 30% chloroform, and 10% glacial acetic acid). After 2 h, the Carnoy’s fixative was drained, and 100% ethanol was added for overnight storage. The following day, tissues were trimmed, cleared with SubX (Surgipath Medical Industries Inc.), and embedded in Polyfin (Polysciences Inc.) paraffin.
Sections (5 µm) were stained for BrdU, as previously described (Kitchell and Dibner, 1989). Briefly, sections were cleared with SubX (Surgipath Medical Industries Inc.), rehydrated with decreasing concentrations of ethanol, and treated with 3% hydrogen peroxide in water for 10 min to block endogenous peroxidase activity. Sections were rinsed in PBS, incubated in 2 N HCl for 30 min, rinsed in PBS, and digested with 0.1% trypsin in Tris-buffered saline for 10 min. A monoclonal anti-BrdU antibody (Sigma Chemical Co.) was diluted at 1:100 in PBS containing 1% BSA, 0.05% Tween, and 0.1% sodium azide, and slides were incubated in the antibody for 2 h in a humidified chamber at 37°C. Sections were rinsed in PBS and incubated at 37°C for 30 min in a biotinylated secondary antibody, rinsed with PBS, and incubated at 37°C for 30 min in an avidin-biotin complex solution (Vectastain ABC peroxidase kit, Vector Laboratories Inc., Burlingame, CA). A chromagen indicator (Vectastain DAB substrate kit, Vector Laboratories) was utilized for color development. Slides were counterstained with methyl green (Vector Laboratories).
Goblet cell counts were collected from 5-µm sections stained with periodic acid-Schiff reagent (Armed Forces Institute of Pathology, 1992). Briefly, tissues were deparaffinized and hydrated, oxidized in periodic acid (5 g/L) for 5 min, rinsed in distilled water, and placed in Coleman’s Schiff reagent (Sigma Chemical Co.) for 30 min. After a 15-min rinse in lukewarm tap water, tissues were counter-stained in hematoxylin, rinsed, dehydrated, and mounted. Positively stained periodic acid-Schiff cells were enumerated on 10 villi/sample, and the means were utilized for statistical analysis.
Migration measurements were taken by measuring the distance of BrdU-positive stained cells from the top of the crypts of the intestinal samples, and they are presented in micrometers of cell migration per hour.
Intestinal Mucus
Immediately after euthanasia and ileal collection for intestinal morphology measurements, ileal segments were collected for mucus quantification (Exp. 2). Samples were collected from birds (n = 8/treatment) on the 0-, 12-, and 24-h FW treatments. One, 1-cm ileal segment was collected, weighed, and used for mucus quantification as described by Corne et al. (1974), with modifications by Smirnov et al. (2004) and with further modifications as described herein. Briefly, the ileal section was opened, everted, and soaked for 2 h in a 0.1% solution of Alcian blue (AB) dissolved in 0.16 M sucrose and buffered with 0.05 M sodium acetate at a pH of 5.8. Sections were washed in a 0.25 M sucrose solution for 15 min and washed again in a fresh 0.25 M sucrose solution for 45 min to extract uncomplexed dye. Sections were placed in a 10 g/L docusate sodium salt solution overnight at room temperature to extract absorbed dye from the tissue then centrifuged at 700 x g. The supernatant was poured into new tubes, and 100 µL of each sample (in triplicate) was plated on a 96-well plate. The standard curve was created using the AB solution, and optical density was measured at 620 nm to determine the amount of absorbed dye in each sample. Results are reported as micrograms of AB/centimeter2 and micrograms of AB/gram of intestine.
Statistical Analysis
The experiment was analyzed as a completely randomized design. Data were analyzed as a continuous variable (i.e., time off of feed) by linear, quadratic, and cubic effects using the REG procedure (SAS Institute Inc., Cary, NC). Statements of significance were made when P 0.05.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Exp. 1.
Feed withdrawal caused a linear decrease in BW and pectoralis major weight (as measured by percentage of BW) as the FW period increased (Table 1
). Corresponding linear regression equations were percentage of BW loss = 0.0665 + 0.3218(FW, h), r2 = 0.87, and pectoralis major weight loss as a percentage of BW = 7.07 – 0.02(FW, h), r2 = 0.09. Additionally, although not quantified, litter was visible in the gizzard and intestines of birds withdrawn from feed for 8 and 12 h, but not at 24 h.
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0.05). The linear regression equation generated for the linear increase in jejunal villus height is as follows: jejunal villus height = 114.82 + 1.55(FW, h), r2 = 0.69. Although no differences were noted in jejunal villi widths, jejunal crypt depths exhibited a quadratic response to FW (Table 2).
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0.05), with the linear regression equation determined to be villus width = 167.79 – 2.11(FW, h), r2 = 0.61. Furthermore, ileal crypt depth also decreased in a linear fashion with increasing periods of FW (P 0.05; Table 2
), with a corresponding equation of ileal crypt depth = 161.49 – 2.30(FW, h), r2 = 0.65.
Exp. 2.
Furthermore, FW did not affect rates of enterocyte migration (Table 3).
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As the FW period increased, ileal mucus content decreased by 2% per h and had decreased by 46% by 24 h of FW (measured as µg of AB/cm2 of ileum). The regression equation generated for the linear reduction of mucus per ileal length as time off feed progresses is mucus quantity = 32.97 – 0.639(FW, h), r2 = 0.29. Numbers of goblet cells were not affected by FW (Table 3).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The linear decrease in BW as the FW period progressed was not surprising, as numerous studies have demonstrated a loss of BW in response to short-term FW. May and Brunson (1955) reported that both male and females had a significant loss in eviscerated yield when starved 24 h before slaughter as compared with birds withheld from feed for 0, 3, 6, or 12 h. In a follow-up study, Brunson (1957) determined that birds fasted 12 to 24 h before slaughter also had significant losses in carcass yields. Subsequent research data has been similar to the early data and indicates that as FW time increases, live weight shrink increases and eviscerated yield decreases in a linear fashion (Scott et al., 1978; Rasmussen and Mast, 1987; Lyon et al., 1991). Similar results were observed in the current studies, in which the weight of the pectoralis major was reduced linearly in response to increasing periods of FW.
Unlike the results of Yamauchi et al. (1996), who determined that laying hen jejunal villus height gradually decreased from 0, 12, and 24 h of FW, our data showed that jejunal villus height was greater after FW and, in fact, showed linear increases in villus height in response to increasing periods of FW. This difference may be attributable to genetic differences between White Leghorn hens and broilers, as Yamauchi and Isshiki (1991) reported that considerable differences exist between the intestinal characteristics of the 2 birds and showed that, although broilers have fewer villi per unit length than White Leghorns, the villi of the broilers are larger and appear to slough more often, suggesting that broiler intestine undergoes a higher rate of cell renewal. In addition, because the jejunum is recognized as the major site of absorption in the small intestine, the increase in villus height could represent an attempt to increase intestinal surface area to maximize absorption once digesta are again present in the lumen. Although apoptosis was not measured in this set of experiments, the increased jejunal villus height could hypothetically be caused by reduced cell turnover and migration, resulting in the retention of epithelial cells on the villi (Holt et al., 1986). A similar justification may also explain the 39% increase and quadratic response in jejunal crypt depth that was noted at 12 h of FW. The increased crypt depth at 12 h may be a reflection of greater numbers of proliferating cells. Because broilers have been selected for growth rates over a short period, and thus have greater absorptive capacity than White Leghorns, jejunal villi and crypts may initially respond to fasting in this manner in an effort to maximize nutrient uptake once nutrients are accessible.
Results from Exp. 1 indicated that villus width was linearly decreased after FW, whereas the crypt depth decreased in a linear fashion at 24 h post-FW. Therefore, changes in villus width and crypt depth occurred in a time-dependent manner. However, Yamauchi et al. (1996) observed marked decreases in duodenal and jejunal villus heights in response to as little as 12 h of fasting in White Leghorns, but determined that villi within the ileum were less responsive to the fasting period and did not decrease in height until 24 h of fasting. Smirnov et al. (2004) also observed that a 72-h fasting period reduced ileal villus length by 26% in 28-d-old broilers. Given the short period of fasting, we could conclude that because the ileum is not the primary site of absorption, it is not as responsive to lack of nutrient stimulation and, therefore, responds more slowly to FW than either the duodenum or jejunum.
A linear reduction in villi width and crypt depth, as observed in Exp. 1, may be in response to the lack of luminal stimulation by the presence of food. Because the ileum is not the primary site of absorption, the ileal response to lack of feed may be inverse to the jejunal response in an effort to conserve energy. In other words, the jejunum may not be as affected as the ileum to maximize absorption once food is presented to the intestine. Further evidence supporting these results can be found in the results of Holt et al. (1986), who reported that ileal crypt depths decreased after 2 d of fasting in rats. Ferraris and Carey (2000) have attributed such changes in morphology to decreases in the migration and proliferation of cells, along with increased rates of cell loss and programmed cell death, or apoptosis.
Interestingly, our data indicated that short-term FW had no effect on ileal epithelial cell migration. If the cell migration rates have not yet decreased in response to the 24-h fasting, then changes in proliferation and apoptosis may not have begun to occur either. Experimental evidence from other trials with longer fasting periods suggests that epithelial cell proliferation and migration is profoundly affected by fasting (>24 h; Habold et al., 2004), partially because the presence of digesta and nutrients within the GIT is known to be a stimulating factor of intestinal cell proliferation (Brown et al., 1963; Clarke, 1976; Goodlad and Wright., 1984) as well as an important factor to maintaining structural integrity of the intestine. Goodlad and Wright (1984) determined that crypt cell production rate decreased by nearly 30% in rats fasted for 4 d, whereas Holt et al. (1986) reported decreases in crypt cell numbers and migration in Wistar rats fasted for 3 d. Others have reported similar results in mice (Goodlad and Wright, 1984). Rose et al. (1971) reported that a 7- or 10-d starvation in rats induced changes in intestinal mucosal cell renewal by increasing the duration of the S and G2 phases of mitotic division and by decreasing the G1 phase of mitotic division.
Feed withdrawal also caused marked reductions in the quantity of the mucus from 0 to 24 h but did not affect the number of goblet cells found on the individual villi. Additionally, FW caused a linear decrease in mucus over each time point measured. This result is similar to the results of Smirnov et al. (2004), who noted significant reductions in mucus-layer thickness but no changes in goblet cell numbers of 28-d-old chicks subjected to 72 h of feed and water deprivation. However, Conour et al. (2002) demonstrated an increase in the number of sulfomucin- and sialomucin-secreting goblet cells in the ileums of piglets subjected to 3 d of total parenteral nutrition. Our results showed a numerical increase in goblet cell numbers after 24 h of FW, but the increase was not statistically significant.
Many functional properties have been ascribed to intestinal mucins, such as lubricating intestinal surfaces, trapping and neutralizing bacteria, detoxifying heavy metal binding, defending the immune system by the accumulation of secretory IgA, acting as a diffusion barrier for nutrients and macromolecules, and protecting the underlying epithelial cells (Forstner and Forstner, 1994). Sloughing of the mucus layers occur regularly, allowing removal of the bacteria that colonize the mucus and preventing those bacteria from attaching to the underlying epithelial cells.
Because the mucus layer contributes significantly to gut barrier function and protection from pathogens, the reduction in the thickness of the layer during FW could potentially aid Salmonella colonization and growth within the ileum during FW periods. To make contact with the apical side of the epithelial cells and, hence, colonize the cells, Salmonella must penetrate the mucus layer. Once the thickness or quantity of the mucus layer is reduced by FW regimens, Salmonella may be able to reach the epithelial cells more efficiently. In fact, a study by McHan et al. (1988) determined that the absence of an intact adherent mucus layer in chicken cecal epithelium allowed greater adherence of Salmonella enterica serovar Typhimurium. Additionally, a recent in vitro study utilizing chicken ileal loops has demonstrated that Salmonella typhimurium attachment increased by 1.5 log in the ileum of broilers when they are withdrawn from feed for 24 h as compared with birds not withdrawn from feed (Burkholder et al., 2003). Thus, the reduction of the mucus layer during FW, particularly the longer periods of FW, poses valid concerns regarding pathogen colonization and growth within the ileum before processing.
Intestinal integrity, or the ability of the intestine to properly defend itself and prevent pathogen colonization, has been shown to be compromised during short- and long-term FW periods. Results from this study imply that physical changes in intestinal morphology may not affect intestinal integrity during short-term FW (24 h) such as those examined in this study. However, the time-dependent and quantitative linear reduction of the overlying ileal mucus layer within 24 h of FW may contribute significantly to Salmonella attachment and shedding during this period. Further research is necessary to better understand this interaction.
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FOOTNOTES |
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Received for publication January 6, 2006. Accepted for publication April 11, 2006.
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