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Nutrition and Disease

Dietary Putrescine (1,4-Diaminobutane) Influences Recovery of Turkey Poults Challenged with a Mixed Coccidial Infection¹

¹ Department of Animal and Poultry Science, Ontario Agricultural College, and ² Department of Pathobiology, Ontario Veterinary College, University of Guelph, Guelph, Ontario N1G 2W1, Canada and Facultad Medicina Veterinariay Zootecnia, Universidad Autónoma de Nuevo León, Monterrey, Nuevo León 64930, México

^* To whom correspondence should be addressed. Email: tsmith{at}uoguelph.ca.

	ABSTRACT

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

 
Exogenous dietary putrescine (1,4-diaminobutane) can increase growth rates of neonatal animals, including calves, chicks, and piglets, under nutritional stress. Turkey poults often have a high mortality rate and this may be due to poor initial feeding behavior and inadequate development of the intestinal tract. We conducted an experiment to determine the effect of dietary putrescine supplementation on growth performance and the role of dietary putrescine in prevention and recovery from a coccidial challenge. A total of 160 1-d-old turkey poults were fed a corn and soybean meal–based starter diet supplemented with 0.0 (control), 0.1, 0.2, and 0.3 g/100 g purified putrescine (8 birds/pen, 5 pens/diet). At 14 d of age, half the birds were infected with 43,000 sporulated oocysts. The experiment lasted 24 d. Fecal samples were gathered from d 3 to d 5 postinfection by total collection. Ten control and 10 infected birds fed each diet were sampled on d 6 and d 10 postinfection. The induced infection produced significant depressions in growth and feed intake and detrimental morphological changes in the small intestine of poults in the absence of mortality. Weight gains, protein content of jejunum, and morphometric indices of duodenum, jejunum, and ileum were greater in challenged poults fed 0.3 g/100 g putrescine than in controls. We conclude that dietary putrescine supplementation may be beneficial to poult growth, mucosal development of the small intestine, and to recovery from subclinical coccidiosis.

	Introduction

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

The growth-promoting potential of exogenous, dietary polyamines appears to be of greatest metabolic importance when intestinal function is compromised. When chicks were fed diets containing raw soybeans with antinutritional factors such as lectins, which inhibit intestinal tract development and function, control levels of growth were restored with dietary putrescine supplementation (4). The substitution of isolated soy protein for milk protein in milk replacer diets for calves (5) and neonatal pigs (6) showed reductions in villus height and polyamine concentrations in the intestinal tract. This effect was partially abrogated by dietary putrescine supplementation. Wang et al. (7) reported that the high turnover rate of the intestinal epithelium, as well as healing after mucosal damage, is dependent on sustained supplies of polyamines. In vitro studies suggest that the addition of putrescine to a culture medium in which cell replication was stopped by a chemical reagent resulted in normal replication. One study suggests that polyamines are essential nutrients for avians (8), and this is exemplified by the effect of polyamine depletion on cell replication.

Coccidiosis is a disease of global importance in poultry production. The protozoan parasites multiply in the intestinal tract and cause tissue damage. Coccidiosis and other enteric diseases are characterized by reduced feed intake, nutrient malabsorption, reduced nutrient use, desquamation of intestinal cells, and hemorrhage of the intestinal tissues. In addition, the gastrointestinal tract is often the entry point for infectious agents or toxins that are detrimental systemically, and the conditions produced are conducive to establishing secondary infections.

Coccidiosis is largely a disease of young animals, because immunity develops quickly after exposure, which protects against later infection. The short life cycle and high reproductive potential of coccidia in poultry intensifies the risk for severe outbreaks of disease in modern poultry houses. The effects can be mild and may escape notice (a result of ingesting a few oocysts), or they may be severe (from ingesting millions of oocysts). Most infections are relatively mild, but because of the potential for disastrous outbreaks and the resulting financial losses, almost all young birds are given continuous medication with prophylactic levels of anticoccidial drugs mixed in the feed ration. The reasons for using coccidia as an agent for gastrointestinal challenge in our experiment were as follows: 1) coccidiosis is one of the most common and important diseases in young birds; 2) challenge material was readily available; and 3) coccidia have a genetically defined life cycle in which a predefined number of intracellular replicative cycles are followed by oocyst formation and termination of an active infection, after which birds are free of coccidia in the absence of environmental reinfection. This is unlike bacterial or viral challenges in which there is no control on the proliferation of the challenge material.

Our objective was to determine both the effect of dietary putrescine supplementation on growth performance and the role of dietary putrescine in prevention and recovery from a coccidial challenge.

	Materials and Methods

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

 
Experimental birds, diets, and design

One hundred and sixty, 1-d-old male hybrid turkey poults (Cold Springs Farm, London ON) were fed a corn and soybean meal–based control diet (Table 1) formulated to meet the nutritional requirements of starter poults (9). Experimental diets were created by adding putrescine (0.0, 0.1, 0.2, and 0.3 g/100 g) at the expense of corn. Poults consumed experimental diets and water ad libitum for 24 d. The birds were housed in the Isolation Unit at the Ontario Veterinary College of the University of Guelph, in 2 rooms with 20 battery cages each. Cages were equipped with external feed and water troughs and each held 4 birds. Each room housed 20 birds (5 cages) from each diet group. Each cage was considered an experimental unit. The birds in room 1 were designated the unchallenged group. Birds in room 2 were infected with coccidia and designated the challenged group. Poults were initially maintained at 29°C and the temperature was lowered by 1°C/wk. On d 14, half the birds were inoculated via crop intubation with 1 mL of a mixed culture of coccidia (Eimeria meleagrimitis, E. meleagridis, E. gallopavonis, and possibly other Eimeria species), with a dose of 43,000 sporulated oocysts/bird. To establish the experimental suitability of the dose of 43,000 oocysts/bird, the oocysts collected from the field were first propagated and titrated to arrive at a clinically relevant infection level. In the propagation step, 10 birds were divided into 2 groups and infected with 100,000 oocysts. The oocysts collected from the excreta of birds used for propagation were then used for titration. In the titration step, 15 birds were divided into 3 groups and challenged with 50,000, 100,000, or 150,000 oocysts/bird. We observed that poults challenged with 50,000 oocysts appeared to meet the criteria of challenge whereas the other group of birds did not. We expected that the challenge would cause a significant reduction in weight gain without mortality. At d 20 and d 24, 20 birds/diet (2 birds/pen) were selected randomly from each room and killed by cervical dislocation. Days 14–20 served as the period of infection in response to challenge, and days 20–24 corresponded to the recovery period. Representative feed samples were taken at the beginning of the experiment and were analyzed for crude protein content by the method of the Association of Official Analytical Chemists, (10). The project was approved by the University of Guelph Animal Care Committee and met the guidelines of the Canadian Council on Animal Care.

    Excreta collection and analysis. Excreta were collected from cage in both rooms from d 17 to d 19 for determination of fat, dry matter, and energy. Samples were oven dried for 3 d and ground thoroughly prior to analyses. Crude fat dry matter and gross energy were determined according to the method of the Association of Official Analytical Chemists (10). Excreta samples were also collected from infected birds from d 21 to d 24. The total number of fecal oocysts was determined. Briefly, the total fecal mass was diluted in water to 1 L total volume. A sample from this mixture was diluted 10-fold by adding 9 parts saturated NaCl (aqueous). After mixing, the sample was loaded into a McMaster counting chamber and the oocysts were allowed to float for 5 min before enumeration.

    Organ weight and tissue lesion measurement. At d 20 and at d 24, 2 birds/pen, (10 birds/diet) were randomly selected and killed by cervical dislocation. Lesions in the small intestine were scored blindly (0 to +4 scale) to compare quantitatively the extent of gross lesions due to coccidiosis, using the method of Johnson and Reid (11). Intestine samples from the duodenum, jejunum, and ileum (each 2.5 cm in length) were fixed in 10% neutral buffered formalin for histology as follows: 1) the apex of the duodenum, 2) midway between the entry point of the bile ducts and the Meckel's diverticulum (jejunum), and 3) 10 cm proximal to the cecal junction (ileum) (12). Intestinal segments were excised, weighed, and flash frozen in liquid nitrogen and stored at –80°C.

    Tissue protein and DNA concentration. DNA extracted from crude mucosal homogenates of duodenum, jejunum, and ileum was quantified fluorometrically (PTI Deltascan 4000, Photon Technology International) by the method of Labarca and Paigen, (13) with 350-nm excitation and 470-nm emission wavelengths. The protein content of the mucosal homogenate was measured spectrophotometrically (Bio-Rad Microplate reader 550) according to the method of Bradford (14).

    Morphometric indices of the duodenum, jejunum, and ileum. Intestinal segment samples of duodenum, jejunum, and ileum were flushed with saline (0.9% NaCl) to remove contents and fixed in 10% neutral buffered formalin for histology. Samples were dehydrated, cleared, and paraffin embedded. Tissues from 10 birds fed each diet were sectioned (5µm), placed on glass slides, and processed by hematoxylin and eosin stain for examination by light microscopy. Morphometric analysis was performed on 15 villi chosen from each tissue segment, using a random number table and a computer-aided light microscope image with Openlab software (Openlab Ver. 2.2.5, Improvision). Variables included villus height from the tip of the villus to the crypt, crypt depth from the base of the villi to the submucosa, villus width at one-third of the villus, muscularis from the submucosa to the external layer of the intestine, and the crypt-to-villus ratio (15). Apparent villus surface area was estimated by trigonometry [(villus width at bottom + villus width at top) x (2 x villus height)^–1], according to Iji et al. (16).

Analysis of polyamines and metabolites

Diets were analyzed for concentrations of polyamines and metabolites by HPLC with postcolumn derivitization and fluorescence detection (17).

Statistical analyses

Data were analyzed by analysis of covariance (ANCOVA) with initial body weight as the covariate (for production variables) or by ANOVA (for other variables), in a completely randomized design using cage as the experimental unit. Least squares means of production criteria are presented after ANOVA and linear and quadratic regression, using the general linear model procedures of SAS software (18). Orthogonal polynomial contrasts were used to determine the nature of the response exhibited by different variables compared with controls. Statements of significance were based on P < 0.05. Due to a lack of replication, no direct comparisons could be made between the challenged and unchallenged groups.

	Results

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

 
Experimental diets

The dietary putrescine concentrations were slightly lower than the planned levels of dietary supplementation (Table 2). Histamine and cadaverine were not detectable in any of the feed samples. Constant concentrations of spermidine were present in diets supplemented with 0, 0.1, 0.2, and 0.3 g/100 g putrescine, whereas a low concentration of spermine was detected only in the control diet (0% putrescine).

The diets did not affect body weight gain, feed intake, or feed conversion in poults at the end of 0–7 and 7–14 d periods before challenge. Dietary putrescine concentrations also did not affect these variables in the unchallenged birds during the challenge period (14–20 d) or the recovery period (21–24 d). There was a linear increase in the weight gain of poults (P = 0.031) at the end of recovery period in challenged birds with increasing levels of putrescine in the diets. A quadratic decrease (P = 0.02) in feed intake was seen at the end of recovery period (21–24 d) in the challenged birds fed dietary putrescine. There was a linear decrease (P = 0.03) and a quadratic decrease (P = 0.03), respectively, in the feed conversion of poults fed graded levels of dietary putrescine at the end of the challenge (14–20 d) and recovery (21–24 d) periods.

Fecal composition and lesion scores

The diets did not affect the excreta fat concentration in challenged (13.4 ± 1.46 g/100 g) or unchallenged (5.73 ± 0.53 g/100 g) birds during the challenge period. The diets also did not affect excreta dry matter digestibility (challenged: 65.9 ± 0.62 g/100 g; unchallenged: 71.6 ± 0.30 g/100 g) or gross energy content (challenged: 16,334 ± 290 MJ/kg; unchallenged: 19,023 ± 211 MJ/kg). Excreta oocyst counts were also unaffected by diet (163,752 ± 68,453 oocysts/g feces). There was no significant effect of diet on lesion scores in duodenum (d 20: 1.37 ± 0.71; d 24: 1.35 ± 0.72), jejunum (d 20: 1.32 ± 0.79; d 24: 1.26 ± 0.61) and ileum (d 20: 1.27 ± 0.37; d 24: 1.17 ± 0.54) at the end of challenge period (d 20) or at the end of recovery period (d 24). No lesions were observed in the unchallenged birds.

Intestinal protein and DNA concentrations

At the end of the challenge period (d 20), dietary putrescine supplementation resulted in a linear increase (P = 0.024) in jejunal protein concentration and a quadratic increase (P = 0.041) in the ileal protein concentration of the challenged group. There was also a linear decrease (P = 0.046) in ileal DNA concentration in the challenged group. A linear increase (P = 0.005) was observed in the jejunal protein-to-DNA ratio in response to dietary putrescine supplementation in the challenged group. The diets had no effect on tissue concentrations of protein or DNA, or on the protein-to-DNA ratio in the unchallenged group. The diets also did not affect these variables at the end of recovery period (d 24) in the challenged or unchallenged groups (data not shown).

Morphometric indices

    Duodenum, challenge period. Morphometric changes in duodenum resulting from the feeding of dietary putrescine during the challenge period (d 14–20) indicated that in the unchallenged group, there was a quadratic decrease (P = 0.028) in villus height and a quadratic increase in the thickness of the submucosa (P = 0.05) (data not shown). In the challenged group, however, there were significant quadratic increases in villus height, crypt depth, villus width, and thickness of the submucosa and muscularis layer, as well as in the apparent surface area of the villus, with increasing levels of putrescine in the diet (Table 3).

    Ileum, challenge period. There was a quadratic decrease (P = 0.04) in the villus height and a linear increase (P = 0.02) in the apparent surface area of the villus in the unchallenged group, in response to dietary putrescine supplementation (data not shown). In the challenged group there were quadratic decreases observed in villus height, height to crypt ratio, and apparent surface area of the villus (Table 3). There were also linear increases in the crypt depth and thickness of the muscularis layer of the villi with increasing levels of dietary putrescine.

    Duodenum, recovery period. Morphometric changes in the duodenum resulting from dietary putrescine showed that, in the unchallenged groups, there was a quadratic increase (P = 0.02) in the thickness of the submucosa. In the challenged group, there was a quadratic decrease in villus height (P = 0.046) and height-to-crypt ratio (P = 0.045) in response to increasing levels of dietary putrescine. There was a quadratic increase (P = 0.02) in villus width in challenged birds fed diets with increasing levels of dietary putrescine (data not shown).

    Jejunum, recovery period. There were quadratic decreases in villus height (P = 0.033) and the height-to-crypt ratio (P = 0.011) of the villi in the unchallenged group in response to diets. In the challenged group, there were similar quadratic decreases in villus height (P = 0.011) and height-to-crypt ratio (P = 0.026) with increasing levels of putrescine in the diets. We also observed a quadratic increase in crypt depth (P = 0.04) and a linear increase (P = 0.039) in thickness of the submucosa. There was a linear decrease (P = 0.032) in the villus width of the poults in the challenged group (data not shown).

    Ileum, recovery period. Linear increases in crypt depth (P = 0.05) and thickness of the muscularis layer (P = 0.04) were seen in unchallenged birds with increasing levels of putrescine in the diets. In the challenged birds, there were significant linear decreases in villus width (P = 0.02) and thickness of the muscularis layer (P = 0.02) and a quadratic increase (P = 0.05) in thickness of the submucosa in response to dietary putrescine supplementation (data not shown).

	Discussion

TOP ABSTRACT Introduction Materials and Methods Results Discussion LITERATURE CITED

 
Polyamine concentrations of the experimental diets

The analyzed dietary putrescine concentrations were lower than expected. The loss of some putrescine in the feed could have occurred during the mixing of the diets. It is also possible that the unstable nature of the purified free-base putrescine used in the study resulted in some lability. The loss of putrescine was small and consistent across the treatments and is in agreement with previous studies (19). No histamine was detected in diets, which is an indication of good quality raw materials. This resulted in no adverse effects of histamine in the trial, as well as no possibility of interaction with other polyamines. Spermidine was fairly constant in all diets, whereas very low quantities of spermine were detected only in the control diet. There is likely no importance to the dietary spermidine and spermine, because these are metabolites of putrescine and substantial quantities of putrescine are metabolized after ingestion as tissue levels rise.

Growth

In the challenged group, reduced growth of birds resulted from the mixed coccidial infection in the absence of mortality. This was because of low feed consumption during the challenge period. Immediately after infection, depending on the dose applied, the growth rate declined during the prepatent period, and then endogenous asexual replicative cycles occurred, where parasites actively multiply within enterocytes and destroy these cells.

There was a decline in the feed conversion ratio of challenged birds, regardless of diet, during the challenge period. This led to consistently reduced weight gains in all birds regardless of diet. The almost similar reduction in rate of weight gain among the dietary treatments in the challenged group shows that the level of dietary putrescine supplementation had no effect on prevention of infection from coccidia. During the recovery period, the significant increase in the feed intake of birds in the challenged group led to a significant increase in weight gains with increasing levels of dietary putrescine. This shows that positive effects of putrescine supplementation on weight gains occurred during the recovery period. This was because of higher feed intake and was also possibly due to beneficial effects of putrescine on the integrity and health of the intestinal mucosa.

Conway et al. (20) concluded, however, that lesions from a coccidial challenge in unmedicated or medicated birds were not necessarily associated with a reduction in weight gain. It appears that the selection of an appropriate species of coccidia is important in setting up a model. In this experiment, a mixed infection was used to mimic field conditions and proved appropriate. The dose of oocysts used was important in developing the appropriate model.

Fecal composition and lesion scores

Diet did not affect fecal composition and lesion scores, which indicates that dietary putrescine had no effect on the replicative potential of coccidia. We conclude that the differences in weight gain between the challenged and unchallenged birds were due to differences in feed intake.

Intestinal protein and DNA concentrations

The significant effects of diet on jejunal protein and DNA during the challenge period may have been due to the initial loss in intestinal protein content, which is a result of desquamation of the mucosa, typical in coccidial infections, followed by the anabolic effect of putrescine.

The decrease in ileal DNA concentration seen with increasing levels of dietary putrescine fed to challenged birds could be due to increasing putrescine toxicity. The ratio of protein to DNA reflects cell size and development of tissues. An increase in this variable in response to higher levels of dietary putrescine in the jejunum in challenged birds indicates that there was an increase in the metabolic activity of the intestinal tissue, due to infection, and the anabolic effect observed was due to exogenous dietary putrescine. This ratio is dependent on the protein content and is the main cause for this response.

Morphometric indices

    Duodenum, challenge period. The effects of challenge were most obvious on villus height, crypt depth, villus width, and thickness of submucosa and muscularis layers. During the prepatent period, coccidial species localize within enterocytes, causing damage to the epithelium of the duodenum. In our experiment, villus height was reduced in the challenged group (villus atrophy) by 200–300 µm, compared with the unchallenged birds, regardless of diet. Although there was a reduction in villus height, such transient changes may not directly affect nutrient use (21). There can be a compensatory mechanism causing increased villus width, which was seen in our experiment. Crypt depth increased (crypt hyperplasia) 80–100 µm more than unchallenged birds, with an increase of 25–30 µm in villus width (villus hyperplasia) compared with unchallenged birds. The morphometric measurements of the mucosa of the small intestine can be affected by other factors, including feed restriction, competition with normal gastrointestinal microflora, intracellular parasitism by coccidia, fiber content of diet, and changes in growth or productive needs (22).

The beneficial effects of dietary putrescine were clear in all morphometric indices studied in the challenged group. Effects were significant, even with 0.1 g/100 g dietary putrescine supplementation, and the improvement in morphometric indices continued to be evident with 0.3 g/100 g dietary putrescine supplementation. There were no evident toxic effects of dietary putrescine on the any of the morphometric indices studied. It appears that the duodenum is extremely receptive to the beneficial effects of exogenous putrescine supplementation in challenged birds.

    Duodenum, recovery period. The overall effects in the recovery period were mainly in villus height, crypt depth, and thickness of the muscularis layer. The villus height in challenged birds was 100–120 µm shorter than for control groups. This shows that substantial healing of the villi had occurred. An increase in crypt depth of 18–20 µm more than control groups presumably represents hyperplasia, to compensate for the lack of production of cells that migrate along the villus and mature to restore full function of the villus. There were beneficial effects of exogenous dietary putrescine on villus height and villus width. These effects were less pronounced, however, than in the challenge period. This could be expected, as a marked response to dietary putrescine was already seen in the challenge period. In the recovery period, birds appeared to be less responsive to the effects of dietary putrescine, with respect to duodenal morphology. This resulted in higher feed intake, better feed conversion ratios, and subsequent higher weight gains in the recovery period. At the tissue level, dietary putrescine prevented damage to the mucosa, which was not reflected in feed intake and weight gain. It appears that feed intake and weight gains can be regarded as secondary effects and it takes time for these effects to appear; hence they were seen in the recovery period.

    Jejunum, challenge period. Infection affected crypt depth, villus width, thickness of the submucosa and muscularis layers, and apparent villus surface area. These findings were similar to the changes in the duodenum during the challenge period. Duodenum and jejunum are affected by different species of coccidia and their pathogenecity depends on several factors. The absence of response to dietary putrescine in the challenged group could be due to species of coccidia affecting the jejunum.

    Jejunum, recovery period. The benefits of 0.3 g/100 g dietary putrescine supplementation on villus height was seen in both the unchallenged and challenged groups. It appeared that the challenged group of poults was more responsive to effects of dietary putrescine than the unchallenged group, and that the benefits of putrescine supplementation in the jejunum of the challenged group were less pronounced than in the duodenum.

    Ileum, challenge period. Supplementation of 0.3 g/100 g putrescine was most beneficial to villus height in both the unchallenged and challenged groups, as well as to crypt depth in challenged birds. In the challenge period, the response of ileum to dietary putrescine was less pronounced than that of jejunum.

    Ileum, recovery period. In the recovery period, the morphometric indices of the unchallenged and challenged groups were similar. The effect of dietary putrescine in unchallenged and challenged groups seemed to be unspecific and no definite conclusions about the response could be made.

The overall study of morphometric indices in the small intestine between the challenge (14–20 d) and recovery periods (21–24 d) indicates that, in the challenge period, the duodenum benefited most from dietary putrescine supplementation, followed by the ileum and jejunum. In the recovery period, however, jejunum of the challenged birds responded most positively to dietary putrescine.

The coccidial challenge resulted in declines in weight gain and negatively affected the morphology of the small intestine of poults during the challenge period. In the recovery period, the poults of the challenged group gained weight at a higher rate than in the challenge period because of higher feed intake, as well as an improvement in the morphometric indices. Overall, it would appear that the benefits of supplemental dietary putrescine were greatest in the recovery period. In conclusion, increasing dietary putrescine reduced the impact of challenge, and increases in feed intake and feed conversion ratio and improved weight gains, resulting from increased recovery of intestinal morphometric indices, were observed in the recovery period. Dietary putrescine supplementation in poult diets may, therefore, promote recovery from subclinical coccidiosis or in other mild gastrointestinal disturbances.

	ACKNOWLEDGMENTS

 
The authors gratefully acknowledge the assistance of Mohammed Tahir and Julie Cobean and the statistical advice of Dr. Ian McMillan and Dr. Margaret Quinton.

	FOOTNOTES

 
¹ Financial support for this study was provided by Ontario Ministry of Agriculture and Food and The Natural Sciences and Engineering Research Council of Canada.

Manuscript received 24 March 2006. Initial review completed 14 April 2006. Revision accepted 5 June 2006.

	LITERATURE CITED

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