Dose-Response Relationship between Dietary Polyphenols from Acorns and Parotid Gland Hypertrophy in Pigs


Proline contents of parotid glands (PG) in pigs constantly increase after the inclusion of different amounts of ripe hulled acorns in the diet providing high polyphenols levels. The dose-response relationship was estimated on natural hydrolizable tannins (expressed as tannic acid equivalent TAE) amounts of 25.8 to 36.1 g TAE/kg DM in experimental diets. Macroscopic and histological morphometry of parotid glands greatly varied according to feed intake and dosages of TAE ingested. The PG response (hypertrophy grade) on acorns’ tannins content in the diet was positively correlated (R2 = 0.748): the response to the protein precipitating activity (PPA) of tannins consisted of a functional parotidomegaly (hypertrophy), 1.34 up to 3.55 folds than control PGs, following an oral dosage 0.596 up 1.72 TAE g·kg body weight·d-1 respectively, after one week exposure.

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M. Cappai, P. Wolf, W. Pinna and J. Kamphues, "Dose-Response Relationship between Dietary Polyphenols from Acorns and Parotid Gland Hypertrophy in Pigs," Food and Nutrition Sciences, Vol. 3 No. 9, 2012, pp. 1261-1268. doi: 10.4236/fns.2012.39166.

1. Introduction

1.1. Salivary Glands and Physiology of Secretion

Salivary glands cover several physiological functions. The usefulness of saliva can be underlined in a series of multiple biological activities, as it moistens food and dissolves some constituent of it to provide the stimulation for taste receptors; helps to form the food particles into a bolus in order to ease the swallowing and passage through cranial parts of the gastrointestinal tract; provides antibacterial enzymes (lysozime), but also a proper medium for microbes growth in ruminants by the neutralization of organic acids produced in the rumen during bacterial fermentation; plays a key-role in the urea cycle and is involved in the digestive role through salivary amylase, or ptyalin, which amylolytic property increases progressively from the cat, fox, dog, rabbit, guinea pig to the pig [1].

1.2. Parotid Gland Secretory Activity as a First Line of Defense against Dietary Tannins

Parotid glands and, to a minor extent, mandibular and submaxillary glands (depending on species and zoological order) are involved in the coping activity with tannins in food, by adapting their secretory function towards dietary biological active substances presence in the mouth. With special regards to parotid gland, the response to those dietary active compounds modulate either quantitatively or qualitatively the salivation. Such strategy developed across animal species, throughout evolutionary adaptation to food seasonal availability and low to high amounts of tannins, can be reasonably considered as a flexible interaction between animals and environment

1.3. Biological Role of Polyphenols

As a matter of fact, polyphenolic compounds are plant secondary metabolites (PSM) which exert to some extent a protective measure for allowing the development of vegetal tissues and organs [2], conferring resistance against predators, above all birds [3,4] and greenbugs [5] and microbial infection, like moulds [4,6] and bacteria [7-9], but also showing some ecological impact by a given control of vegetal sprouting: tannins bond to nitrogen in decaying vegetal tissue, contribute to the limitation of new organic matter building up in the soil [10]. From a nutritional point of view, high tannins diets consumption leads to different episodes in humans and animals. Scientific references report evident correlation between dietary polyphenols rich diets and health enhancing properties: antioxidant properties [11-13], antibacterial activity on different bacterial strains in vitro and in vivo [7,14-20], antiparasitic [21], antiulcerogenic [22-24] antidiarrhoic [25], antimutagenic [26-33], antitumor [34-38], and some neoplastic cell line apoptosis [39,40]. On the other hand, high tannins diets might also result in detrimental effects like hepatotoxicity [41,42], toxic nephrosis [43], oesphageal cancer [44], depression of feed intake and growth rate in many animal species [45-51].

1.4. Salivary Tannins Binding Proteins: The Role of Proline Rich Proteins (PRPs) across Animal Species

The parotid gland hypertrophic response to counteract the protein precipitating activity exerted by acorns tannins from own previous trials (unpublished data) showed to be more intense in young pigs, rather than in elder pigs, but independent on time of exposure, when one week vs four 4 weeks of experimental feeding were compared: a very fast and constant reaction towards an inclusion of 50% of acorns in the diet (25.8 g TAE/kg DM), started to be detected from 24 h on, after the first consumption of the acorns combined diet. As reported in literature, common characteristics of proteins and polypeptides with high affinity for tannins are their open loose structure, a high proline content and small size [46,52,53]. The capability of some animal species to counteract high dietary tannins was seen to be linked to salivary proline rich proteins (PRPs) ancestral function in the maintenance of oral health at a basal level of mucoproteins secretion, increased by high tannins presence in the diet [54], as observed in pigs [55], in which an increase up to a 16.8% of proline/crude protein ratio of parotid glands chemical composition was seen (Figure 1) after the inclusion of a 70% of acorns in the diet, providing high amounts of hydrolizable tannins (36.1 g TAE·kg–1 DM, expressed as tannic acid equivalents). Clauss, et al. (2005) [56] refer that from carnivores through omnivores to exclusive plant-eaters, the dietary nitrogen level is progressively reduced while the presence of dietary tannins increases. Due to selective pressure, the evolutionary adaptation of animal species induced from a milder up to a stronger capability to cope with high tannins amounts in the diet, can explain why some species are able to counteract dietary tannins PPA while others do not [56,57]. Such evolutionary adaptation is more efficient in animals which might get advantage of a pulsed production of salivary tannins binding protein (TBP), increased from basal levels, depending on seasonal variation of tannins ingestion with food [56]. The hypothesis tested in the present study considered the correlation between different percentages of acorns inclusion in the diet (50% and 70% of the diet, as fed) and the consequent parotid gland response in terms of hypertrophy grades and secretory activity at microscopic level of the gland to the different amounts of dietary tannins based on different dosages, in pigs used as an animal experimental model, capable to tolerate high amounts of tannins in the diet.

Figure 1. Analyzed chemical composition of parotid glands in pigs fed on control diet (left) vs acorns combined diet (right) for proline and crude protein contents. The proline/ crude protein ratio in pigs fed on acorns combined diets averagely increases of a 16.8% ± 11% (Mean ± SD). In the graph, the range of values expressed as percentage is displayed on increased proline to total crude protein of parotid glands from pigs exposed to acorns tannins.

2. Materials and Methods

2.1. Animals, Diets and Feeding Plan

A total of 24 German Landrace cross-bred pigs without contact to acorns before, were fed three different experimental diets for 7 days. Different proportions of fresh acorns included in the diet were used: diet A, 70% acorns, providing 36.1 g TAE/kg DM; diet B, 50% acorns, providing 25.8 g TAE/kg DM; diet C, 0% acorns, providing undetectable TAE and representing the control, based totally on a pelleted complete diet. Chemical composition of the diets was determined by Weende analysis described by Naumann and Bassler (2004) [58] on replicates while the polyphenols contents were estimted by Folin-Ciocalteau (1927) method, modified by Waterman and Mole (1994) [59]. The chemical composition of the three experimental diets is reported in Table 1. Real intake of feed by each pig individually housed was reported daily and averaged to estimated DM intake/kg body weight and g TAE·kg1 BW·d1 ingested. All animals were sacrificed eight h after the last meal (on day 8).

2.2. Parotid Glands Inspection and Microscopic Check

Both PGs of each sacrificed pig were surgically removed from the carcass, taking care of the excision in toto. After removing the separable fat, lymphnodes and associated vessels, each PG was immediately weighed on a digital scale to report fresh weight (g). Morphometric characteristics and macroscopic evaluation at visual inspection followed specific standard criteria developed in own previous trials [55]. Relative fresh weight of each parotid gland was calculated according to the body weight (BW) of the respective animal and expressed as percentage. Left and

Table 1. Analyzed chemical composition of the experimental diets.

right parotid glands were immediately fixed in formaldehyde (10%) for histological analysis. After dehydration and waxy paraffin embedding, two μm thick tissues sections were stained using Haematoxylin-Eosin (HE) and Periodic Acid’s Schiff stain (PAS). Slides were checked up by confocal microscope. Morphology and cytoplasm appearance of secretory cells followed criteria adopted in own previous trials [55]. Hyperplasia vs hypertrophy was evaluated. A statistic correlation and linear regression coefficients between tannins dosages and enlargement factors representing the parotidomegaly were calculated.

3. Results

3.1. Daily Feed Intakes and Dietary Tannins Ingestion from Different Acorns Inclusion in the Experimental Diets

The daily DM intake (in grams), expressed as percentage of body weight, did not differ statistically between pigs fed on diets including 50% either 70% of acorns. By contrast, daily DM intake in pigs fed on the control diet (0% acorns), appeared lower. This was explained as a way to fulfill energy requirements of animals, since the dry matter contents of the diets differed according to the inclusion of fresh unprocessed acorns, responsible to reduce the energy density of the combined pelleted complete diet. In addition, acorns provide high amounts of crude fibres (including lignin, above all), resulting in reduced digestibility rate of organic matter and lower expected metabolizable energy of the diet. Feed intake depression from acorns tannins in the diet can be excluded and this finding is in contrast with references [45-51] on reduced feed intake in different animal species observed after high tannins (from different botanical origin or synthetic included in the formulation) inclusion in diets. Different dosages of ingested tannins (g TAE·kg1 BW·d1) followed different DM intakes of combined diets, proportionally, up to a maximum of 1.71 g TAE·kg1 BW·d1.

3.2. Parotidomegaly Occurrence and Macroscopic Score (Enlargement Factor, EF)

Table 2 reports tannins intakes recorded throughout the experimental feeding (one week) for the three groups of animals according to acorns inclusion in the diet (70% vs 50% vs 0%) and entity of parotidomegaly, expressed as percentage of mass increase (70% and 50% acorns combined diets groups) compared to the parotid gland from the control diet (0% acorns combined diets).

Conflicts of Interest

The authors declare no conflicts of interest.


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