Effects of induced-kwashiorkor on salivary parameters in Wistar rats

Rezumat

Background: This study was undertaken to determine changes induced by protein malnutrition (kwashiorkor) in
the secretory functions of salivary glands and biochemical parameters of salivary fluid using rats.

Methods: Eighteen male Wistar rats were randomly divided into two groups (control and kwarshiorkor) of 9 rats each. The rats were fed with normal diet and low protein diet (2% protein) respectively for a period of 6 weeks. Stimulated saliva samples using pilocarpine (10mg/kg body weight i.p.) were collected and salivary glands (parotid and submandibular) were surgically removed. Biochemical analysis of salivary secretion using salivary lag time, flow rate, pH, total protein and concentrations of electrolytes (Na+ , K+ , Ca++, Cl- , HCO2- 3, PO4 ) were
conducted and compared. Morphological assessment of the salivary glands was done using heamatoxyline-eosin and Alcian blue stains.

Results: Body weights decreased in the kwashiorkor group. Weights of submandibular and parotid glands (right and left) were lower in the kwashiorkor group compared to the normal diet group. The mean salivary lag time was increased while the salivary flow rate was reduced in the kwashi orkor group compared to normal diet group. Salivary electrolytes and total protein analysis showed reduced concentration of sodium while potassium and bicarbonate concentrations were increased in the kwashiorkor group compared to the normal diet group. Histological analysis of the H–E and alcian blue stained salivary glands in the kwashiorkor group exhibited moderate to severe acinar cell atrophy, periductal fibrosis and reduced mucin content.

Conclusion: These findings suggest the role of functional and biochemical changes in salivary secretion in the pathophysiology of oral diseases associated with protein malnutrition.

Keywords: Kwashiorkor; protein malnutrition; salivary glands; salivary lag time; salivary flow rate, rats

Résumé
Contexte: Cette étude a été entreprise pour déterminer les changements induits par la malnutrition protéique (kwashiorkor) dans les fonctions de sécrétion des glandes salivaires et les paramètres biochimiques de fluide salivaire en utilisant des rats.

Méthode: Dix-huit rats Wistar mâles ont été divisés au hasard en deux groupes de 9 rats chacun (contrôle et kwashiorkor). Les rats ont été nourris avec un régime alimentaire de régime normal en protéines et de régime faible en protéines (protéine 2%), respectivement, pour une période de 6 semaines. Des échantillons de salive stimulée en utilisant la pilocarpine (10 mg / kg de poids corporel i.p.) ont été recueillies et les glandes salivaires (parotides et sous-maxillaires) ont été enlevées chirurgicalement. L’analyse biochimique de la sécrétion salivaire utilisant le temps de latence salivaire, débit, pH, protéines totales et les concentrations d’électrolytes (Na +, K +, Ca ++, Cl-, HCO2-3, PO4) ont été réalisées et comparées. L’évaluation morphologique des glandes salivaires a été effectuée à l’aide d’hématoxyline-éosine et de taches Alcian bleues.

Résultats: Le poids corporel a diminué dans le groupe de kwashiorkor. Poids des glandes sous-maxillaires et parotides (droite et gauche) étaient plus faibles dans le groupe de kwashiorkor par rapport au groupe de régime alimentaire normal. Le temps moyen de latence salivaire a augmenté tandis que le taux de flux salivaire a été réduit dans le groupe de kwashiorkor par rapport au groupe de régime alimentaire normal. Les électrolytes salivaires et l’analyse de protéines totales ont montré une réduction en concentration de sodium tandis que les concentrations de potassium et de bicarbonate ont étéaugmentéesdanslegroupekwashi orkorparrapport aug roupederégi me ali mentairenormal.L’analysehi st ologi quedel’H–Eetde tachesAlci anbleuesdesglandessali vai resdanslegroupe dekwashi orkoront exposéesuneatrophi edes cellulesaci neuses allantdemodérée àsévère,fi brosepéri –canal et contenue rédui te en muci ne.

Conclusion: Ces résultats suggèrent le rôle des changements fonctionnels et biochimiques en sécrétion salivaire dans la physiopathologie des maladies buccales associées à la malnutrition protéique.

Mots-clés: kwashiorkor; malnutrition en protéines; glandes salivaires; temps de latence salivaires; débit salivaire, rats

Correspondence: Dr. Taye J. Lasisi, Department of Physiology, College of Medicine, University of Ibadan, Ibadan, Email: jameelahlasisi@yahoo.com

pdf (engleză)

Referințe

Greabu M, Battino M, Mohora M, et al. Saliva –a diagnostic window to the body both in health and in disease. J Med Life 2009; 2:124-132.

Farnaud SJ, Kostic O, Getting SJ and Renshaw D. Saliva: physiology and diagnostic potential in health and disease. Scientific World Journal. 2010;10: 434-456.

Kaufman E and Lamster IB. The diagnostic applications of saliva – a review. Crit Rev Oral Biol Med. 2002;13:197-212.

Forde MD, Koka S, Eckert SE, et al. Systemic assessments utilizing saliva: part 1. General consideration and current assessments. Int J Prosthodont. 2006;19:43-52.

Fujimaki Y, Tsunoda K, Ishimito S, et al. Non-invasive objective evaluation of radiotherapy induced dry mouth. J Oral Pathol Med 2014;43:97-102.

Lasisi TJ and Fasanmade AA. Saliva composition in diabetic and non-diabetic patients.Niger J Physiol Sci. 2012;27:79-82.

Wendy SG. Kwashiorkor and the gut microbioata. N Engl J Med. 2013;368:1746-1747.

Luchuo EB, Paschal KA, Ngia G, et al. Malnutrition in Sub – Saharan Africa: burden, causes and prospects. Pan Afr Med J. 2013;15:120.

Watson RR, John TG, McMurray DN and Reyes MA. Pancreatic and salivary amylase activity in under nourished Colombian children. Am J Clin Nutr. 1977;30:599-604.

Menaker L and Navia JM. Effect of under nutrition during the perinatal period on caries development in the rat: effects of under nutrition on biochemical parameters in the developing submandibular salivary glands. J Dent Res. 1973;52:688-691.

Elverdin JC, Chiarenza A and Luchelli MA. Protein free diet feeding: effects on sympathetic activity and salivary evoked secretion in the submandibular gland of rat. Arch Oral Biol. 2006;51:621-628.

Marosti AR, Natali de Almeida F, Franzoi de Moraes S, et al. Effects of the cafeteria diet on the salivary glands of trained and sedentary Wister rats. Acta Scientiarum Biological Sci 2012; 34(1):113-118.

Watson RR and Antal M. Effect of moderate chronic protein deficiency on rat salivary components. J Nutr. 1980;110:771-777.

Johansson I and Ericsson T. Saliva composition and caries development during protein deficiency and beta receptor stimulation or inhibition. J Oral Pathol. 1987;16:145-149.

Johansson I, Lenander-Limikari M and Saellstrom AK. Saliva composition in Indian Children with chronic protein energy malnutrition. J Dent Res. 1994;7:11-19

Olowookere JO, Konji VN, Makawiti DW, et al. Defects in resting metabolic rates and mitochondrial respiration in kwashiorkor and dietary obese rats. J Comp Physiol B. 1991;161:319-322.

Choi JS, Park IS, Kim SK, et al. Analysis of age related changes in the functional morphologies of salivary glands in mice. Arch Oral Biol. 2013;58:1635-1642.

Schales O and Schales SS. A simple and accurate method for the determination of chloride in biological fluids. J. Biol. Chem.1941; 140 (5); 879-882.

Bing Q, Takanori N, Heroshi S and Masataka M. Pilocarpine induced salivary fluid secretion in the perfused submandibular gland of rat. J Med Invest. 2009;56(Suppl):281-283.

Carpenter GH, Osailan SM, Correia P, et al. Rat salivary gland ligation causes reversible secretory hypofunction. Acta Physiol. 2007;189:241-249.

Anderson LC and Garrett JR. Neural regulation of blood flow in the rat submandibular gland. Eur J Morphol. 1998;36:213-218.

Stojic D, Pesic S, Radenkovic M, et al. Responses of human submandibular artery to Ach and VIP. J Dent Res. 2007;86:565-570.

Ekstrom J. Role of nonadrenergic, noncholinergic autonomic transmitters in salivary glandular activities in vivo. In: Garrett JR, Ekstrom J, Anderson LC (eds). Neural Mechanisms of Salivary Secretion 1999, pp. 94-130. Karger, Basel.

Baum BJ and Wellner RB. Receptors in salivary glands. In: Garrett, J.R., Ekstrom, J. and Anderson, L.C. (eds) Neural Mechanisms of Salivary Secretion 1999, pp. 44-58. Karger, Basel.

Harmer AR, Gallacher DV and Smith PM. Role of Ins (1,4,5)P-3, cADP-ribose and nicotinic acid-adenine dinucleotide phosphate in Ca2+ signaling in mouse submandibular acinar cells. Biochem J. 2001; 353:555-560.

Psoter WJ, Spielman AL, Gebrian B, et al. Effects of childhood malnutrition on salivary flow and pH. Arch Oral Biol. 2008;53(3):231-237.

Anderson LC, Martin DJ, Phillips DL, et al. The influence of gender on parasympathetic vasodilation in the submandibular gland of rat. Exp Physiol. 2006; 91:435-444.

Garrett JR, Proctor GB, Zhang XS, et al. Constitutive secretion of kallikrein in vivo from rat submandibular glands, Eur J Morphol. 1998; 36:86-91.

Schneyer LH, Young JA and Schneyer CA. Salivary secretion of electrolytes. Physiol Rev. 1972;52:720-727.

Lee MG, Ohana E, Park HW, et al. Molecular mechanism of pancreatic and salivary gland fluid and HCO3 secretion. Physiol Rev. 2012;92:39-74.

Cook DI, Dinudom A, Komwatana P, et al. Patch clamp studies on epithelial sodium channels in salivary duct cells. Cell Biochem Biophys. 2002;36:105-113.

Etukudo M, Agbedana O, Akang O and Osifo B. Biochemical changes and liver tissue pathology in weaning Wistar albino rats with protein energy malnutrition (PEM). Afr J Med Med Sci. 1999;28:43-47.

Erinoso HO, Akinbami FO and Akinyinka OO. Prognostic factors in severely malnourished hospitalized Nigerian children. Anthropometric and biochemical factors. Trop Geogr Med. 1993;45:290-293.

Mann MD, Bowie MD and Hanse JD. Total body potassium and serum electrolyte concentrations in protein energy malnutrition. S Afr Med J. 1975;49:76-78.

Frenk S, Peres-Ortis B, Murquia T, et al. Serum ionized calcium in Mexican protein energy malnourished children. Arch Med Res. 2000;31:497-499.

Freiman I, Pettifor JM and Moodley GM. Serum phosphorus in protein energy malnutrition. J Pediatr Gastroenterol Nutr. 1982;1:547-550.

Waterlow JC and Golden MH. Serum inorganic phosphate in protein energy malnutrition. Eur J Clin Nutr. 1994;48:503-506.

Takahashi S, Shinzoto K, Nakamura S, et al. The role of apoptosis and mitosis in atrophy of rat sub lingual gland. Tissue cell. 2002;34:297-304.

Ferreira AM, Piza IG and Fava de Moraes F. Histological, morphometric and histochemical changes in the submandibular gland of the rat under experimental protein calorie malnutrition. J Biol Buccale. 1985;13:45-53.

Brooks SE and Golden MH. The exocrine pancreas in kwashiorkor and marasmus. Light and electron microscopy. West Indian med J. 1992; 41:56-60.

Choi JS, Park IS, Kim SK, et al. Morphometric and functional changes of salivary gland dysfunction after radioactive iodine ablation in a murine model. Thyroid. 2013;23:1445-1451.