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Impact of Experimental Hyperlipidemia on Histology of Major Salivary Glands

Year 2009, Volume: 2009 Issue: 4, 283 - 291, 01.04.2009

Abstract

Objectives: To examine the histologic structure of major salivary glands in high-fat diet induced hyperlipidemic rats. Materials and Methods: Sixteen Wistar Albino rats were grouped as control group (CG) and hyperlipidemic group (HG). CG was fed a standard chow and HG was fed a high-fat diet. At the end of three months, blood samples were obtained for lipid analyses. For histological analysis, major salivary glands were evaluted under light microscopy. Results: In HG; the number of intracellular lipid droplets (ILD) in the major salivary glands significantly increased while the diameter of ILD significantly increased in the parotid and sublingual glands (p< 0.01). The cell types mainly affected were serous cells in the parotid and submandibular, serous demilunar cells and, to a lesser extent, mucous cells in the sublingual gland. Serum levels of all lipids were significantly correlated with the lipid numbers in the parotid and the sublingual glands. In the submandibular gland, only serum LDL and cholesterol levels were found to be significantly correlated with the lipid numbers (p<0.05). Conclusion: High-fat diet caused intracellular lipid accumulation in the parotid and sublingual glands without any structural alteration. Submandibular gland exerted a partial resistance to intracellular lipid accumulation. Turkish Başlık: Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi Anahtar Kelimeler: Deneysel hiperlipidemi; büyük tükürük bezleri; lipid birikimi ve Oil red O Amaç: Yağ içeriği zengin diyet ile beslenerek hiperlipidemi oluşturulan sıçanlarda, büyük tükürük bezlerinin histolojik yapısını incelemektir. Gereç ve Yöntemler: On altı adet Wistar Albino sıçanı kontrol grubu (KG) ve hiperlipidemik grup (HG) olmak üzere ikiye ayrıldı. CG standart yem, HG ise yağ içeriği zengin diyet ile beslendi. Üç ay sonunda, lipit analizi için kan örnekleri alındı. Histolojik değerlendirme için, büyük tükürük bezleri ışık mikroskobu ile incelendi. Bulgular: Hiperlipidemik gruba ait büyük tükürük bezlerinde hücre içi lipit damlacıklarının sayısında anlamlı bir artış görülürken, sublingual ve parotis bezinin hücre içi lipit damlacıklarının çapında anlamlı derecede artış tespit edildi (p<0.01). Parotis ve submandibular bezlerde esas olarak seröz hücreler, sublingual bezde ise seröz yarımlar ve daha az derecede müköz hücreler hiperlipidemiden etkilendi. Tüm serum lipit düzeyleri ile sublingual ve parotis bezde biriken lipit damlacıkları sayısı arasında istatistiksel olarak anlamlı korelasyon saptandı. Submandibular bezde ise, sadece LDL ve kolesterol düzeyleri ile lipit damlacıkları sayısı arasında anlamlı bir korelasyon tespit edildi (p<0.05). Sonuç: Yüksek yağ içeren diyet, parotis ve sublingual bezlerde yapısal bir değişikliğe neden olmaksızın, hücre içi lipit birikimine neden olmaktadır. Submandibular bez ise intraselüler lipit birikimine karşı kısmi bir direnç göstermektedir.

References

  • Han SS. An electron microscopic and radioauto- graphic study of the rat parotid gland after actino- mycin D administration. Am J Anat 1967;120:161-83.
  • Morris PA, Prout RE, Proctor GB, Garrett JR, Anderson LC. Lipid analysis of the major salivary glands in streptozotocin-diabetic rats and the effects of insulin treatment. Arch Oral Biol 1992;37:489-94.
  • Anderson LC, Suleiman AH, Garrett JR. Morphological effects of diabetes on the granular ducts and acini of the rat submandibular gland. Microsc Res Techn 1994;27:61-70.
  • Mahay S, Adeghate E, Lindley MZ, Rolph CE, Singh J. Streptozotocin-induced type 1 diabetes mellitus alters the morphology, secretory function and acyl lipid contents in the isolated rat parotid salivary gland. Mol Cell Biochem 2004;261:175-81.
  • Oliver C, Auth RE, Hand AR. Formation and fate of ethionine-induced cytoplasmic crystalloids in rat parotid acinar cells. Am J Anat 1979;155:185-99.
  • Radley JM. Ultrastructural changes in the rat sub- maxillary gland following isoprenaline. Z Zellforsch Mikrosk Anat 1969;97:196-211.
  • Sodicoff M, Pratt NE, Sholley MM. Ultrastructural radiation injury of rat parotid gland: a histopatholog- ic dose-response study. Radiat Res 1974;58:196-208.
  • Hand AR, Ho B. Liquid-diet-induced alterations of rat parotid acinar cells studied by electron micros- copy and enzyme cytochemistry. Arch Oral Biol 1981;26:369-80.
  • Hand AR. The effects of acute starvation on parotid acinar cells. Ultrastructural and cytochemical obser- vations on ad libitum-fed and starved rats. Am J Anat 1972;135:71-92.
  • Morawa AP, Han SS. Studies on hypoxia. 8. Ultrastructural and biochemical effects of prolonged exposure on rat parotid glands. Exp Mol Pathol 1974;21:268-87.
  • Kim SK, Allen ED. Structural and functional changes in salivary glands during aging. Microsc Res Tech 1994;28:243-53.
  • Maron DJ, Grundy SM, Ridker PM, Pearson TA. Dyslipidemia, other risk factors, and the prevention of coronary heart disease. In: Fuster V, Alexander RW, O’Rourke RA, Roberts R, King SB, Prystowsky EN, et al, editors. Hurst’s the heart. 11th ed. New York: McGraw-Hill; 2004. p. 1093-122.
  • Tuğrul A. Diabetes mellitus ve hipertansiyon. Trakya Univ Tip Fak Derg 2002;19:44-54.
  • Tuğrul A. Diabetes mellitus ve aterosklero- tik komplikasyonlar. Trakya Univ Tip Fak Derg 1994;11:305-11.
  • Rothbell EN, Duggan JJ. Enlargement of the parotid gland in disease of the liver. Am J Med 1957;22:367-72.
  • Markitziu A, Lustmann J, Uzieli B, Krausz Y, Chisin R. Salivary and lacrimal gland involvement in a patient who had undergone a thyroidectomy and was treated with radioiodine for thyroid cancer. Oral Surg Oral Med Oral Pathol 1993;75:318-22.
  • Scott J, Burns J, Flower EA. Histological analysis of parotid and submandibular glands in chron- ic alcohol abuse: a necropsy study. J Clin Pathol 1988;41:837-40.
  • Emekli-Alturfan E, Kasikci E, Yarat A. Peanuts improve blood glutathione, HDL-cholesterol level and change tissue factor activity in rats fed a high- cholesterol diet. Eur J Nutr 2007;46:476-82.
  • Arafa HM. Curcumin attenuates diet-induced hypercholesterolemia in rats. Med Sci Monit 2005;11:BR228-34.
  • Luna LG. Manual of histologic staining methods of the Armed Forces Institute of Pathology. New York: McGraw-Hill; 1960.
  • Frings CS, Fendley TW, Dunn RT, Queen CA. Improved determination of total serum lipids by the sulfo-phospho-vanillin reaction. Clin Chem 1972;18:673-4.
  • Naito HK. Hyperlipidemia, laboratory approaches. In: Pesce AJ, Kaplan LA, editors. Methods in clinical chemistry. Washington DC: Mosby Company; 1987. p. 1140-5.
  • Nguyen NT, Varela E, Sabio A, Tran CL, Stamos M, Wilson SE. Resolution of hyperlipidemia after lap- aroscopic Roux-en-Y gastric bypass. J Am Coll Surg 2006;203:24-9.
  • Davis HR, Vesselinovitch D, Wissler RW. Reticuloendothelial system response to hyperlipi- demia in rhesus and cynomolgus monkeys. J Leukoc Biol 1984;36:63-80.
  • Sano J, Shirakura S, Oda S, Hara T, Ishihara T. Foam cells generated by a combination of hyperglycemia and hyperlipemia in rats. Pathol Int 2004;54:904-13.
  • Goodpaster BH, Theriault R, Watkins SC, Kelley DE. Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 2000;49:467-72.
  • Wolf AM, Busch B, Kuhlmann HW, Beisiegel U. Histological changes in the liver of morbidly obese patients: correlation with metabolic parameters. Obes Surg 2005;15:228-37.
  • Nagato T, Masuno H. Lipid droplet accumulation and lipoprotein lipase activity in the rat salivary gland during the perinatal period. Arch Oral Biol 1993;38:1127-34.
  • Anderson LC, Garrett JR. Lipid accumulation in the major salivary glands of streptozotocin-diabetic rats. Arch Oral Biol 1986;31:469-75.
  • Anderson LC. Salivary gland structure and func- tion in experimental diabetes mellitus. Biomed Rev 1998;9:107-19.
  • Hand AR, Weiss RE. Effects of streptozotocin- induced diabetes on the rat parotid gland. Lab Invest 1984;51:429-40.
  • Stubbs CD, Smith AD. The modification of mamma- lian membrane polyunsaturated fatty acid composi- tion in relation to membrane fluidity and function. Biochim Biophys Acta 1984;779:89-137.
  • Spector AA, Yorek MA. Membrane lipid composition and cellular function. J Lipid Res 1985;26:1015-35.
  • Alam SQ, Ren YF, Alam BS. Effect of cholester- ol feeding on membrane fluidity, (Na+ + K+) ATPase, adenylate cyclase, [3H]-ouabain-, and [3H]-dihydroalprenolol-binding in rat submandibu- lar salivary glands. J Dent Res 1987;66:605-7.
  • McMurchie EJ. Dietary lipids and the regulation of membrane fluidity and function. In: Aloia RC, Curtain CC, Gordon LM, editors. Physiological regu- lation of membrane fluidity. New York: Alan R. Liss Inc.; 1988. p. 189-237.
  • Alam SQ, Mannino SJ, Alam BS. Reversal of diet- induced changes in adenylate cyclase activity and fatty acid composition of rat submandibular salivary gland lipids. Arch Oral Biol 1993;38:387-91.
  • Alam SQ, Abdel-Hakim SM, Alam BS, Ibrahim IY. Effect of essential fatty acid deficiency on G-proteins, cAMP-dependent protein kinase activity and mucin secretion in the rat submandibular salivary glands. Cell Signal 1995;7:773-81.
  • Izumi M, Hida A, Takagi Y, Kawabe Y, Eguchi K, Nakamura T. MR imaging of the salivary glands in sicca syndrome: comparison of lipid profiles and imaging in patients with hyperlipidemia and patients with Sjögren's syndrome. AJR Am J Roentgenol 2000;175:829-34.
  • Azevedo LR, Damante JH, Lara VS, Lauris JR. Age- related changes in human sublingual glands: a post mortem study. Arch Oral Biol 2005;50:565-74.
  • Sheikh JS, Sharma M, Kunath A, Fritz DA, Glueck CJ, Hess EV. Reversible parotid enlargement and pseudo-Sjögren's syndrome secondary to hypertrig- lyceridemia. J Rheumatol 1996;23:1288-91.
  • Kaltreider HB, Talal N. Bilateral parotid gland enlargement and hyperlipoproteinemia. JAMA 1969;210:2067-70.
  • Ramos-Casals M, Brito-Zerón P, Sisó A, Vargas A, Ros E, Bove A, et al. High prevalence of serum metabolic alterations in primary Sjögren's syndrome: influence on clinical and immunological expression. J Rheumatol 2007;34:754-61.
  • Anttila SS, Knuuttila ML, Sakki TK. Depressive symptoms as an underlying factor of the sensation of dry mouth. Psychosom Med 1998;60:215-8.

Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi

Year 2009, Volume: 2009 Issue: 4, 283 - 291, 01.04.2009

Abstract

Amaç: Yağ içeriği zengin diyet ile beslenerek hiperlipidemi
oluşturulan sıçanlarda, büyük tükürük bezlerinin
histolojik yapısını incelemektir.
Gereç ve Yöntemler: On altı adet Wistar Albino
sıçanı kontrol grubu (KG) ve hiperlipidemik grup (HG)
olmak üzere ikiye ayrıldı. CG standart yem, HG ise
yağ içeriği zengin diyet ile beslendi. Üç ay sonunda,
lipit analizi için kan örnekleri alındı. Histolojik değerlendirme
için, büyük tükürük bezleri ışık mikroskobu
ile incelendi.
Bulgular: Hiperlipidemik gruba ait büyük tükürük bezlerinde
hücre içi lipit damlacıklarının sayısında anlamlı
bir artış görülürken, sublingual ve parotis bezinin hücre
içi lipit damlacıklarının çapında anlamlı derecede artış
tespit edildi (p < 0.01). Parotis ve submandibular bezlerde
esas olarak seröz hücreler, sublingual bezde ise seröz
yarımlar ve daha az derecede müköz hücreler hiperlipidemiden
etkilendi. Tüm serum lipit düzeyleri ile sublingual
ve parotis bezde biriken lipit damlacıkları sayısı
arasında istatistiksel olarak anlamlı korelasyon saptandı.
Submandibular bezde ise, sadece LDL ve kolesterol
düzeyleri ile lipit damlacıkları sayısı arasında anlamlı bir
korelasyon tespit edildi (p < 0.05).
Sonuç: Yüksek yağ içeren diyet, parotis ve sublingual
bezlerde yapısal bir değişikliğe neden olmaksızın, hücre
içi lipit birikimine neden olmaktadır. Submandibular bez
ise intraselüler lipit birikimine karşı kısmi bir direnç göstermektedir.

References

  • Han SS. An electron microscopic and radioauto- graphic study of the rat parotid gland after actino- mycin D administration. Am J Anat 1967;120:161-83.
  • Morris PA, Prout RE, Proctor GB, Garrett JR, Anderson LC. Lipid analysis of the major salivary glands in streptozotocin-diabetic rats and the effects of insulin treatment. Arch Oral Biol 1992;37:489-94.
  • Anderson LC, Suleiman AH, Garrett JR. Morphological effects of diabetes on the granular ducts and acini of the rat submandibular gland. Microsc Res Techn 1994;27:61-70.
  • Mahay S, Adeghate E, Lindley MZ, Rolph CE, Singh J. Streptozotocin-induced type 1 diabetes mellitus alters the morphology, secretory function and acyl lipid contents in the isolated rat parotid salivary gland. Mol Cell Biochem 2004;261:175-81.
  • Oliver C, Auth RE, Hand AR. Formation and fate of ethionine-induced cytoplasmic crystalloids in rat parotid acinar cells. Am J Anat 1979;155:185-99.
  • Radley JM. Ultrastructural changes in the rat sub- maxillary gland following isoprenaline. Z Zellforsch Mikrosk Anat 1969;97:196-211.
  • Sodicoff M, Pratt NE, Sholley MM. Ultrastructural radiation injury of rat parotid gland: a histopatholog- ic dose-response study. Radiat Res 1974;58:196-208.
  • Hand AR, Ho B. Liquid-diet-induced alterations of rat parotid acinar cells studied by electron micros- copy and enzyme cytochemistry. Arch Oral Biol 1981;26:369-80.
  • Hand AR. The effects of acute starvation on parotid acinar cells. Ultrastructural and cytochemical obser- vations on ad libitum-fed and starved rats. Am J Anat 1972;135:71-92.
  • Morawa AP, Han SS. Studies on hypoxia. 8. Ultrastructural and biochemical effects of prolonged exposure on rat parotid glands. Exp Mol Pathol 1974;21:268-87.
  • Kim SK, Allen ED. Structural and functional changes in salivary glands during aging. Microsc Res Tech 1994;28:243-53.
  • Maron DJ, Grundy SM, Ridker PM, Pearson TA. Dyslipidemia, other risk factors, and the prevention of coronary heart disease. In: Fuster V, Alexander RW, O’Rourke RA, Roberts R, King SB, Prystowsky EN, et al, editors. Hurst’s the heart. 11th ed. New York: McGraw-Hill; 2004. p. 1093-122.
  • Tuğrul A. Diabetes mellitus ve hipertansiyon. Trakya Univ Tip Fak Derg 2002;19:44-54.
  • Tuğrul A. Diabetes mellitus ve aterosklero- tik komplikasyonlar. Trakya Univ Tip Fak Derg 1994;11:305-11.
  • Rothbell EN, Duggan JJ. Enlargement of the parotid gland in disease of the liver. Am J Med 1957;22:367-72.
  • Markitziu A, Lustmann J, Uzieli B, Krausz Y, Chisin R. Salivary and lacrimal gland involvement in a patient who had undergone a thyroidectomy and was treated with radioiodine for thyroid cancer. Oral Surg Oral Med Oral Pathol 1993;75:318-22.
  • Scott J, Burns J, Flower EA. Histological analysis of parotid and submandibular glands in chron- ic alcohol abuse: a necropsy study. J Clin Pathol 1988;41:837-40.
  • Emekli-Alturfan E, Kasikci E, Yarat A. Peanuts improve blood glutathione, HDL-cholesterol level and change tissue factor activity in rats fed a high- cholesterol diet. Eur J Nutr 2007;46:476-82.
  • Arafa HM. Curcumin attenuates diet-induced hypercholesterolemia in rats. Med Sci Monit 2005;11:BR228-34.
  • Luna LG. Manual of histologic staining methods of the Armed Forces Institute of Pathology. New York: McGraw-Hill; 1960.
  • Frings CS, Fendley TW, Dunn RT, Queen CA. Improved determination of total serum lipids by the sulfo-phospho-vanillin reaction. Clin Chem 1972;18:673-4.
  • Naito HK. Hyperlipidemia, laboratory approaches. In: Pesce AJ, Kaplan LA, editors. Methods in clinical chemistry. Washington DC: Mosby Company; 1987. p. 1140-5.
  • Nguyen NT, Varela E, Sabio A, Tran CL, Stamos M, Wilson SE. Resolution of hyperlipidemia after lap- aroscopic Roux-en-Y gastric bypass. J Am Coll Surg 2006;203:24-9.
  • Davis HR, Vesselinovitch D, Wissler RW. Reticuloendothelial system response to hyperlipi- demia in rhesus and cynomolgus monkeys. J Leukoc Biol 1984;36:63-80.
  • Sano J, Shirakura S, Oda S, Hara T, Ishihara T. Foam cells generated by a combination of hyperglycemia and hyperlipemia in rats. Pathol Int 2004;54:904-13.
  • Goodpaster BH, Theriault R, Watkins SC, Kelley DE. Intramuscular lipid content is increased in obesity and decreased by weight loss. Metabolism 2000;49:467-72.
  • Wolf AM, Busch B, Kuhlmann HW, Beisiegel U. Histological changes in the liver of morbidly obese patients: correlation with metabolic parameters. Obes Surg 2005;15:228-37.
  • Nagato T, Masuno H. Lipid droplet accumulation and lipoprotein lipase activity in the rat salivary gland during the perinatal period. Arch Oral Biol 1993;38:1127-34.
  • Anderson LC, Garrett JR. Lipid accumulation in the major salivary glands of streptozotocin-diabetic rats. Arch Oral Biol 1986;31:469-75.
  • Anderson LC. Salivary gland structure and func- tion in experimental diabetes mellitus. Biomed Rev 1998;9:107-19.
  • Hand AR, Weiss RE. Effects of streptozotocin- induced diabetes on the rat parotid gland. Lab Invest 1984;51:429-40.
  • Stubbs CD, Smith AD. The modification of mamma- lian membrane polyunsaturated fatty acid composi- tion in relation to membrane fluidity and function. Biochim Biophys Acta 1984;779:89-137.
  • Spector AA, Yorek MA. Membrane lipid composition and cellular function. J Lipid Res 1985;26:1015-35.
  • Alam SQ, Ren YF, Alam BS. Effect of cholester- ol feeding on membrane fluidity, (Na+ + K+) ATPase, adenylate cyclase, [3H]-ouabain-, and [3H]-dihydroalprenolol-binding in rat submandibu- lar salivary glands. J Dent Res 1987;66:605-7.
  • McMurchie EJ. Dietary lipids and the regulation of membrane fluidity and function. In: Aloia RC, Curtain CC, Gordon LM, editors. Physiological regu- lation of membrane fluidity. New York: Alan R. Liss Inc.; 1988. p. 189-237.
  • Alam SQ, Mannino SJ, Alam BS. Reversal of diet- induced changes in adenylate cyclase activity and fatty acid composition of rat submandibular salivary gland lipids. Arch Oral Biol 1993;38:387-91.
  • Alam SQ, Abdel-Hakim SM, Alam BS, Ibrahim IY. Effect of essential fatty acid deficiency on G-proteins, cAMP-dependent protein kinase activity and mucin secretion in the rat submandibular salivary glands. Cell Signal 1995;7:773-81.
  • Izumi M, Hida A, Takagi Y, Kawabe Y, Eguchi K, Nakamura T. MR imaging of the salivary glands in sicca syndrome: comparison of lipid profiles and imaging in patients with hyperlipidemia and patients with Sjögren's syndrome. AJR Am J Roentgenol 2000;175:829-34.
  • Azevedo LR, Damante JH, Lara VS, Lauris JR. Age- related changes in human sublingual glands: a post mortem study. Arch Oral Biol 2005;50:565-74.
  • Sheikh JS, Sharma M, Kunath A, Fritz DA, Glueck CJ, Hess EV. Reversible parotid enlargement and pseudo-Sjögren's syndrome secondary to hypertrig- lyceridemia. J Rheumatol 1996;23:1288-91.
  • Kaltreider HB, Talal N. Bilateral parotid gland enlargement and hyperlipoproteinemia. JAMA 1969;210:2067-70.
  • Ramos-Casals M, Brito-Zerón P, Sisó A, Vargas A, Ros E, Bove A, et al. High prevalence of serum metabolic alterations in primary Sjögren's syndrome: influence on clinical and immunological expression. J Rheumatol 2007;34:754-61.
  • Anttila SS, Knuuttila ML, Sakki TK. Depressive symptoms as an underlying factor of the sensation of dry mouth. Psychosom Med 1998;60:215-8.
There are 43 citations in total.

Details

Primary Language Turkish
Journal Section Articles
Authors

Rabia Pişiriciler This is me

Esin Çalışkan-ak This is me

Ebru Emekli-alturfan This is me

Ayşen Yarat This is me

Yurdagül Canberk This is me

Publication Date April 1, 2009
Published in Issue Year 2009 Volume: 2009 Issue: 4

Cite

APA Pişiriciler, R., Çalışkan-ak, E., Emekli-alturfan, E., Yarat, A., et al. (2009). Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi. Balkan Medical Journal, 2009(4), 283-291.
AMA Pişiriciler R, Çalışkan-ak E, Emekli-alturfan E, Yarat A, Canberk Y. Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi. Balkan Medical Journal. April 2009;2009(4):283-291.
Chicago Pişiriciler, Rabia, Esin Çalışkan-ak, Ebru Emekli-alturfan, Ayşen Yarat, and Yurdagül Canberk. “Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi”. Balkan Medical Journal 2009, no. 4 (April 2009): 283-91.
EndNote Pişiriciler R, Çalışkan-ak E, Emekli-alturfan E, Yarat A, Canberk Y (April 1, 2009) Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi. Balkan Medical Journal 2009 4 283–291.
IEEE R. Pişiriciler, E. Çalışkan-ak, E. Emekli-alturfan, A. Yarat, and Y. Canberk, “Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi”, Balkan Medical Journal, vol. 2009, no. 4, pp. 283–291, 2009.
ISNAD Pişiriciler, Rabia et al. “Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi”. Balkan Medical Journal 2009/4 (April 2009), 283-291.
JAMA Pişiriciler R, Çalışkan-ak E, Emekli-alturfan E, Yarat A, Canberk Y. Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi. Balkan Medical Journal. 2009;2009:283–291.
MLA Pişiriciler, Rabia et al. “Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi”. Balkan Medical Journal, vol. 2009, no. 4, 2009, pp. 283-91.
Vancouver Pişiriciler R, Çalışkan-ak E, Emekli-alturfan E, Yarat A, Canberk Y. Deneysel Hiperlipideminin Büyük Tükürük Bezlerinin Histolojisi Üzerine Etkisi. Balkan Medical Journal. 2009;2009(4):283-91.