Histopathological features and metabolic disorders in Tunisian rodent Psammomys obesus fed high-caloric diets

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Souhaieb Chrigui Zohra Haouas Sameh Hadj Taieb Hedya Jemai Monssef Feki Ayachi Zemmel Nourhene Boudhrioua Rafika Ben Chaouacha-Chekir

Abstract

This study aimed at investigating the alteration of lipid serum profile and histopathological damage in Psammomys obesus fed different high calorie diets. Animals were randomly assigned to four groups. P. obesus of the control group were fed with a Low-Calorie natural Diet, the Chenopodicae plant (0.42 kcal/g). The three other groups were fed high calorie diets rich in carbohydrates and protein or rich in carbohydrates and fat (~3.5 - 4.7 kcal/g). Lipid serum profile was assessed bimonthly during seven-month diets. The recorded energy intake was significantly high in the groups fed high calorie diets compared with the control group. Body weight was significantly increased in animal groups fed high calorie diets. All Psammomys obesus fed high-calorie diets developed dyslipidemia with the distinction of different sub-groups developing or not obesity and diabetes. High calorie diets rich in carbohydrates and fat induced a remarkable increase in lipid serum biomarkers indicating a fast induction of dyslipidemia from the first month of the experiment with a significant increase in transaminase activities after two months revealing pronounced hepatotoxicity and nephrotoxicity which were confirmed by a significant increase in liver and kidney relative weight and adiposity index. Severe histological alterations were recorded in obese, diabetic and dyslipidemic Psammomys obesus with a noticeable hypertrophy of the adipocytes, glomeruli and islets of Langerhans, as well as increased hepatic lipid droplet accumulation, apoptosis, necrosis and inflammation. A significant decrease in the thickness of the whole retinal layer was also observed after seven-months diet.  Animals fed Low-calorie natural diet don’t show any signs of obesity, dyslipidemia or diabetes. The high calorie diets induced rapid and severe changes in body weight, severe metabolic syndrome and histopathological features causing organ structural and functional injuries. Psammomys obesus seems like an excellent model for studying nutritional pathophysiological-metabolic disorders including obesity, diabetes, dyslipidemia and their complications, particularly diabetic retinopathy, comparable to those of human metabolic processes.

Keywords: High calorie diet, Psammomys obesus, obesity, dyslipidemia, type 2 diabetes

Article Details

How to Cite
CHRIGUI, Souhaieb et al. Histopathological features and metabolic disorders in Tunisian rodent Psammomys obesus fed high-caloric diets. Medical Research Archives, [S.l.], v. 12, n. 4, apr. 2024. ISSN 2375-1924. Available at: <https://esmed.org/MRA/mra/article/view/5171>. Date accessed: 21 nov. 2024. doi: https://doi.org/10.18103/mra.v12i4.5171.
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Research Articles

References

1. Feng K, Zhu X, Chen T, Peng B, Lu M, Zheng H, Huang Q, Ho CT, Chen Y, Cao Y. Prevention of obesity and hyperlipidemia by heptamethoxyflavone in high-fat diet-induced rats. J. Agric. Food Chem. 2019; 67(9): 2476-2489. https://doi.org/10.1021/acs.jafc.8b05632.
2. Baker KD, Loughman A, Spencer SJ, Reichelt AC. The impact of obesity and hypercaloric diet consumption on anxiety and emotional behavior across the lifespan. Neurosci. Biobehav. Rev. 2017; 83: 173-182. https://doi.org/10.1016/j.neubiorev.2017.10.014.
3. Dow C, Mancini F, Rajaobelina K, Boutron-Ruault MC, Balkau B, Bonnet F, Fagherazzi G. Diet and risk of diabetic retinopathy: a systematic review. Eur. J. Epidemiol. 2018; 33(2): 141-156. https://doi.org/10.1007/s10654-017-0338-8.
4. Jiang B, Liang Y, Sun X, Liu X, Tian W, Ma X. Potent inhibitory effect of chinese dietary spices on fatty acid synthase. Plant Foods Hum. Nutr. 2015; 70(3): 257-262. https://doi.org/10.1007/s11130-015-0486-5.
5. Dharmalingam M, Yamasandhi PG. Nonalcoholic fatty liver disease and type 2 diabetes mellitus. Indian J. Endocrinol. Metab. 2018; 22(3): 421.https://doi.10.4103/ijem.IJEM_585_17
6. Kowluru RA. Retinopathy in a diet-induced type 2 diabetic rat model and role of epigenetic modifications. Diabetes. 2020; 69(4): 689-698. https://doi.org/10.2337/db19-1009.
7. Ronkainen J, Huusko TJ, Soininen R, Mondini E, Cinti F, Mäkelä KA, Kovalainen M, Herzig KH, Järvelin MR, Sebert S. Fat mass-and obesity-associated gene Fto affects the dietary response in mouse white adipose tissue. Sci. rep. 2015; 5: 9233. https://DOI: 10.1038/srep09233
8. Hebi M, Eddouks M. Hypolipidemic activity of Tamarix articulata Vahl. in diabetic rats. J. Integr. Med. 2017; 15(6): 476-482. http://dx.doi.org/10.1016/S2095-4964(17)60361-3.
9. Hammoum I, Mbarek S, Dellaa A, Dubus E, Baccouche B, Azaiz R, Charfeddine R, Picaud S, Chaouacha-Chekir RB. Study of retinal alterations in a high fat diet-induced type ii diabetes rodent: Meriones shawi. Acta histochem. 2017; 119(1): 1-9. https://doi.org/10.1016/j.acthis.2016.05.005.
10. Schmidt-Nielsen K, Haines HB, Hackel DB. Diabetes mellitus in the sand rat induced by standard laboratory diets. Science. 1964; 143(3607):689-90. https://doi.org/ 10.1126/science.143.3607.689.
11. Sihali-Beloui O, Aroune D, Benazouz F, Hadji A, El-Aoufi S, Marco S. A hypercaloric diet induces hepatic oxidative stress, infiltration of lymphocytes, and mitochondrial reshuffle in Psammomys obesus, a murine model of insulin resistance. C R Biol. 2019; 342(5-6): 209-219. https://doi.org/10.1016/j.crvi.2019.04.003.
12. Baccouche B, Benlarbi M, Barber AJ, Ben Chaouacha-Chekir R. Short-term administration of astaxanthin attenuates retinal changes in diet-induced diabetic Psammomys obesus. Curr. Eye Res. 2018; 43(9):1177-89. https://doi.org/10.1080/02713683.2018.1484143.
13. Chrigui S, Hadj Taieb S, Jemai H, Mbarek S, Benlarbi M, Feki M, Haouas Z, Zemmel A, Chaouacha-Chekir RB, Boudhrioua N. Anti-Obesity and Anti-Dyslipidemic Effects of Salicornia arabica Decocted Extract in Tunisian Psammomys obesus Fed a High-Calorie Diet. Foods. 2023; 12(6): 1185. https://doi.org/10.3390/ foods12061185.
14. Rocha VD, Claudio ER, Da Silva VL, Cordeiro JP, Domingos LF, Da Cunha MR, Mauad H, Nascimento TB, Lima-Leopoldo AP, Leopoldo AS. High-fat diet-induced obesity model does not promote endothelial dysfunction via increasing Leptin/Akt/eNOS signaling. Front. physiol. 2019; 10:268. https://doi:10.3389/fphys.2019.00268.
15. Saidi T, Chaouacha-Chekir R, Hicks D. Advantages of Psammomys obesus as an animal model to study diabetic retinopathy. J Diabetes Metab. 2012; 3(207): 2. https://doi.org/0.4172/2155-6156.1000207.
16. Benlarbi‐Ben Khedher M, Hajri K, Dellaa A, Baccouche B, Hammoum I, Boudhrioua‐Mihoubi N, Dhifi W, Ben Chaouacha‐Chekir R. Astaxanthin inhibits aldose reductase activity in Psammomys obesus, a model of type 2 diabetes and diabetic retinopathy. Food Sci Nutr. 2019; 7(12): 3979-85. https://DOI: 10.1002/fsn3.1259.
17. Ji G, Zhao X, Leng L, Liu P, Jiang Z. Comparison of dietary control and atorvastatin on high fat diet induced hepatic steatosis and hyperlipidemia in rats. Lipids Health Dis. 2011; 10: 1-0. https://doi.org/10.1186/1476-511X-10-23
18. Nascimento AF, Sugizaki MM, Leopoldo AS, Lima-Leopoldo AP, Luvizotto RA, Nogueira CR, Cicogna AC. A hypercaloric pellet-diet cycle induces obesity and co-morbidities in Wistar rats. Arq. Bras. Endocrinol. Metabol. 2008; 52: 968-74. https://doi:10.1590/s0004-27302008000600007
19. Wali JA, Jarzebska N, Raubenheimer D, Simpson SJ, Rodionov RN, O’Sullivan JF. Cardio-metabolic effects of high-fat diets and their underlying mechanisms—A narrative review. Nutrients. 2020; 12(5):1505. https://doi.org/10.3390/nu12051505
20. Einat H, Kronfeld-Schor N, Eilam D. Sand rats see the light: short photoperiod induces a depression-like response in a diurnal rodent. Behav. Brain Res. 2006; 173(1): 153-7. https://doi.org/10.1016/j.bbr.2006.06.006
21. Dellaa A, Mbarek S, Kahloun R, Dogui M, Khairallah M, Hammoum I, Rayana‐Chekir NB, Charfeddine R, Lachapelle P, Chaouacha‐Chekir RB. Functional alterations of retinal neurons and vascular involvement progress simultaneously in the Psammomys obesus model of diabetic retinopathy. J. Comp. Neurol. 2021; 529(10): 2620-35. https://doi.org/10.1002/cne.25114
22. Benkalfat NB, Merzouk H, Bouanane S, Merzouk SA, Bellenger J, Gresti J, Tessier C, Narce M. Altered adipose tissue metabolism in offspring of dietary obese rat dams. Clin. sci. 2011; 121(1): 19-28. https://doi.org/10.1042/CS20100534.
23. Rodrigues L, Mouta R, Costa AR, Pereira A, e Silva FC, Amado F, Antunes CM, Lamy E. Effects of high-fat diet on salivary α-amylase, serum parameters and food consumption in rats. Arch. Oral Biol. 2015; 60(6): 854-62. https://doi:10.1016/j.archoralbio.2015.02.015.
24. Coate KC, Scott M, Farmer B, Moore MC, Smith M, Roop J, Neal DW, Williams P, Cherrington AD. Chronic consumption of a high-fat/high-fructose diet renders the liver incapable of net hepatic glucose uptake. Am. J. Physiol. - Endocrinol. Metab. 2010; 299(6): E887-98. https://doi.org/10.1152/ajpendo.00372.2010.
25. Ulla A, Alam MA, Sikder B, Sumi FA, Rahman MM, Habib ZF, Mohammed MK, Subhan N, Hossain H, Reza HM. Supplementation of Syzygium cumini seed powder prevented obesity, glucose intolerance, hyperlipidemia and oxidative stress in high carbohydrate high fat diet induced obese rats. BMC Complement Altern Med. 2017; 17: 1-3. https://doi.org/10.1186/s12906-017-1799-8.
26. Feng R, Luo C, Li C, Du S, Okekunle AP, Li Y, Chen Y, Zi T, Niu Y. Free fatty acids profile among lean, overweight and obese non-alcoholic fatty liver disease patients: a case–control study. Lipids Health Dis. 2017; 16(1): 1-9. https://doi.org/10.1186/s12944-017-0551-1.
27. Ragab SM, Abd Elghaffar SK, El-Metwally TH, Badr G, Mahmoud MH, Omar HM. Effect of a high fat, high sucrose diet on the promotion of non-alcoholic fatty liver disease in male rats: the ameliorative role of three natural compounds. Lipids Health Dis. 2015; 14(1): 1-1. https://doi.org/10.1186/s12944-015-0087-1.
28. Arner E, Westermark PO, Spalding KL, Britton T, Rydén M, Frisén J, Bernard S, Arner P. Adipocyte turnover: relevance to human adipose tissue morphology. Diabetes. 2010; 59(1): 105-109. https://doi.org/10.2337/db09-0942
29. Lönn M, Mehlig K, Bengtsson C, Lissner L. Adipocyte size predicts incidence of type 2 diabetes in women. The FASEB journal. 2010; 24(1): 326-31. https://doi.org/10.1096/fj.09-133058
30. Timmers S, De Vogel-Van Den Bosch J, De Wit N, Schaart G, Van Beurden D, Hesselink M, Van Der Meer R, Schrauwen P. Differential effects of saturated versus unsaturated dietary fatty acids on weight gain and myocellular lipid profiles in mice. Nutr Diabetes. 2011; 1(7): e11-e11. https://doi.org/10.1038/nutd.2011.7
31. Bouderba S, Sanchez‐Martin C, Villanueva GR, Detaille D, Koceïr EA. Beneficial effects of silibinin against the progression of metabolic syndrome, increased oxidative stress, and liver steatosis in Psammomys obesus, a relevant animal model of human obesity and diabetes. J. Diabetes. 2014; 6(2): 184-92. https://doi.org/10.1111/1753-0407.12083
32. Kanety H, Moshe S, Shafrir E, Lunenfeld B, Karasik A. Hyperinsulinemia induces a reversible impairment in insulin receptor function leading to diabetes in the sand rat model of non-insulin-dependent diabetes mellitus. PNAS. 1994; 91(5): 1853-7. https://doi.org/10.1073/pnas.91.5.1853.
33. Gadot M, Leibowitz G, Shafrir E, Cerasi E, Gross DJ, Kaiser N. Hyperproinsulinemia and insulin deficiency in the diabetic Psammomys obesus. Endocrinology. 1994; 135(2): 610-616. https://doi.org/10.1210/en.135.2.610.
34. Kamgang R, Mboumi RY, N’dillé GPRM, Yonkeu JN. Cameroon local diet-induced glucose intolerance and dyslipidemia in adult Wistar rat. Diabetes Res Clin Pract. 2005; 69(3): 224-230. https://doi.org/10.1016/j.diabres.2005.02.005.
35. Monnier L, Lapinski H, Colette C. Contributions of fasting and postprandial plasma glucose increments to the overall diurnal hyperglycemia of type 2 diabetic patients: variations with increasing levels of HbA1c. Diabetes care. 2003; 26(3): 881-885. https://doi.org/10.2337/diacare.26.3.881.
36. Klop B, Elte JWF, Cabezas MC. Dyslipidemia in obesity: mechanisms and potential targets. Nutrients. 2013; 5(4): 1218-1240. https://doi.org/10.3390/nu5041218.
37. Raveh O, Pinchuk I, Fainaru M, Lichtenberg D. Kinetics of lipid peroxidation in mixtures of HDL and LDL, mutual effects. Free Radic. Biol. Med. 2001; 31(11): 1486-1497. https://doi.org/10.1016/S0891-5849(01)00730-4.
38. Kaiser Ν, Leibowitz G, Nesher R. Glucotoxicity and β-cell failure in type 2 diabetes mellitus. J. Pediatr. Endocrinol. Metab. 2003; 16(1): 5-22. https://doi.org/10.1515/JPEM.2003.16.1.5.
39. Leibowitz G, Kaiser N, Cerasi E. β‐Cell failure in type 2 diabetes. J. Diabetes Investig. 2011; 2(2): 82-91. https://doi.org/10.1111/j.2040-1124.2010.00094.x.
40. Spolding B, Connor T, Wittmer C, Abreu LL, Kaspi A, Ziemann M, Kaur G, Cooper A, Morrison S, Lee S, Sinclair A. Rapid development of non-alcoholic steatohepatitis in Psammomys obesus. PloS One. 2014; 9(3): e92656. https://doi.org/10.1371/journal.pone.0092656.
41. Kharb S, Garg MK, Puri P, Nandi B, Brar KS, Gundgurthi A, Pandit A. Assessment of adrenal function in liver diseases. Indian J. Endocrinol. Metab. 2013; 17(3): 465. https://doi.org/10.4103/2230-8210.111643.
42. Lin SC, Chung TC, Lin CC, Ueng TH, Lin YH, Lin SY, Wang LY. Hepatoprotective effects of Arctium lappa on carbon tetrachloride-and acetaminophen-induced liver damage. Am. J. Chin. Med. 2000; 28(02): 163-73. https://doi.org/10.1142/S0192415X00000210.
43. Jung UJ, Choi MS. Obesity and its metabolic complications: the role of adipokines and the relationship between obesity, inflammation, insulin resistance, dyslipidemia and nonalcoholic fatty liver disease. Int. J. Mol. Sci. 2014; 15(4): 6184-6223. https://doi.org/10.3390/ijms15046184.
44. Esquinas P, Rios R, Raya AI, Pineda C, Rodriguez M, Aguilera-Tejero E, Lopez I. Structural and ultrastructural renal lesions in rats fed high-fat and high-phosphorus diets. Clin. Kidney J. 2021; 14(3): 847-54. https://doi.org/10.1093/ckj/sfaa009.
45. Madić V, Petrović A, Jušković M, Jugović D, Djordjević L, Stojanović G, Vasiljević P. Polyherbal mixture ameliorates hyperglycemia, hyperlipidemia and histopathological changes of pancreas, kidney and liver in a rat model of type 1 diabetes. J. Ethnopharmacol. 2021; 265: 113-210. https://doi.org/10.1016/j.jep.2020.113210.
46. Vidal E, Lalarme E, Maire MA, Febvret V, Grégoire S, Gambert S, Acar N, Bretillon L. Early impairments in the retina of rats fed with high fructose/high fat diet are associated with glucose metabolism deregulation but not dyslipidaemia. Sci. Rep. 2019; 9(1): 5997. https://doi.org/10.1038/s41598-019-42528-9.
47. Clarkson-Townsend DA, Douglass AJ, Singh A, Allen RS, Uwaifo IN, Pardue MT. Impacts of high fat diet on ocular outcomes in rodent models of visual disease. Exp. Eye Res. 2021; 204: 108-440. https://doi.org/10.1016/j.exer.2021.108440.
48. Hombrebueno JR, Chen M, Penalva RG, Xu H. Loss of synaptic connectivity, particularly in second order neurons is a key feature of diabetic retinal neuropathy in the Ins2Akita mouse. PloS one, 2014; 9(5): e97970. https://doi.org/10.1371/journal.pone.0097970.
49. Sasaki M, Ozawa Y, Kurihara T, Kubota S, Yuki K, Noda K, Kobayashi S, Ishida S, Tsubota K. Neurodegenerative influence of oxidative stress in the retina of a murine model of diabetes. Diabetologia. 2010; 53: 971-9. https://doi.org/10.1007/s00125-009-1655-6.
50. Kern TS, Barber AJ. Retinal ganglion cells in diabetes. J physiol. 2008; 586(18): 4401-4408. https://doi.org/10.1113/jphysiol.2008.156695