Structural characterization of rat ventricular tissue exposed to the smoke of two types of waterpipe

Document Type: Original Article


1 Department of Biology and Biotechnology, American University of Madaba, Madaba, Jordan

2 Department of Biological Sciences, The University of Jordan, Amman, Jordan


Objective(s):this study focused on the effect of waterpipe smoke exposure toxicity on the structure of albino rat’s ventricular tissue and their recovery.
Materials and Methods: Albino rats were divided into three groups: control, flavored, and unflavored. The control group was exposed to normal air while the flavored and unflavored groups were exposed to waterpipe smoke for a period of 90 days. Each group was followed by a period of 90 days of fresh air exposure. Following each period, the ventricular tissue was removed for biochemical and histopathological studies.
Results:The ventricular tissues of waterpipe exposed rats showed some degree of separation between cardiac muscle fibers, infiltration of lymphocytes, and congestion of blood vessel. Also, thin cross sections of ventricular cells revealed pleomorphic mitochondria with partially disrupted cristae, partial disruption of the myofibrils, and deposited toxic materials. The unflavored waterpipe has more deleterious effects on heart ventricular tissues than the flavored one. Waterpipe smoke didn't induce apoptosis in the ventricular tissue. We also found very high levels of plasma thiocyanate after exposure to smoke in the flavored and unflavored groups, while the control group showed no increase. After the recovery period, those tissues showed partial recovery.
Conclusion: Waterpipe smoke induces structural changes in the heart ventricle tissues, causing a negative impact on the capacity of the cardiac muscle for pumping blood and may lead to heart attack due to accumulation of free radicals and tissue inflammation. Cessation of smoking is important in returning most of these changes to their normal structure.


1. Hoffmann D, Wynder EL. Chemical constituents and bioactivity of tobacco smoke. IARC Sci Publ 1986; 74:145–165.

2. Chaouachi, K. Hookah (Shisha, Narghile) smoking and environmental tobacco smoke (ETS), a critical review of the relevant literature and the public health consequences. Int J Environ Res Publ Health 2009; 6: 798-843.

3. Chaouachi K. Public health intervention for narghile (hookah, shisha) use requires a radical critique of the related “standardised” smoking machine. J Public Health 2010; 18:69-73.

4. Monzer B, Sepetdjian E, Saliba N, Shihadeh A. Charcoal emissions as a source of CO and carcinogenic PAH in mainstream narghile waterpipe smoke. Food Chem Toxicol 2008; 46:2991-2995.

5. Shihadeh A. Investigation of the mainstream smoke aerosol of the argileh water pipe. Food Chem Toxicol 2003; 41:143-152.

6. US Public Health Service’ Smoking and Health. A Report of the Surgeon General. U. S. Department of Health Education, and Welfare, Public Health Service 2005; 79:2-47.

7. FitzGerald GA. Cigarettes and the wages of sn-2: oxidized species of PAF in smoking hamsters. J Clin Invest 1997; 99:2300-2301.

8. Leone A. Cardiovascular damage from smoking: a fact or belief? Int J Cardiol 1993; 38:113-117.

9. Leone A. Cigarette smoking and health of the heart. J R Soc Health 1995; 115:354-355.

10. Ambrose JA, Barua RS. The pathophysiology of cigarette smoking and cardiovascular disease: an update. J Am Coll Cardiol 2004; 43:1731–1737.

11. Arab MR, Mirzaei Ramezan KM, Mashhadi R. The study of histological effects of solder fumes in rat lungs. Iran J Basic Med Sci 2010; 13:63-68.

12. Goich J. Cardiovascular disease secondary to active and passive smoking. Rev Med Chil 1995; 122:556-562.

13. Nakamura K, Barzi F, Lam L, Huxley R, Feigin V, Ueshima H, et al.  Woodward cigarette smoking, systolic blood pressure, and cardiovascular diseases in the Asia-Pacific Region. Stroke 2008; 39:1694-1602.

15. Al-Kubati M, Al-Kubati AS, Al-Absi M, Fiser B. The short-term effect of water-pipe smoking on the baroreflex control of heart rate in normotensives. Auton Neurosci 2006; 30:126-127.

16. Boskabady MH, Farhang L, Mahmodinia M, Boskabady M, Heydari GR. Comparison of pulmonary function and respiratory symptoms in water pipe and cigarette smokers. Respirology 2012; 17:950–956.

17. Boskabady MH, Farhang L, Mahmoodinia M, Boskabady M, Heydari GR. Prevalence of water pipe smoking in the city of Mashhad (North East of Iran) and its effect on respiratory symptoms and pulmonary function tests. Lung India 2014; 31:237–243.

18. Boskabady MH, Mahmoodinia M, Boskabady M, Heydari GR.  Pulmonary function tests and respiratory symptoms among smokers in the city of mashhad (north east of Iran). Rev Port Pneumol 2011; 17:199–204.

19. Boskabady MH, Ferhadi H. Correlation between airway responsiveness to salbutamol and methacholine in smokers. Med Sci Monit 2005; 11:CR344–350.

20. Shraideh Z, Najjar H. Histological changes in tissues of trachea and lung alveoli of albino rats exposed to the smoke of two types of narghile tobacco products. JJBS 2011; 4:219-224.

21. Al-Awaida W, Shraideh Z, Badran D, Shehadeh H. The assessment of tobacco smoke toxicity on selected tissues from the cardiovascular and respiratory systems of the albino rat, an Ultrastructural Study. Annu Res Rev Biol 2014; 4:3666-3686.

22. Shraideh Z, Awaida W, Najar H, Musleh M. A modified smoking  machine for monitoring the effect of tobacco smoke on albino rats. JJBS 2011; 4:109-112.

23. Strickland A, Wang RY, Hoffman RS, Goldfrank LR. Blood cyanide concentrations aftersmoke inhalation. N Engl J Med 1992; 14:1326-1362.

24. Avti A, Kumar S, Pathak C, Vaiphei K, Khanduja K. Smokeless tobacco impairs the antioxidant defense in liver, lung, and kidney of rats. Toxicol Sci 2006; 89:547-553.

25. Reynolds ES. The use of lead citrate at high pH as an electron-opaque stain in electron  microscopy. J Cell Biol 1963; 17:208-212.

26. Karnovsky MJ. A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 1965; 27:137-138.

27. Alarifi SA, Mubarak MM, Alokail MS. Ultrastructural changes of pneumocytes of rat exposed to Arabian incense (Bakhour). Saudi Med J 2004; 25:1689-1693.

28. Waage H, Silsand T, Urdal P, Langard S. Discrimination of smoking status by thiocyanate and cotinine in serum, and carbon monoxide in expired air. Int J Epidemiol 1992; 21:488– 493.

29. Al-Awaida W, Akash M, Aburubaiha Z, Talib WH, Shehadeh H. Chinese green tea (Lung Chen) consumption reduces oxidative stress, inflammation and tissues damage in smoke exposed rats. Iran J Basic Med Sci 2014; 17:740-746.

30. Ben Saad H, Babba M, Boukamcha R, Latiri I, Knani J, Slama R, et al. Submaximal exercise capacity and quality of life in exclusive water-pipe smokers. Rev Mal Respir 2010; 27:489-495.

31. Sharma R, Deva C, Behera D. Reactive oxygen species formation in peripheral blood neutrophils in different types of smokers. Indian J Med Res 1997; 106:475-480.

32. Al-Numair K, Barber-Heidal K, Al-Assaf A, El-Desoky G. Water-pipe (shisha) smoking influences total antioxidant capacity and oxidative stress of healthy Saudi males. Int J Food Agric  Environ 2006; 5:17-22. 

33. Wolfram RM, Chehne F, Oguogho A, Sinzinger H. Narghile (water pipe) smoking influences platelet function and (iso-)eicosanoids. Life Sci 2003; 74:47-53.

34. Kurus M, Firat Y, Cetin A, Kelles M, Otlu A. The effect of resveratrol in tracheal tissue of rats exposed to cigarette smoke. Inhal Toxicol 2009; 21:979-984.

35. Baud FJ, Barriot P, Toffis V. Elevated blood cyanide concentrations in victims of smoke inhalation. N Engl J Med 1991; 325:1761–1766.

36. Masubuchi T, Koyama S, Sato E, Takamizawa A, Kubo K, Sekiguchi M, et al. Izumi smoke extract stimulates lung epithelial cells to release neutrophil and monocyte chemotactic activity. Am J Pathol 1998; 53:1903–1912.

37. Lough J. Cardiomyopathy produced by cigarette smoke. Arch Pathol Lab Med 1987;102:377-380.

38. Thomas D. Tobacco smoking and cardiovascular diseases. Rev Pract  1993; 43:1218–1222.

39. Maziak W, Eissenberg T, Rastam S, Eissenberg T. Beliefs and attitudes related to narghile (waterpipe) smoking among university students in Syria. Ann Epidemiol 2004; 14:646–654.

40. Asadi E, Jahanshahi M, Golalipour MJ. Effect of vitamin E on oocytes apoptosis in nicotine-treated Mice. Iran J Basic Med Sci 2012; 15:880–884.

41. Kuo WH, Chen JH, Lin HH, Chen BC, Hsu JD, Wang CJ. Induction of apoptosis in the lung tissue from rats exposed to cigarette smoke involves p38/JNK MAPK pathway. Chem Biol Interact 2005; 155:31–42.

42. Al-Awaida W, Abuereish G, Shraideh Z.  Correlation of antioxidant and NADPH generating enzymes activities with tissues inflammation during smoke exposure of rats and smoke cessation. Res Opin Anim Vet Sci 2013; 3:41-49.

43. Cardellach F, Alonso JR, Lopez S, Casademont J,
Miro O. Effect of smoking cessation on mitochondrial respiratory chain function. J Toxicol Clin Toxicol 2003; 41:223-228.

44. Cotter TG, Martin SJ, Gorman A, McCarthy J, Finucane D, Reville W, et al. Morphological assessment of apoptosis, Techniques in apoptosis. In: Cotter TG, Martin SJ.editors. A user's guide. London: Portland Press; 1996.p.1–20.