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. 2024 Feb 2:15:1286366.
doi: 10.3389/fphys.2024.1286366. eCollection 2024.

Impact of prolonged exposure to occasional and regular waterpipe smoke on cardiac injury, oxidative stress and mitochondrial dysfunction in male mice

Naserddine Hamadi  1 , Suhail Al-Salam  2   3 , Sumaya Beegam  4 , Nur Elena Zaaba  4 , Ozaz Elzaki  4 , Abderrahim Nemmar  3   4
Affiliations

Impact of prolonged exposure to occasional and regular waterpipe smoke on cardiac injury, oxidative stress and mitochondrial dysfunction in male mice

Naserddine Hamadi et al. Front Physiol. .

Abstract

Regular waterpipe smoking (Reg-WPS) is well recognized for its deleterious effect on the heart. However, there is a paucity of experimental studies on the impact of occasional waterpipe smoking (Occ-WPS), also known as nondaily smoking, versus Reg-WPS on cardiac homeostasis, and the mechanisms underlying these effects. Hence, we aimed, in the present study, to investigate the effect of Occ-WPS (30 min/day, 1 day/week) versus Reg-WPS (30 min/day, 5 days/week) for 6 months on systolic blood pressure (SBP), cardiac injury, oxidative markers, chemokines, proinflammatory cytokines, DNA damage and mitochondrial function compared with air (control) exposed mice. Our results show that SBP was increased following exposure to either Occ-WPS or Reg-WPS compared with air-exposed mice. Moreover, we found that only Reg-WPS induced a significant elevation in the levels of troponin I, brain natriuretic peptide, lactate dehydrogenase, and creatine phosphokinase. However, the atrial natriuretic peptide (ANP) was significantly increased in both Occ-WPS and Reg-WPS groups. Compared with air-exposed mice, the levels of lipid peroxidation, reduced glutathione and monocyte chemoattractant protein-1 were only significantly augmented in the Reg-WPS. However, catalase, superoxide dismutase, and CXCL1 were significantly increased in both Occ-WPS and Reg-WPS. The concentrations of the adhesion molecules E-selectin, vascular cell adhesion molecule-1, and intercellular adhesion molecule-1 were solely elevated in the heart of mice exposed to Reg-WPS. Similarly, the concentrations of interleukin-1β and tumor necrosis factor α were only significantly augmented in the Reg-WPS. However, both Occ-WPS and Reg-WPS triggered significant augmentation in the levels of IL17 and DNA damage compared to the control groups. Furthermore, while Occ-WPS induced a slight but statistically insignificant elevation in the concentrations of mammalian targets of rapamycin and nuclear factor erythroid-derived 2-like 2 (Nrf2) expression, Reg-WPS exposure increased their levels substantially, in addition to p53 and mitochondrial complexes II & III, and IV activities compared with air-exposed mice. In conclusion, our findings show that while the long-term Occ-WPS exposure induced an elevation of SBP, ANP, antioxidant enzymes, IL17, CXCL1, and cardiac DNA damage, Reg-WPS exposure was consistently associated with the elevation of SBP and occurrence of cardiac damage, inflammation, oxidative stress, DNA damage and mitochondrial dysfunction.

Keywords: cardiac damage; inflammation; occasional; regular; waterpipe smoke.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The author(s) declared that they were an editorial board member of Frontiers, at the time of submission. This had no impact on the peer review process and the final decision.

Figures

FIGURE 1
FIGURE 1
Systolic blood pressure (SBP) at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). Data are mean ± SEM (n = 7–8).
FIGURE 2
FIGURE 2
Troponin I (A), brain natriuretic peptide BNP, (B), atrial natriuretic peptide ANP, (C), lactate dehydrogenase LDH, (D), and creatine phosphokinase CK, (E) levels in the heart of mice at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). Data are mean ± SEM (n = 7–8).
FIGURE 3
FIGURE 3
Lipid peroxidation LPO, (A), reduced glutathione GSH, (B), catalase (C) and superoxide dismutase SOD, (D) levels in the heart of mice at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). Data are mean ± SEM (n = 7–8).
FIGURE 4
FIGURE 4
Monocyte chemoattractant protein-1 MCP-1, (A) and chemokine CXCL1 (B) concentrations in the heart of mice at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). Data are mean ± SEM (n = 7–8).
FIGURE 5
FIGURE 5
E-selectin (A), vascular cell adhesion molecule-1 VCAM-1, (B), and intercellular adhesion molecule-1 ICAM-1, (C) concentrations in the heart of mice at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). Data are mean ± SEM (n = 7–8).
FIGURE 6
FIGURE 6
Interleukin-1β IL-1β, (A), tumor necrosis factor α TNFα, (B) and interleukin 17 IL17, (C) concentrations in the heart of mice at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). Data are mean ± SEM (n = 7–8).
FIGURE 7
FIGURE 7
DNA migration was assessed by COMET assay in heart tissues of mice at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). Data are mean ± SEM (n = 7–8).
FIGURE 8
FIGURE 8
Mammalian target of rapamycin (mTOR) (A) and p53 (B) levels in heart tissues of mice at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). Data are mean ± SEM (n = 7–8).
FIGURE 9
FIGURE 9
Immunohistochemical staining of the heart tissue sections of mice for the detection of nuclear factor erythroid-derived 2-like 2 (Nrf2) at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). (A) representative section of the heart of air-exposed group showing focal mild expression of Nrf2 by cardiac myocytes (thin arrow) and endothelial cells (arrow head). (B) representative section of the heart of Occ-WPS exposure showing expression of Nrf2 by endothelial cells (arrow head) and cardiac myocytes (thin arrow). (C) representative section of the heart of Reg-WPS exposure showing expression of Nrf2 by endothelial cells (arrow head) and cardiac myocytes (thin arrow). (D) Semiquantitative quantification of the % of immunohistochemical assessment of the heart tissue for Nrf2 of air, Occ-WPS or Reg-WPS groups. Data are mean ± SEM (n = 6). Scale bars: 50 μm.
FIGURE 10
FIGURE 10
Mitochondrial complexes I (A), II& III (B) and IV (C) activities in heart tissues of mice at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). Data are mean ± SEM (n = 7–8).
FIGURE 11
FIGURE 11
Cotinine concentrations measured in the plasma of mice at the end of the 6 months exposure period to air (control) or occasional waterpipe smoke (Occ-WPS) or regular WPS (Reg-WPS). Data are mean ± SEM (n = 7–8).
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