Next Article in Journal
Mild-to-Moderate Traumatic Brain Injury: A Review with Focus on the Visual System
Previous Article in Journal
Trigeminal Herpes Zoster Transited to Ipsilateral Occipital Neuralgia
 
 
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Article

Effect Comparison of E-Cigarette and Traditional Smoking and Association with Stroke—A Cross-Sectional Study of NHANES

1
Department of Public Health, Icahn School of Medicine at Mount Sinai, New York, NY 10029, USA
2
Department of Public Health, University of California, Berkeley, CA 92093, USA
3
Department of Biology, York University, Toronto, ON M3J 1P3, Canada
4
Department of Public Health, Milken Institute School of Public Health, George Washington University, Washington, DC 20052, USA
5
Department of Neurology, Larkin Community Hospital, Miami, FL 33143, USA
6
Department of Internal Medicine, Texas Tech University Health Sciences Center, Transmountain Campus, El Paso, TX 79430, USA
7
Department of Internal Medicine, Hudson Regional Hosp, Secaucus, NJ 07094, USA
8
Department of Child Neurology, Jersey Shore University Medical Center, Neptune City, NJ 07753, USA
9
Department of Internal Medicine, Geisinger Med Center, Danville, PA 17822, USA
10
Department of Epidemiology and Biostatistics, Boston University School of Public Health, Boston, MA 02118, USA
11
Department of Neurology, Mayo Clinic, Albert Lea, MN 56007, USA
12
Department of Neurology, Stormont Vail Health, Topeka, KS 66604, USA
*
Author to whom correspondence should be addressed.
Neurol. Int. 2022, 14(2), 441-452; https://doi.org/10.3390/neurolint14020037
Submission received: 1 May 2022 / Revised: 19 May 2022 / Accepted: 23 May 2022 / Published: 27 May 2022

Abstract

:
Introduction: Tobacco use is one of the most significant risk factors for stroke. Besides traditional cigarettes and combustible products, the use of e-cigarettes and electronic nicotine delivery products has been widespread among young adults in the recent era. Furthermore, the trend of vaping has increased over the last decade. However, the relationship between e-cigarettes and stroke is largely unknown. The aim of this study was to evaluate the prevalence and identify the relationship between e-cigarette smoking and stroke. Methods: A cross-sectional study was performed using the NHANES database of the US population. Adults with a history of smoking were considered in our study and divided into three groups, e-cigarette users, traditional, and dual smokers. The Chi-squared test, Wilcoxon rank-sum test, and multivariable logistic regression analysis were used to identify the prevalence and association of e-cigarette consumption and stroke. Results: Out of a total of 266,058 respondents from 2015 to 2018, we found 79,825 respondents who smoked e-cigarettes (9.72%) or traditional (29.37%) or dual smoking (60.91%). Stroke prevalence among e-cigarette smokers was 1.57%. Stroke was more prevalent among traditional smokers than among e-cigarette smokers. (6.75% vs. 1.09%; p < 0.0001) E-cigarette smokers had early onset of stroke in comparison with traditional smokers. (median age: 48 vs. 59 years; p < 0.0001). Among females with stroke, the prevalence of e-cigarette use was higher in comparison with traditional smoking (36.36% vs. 33.91%; p < 0.0001). Among the stroke population, the prevalence of e-cigarette use was higher among Mexican-Americans (21.21% vs. 6.02%) and other Hispanics (24.24% vs. 7.70%) compared with traditional smoking (p < 0.0001). The regression analysis found higher odds of stroke history among e-cigarette users than traditional smokers [aOR: 1.15; 95% CI: 1.15–1.16)]. Conclusion: Though stroke was more prevalent in traditional smokers, the incidence of stroke was early-in-onset and was strongly associated with e-cigarette use compared to traditional smokers. We have also identified vascular effects of e-cigarettes components as possible triggers for the stroke.

1. Introduction

The prevalence, mortality, and disability-adjusted life years (DALYs) associated with stroke have steadily increased globally, from 1990 to 2019, reaching approximately 101 million (95% UI: 93.2 to 111 million); death from stroke has decreased over the past decade in the USA [1,2]. Stroke continues to be the fifth-leading cause of death [1]. Tobacco consumption is a major modifiable risk factor associated with stroke, CVD, and silent infarction [2,3] Globally, smoking is the second-leading cause of death and the leading cause of DALYs [2]. There are various forms of tobacco consumption [4], of which vaping is very popular among adolescents [5]. The popularity of vaping has sharply increased over the last two decades [2011: 1.5% to 2018: 20.8%] [2], and the most recent data shows that 20% of students in grades 7–12 are current vapers, and 34% have tried it at least once. Another study found a 112% increase in the rate of vaping among youth from 2017 to 2019 [6].
The few studies that have shown a positive association between the use of e-cigarettes and combustible cigarettes with vascular disorders were limited either by choosing specific target populations [5,7] or being not specific to stroke [7]. Parekh et al. showed that dual use of e-cigarettes and combustible cigarettes was associated with 2.9 times higher odds of stroke but no association between isolated e-cigarette use with stroke (0.69; 95% CI: 0.3–1.4) among the population of 18–44-year-olds [5]. Kaiser et al. showed that the use of nicotine and/or vaping leads to worsening outcomes in stroke, secondary to a state of glucose deprivation in the neurovascular unit, which augments neuronal damage and enhances ischemic brain injury [8]. The limited information on long-term health effects of e-cigarettes on CVD is one of the reasons why AHA maintains its stand on e-cigarette regulation and health care screening precisely like other forms of tobacco [9].
Hence, we aim to investigate the association of e-cigarettes and traditional smoking with ischemic stroke using the National Health and Nutrition Examination Survey (NHANES) among the general population of the USA. The risk of stroke incidence and hospitalizations due to tobacco consumption has increased among adults. However, the association between e-cigarette smoking and stroke development in this population remains unknown. This study aims to examine the effect of e-cigarettes and traditional smoking on stroke.

2. Methods

2.1. Details of Data

The National Health and Nutrition Examination Survey (NHANES) is a population-based cross-sectional survey study program designed to assess the health and nutritional status of adults and children in the United States. NHANES is a part of the National Center for Health Statistics (NCHS) and the Centers for Disease Control and Prevention (CDC). The NHANES includes socio-demographic, dietary, examination, lab findings, and health-related questions. The dataset is available at the CDC website https://www.cdc.gov/nchs/nhanes/about_nhanes.htm, accessed on 30 August 2021, and details of the respondents are de-identified, so institutional IRB was not required.

2.2. Demographic Characteristics of the Study Population

A cross-sectional retrospective population-based study was performed using the NHANES database 2015–2018 of the US. Participants 18 or older with a history of smoking were considered in our study and divided into three groups, exclusive e-cigarette users, traditional smokers, and dual (e-cigarette + traditional) smokers. The confirmed history of stroke among all three groups was extracted.
Exclusive e-cigarettes, vaping, or electronic nicotine delivery systems (ENDS) use was defined by “SMQ900” (Ever used an e-cigarette?) and “SMQ905” (During the past 30 days, how many days have you used an e-cigarette?). Exclusive traditional smoking was defined by either “SMQ020” (Smoked at least 100 cigarettes in life) or “SMQ040” (Do you now smoke cigarettes?). Dual smokers were defined by respondents who responded “yes” to both e-cigarettes and traditional smoking. Stroke was defined by “MCQ160f” (Has a doctor or other health professional ever told you had a stroke?) and “MCQ180f”—(Age when told you had a stroke?).
We have included socio-demographic variables like age, race, annual household income, and comorbidities like diabetes, cholesterol, hypertension, depression, obesity, cancer, substance abuse (marijuana, cocaine/heroin/methamphetamine, illegal injectable drug), alcohol use (median average # of drinks/day and binge drinking (women: 4 or more and men: 5 or more drinks/day in past 12 months), and preventive aspirin use. We have collected data on high blood pressure on two occasions, recent systolic and diastolic blood pressure, body mass index (BMI), S. cholesterol, S. LDL, S. TG, and HbA1C.

2.3. Outcomes

The primary aim of this study is to evaluate the prevalence of e-cigarette, traditional, and dual smokers among respondents with a history of stroke. The secondary aim of this study is to evaluate the odds of different methods of nicotine consumption among respondents with a history of stroke. We have also evaluated the odds of e-cigarette use in the past 30 days among the population having a history of stroke.

2.4. Statistical Analysis

We analyzed the data using SAS software (Version 9.4, SAS Institute Inc., Cary, NC, USA). We performed univariate analysis to find out socio-demographic characteristics of the respondents with different methods of nicotine consumption among the stroke population, using Chi-square for categorical variables and a t-test and Wilcoxon ransom test for continuous variables. Multivariable logistic regression models were generated to calculate the odds of e-cigarettes among the stroke population in comparison with traditional smokers after adjusting for confounding variables. There was no pre-decided sample size calculation. p-value < 0.05 was considered significant, and an adjusted odds ratio (aOR) with a 95% confidence interval (95% CI) was calculated.
In regression analysis, the models were adjusted with socio-demographic variables, like age, gender, and annual household income, and comorbidities, like diabetes, cholesterol, hypertension, depression, cancer, substance abuse (marijuana, cocaine/heroin/methamphetamine, illegal injectable drug), alcohol use (median average # of drinks/day and binge drinking (women: 4 or more and men: 5 or more drinks/day in past 12 months), and preventive aspirin use. We collected data on high blood pressure on two occasions, recent systolic and diastolic blood pressure, and body mass index (BMI).

3. Results

Out of 266,058 respondents from 2015 to 2018 in the NHANES survey, we found 79,825 respondents who smoked e-cigarettes or traditional smoking or dual smoking, after excluding patients with age < 18 years and admissions with missing data for age, gender, or ethnicity. Out of 79,825 respondents, 7756 (9.72%) were e-cigarette smokers, 23,444 (29.37%) were dual smokers, and 48,625 (60.91%) were traditional smokers. The overall prevalence of stroke was 5.41% (n = 4194) among various types of smokers. The overall prevalence of stroke among e-cigarette smokers was 1.57%, among traditional smokers was 78.04%, and among dual smokers was 20.39%. Stroke was more prevalent among traditional smokers than e-cigarette and dual smokers (6.75% vs. 1.09% vs. 3.72% p < 0.0001). E-cigarette smokers have an early onset of stroke compared to dual and traditional smokers, respectively (median age in years: 48 vs. 50 vs. 59; p < 0.0001) (Table 1).

3.1. Socio-Demographic Characteristics and Comorbidities

Among 4194 respondents with a history of stroke, males had higher use of e-cigarettes in comparison to females (1.61% vs. 1.52%; p < 0.0001). Among females with stroke, the prevalence of e-cigarette use was higher than traditional smoking (36.36% vs. 33.91%; p < 0.0001) Among Mexican-Americans (21.21% vs. 6.02%) and other Hispanics (24.24% vs. 7.70%), the prevalence of e-cigarette use was higher than traditional smoking. (p < 0.0001) Overall, e-cigarette use was higher among other Hispanics than among Mexican-Americans and among other races. (5.13% vs. 4.52% vs. 1.37% vs. 2.82%; p < 0.0001) (Table 2).
Among stroke respondents with congestive heart failure, the prevalence of e-cigarette utilization (25.76%) was higher compared to that of traditional smokers (16.59%) and dual smokers (21.75%). (p < 0.0001). Among respondents with high blood pressure, the prevalence of dual smoking was higher in comparison to traditional smoking. (98.02% vs. 80.91%; p < 0.0001). The prevalence of dual smokers was higher among people with high cholesterol levels than traditional smoking. (60.58% vs. 58.11%, p < 0.0001) E-cigarette smokers had a higher percentage of diabetes in comparison to traditional smokers. (50.0% vs. 36.63%; p < 0.0001) E-cigarette use was higher in people who had depression nearly every day than in traditional smokers (21.21% vs. 7.46%, p < 0.0001). Similarly, we found higher e-cigarette utilization with liver disorders (21.21% vs. 9.84%, p < 0.0001). Among substance users with a history of stroke, the prevalence of marijuana or hashish (100.00% vs. 66.20%), cocaine/heroin/methamphetamine (71.21% vs. 31.64%), and injectable illegal drug abuse (21.21% vs. 4.63%) were higher among e-cigarette users compared to traditional smoking. (p < 0.0001) (Table 2).

3.2. Multivariable Logistic Regression Showing Association between Stroke and Smoking Habits

In multivariable logistic regression analysis, after adjusting for socio-demographic characteristics and comorbidities, the odds of having a history of stroke was higher among e-cigarette in comparison with traditional smokers (adjusted odds ratio (aOR): 1.15; 95% CI: 1.15–1.16; p < 0.0001). Dual smoker respondents had 14% higher odds of stroke history in comparison with traditional smokers (aOR: 1.14; 95% CI: 1.14–1.15; p < 0.0001). Respondents who smoked e-cigarettes in the last 30 days were also associated with higher odds of stroke prevalence in comparison to non-e-cigarette smokers in the last 30 days (aOR: 1.14; 95% CI: 1.14–1.15; p < 0.0001) (Table 3).

4. Discussion

Although stroke was more prevalent in traditional smokers, our cross-sectional study found that e-cigarette smokers had an early onset of stroke compared to traditional and dual smokers. Furthermore, the odds of having a history of stroke was 1.15 times higher among e-cigarette and 1.14 times higher in dual smokers compared to traditional smokers. These findings have clear implications in helping physicians, healthcare policymakers, and tobacco product regulatory authorities to call for strict new regulations on e-cigarette access, sales, and marketing.
Tobacco consumption, a known modifiable risk factor, is associated with stroke and cardiovascular disease, including myocardial infarction [10,11]. Although death from stroke has decreased in the last decade, the use of tobacco products such as e-cigarettes and vaping has trended upward in the last two decades [12]. According to the World Health Organization 2018, vaping has increased from around 7 million users in 2011 to 41 million in 2018, with a projection of more than 55 million by 2021 [13]. Globally, tobacco consumption is worth an estimated $19.3 billion, up from around $7 billion five years ago, of which the US is one of the biggest markets [14]. Prior studies have shown that e-cigarettes are less harmful than tobacco cigarettes and can help smokers quit or reduce tobacco use [15,16,17,18,19]. But our study reveals that e-cigarette users had higher odds of stroke than traditional smokers. In addition, we found that dual smokers (e-cigarette plus traditional) had 14% higher odds of stroke than traditional smokers alone. The higher odds of stroke in dual smokers suggest that e-cigarettes may have an additive effect on traditional smokers. The additive effect may be attributed to e-cigarette ingredients other than nicotine, like carbonyls, including aldehydes such as formaldehyde, acetaldehyde, and acrolein; fine and ultrafine particulate matter (PMs); benzene; toluene; ethylbenzene; and xylenes (BTEX) [8,20,21,22,23]. Parekh et al. also found higher odds of stroke among the young adult population (18–44 years) secondary to the additive effect of e-cigarettes (aOR: 2.91) on current or former traditional smokers (sole combustible cigarette OR: 1.83), without establishing a relationship between sole e-cigarette use and stroke [5].
Long-term exposure to higher nicotine levels is known to increase the risk of atherosclerosis and further promote stroke risk [11,24]. According to Kaiser et al., e-cigarettes, like traditional smoking, can cause a loss of blood–brain barrier (BBB) integrity and vascular inflammation [25]. Several studies have documented the detrimental effect of non-nicotinic ingredients of e-cigarettes on cerebral and cardiovascular systems (Table 4). Acrolein and PM inhalation from smoking and ambient air pollution have previously been reported to have various deleterious effects on the vascular system, including increasing blood pressure; increasing vascular injury by impairing vascular repair capacity; and increasing the risk of thrombosis and atherosclerosis due to endothelial dysfunction, dyslipidemia, and platelet activation [11,26,27,28,29,30,31,32,33,34]. Kuntic et al. found that E-cigarette vapor exposure increases vascular, cerebral, and pulmonary oxidative stress through toxic aldehyde(acrolein)-mediated NOX-2-dependent mechanisms [35].
A few studies have reported that e-cigarette use negatively impacts heart rate and blood pressure [36,37,38,39]. In addition, E-cigarettes cause endothelial cell dysfunction, vascular injury, and oxidative stress, which play important roles in the pathogenesis of stroke [40,41]. Furthermore, e-cigarette vapor extracts (toxic chemical, fine particulate matter: 2.5 μm and smaller, and nicotine) were found to enhance platelets’ activation (aggregation-adhesion-inflammation), which potentiates the atherosclerosis process [42]. S. Hom et al. found that e-vapor extracts have the same effect on the vascular system as traditional tobacco products, including myocardial infarction and stroke, and they noticed that it is fine particulate matter (PMs), not nicotine or toxic combustion products, that activates the hemostatic system/platelet activation. Thus, it is plausible that just reducing exposure to the fine particulate matter may reduce some of the risks associated with CVD development [42]. Acute and chronic effects of e-cigarette extract as a possible risk factor and trigger for the stroke were summarized in Figure 1 and described in detail in Table 5.
Table 5. Acute and chronic effects of e-cigarettes as a possible risk factor and trigger for stroke.
Table 5. Acute and chronic effects of e-cigarettes as a possible risk factor and trigger for stroke.
Acute Direct Effect
Kuntic et al. [35]E-cigarette product acrolein (reactive aldehydes) mediated NOX-2-driven oxidative stress and cerebrovascular inflammation
Caporale et al. [43]Transient impairment of cerebrovascular reactivity and endothelial function
Sifat et al. [8]Induces a state of glucose deprivation at the neurovascular unit, leading to enhanced ischemic brain injury and/or stroke risk
Acute Indirect Effect
Antoniewicz et al.,
Mitchelle et al. [44,45]
Increased HR; increased arterial stiffness is an independent risk factor for cardio and cerebrovascular events such as myocardial infarctions and stroke
Nocella et al. [46]Increase the soluble CD40L and P-selectin; enhance platelet aggregation
Boas et al. [47]Activation of splenocardiac axis (increase oxidative stress and increase sympathetic activity)
Carnevale et al. [40]Increase oxidative stress and endothelial dysfunction by increasing soluble NOX-mediated peptides and decreasing NO bioavailability and vitamin E
Chronic Direct Effect
Kuntic et al. [35]Endothelial dysfunction and narrowing of vessels
Kaisar et al. [25]Alter blood-brain barrier (BBB) permeability and vascular inflammation
Qasim et al. [48]In mice, alter physiological hemostasis and increase the risk of thrombogenic events; platelet activation
Chronic Indirect Effect
Alzahrani et al. [49]Increased odds of having myocardial infarction (OR = 1.79, 95% CI = 1.20, 2.66, p = 0.004)
Moheimani et al. [50]Increases in cardiac sympathetic activity and oxidative stress, both of which increase the risk of vascular disease
Frederik Franzen et al. [51]Increase peripheral and central blood pressure and pulse wave velocity
Vlachopoulos et al. [52]Increase aortic stiffness and increase blood pressure
In our study, among respondents with a history of stroke, males had higher use of e-cigarettes in comparison to females. However, among females with stroke, the prevalence of e-cigarette use was higher in comparison with traditional smoking. This study reveals that the stroke population with coexisting conditions like congestive heart failure, depression, and hypertension had higher odds of e-cigarette utilization compared to traditional smoking. Previous studies have also reported a strong association between e-cigarette use and level of stress, depression, CHF, and hypertension [26,28,31,53]. Our study also reports that the prevalence of marijuana or hashish, cocaine, heroin, methamphetamine, and injectable illegal drug abuse was higher among e-cigarette users than traditional smoking.
Secondly, we have also evaluated the odds of e-cigarette use in the last 30 days in stroke population. In the VESUVIUS study, George et al. reported short-term beneficial effects from switching to e-cigarette smoking on vascular function and found a significant improvement in endothelial function and vascular stiffness in e-cigarette smokers who had switched from traditional smoking to e-cigarette smoking within the last 30 days [54]. However, in contrast, we found higher odds of stroke prevalence compared to non-e-cigarette smokers in respondents who smoked e-cigarettes in the previous 30 days. This results from the acute harmful effects of e-cigarettes on vascular function, including high blood pressure and heart rate, increased arterial stiffness, endothelial dysfunction, and increased cerebrovascular oxidative stress [40,43,44,45]. This finding of our study is limited by the fact that ‘non-e-cigarette smokers in the last 30 days’ could have smoked e-cigarettes outside the last 30 days of the time frame, and stroke could occur before smokers switch from traditional smoking.

5. Strength and Limitations

Our study has several limitations. First, because of the study’s cross-sectional design, causal inferences may be limited, with the possibility of reverse temporality, as we considered isolated e-cigarettes smokers separate from traditional and dual smokers (history of traditional and e-cigarette smoking at least once). We have assumed that isolated e-cigarette smokers, as mentioned in the survey, never had a history of traditional smoking. So if they had a stroke, they would not start or switch their form of smoking. Thus, this stroke episode happened after e-cigarettes had started. Secondly, the study cannot determine the amount or type of e-cigarette use, timing, frequency, nature of stroke, stroke severity, or timing. We could not evaluate the role of e-cigarettes as a trigger of stroke. This survey study also has respondents and recall bias due to limited responses from survey respondents. Despite major limitations, NHANES data represent a diverse sample of the US population, covering populations of all ages, sex, race, and socioeconomic status from all geographic distributions.

6. Future Directions

We propose more studies to evaluate the short- and long-term effects of e-cigarette ingredients, including but not limited to acetaldehyde, acrolein, fine and ultrafine PMs, and BTEX on cardio and cerebrovascular systems. The use of e-cigarettes might be more harmful to the female and Hispanic population, so more awareness should be created among these sub-groups of the population. Future guidelines for the quantification of e-cigarettes in regards to cardio and cerebrovascular risk stratification may provide additional insight to mitigate the burden.

7. Conclusions

Stroke is more prevalent in traditional smokers than among e-cigarette users, but we found that the incidence of stroke was early in onset in e-cigarette smokers compared to traditional smokers. There were higher odds of stroke prevalence for those who smoked e-cigarettes in the last 30 days compared to non-e-cigarette smokers in the last 30 days. More prospective studies are needed to evaluate the long-term effects and safety of e-cigarettes to mitigate the risk of cardio and cerebrovascular disorders.

Author Contributions

U.P. and S.S. had full access to all of the study data and took responsibility for the integrity and accuracy of the data analysis. Study concept and design: All authors. Acquisition, analysis, and interpretation of data: All authors. Drafting of the manuscript: All authors. Critical revision of the manuscript for valuable intellectual content: All authors. Statistical analysis: U.P. Administrative, technical, or material support: All authors. Study supervision: U.P., S.S. and K.A. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Informed Consent Statement

The data has been taken from National Health and Nutrition Examination Survey (NHANES), a de-identified database from the Disease Control and Prevention (CDC), so informed consent or IRB approval was not needed for the study.

Data Availability Statement

The data is publicly available at https://wwwn.cdc.gov/nchs/nhanes/Default.aspx and raw data analysis will be made available upon request.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Roth, G.A.; Mensah, G.A.; Johnson, C.O.; Addolorato, G.; Ammirati, E.; Baddour, L.M.; Barengo, N.C.; Beaton, A.; Benjamin, E.J.; Benziger, C.P.; et al. Global Burden of Cardiovascular Diseases and Risk Factors, 1990–2019: Update From the GBD 2019 Study. J. Am. Coll. Cardiol. 2020, 76, 2982–3021. [Google Scholar] [CrossRef] [PubMed]
  2. Virani, S.S.; Alonso, A.; Benjamin, E.J.; Bittencourt, M.S.; Callaway, C.W.; Carson, A.P.; Chamberlain, A.M.; Chang, A.R.; Cheng, S.; Delling, F.N.; et al. Heart Disease and Stroke Statistics—2020 Update: A Report From the American Heart Association. Circulation 2020, 141, e139–e596. [Google Scholar] [CrossRef] [PubMed]
  3. Kernan, W.N.; Ovbiagele, B.; Black, H.R.; Bravata, D.M.; Chimowitz, M.I.; Ezekowitz, M.D.; Fang, M.C.; Fisher, M.; Furie, K.L.; Heck, D.V.; et al. Guidelines for the Prevention of Stroke in Patients with Stroke and Transient Ischemic Attack: A Guideline for Healthcare Professionals from the American Heart Association/American Stroke Association. Stroke 2014, 45, 2160–2236. [Google Scholar] [CrossRef] [PubMed]
  4. National Institute on Drug Abuse (NIDA). Cigarettes and Other Tobacco Products DrugFacts. Available online: https://www.drugabuse.gov/publications/drugfacts/cigarettes-other-tobacco-products (accessed on 30 August 2021).
  5. Parekh, T.; Pemmasani, S.; Desai, R. Risk of Stroke With E-Cigarette and Combustible Cigarette Use in Young Adults. Am. J. Prev. Med. 2020, 58, 446–452. [Google Scholar] [CrossRef] [Green Version]
  6. Heart and Stroke Foundation. Vaping What You Need to Know. Available online: https://www.heartandstroke.ca/articles/vaping-what-you-need-to-know (accessed on 30 August 2021).
  7. Yatsuya, H.; Folsom, A.R. Risk of Incident Cardiovascular Disease among Users of Smokeless Tobacco in the Atherosclerosis Risk in Communities (ARIC) Study. Am. J. Epidemiol. 2010, 172, 600–605. [Google Scholar] [CrossRef] [Green Version]
  8. Sifat, A.E.; Vaidya, B.; Kaisar, M.A.; Cucullo, L.; Abbruscato, T.J. Nicotine and Electronic Cigarette (E-Cig) Exposure Decreases Brain Glucose Utilization in Ischemic Stroke. J. Neurochem. 2018, 147, 204. [Google Scholar] [CrossRef] [Green Version]
  9. Bhatnagar, A.; Whitsel, L.P.; Ribisl, K.M.; Bullen, C.; Chaloupka, F.; Piano, M.R.; Robertson, R.M.; McAuley, T.; Goff, D.; Benowitz, N. Electronic Cigarettes: A Policy Statement from the American Heart Association. Circulation 2014, 130, 1418–1436. [Google Scholar] [CrossRef] [Green Version]
  10. Ndunda, P.M.; Muutu, T.M. Abstract 9: Electronic Cigarette Use Is Associated with a Higher Risk of Stroke. Stroke 2019, 50 (Suppl. 1), A9. [Google Scholar] [CrossRef]
  11. Qasim, H.; Karim, Z.A.; Rivera, J.O.; Khasawneh, F.T.; Alshbool, F.Z. Impact of Electronic Cigarettes on the Cardiovascular System. J. Am. Heart Assoc. 2017, 6, e006353. [Google Scholar] [CrossRef]
  12. FDA. 2018 NYTS Data: A Startling Rise in Youth E-Cigarette Use. Available online: https://www.fda.gov/tobacco-products/youth-and-tobacco/2018-nyts-data-startling-rise-youth-e-cigarette-use (accessed on 30 August 2021).
  13. Euromonitor.com. Growth in Vapour Products. Available online: https://www.euromonitor.com/article/growth-vapour-products (accessed on 30 August 2021).
  14. Gentzke, A.S.; Creamer, M.; Cullen, K.A.; Ambrose, B.K.; Willis, G.; Jamal, A.; King, B.A. Vital Signs: Tobacco Product Use Among Middle and High School Students—United States, 2011–2018. MMWR. Morb. Mortal. Wkly. Rep. 2019, 68, 157–164. [Google Scholar] [CrossRef] [Green Version]
  15. Bullen, C.; Howe, C.; Laugesen, M.; McRobbie, H.; Parag, V.; Williman, J.; Walker, N. Electronic Cigarettes for Smoking Cessation: A Randomised Controlled Trial. Lancet 2013, 382, 1629–1637. [Google Scholar] [CrossRef]
  16. Harrell, P.T.; Simmons, V.N.; Correa, J.; Padhya, T.A.; Brandon, T.H. Electronic Nicotine Delivery Systems (“e-Cigarettes”): Review of Safety and Smoking Cessation Efficacy. Otolaryngol. Head Neck Surg. 2014, 151, 381–393. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  17. Farsalinos, K.E.; Spyrou, A.; Tsimopoulou, K.; Stefopoulos, C.; Romagna, G.; Voudris, V. Nicotine Absorption from Electronic Cigarette Use: Comparison between First and New-Generation Devices. Sci. Rep. 2014, 4, 4133. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  18. Vardavas, C.; Filippidis, F.T.; Agaku, I.T. Determinants and Prevalence of E-Cigarette Use throughout the European Union: A Secondary Analysis of 26 566 Youth and Adults from 27 Countries. Tob. Control 2015, 24, 442–448. [Google Scholar] [CrossRef]
  19. Lee, S.; Grana, R.A.; Glantz, S.A. Electronic Cigarette Use among Korean Adolescents: A Cross-Sectional Study of Market Penetration, Dual Use, and Relationship to Quit Attempts and Former Smoking. J. Adolesc. Health 2014, 54, 684–690. [Google Scholar] [CrossRef] [Green Version]
  20. Lee, H.-W.; Park, S.-H.; Weng, M.; Wang, H.-T.; Huang, W.C.; Lepor, H.; Wu, X.-R.; Chen, L.-C.; Tang, M. E-Cigarette Smoke Damages DNA and Reduces Repair Activity in Mouse Lung, Heart, and Bladder as Well as in Human Lung and Bladder Cells. Proc. Natl. Acad. Sci. USA 2018, 115, E1560–E1569. [Google Scholar] [CrossRef] [Green Version]
  21. Hutzler, C.; Paschke, M.; Kruschinski, S.; Henkler, F.; Hahn, J.; Luch, A. Chemical Hazards Present in Liquids and Vapors of Electronic Cigarettes. Arch. Toxicol. 2014, 88, 1295–1308. [Google Scholar] [CrossRef]
  22. Goniewicz, M.L.; Knysak, J.; Gawron, M.; Kosmider, L.; Sobczak, A.; Kurek, J.; Prokopowicz, A.; Jablonska-Czapla, M.; Rosik-Dulewska, C.; Havel, C.; et al. Levels of Selected Carcinogens and Toxicants in Vapour from Electronic Cigarettes. Tob. Control 2014, 23, 133–139. [Google Scholar] [CrossRef] [Green Version]
  23. Palmisani, J.; Abenavoli, C.; Famele, M.; Gilio, A.D.; Palmieri, L.; Gennaro, G.d.; Draisci, R. Chemical Characterization of Electronic Cigarette (e-Cigs) Refill Liquids Prior to EU Tobacco Product Directive Adoption: Evaluation of BTEX Contamination by HS-SPME-GC-MS and Identification of Flavoring Additives by GC-MS-O. Atmosphere 2020, 11, 374. [Google Scholar] [CrossRef] [Green Version]
  24. Bradford, S.; Stamatovic, S.M.; Dondeti, R.S.; Keep, R.; Andjelkovic, A.V. Nicotine Aggravates the Brain Postischemic Inflammatory Response. Am. J. Physiol. Heart Circ. Physiol. 2011, 300, H1518–H1529. [Google Scholar] [CrossRef] [Green Version]
  25. Kaisar, M.A.; Villalba, H.; Prasad, S.; Liles, T.; Sifat, A.E.; Sajja, R.K.; Abbruscato, T.J.; Cucullo, L. Offsetting the Impact of Smoking and E-Cigarette Vaping on the Cerebrovascular System and Stroke Injury: Is Metformin a Viable Countermeasure? Redox Biol. 2017, 13, 353–362. [Google Scholar] [CrossRef] [PubMed]
  26. Perez, C.M.; Hazari, M.S.; Ledbetter, A.D.; Haykal-Coates, N.; Carll, A.P.; Cascio, W.E.; Winsett, D.W.; Costa, D.L.; Farraj, A.K. Acrolein Inhalation Alters Arterial Blood Gases and Triggers Carotid Body-Mediated Cardiovascular Responses in Hypertensive Rats. Inhal. Toxicol. 2015, 27, 54–63. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  27. Hazari, M.S.; Haykal-Coates, N.; Winsett, D.W.; Krantz, Q.T.; King, C.; Costa, D.L.; Farraj, A.K. TRPA1 and Sympathetic Activation Contribute to Increased Risk of Triggered Cardiac Arrhythmias in Hypertensive Rats Exposed to Diesel Exhaust. Environ. Health Perspect. 2011, 119, 951. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  28. Wheat, L.A.; Haberzettl, P.; Hellmann, J.; Baba, S.P.; Bertke, M.; Lee, J.; McCracken, J.; O’Toole, T.E.; Bhatnagar, A.; Conklin, D.J. Acrolein Inhalation Prevents Vascular Endothelial Growth Factor-Induced Mobilization of Flk-1+/Sca-1+ Cells in Mice. Arterioscler. Thromb. Vasc. Biol. 2011, 31, 1598–1606. [Google Scholar] [CrossRef]
  29. Sithu, S.D.; Srivastava, S.; Siddiqui, M.A.; Vladykovskaya, E.; Riggs, D.; Conklin, D.J.; Haberzettl, P.; O’Toole, T.E.; Bhatnagar, A.; D’Souza, S.E. Exposure to Acrolein by Inhalation Causes Platelet Activation. Toxicol. Appl. Pharmacol. 2010, 248, 100–110. [Google Scholar] [CrossRef] [Green Version]
  30. Peters, A.; Dockery, D.W.; Muller, J.E.; Mittleman, M.A. Increased Particulate Air Pollution and the Triggering of Myocardial Infarction. Circulation 2001, 103, 2810–2815. [Google Scholar] [CrossRef] [Green Version]
  31. Sullivan, J.; Sheppard, L.; Schreuder, A.; Ishikawa, N.; Siscovick, D.; Kaufman, J. Relation between Short-Term Fine-Particulate Matter Exposure and Onset of Myocardial Infarction. Epidemiology 2005, 16, 41–48. [Google Scholar] [CrossRef]
  32. Wang, T.; Lang, G.D.; Moreno-Vinasco, L.; Huang, Y.; Goonewardena, S.N.; Peng, Y.J.; Svensson, E.C.; Natarajan, V.; Lang, R.M.; Linares, J.D.; et al. Particulate Matter Induces Cardiac Arrhythmias via Dysregulation of Carotid Body Sensitivity and Cardiac Sodium Channels. Am. J. Respir. Cell Mol. Biol. 2012, 46, 524–531. [Google Scholar] [CrossRef] [Green Version]
  33. Conklin, D.J.; Barski, O.A.; Lesgards, J.-F.; Juvan, P.; Rezen, T.; Rozman, D.; Prough, R.A.; Vladykovskaya, E.; Liu, S.; Srivastava, S.; et al. Acrolein Consumption Induces Systemic Dyslipidemia and Lipoprotein Modification. Toxicol. Appl. Pharmacol. 2009, 243, 1–12. [Google Scholar] [CrossRef] [Green Version]
  34. Srivastava, S.; Sithu, S.D.; Vladykovskaya, E.; Haberzettl, P.; Hoetker, D.J.; Siddiqui, M.A.; Conklin, D.J.; D’Souza, S.E.; Bhatnagar, A. Oral exposure to acrolein exacerbates atherosclerosis in apoE-null mice. Atherosclerosis 2011, 215, 301–308. [Google Scholar] [CrossRef] [Green Version]
  35. Kuntic, M.; Oelze, M.; Steven, S.; Kröller-Schön, S.; Stamm, P.; Kalinovic, S.; Frenis, K.; Vujacic-Mirski, K.; Bayo Jimenez, M.T.; Kvandova, M.; et al. Short-Term e-Cigarette Vapour Exposure Causes Vascular Oxidative Stress and Dysfunction: Evidence for a Close Connection to Brain Damage and a Key Role of the Phagocytic NADPH Oxidase (NOX-2). Eur. Heart J. 2020, 41, 2472–2483. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  36. Vansickel, A.R.; Eissenberg, T. Electronic Cigarettes: Effective Nicotine Delivery After Acute Administration. Nicotine Tob. Res. 2013, 15, 267. [Google Scholar] [CrossRef] [Green Version]
  37. Nides, M.A.; Leischow, S.J.; Bhatter, M.; Simmons, M. Nicotine Blood Levels and Short-Term Smoking Reduction with an Electronic Nicotine Delivery System. Am. J. Health Behav. 2014, 38, 265–274. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  38. Yan, X.S.; D’Ruiz, C. Effects of Using Electronic Cigarettes on Nicotine Delivery and Cardiovascular Function in Comparison with Regular Cigarettes. Regul. Toxicol. Pharmacol. 2015, 71, 24–34. [Google Scholar] [CrossRef] [PubMed]
  39. Vlachopoulos, C.; Ioakeimidis, N.; Abdelrasoul, M.; Terentes-Printzios, D.; Georgakopoulos, C.; Pietri, P.; Stefanadis, C.; Tousoulis, D. Electronic Cigarette Smoking Increases Aortic Stiffness and Blood Pressure in Young Smokers. J. Am. Coll. Cardiol. 2016, 67, 2802–2803. [Google Scholar] [CrossRef] [PubMed]
  40. Carnevale, R.; Sciarretta, S.; Violi, F.; Nocella, C.; Loffredo, L.; Perri, L.; Peruzzi, M.; Marullo, A.G.; De Falco, E.; Chimenti, I.; et al. Acute Impact of Tobacco vs Electronic Cigarette Smoking on Oxidative Stress and Vascular Function. Chest 2016, 150, 606–612. [Google Scholar] [CrossRef]
  41. Antoniewicz, L.; Bosson, J.A.; Kuhl, J.; Abdel-Halim, S.M.; Kiessling, A.; Mobarrez, F.; Lundbäck, M. Electronic Cigarettes Increase Endothelial Progenitor Cells in the Blood of Healthy Volunteers. Atherosclerosis 2016, 255, 179–185. [Google Scholar] [CrossRef] [Green Version]
  42. Hom, S.; Chen, L.; Wang, T.; Ghebrehiwet, B.; Yin, W.; Rubenstein, D.A. Platelet Activation, Adhesion, Inflammation, and Aggregation Potential Are Altered in the Presence of Electronic Cigarette Extracts of Variable Nicotine Concentrations. Platelets 2016, 27, 694–702. [Google Scholar] [CrossRef]
  43. Caporale, A.; Langham, M.C.; Guo, W.; Johncola, A.; Chatterjee, S.; Wehrli, F.W. Acute Effects of Electronic Cigarette Aerosol Inhalation on Vascular Function Detected at Quantitative MRI. Radiology 2019, 293, 97–106. [Google Scholar] [CrossRef]
  44. Antoniewicz, L.; Brynedal, A.; Hedman, L.; Lundbäck, M.; Bosson, J.A. Acute Effects of Electronic Cigarette Inhalation on the Vasculature and the Conducting Airways. Cardiovasc. Toxicol. 2019, 19, 441–450. [Google Scholar] [CrossRef] [Green Version]
  45. Mitchell, G.F.; Hwang, S.-J.; Vasan, R.S.; Larson, M.G.; Pencina, M.J.; Hamburg, N.M.; Vita, J.A.; Levy, D.; Benjamin, E.J. Arterial Stiffness and Cardiovascular Events: The Framingham Heart Study. Circulation 2010, 121, 505–511. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  46. Nocella, C.; Biondi-Zoccai, G.; Sciarretta, S.; Peruzzi, M.; Pagano, F.; Loffredo, L.; Pignatelli, P.; Bullen, C.; Frati, G.; Carnevale, R. Impact of Tobacco Versus Electronic Cigarette Smoking on Platelet Function. Am. J. Cardiol. 2018, 122, 1477–1481. [Google Scholar] [CrossRef]
  47. Boas, Z.; Gupta, P.; Moheimani, R.S.; Bhetraratana, M.; Yin, F.; Peters, K.M.; Gornbein, J.; Araujo, J.A.; Czernin, J.; Middlekauff, H.R. Activation of the “Splenocardiac Axis” by Electronic and Tobacco Cigarettes in Otherwise Healthy Young Adults. Physiol. Rep. 2017, 5, e13393. [Google Scholar] [CrossRef] [PubMed]
  48. Qasim, H.; Karim, Z.A.; Silva-Espinoza, J.C.; Khasawneh, F.T.; Rivera, J.O.; Ellis, C.C.; Bauer, S.L.; Almeida, I.C.; Alshbool, F.Z. Short-Term E-Cigarette Exposure Increases the Risk of Thrombogenesis and Enhances Platelet Function in Mice. J. Am. Heart Assoc. 2018, 7, e009264. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  49. Alzahrani, T.; Pena, I.; Temesgen, N.; Glantz, S.A. Association between Electronic Cigarette Use and Myocardial Infarction. Am. J. Prev. Med. 2018, 55, 455–461. [Google Scholar] [CrossRef] [PubMed]
  50. Moheimani, R.S.; Bhetraratana, M.; Yin, F.; Peters, K.M.; Gornbein, J.; Araujo, J.A.; Middlekauff, H.R. Increased Cardiac Sympathetic Activity and Oxidative Stress in Habitual Electronic Cigarette Users: Implications for Cardiovascular Risk. JAMA Cardiol. 2017, 2, 278–284. [Google Scholar] [CrossRef] [PubMed] [Green Version]
  51. Franzen, K.F.; Willig, J.; Talavera, S.C.; Meusel, M.; Sayk, F.; Reppel, M.; Dalhoff, K.; Mortensen, K.; Droemann, D. E-Cigarettes and Cigarettes Worsen Peripheral and Central Hemodynamics as Well as Arterial Stiffness: A Randomized, Double-Blinded Pilot Study. Vasc. Med. 2018, 23, 419–425. [Google Scholar] [CrossRef]
  52. Vlachopoulos, C.; Kosmopoulou, F.; Panagiotakos, D.; Ioakeimidis, N.; Alexopoulos, N.; Pitsavos, C.; Stefanadis, C. Smoking and Caffeine Have a Synergistic Detrimental Effect on Aortic Stiffness and Wave Reflections. J. Am. Coll. Cardiol. 2004, 44, 1911–1917. [Google Scholar] [CrossRef] [Green Version]
  53. Besaratinia, A.; Tommasi, S. Vaping: A Growing Global Health Concern. EClinicalMedicine 2019, 17, 100208. [Google Scholar] [CrossRef] [Green Version]
  54. George, J.; Hussain, M.; Vadiveloo, T.; Ireland, S.; Hopkinson, P.; Struthers, A.D.; Donnan, P.T.; Khan, F.; Lang, C.C. Cardiovascular Effects of Switching from Tobacco Cigarettes to Electronic Cigarettes. J. Am. Coll. Cardiol. 2019, 74, 3112. [Google Scholar] [CrossRef]
Figure 1. Acute and chronic effects of e-cigarettes smoking on cerebrovascular and cardiovascular systems.
Figure 1. Acute and chronic effects of e-cigarettes smoking on cerebrovascular and cardiovascular systems.
Neurolint 14 00037 g001
Table 1. Prevalence of stroke among various smoking habits among NHANES respondents 2015–2018 (n = 79,825).
Table 1. Prevalence of stroke among various smoking habits among NHANES respondents 2015–2018 (n = 79,825).
E-Cigarette Smokers
n = 7756 (9.72%)
Dual E-Cigarette + Traditional Smokers
n = 23,444 (29.37)
Traditional Smokers n = 48,625 (60.91%)Total
n = 79,825 (100)
p Values
Stroke (n)
(Prevalence %)
(Column % comparison between different smoking habits)
66
(1.57)
(1.09)
855
(20.39)
(3.72)
3273
(78.04)
(6.75)
4194
(100)
(5.41)
<0.0001
Age of onset of stroke in years
(Median + IQR)
48 (42–58)50 (40–58)59 (50–69) <0.0001
Table 2. Socio-demographics characteristics of various smoking habits among respondents with history of stroke (n = 4194).
Table 2. Socio-demographics characteristics of various smoking habits among respondents with history of stroke (n = 4194).
E-Cigarette Smokers with History of Stroke
n = 66
(1.57%)
Dual E-Cigarette + Traditional Smokers with History of Stroke
n = 855 (20.39%)
Traditional Smokers with History of Stroke n = 3273 (78.04%)Total
n = 4194 (100)
p Value
Age in years at screening
(Median + IQR)
50 (45–63)55 (47–64)69 (62–80) <0.0001
Sex (%) <0.0001
Female36.3651.9333.9137.63
Male63.6448.0766.0962.37
Race (%) <0.0001
Mexican-American21.2111.586.027.39
Other Hispanic24.245.157.707.44
Non-Hispanic White37.8847.1342.7743.59
Non-Hispanic Black0.0024.0931.2929.33
Non-Hispanic Asian0.000.003.792.96
Other Race—Including Multi-Racial16.6712.058.439.30
Annual Household Income (%) <0.0001
$0–$25,00057.5859.1550.6752.44
$25,000–$65,00016.6732.1832.4932.16
$65,000–$100,00025.764.277.997.57
>$100,0000.004.418.857.83
Comorbidities (%)
Coronary Heart Disease (%)25.7615.3227.6225.08<0.0001
Congestive Heart Failure (%)25.7621.7516.5917.79<0.0001
High Blood Pressure—2+ Times (%)60.9898.0280.9184.11<0.0001
Recent Systolic Blood Pressure in mmHg
(Median) *
118120134 <0.0001
Recent Diastolic Blood Pressure in mmHg
(Median) *
708080 <0.0001
Taking Prescribed Medicine For HBP (%)100.0081.6689.3387.89<0.0001
High Cholesterol Level (%)25.7660.5858.1158.11<0.0001
Taking Prescribed Medicine High Cholesterol (%)100.0082.5284.3981.830.2876
LDL-Cholesterol, NIH Equation 2 (mg/dL) (Median) *112101110 <0.0001
Diabetes (%)50.0019.0636.6333.26<0.0001
Last Hb A1C Level (Median) *5.77.27.9 <0.0001
Feeling Down, Depressed, Or Hopeless (%) <0.0001
Several Days12.1217.5618.2417.99
More Than Half The Days0.0013.598.919.73
Nearly Every Day21.2119.877.4610.29
Liver Disorders (%)21.216.439.849.32<0.0001
Cancer Or Malignancy (%)25.7617.1924.3522.91<0.0001
Alcohol use disorder—Heavy drinking (%) 30.9141.9761.2456.03<0.0001
Marijuana or Hashish (%)100.0092.1566.2078.61<0.0001
Cocaine/Heroin/Methamphetamin (%)71.2138.8531.6434.93<0.0001
Inject Illegal Drug (%)21.211.774.634.63<0.0001
Percentage in brackets are column %, indicating a direct comparison between e-cigarette users vs. dual smokers vs. traditional smokers. * Due to positive skewed data and absence of 75th percentile (Q3) value, IQR for the median was not mentioned Heavy drinking: for women, 8 or more drinks per week, and for men, 15 or more drinks per week.
Table 3. Regression analysis showing relationship between various types of tobacco consumption and stroke.
Table 3. Regression analysis showing relationship between various types of tobacco consumption and stroke.
VariableMultivariable Analysis *
Odds Ratio (95% Confidence Interval); p Value
c-Value (Area under ROC)
Possibility of having history of stroke = 1
Non-smokersReference
E-cigarette smokers vs. Traditional smokers1.15 (1.15–1.16); p < 0.00010.733
Dual smokers vs. Traditional smokers1.14 (1.14–1.15); p < 0.0001
E-cigarette smoking in last 30-days vs. no-E-cigarette smoking in last 30-days1.60 (1.60–1.61); p < 0.00010.894
* Model for multivariable regression analysis was adjusted with sociodemographic variables like age, gender, race, annual household income, and comorbidities.
Table 4. Potential vascular effects of e-cigarette components.
Table 4. Potential vascular effects of e-cigarette components.
Component Potentially InvolvedEffect [11,26,27,28,29,30,31,32,33,34]
Acrolein, PMs, nicotineIncreased blood pressure
AcroleinMyocardial dysfunction and cardiomyopathy, impaired vascular repair, and vascular injury
Acrolein, PMsReduced cardiac contractility, Increased risk of thrombosis, increased risk of ventricular arrhythmias
PMs, nicotineCoronary artery disease and myocardial infarction
PMs: fine and ultrafine particulate matters.
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Patel, U.; Patel, N.; Khurana, M.; Parulekar, A.; Patel, A.; Ortiz, J.F.; Patel, R.; Urhoghide, E.; Mistry, A.; Bhriguvanshi, A.; et al. Effect Comparison of E-Cigarette and Traditional Smoking and Association with Stroke—A Cross-Sectional Study of NHANES. Neurol. Int. 2022, 14, 441-452. https://doi.org/10.3390/neurolint14020037

AMA Style

Patel U, Patel N, Khurana M, Parulekar A, Patel A, Ortiz JF, Patel R, Urhoghide E, Mistry A, Bhriguvanshi A, et al. Effect Comparison of E-Cigarette and Traditional Smoking and Association with Stroke—A Cross-Sectional Study of NHANES. Neurology International. 2022; 14(2):441-452. https://doi.org/10.3390/neurolint14020037

Chicago/Turabian Style

Patel, Urvish, Neel Patel, Mahika Khurana, Akshada Parulekar, Amrapali Patel, Juan Fernando Ortiz, Rutul Patel, Eseosa Urhoghide, Anuja Mistry, Arpita Bhriguvanshi, and et al. 2022. "Effect Comparison of E-Cigarette and Traditional Smoking and Association with Stroke—A Cross-Sectional Study of NHANES" Neurology International 14, no. 2: 441-452. https://doi.org/10.3390/neurolint14020037

APA Style

Patel, U., Patel, N., Khurana, M., Parulekar, A., Patel, A., Ortiz, J. F., Patel, R., Urhoghide, E., Mistry, A., Bhriguvanshi, A., Abdulqader, M., Mehta, N., Arumaithurai, K., & Shah, S. (2022). Effect Comparison of E-Cigarette and Traditional Smoking and Association with Stroke—A Cross-Sectional Study of NHANES. Neurology International, 14(2), 441-452. https://doi.org/10.3390/neurolint14020037

Article Metrics

Back to TopTop