|Year : 2020 | Volume
| Issue : 4 | Page : 147-155
Smoking history, smoking intensity, and type of cigarette as risk factors of bladder cancer: A literature review
Sawkar Vijay Pramod1, Ferry Safriadi1, Bethy S Hernowo2, Reiva Farah Dwiyana3, Baskara Batista1
1 Department of Urology, Hasan Sadikin Academic Medical Center, Universitas Padjajaran Bandung, Bandung, Indonesia
2 Department of Anatomy Pathology, Hasan Sadikin Academic Medical Center, Universitas Padjajaran Bandung, Bandung, Indonesia
3 Faculty of Medicine, Universitas Padjadjaran - Hasan Sadikin Academic Medical Center, Bandung, Indonesia
|Date of Submission||21-Jan-2020|
|Date of Decision||17-Mar-2020|
|Date of Acceptance||15-Apr-2020|
|Date of Web Publication||25-Jul-2020|
Sawkar Vijay Pramod
Department of Urology, Hasan Sadikin Academic Medical Center, Jl. Pasteur 38, Bandung 40161
Source of Support: None, Conflict of Interest: None
Smoking is a major risk factor that plays a role in the incidence of bladder cancer. Carcinogens from cigarettes are excreted through the urine, so direct contact with the urinary tract occurs and increases the risk of malignancy. Literature is obtained from the search results of PubMed, Medscape, and Science Direct electronic databases with some keywords used. Starting in 2009, 88 literature results were collected through the electronic databases of PubMed, Medscape, and Science Direct. After applying the exclusion criteria, 12 articles are included in this literature review with 536,989 bladder cancer patients and 52,753 controls in total. High clove cigarette smoking intensity (>40 cigarettes/day) is a risk of causing urothelial carcinoma bladder cancer. Clove cigarettes pose the highest risk of bladder cancer. Compared to clove cigarette, cigars, and tobacco pipes have relatively lower risk of causing bladder cancer. Meanwhile, other types of cigarettes, such as shisha and electronic cigarettes, do not eliminate the risk of bladder cancer. Smoking is a modifiable risk factor for bladder cancer. The current smoking history was associated with a higher risk of bladder cancer compared to the former history of smoking. Different types of smoking have different risks of bladder cancer.
Keywords: Bladder cancer, risk factors, smoking
|How to cite this article:|
Pramod SV, Safriadi F, Hernowo BS, Dwiyana RF, Batista B. Smoking history, smoking intensity, and type of cigarette as risk factors of bladder cancer: A literature review. Urol Sci 2020;31:147-55
|How to cite this URL:|
Pramod SV, Safriadi F, Hernowo BS, Dwiyana RF, Batista B. Smoking history, smoking intensity, and type of cigarette as risk factors of bladder cancer: A literature review. Urol Sci [serial online] 2020 [cited 2020 Sep 23];31:147-55. Available from: http://www.e-urol-sci.com/text.asp?2020/31/4/147/290858
| Introduction|| |
Bladder cancer is a malignancy originating from the urothelial lining of the bladder, renal pelvis, ureter, and urethra. Most bladder cancers are found in the bladder, while tumors in the ureter, urethra, and renal pelvis are only found in small amounts. Bladder cancer is the 4th most common malignancy in men in Germany and the 19th globally. Bladder cancer was also the 13th leading cause of death associated with malignancy. In 2016, there were reportedly 437,442 new cases of bladder cancer globally. This figure increased by 31% compared to new cases of bladder cancer in 2006. Global mortality from bladder cancer in 2016 increased by 64% compared to that in 1990, which was as many as 186,199 deaths. Epidemiological studies in Egypt showed that bladder cancer is often experienced in men with a ratio of women: men ranging from 1:4 to 1:7. The incidence of bladder cancer in Indonesia was still uncertain. Based on data from bladder cancer at Hasan Sadikin Hospital in Bandung, there were 351 cases of bladder cancer in the past 7 years. Patients who had bladder cancer have a mean age of 60.8 years, and it is more common in men with a male: female ratio of 6:1. Bladder cancer patients usually complain of massive or microscopic hematuria with/without frequency symptoms and pain during micturating., Patients with these symptoms are advised to undergo computed tomography urography or magnetic resonance imaging to evaluate the upper urinary tract and cystoscopy to evaluate the lower urinary tract. Inflammatory tumors or areas visualized during a cystoscopic procedure are taken into consideration to determine the pathology of the disease known as the transurethral resection of bladder tumor. Histologically, the most common bladder cancer is nonmuscle invasive bladder cancer which covers 70%–80% of overall cases and 90.8% in epidemiological studies at Hasan Sadikin Hospital in Bandung., Risk factors for bladder cancer are divided into two groups: those that cannot be modified and those that can be modified. Gender is a risk factor for bladder cancer that cannot be modified. Men are reported to be three times more likely to suffer from bladder cancer than women. However, the mortality rate is reported to be higher in women with bladder cancer. The risk factors for bladder cancer that can be modified include smoking and the environment/exposure to chemicals at work. Smoking is a major risk factor that plays a role in 50% of the incidence of bladder cancer., Carcinogens contained in cigarettes are excreted through the urine, so direct contact with the urinary tract occurs and increases the risk of malignancy. Exposure to chemicals such as aromatic amines, polycyclic aromatic hydrocarbons, and chlorine hydrocarbons often found in the paint, metal, and fuel industries is also a risk factor for bladder cancer. Other risk factors associated with the incidence of bladder cancer are chronic inflammation due to chronic urinary infection and schistosomiasis, genetic abnormalities, nutrition, radiotherapy, and drugs., Bladder cancer is a disorder with a high recurrence rate of up to 75%. Bladder cancer is also associated with a significant financial burden on individuals and health services. With knowing the risk factors associated with bladder cancer, the risk of having bladder cancer can be reduced. This review will discuss smoking, the type of cigarette, the intensity of smoking, and the mechanisms contributing to the incidence of bladder cancer.
| Methods|| |
Literature search strategy
Literature is obtained from the search results of PubMed, Medscape, and Science Direct electronic databases with the following keywords: “Bladder cancer risk factors,” “cigar and bladder cancer,” “tobacco pipe and bladder cancer,” and “e-cigarette and bladder cancer.” References cited in the relevant literature are taken manually and only from full articles.
Inclusion and exclusion criteria
Based on the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines, the literature found was conducted by reviewing Population, Intervention, Comparator, Outcome, and Study design to determine the feasibility of the study. Studies are considered feasible if they meet the inclusion criteria, including (1) patients diagnosed with bladder cancer; (2) examining one of the following variables: (i) Smoking history, (ii) intensity of smoking, and (iii) types of cigarettes; and (3) analyzing the relationship of smoking history, intensity of smoking, and type of cigarette with bladder cancer. Literature in the form of case reports, only abstracts, report meetings, conferences, editorial comments, reviews (not systematic literature reviews and meta-analyses), studies with irrelevant results, inaccessible literature, duplications from previous literature publications, and studies not written in English are excluded.
Systematic literature review process
After the exclusion of multiple literatures, the evaluation of the abstract and title of the relevant literature was carried out. From the evaluation of abstracts and titles, literature that fulfilled the requirements for a full evaluation was obtained. Data are then extracted and presented in a table. The table consists of the name of the author, year of publication, country of origin, study design, number of samples, smoking, type of cigarette, and intensity of smoking, as well as the relationship of smoking, type of cigarette, and the intensity of smoking with bladder cancer. The PRISMA diagram that describes the literature review process and literature selection is shown in [Figure 1].
|Figure 1: Preferred reporting items for systematic reviews and meta-analysis diagram that describes the search process for literature review and literature selection|
Click here to view
| Results|| |
Literature search results
Starting in 2009, 88 articles were collected through the electronic databases of PubMed, Medscape, and Science Direct. After the exclusion of multiple literatures, 60 relevant literatures were obtained for the evaluation of abstracts and titles. From the results of the evaluation of abstracts and titles, 37 literatures met the requirements for a full evaluation. Following all the inclusion and exclusion criteria mentioned earlier, 12 literatures were finally selected and included in this literature review.
This literature involved 536,989 bladder cancer patients and 52,753 controls in total. The included literature consisted of 6 case–control studies, 2 cross-sectional studies, 3 cohort studies, and 1 meta-analysis study that examined the relationship of smoking, the type of cigarette, and the intensity of smoking with bladder cancer [Table 1]. Bladder cancer distribution based on smoking history is as described in [Table 2]. Bladder cancer distribution by the intensity of smoking and type of cigarette is as described in [Table 3] and [Table 4].
| Discussion|| |
Smoking history and bladder cancer
Smoking is a modifiable risk factor for bladder cancer. Smoking has been linked to the incidence of various malignancies. In western countries, at least 50% of bladder cancer diagnoses are due to smoking. Bladder cancer is the second-most common tobacco-related malignancy and attacks the lungs, and there is a relative risk of oral and upper gastrointestinal cancers between tobacco users and nontobacco users. As in patients with lung cancer and otolarynx, newly diagnosed bladder cancer patients who continue to smoke can increase the likelihood of a second primary recurrence, development, and malignancy.
Regarding the characteristics shown in the Andrew et al. study sample, it was found that 51% of each population of bladder cancer had a previous history of smoking. This indicates that smoking is a factor that cannot be ignored in studies of bladder cancer risk factors. The current smoking history was associated with a higher risk of bladder cancer (odds ratio [OR] 3.49; 95% confidence interval [CI]: 2.59–4.70) compared to the previous history of smoking (OR 2.06; 95% CI: 1.69–2.50). Similar findings were demonstrated by Lukas et al., where individuals with the current smoking history (OR 1.96; 95% CI: 0.71–5.42) had risk factors for higher bladder cancer compared to subjects with previous smoking history (OR 1.46; 95% CI: 0.83–2.57). Sun et al. also showed that there is a higher risk of bladder cancer in the current smokers (OR 1.36; 95% CI: 0.83–2.23) compared to individuals with previous smoking history (OR 0.89; 95% CI: 0.49–1.64).
When reviewed based on luminal-like and basal-like bladder cancer subtypes, current smokers were more likely to develop luminal-like bladder cancer, while individuals with a former history of smoking were more likely to have basal-like bladder cancer. The grade and stage of basal-like type tumors are higher in current smokers. However, this finding is not statistically significant and is influenced by other risk factors.
Exposure to cigarette smoke was also reported to have a statistically significant association with bladder cancer (P = 0.003). The number of bladder cancer patients exposed to cigarette smoke either inside or outside their homes was more than those exposed to cigarette smoke inside and outside the home, and the relationship between them was statistically significant (52.6% vs. 10.2%). The results of this study indicate that smoke and smoking environments are also risk factors for causing bladder cancer.
It was mentioned earlier that smoking and jobs such as the paint industry are high risk factors for causing bladder cancer, but smoking is reported to be the highest risk factor for bladder cancer. Smoking is a major risk factor that plays a role in 50% of the incidence of bladder cancer.,, Cigarettes contain hydrocarbons, aromatic amines, 2-naphtylamine, and N-nitroso which can damage DNA by forming bulky adducts and damaging single and multiple DNA chains and basal modification resulting in uncontrolled cell growth and inhibition of the tumor growth inhibitory mechanism. Carcinogens in cigarettes are generally metabolized by xenobiotic enzymes, such as N-acetyltransferase (NAT) and glutathione S-transferase. Carcinogens contained in cigarettes are excreted through the urine, so direct contact with the urinary tract occurs and increases the risk of malignancy. If someone has a slow NAT2 acetylation activity (generally found in smokers), there will be a reduction in the efficiency of carcinogen detoxification as carcinogens accumulate in high levels of the urothelium.,
The intensity of smoking and bladder cancer
Studies that examined the effect of the intensity of clove cigarette smoking on bladder cancer did not show a statistically significant difference (P = 0.49). Different results are indicated if the variable intensity of cigarettes is categorized based on cigarettes per year. Another study found that most patients of all urinary cancer subtypes smoked at least 20 clove cigarettes/day. Fuller et al. found that 84.6% of subjects who smoked electronic cigarettes 28 times/week had increased levels of o-toluidine and 2-naphthylamine.
When reviewed based on bladder cancer subtypes, in individuals with urothelial carcinoma who smoked clove cigarettes, the highest risk of the incidence of bladder cancer was found in patients who smoked >40 cigarettes/day (OR 2.3; 95% CI 1.4–3.6), while the risk of occurrence of squamous cell carcinoma was found to be the highest in subjects who smoked 1–10 cigarettes/day (OR 1.6; 95% CI 1.2–22). This study concluded that clove smoking was associated with the risk of urothelial carcinoma and was not significantly associated with squamous cell carcinoma, whereas, in the smoking intensity variable with a waterpipe, there was no significant relationship between the intensity of smoking waterpipe (hagar) and bladder cancer. The risk of urothelial carcinoma was found to be the highest in individuals who smoked ≤1 hagar/day (OR 1.8; 95% CI 1.0–3.1), but this risk was not found to increase with increasing intensity of smoking, while the risk of squamous, cell carcinoma was found to be the highest in individuals who smoked 2–5 hagar/day (OR 1.6; 95% CI 1.1–2.5). The absence of a significant relationship is thought to be due to the subject not being dependent on tobacco products as they only consume small amounts of tobacco.
Compared to nonsmokers, the pooled odd ratio and the corresponding 95% CIs of bladder cancer were 1.64 (1.5–3.3) for smoking with low heterogeneities (I 2 8.43%, P = 0.001).
Funnel plot of the studies showed that 9 studies included in this systematic review were symmetrically distributed among the pyramid. This means that the bias was minimal [Figure 2] and [Figure 3].
Types of cigarettes and bladder cancer
A study that examined the relationship of clove cigarettes with bladder cancer reported that clove cigarettes were of risk of causing bladder cancer (OR 4.2; 95% CI 2.3–3.7). Bassett et al. found that most patients with bladder cancer are previous clove cigarette smokers (57%), while 17.4% of 344 bladder cancer patients are current smokers. The study also states that a diagnosis of bladder cancer is effective in the cigarette cessation program. Forty-eight percent of smokers will quit smoking after receiving a bladder cancer diagnosis. The study by Wolpert also states that clove smoking is associated with a risk of bladder cancer (P = 0.03). Wolpert et al. found that 4 out of 5 women with clove cigarettes had bladder cancer.
When specifically reviewing the risk of clove cigarettes on the types of bladder cancer histology, namely, urothelial carcinoma and squamous cell carcinoma, a history of previous clove cigarettes is currently associated with an increased risk of urothelial carcinoma which is greater (OR 1.2; 95% CI: 0.9–1.7; OR 2.1; 95% CI: 1.7–2.6) compared to squamous cell carcinoma (OR 0.9; 95% CI: 0.6–1.3; OR 1.4; 95% CI: 1.0–1.8). In the low-grade, high-grade, and muscle-invasive bladder cancer subtypes, kretek smokers are more at risk of developing invasive muscle bladder cancer (OR 3.7; 95% CI: 2.5–5.5). This level of risk is followed by high-grade subtypes (OR 2.7; 95% CI: 2.1–3.6) and low-grade subtypes (OR 2.2; 95% CI: 1.8–2.8). The risk of developing tumors is reported to be higher in high-grade subtypes, whereas invasive muscle tumors tend to have a worse prognosis and tendency to metastasize.
The mechanism of clove cigarettes causing bladder cancer is still unclear. Zeegers et al. assumed that the risk of bladder cancer is associated with a large number of chemicals contained in cigarette smoke, such as 2-naphthylamine and 4-aminobiphenyl., When viewed from the mechanism of bladder cancer, it was estimated that different molecular pathways are involved in tumor carcinogenesis invasive muscle compared to superficial tumors. Low-grade bladder cancer is characterized by activation of the Ras-mitogen-activated protein kinase (MAPK) constitutive pathway., Changes in the RAS-MAPK and PI3K-Akt pathways are primarily the cause of abnormal cell growth in urothelial neoplasia. Active mutations in RAS lead to the activation of MAPK and PI3K pathways.,, The stimulation of RAS-MAPK and PIK3T-AKT pathway by fibroblast growth factor receptor 3 which mediates fibroblast growth factors will stimulate and trigger cell proliferation and differentiation. Invasive muscle tumors are characterized by inactivation of pathways p53, p16, and pRb. Tumor invasion is also triggered by factors that alter the tumor microenvironment such as excessive expression of cyclooxygenase 2. Cigarette tobacco produces polycyclic aromatic hydrocarbons that can affect TP53 mutations in the pathogenesis of bladder cancer.,
The results of the Wolpert et al.'s study showed that the risk of bladder cancer was higher in patients with a history of smoking shisha/waterpipe currently compared to those with a previous history of smoking shisha/waterpipe (100% vs. 0%, P = 0.01). In bladder cancer subtype, individuals with a previous smoking history of waterpipe were associated with an increased risk for squamous cell carcinoma (OR 1.8; 95% CI: 1.0–3.3) than for urothelial carcinoma (OR 1.3; 95% CI: 0.7–2.2), whereas individuals with current waterpipe history were associated with a greater risk for urothelial carcinoma (OR 1.5; 95% CI: 1.1–2.0) than for squamous cell carcinoma (OR 1.2; 95% CI: 0.9–1.8). The risk of a history of clove smoking against bladder cancer greater than this waterpipe indicates that the waterpipe is no more dangerous than clove cigarettes.
Waterpipes contain toxic substances and carcinogens that are known to be associated with smoking-related diseases. Cigarette waterpipes are reported to increase the levels of carcinoembryonic antigen compared to nonsmokers. Another study also reported that carcinogenesis in waterpipe smokers is caused by genotoxic and clastogenic components contained in waterpipes, such as tar and polycyclic aromatic hydrocarbons. The waterpipe was reported to have significantly higher micronucleus in exfoliated oral cavity cells which showed a genotoxic effect of waterpipes, thus increasing the risk of urothelial carcinoma and squamous cell carcinoma. Another study states that there is an increase in the take-up of chemicals contained in waterpipes, such as nicotine, carbon monoxide, polyaromatic hydrocarbons, and/or N-nitrosamines, compared to clove smokers.
Based on the type of cigarette, the type of tobacco used in cigars is black tobacco. The cigar also does not have filters. Smoke of cigars is reported to contain 200% mutagenic ingredients per nicotine than clove cigarettes. Furthermore, cigar smoke contains dangerous mixtures such as aromatic amines, tar, carbon monoxide, benzo (a) pyrene, and high levels of Nicotine-derived nitrosamine ketone (NNK), so the use of this product will result in greater exposure than clove cigarettes.,
Malhotra et al. reported that the risk of bladder cancer increased in cigar smokers compared to nonsmokers (OR 1.14, 95% CI 0.88–1.58). The risk of bladder cancer was also increased by 1.78 times (95% CI 1.33–2.38) up to 1.9 times (95% CI 0.6–3.5) in cigar smokers compared to nonsmokers., This risk is lower than that of kretek smokers. On the other hand, fewer cigar smokers than kretek smokers explain that there is no increased risk through systemic effects (such as bladder cancer).,
Tobacco cigarette smoke contains more dangerous mixtures than clove cigarettes, such as benzo (a) pyrene. Tobacco pipes are also reported to contain 44% more mutagenic ingredients per nicotine than clove cigarettes. Malhotra et al. reported that the risk of bladder cancer increased 1.4 times with CI 1.07–1.84 in tobacco pipe smokers compared to nonsmokers. This risk is found to be lower than for kretek and shisha smokers, but higher than for cigar smokers. Other studies show a higher risk, namely, risk of tobacco pipe smoker 1.62 times (95% CI 1.23–2.14) and cigar smokers 1.8 times (95% CI 0.9–3.4) compared to nonsmokers.,,
Electronic cigarettes are battery-powered cigarettes that work by heating liquids (e-liquids) to produce aerosols for inhalation to help smokers stop smoking or reduce the intensity of smoking. There are three main components of e-liquids, including propylene glycol and/or glycerol, nicotine, and flavoring. The nicotine concentration used varies, namely, 0 to 36 mg/ml, with levels of 18 mg/ml which are the most commonly used levels. The most widely used flavors are tobacco flavor, fruit, and mint/menthol.
Fuller et al. reported that users of electronic cigarettes had a significant increase in o-toluidine and 2-naphthylamine levels compared to the control group (not electronic cigarette users and nonsmokers) (P = 0.0013; P = 0.014). The concentration of o-toluidine and 2-naphthylamine in electronic cigarette users was 2.33 ng/ml and 1.46 ng/ml, respectively. Recent studies explain the chemicals contained in electronic cigarettes. Electronic cigarettes are reported to contain carcinogens such as nitrosamines specific to tobacco, formaldehyde, polyaromatic hydrocarbons, and heavy metals that are known to cause malignancy. Polyaromatic hydrocarbons, aldehydes, aromatic amines (2-naphthylamine and o-toluidine), and cresol (aerosols in electronic cigarettes) are carcinogenic, which when inhaled on the long term can cause bladder cancer. The mechanism of aromatic amine causes bladder cancer to be relevant in genetically susceptible individuals. N-acetylation in the liver detoxifies aromatic amines and is largely metabolized by NAT2 enzymes. Reduced NAT2 functional alleles cause acetylation to slow down and increase the risk of bladder cancer when exposed to aromatic amines. However, the levels of aromatic amines that can induce bladder cancer are unknown., Besides, nicotine itself is also thought to be a malignant initiator in the urinary tract system. The use of nicotine can induce higher cell death and double chain DNA damage.,, The presence of bladder carcinogens in urine specimens of users of electronic cigarettes at higher concentrations than controls requires close supervision of the composition of liquid electronic cigarettes, given the unknown limit exposure that can induce bladder cancer in genetically susceptible patients.
| Conclusion|| |
Smoking is a modifiable risk factor for bladder cancer. Various studies have found that a former history of smoking and current smoking increase the risk of bladder cancer. Smoking produces carcinogens such as NAT and glutathione S-transferase which are excreted through the urine and experience direct contact with bladder cells.
Individuals with high clove cigarette smoking intensity (>40 cigarettes/day) are at risk of having urothelial carcinoma bladder cancer. Although there was no significant relationship between smoking shisha and bladder cancer, it was found that it increases the risk of causing squamous cell carcinoma bladder cancer along with the increased intensity of smoking.
The use of different types of tobacco and cigarettes does not eliminate the risk of bladder cancer. Clove cigarette is a type of cigarette that is the highest risk factor for bladder cancer. The use of different types of tobacco, such as cigars and tobacco pipes, is a slightly lower risk factor for bladder cancer compared to clove cigarette. Shisha and electronic cigarettes though very small does not eliminate the risk of bladder cancer.
Financial support and sponsorship
This study was supported by Universitas Padjadjaran Internal Research Grant.
Conflicts of interest
There are no conflicts of interest.
| References|| |
Thuener JE. Urologic Malignancies. Prim Care 2019;46:275-85. doi:10.1016/j.pop.2019.02.009.
Ferlay J, Soerjomataram I, Ervik M, Dikshit R, Eser S, Mathers C, et al
. GLOBOCAN 2012 v1.1, Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 11. Lyon, France: International Agency for Research on Cancer; 2014.
Ebrahimi H, Amini E, Pishgar F, Moghaddam SS, Nabavizadeh B, Rostamabadi Y, et al
. Global, regional and national burden of bladder cancer, 1990 to 2016: Results from the GBD study 2016. J Urol 2019;201:893-901.
Umbas R, Hardjowijoto S, Mochtar CA, Safriadi F, Djatisoesanto W, Oka AAG, et al
. Panduan Penanganan Kanker Kandung Kemih Tipe Urotelial. Ikatan Ahli Urologi Indonesia; 2014.
Zeegers MP, Kellen E, Buntinx F, van den Brandt PA. The association between smoking, beverage consumption, diet and bladder cancer: A systematic literature review. World J Urol 2004;21:392-401.
Chang SS, Boorjian SA, Chou R, Clark PE, Daneshmand S, Konety BR, et al
. Diagnosis and treatment of non-muscle invasive bladder cancer: AUA/SUO Guideline. J Urol 2016;196:1021-9.
Freedman ND, Silverman DT, Hollenbeck AR, Schatzkin A, Abnet CC. Association between smoking and risk of bladder cancer among men and women. J Am Med Assoc 2011;306:737-45.
Westhoff E, Maria de Oliveira-Neumayer J, Aben KK, Vrieling A, Kiemeney LA. Low awareness of risk factors among bladder cancer survivors: New evidence and a literature overview. Eur J Cancer 2016;60:136-45.
Gandomani HS, Tarazoj AA, Siri FH, Karimirozveh A, Hosseini S, Borujeni NN, et al
. Essentials of bladder cancer worldwide: Incidence, mortality rate and risk factors. Biomed Res Ther 2017;4:1638-55.
Heney NM, Ahmed S, Flanagan MJ, Frable W, Corder MP, Hafermann MD, et al
. Superficial bladder cancer: Progression and recurrence. J Urol 1983;130:1083-6.
Wolpert BJ, Amr S, Ezzat S, Saleh DA, Gouda I, Loay I, et al
. Estrogen exposure and bladder cancer risk in Egyptian women. Maturitas 2010;67:353-7.
Jiang X, Castelao JE, Yuan JM, Stern MC, Conti DV, Cortessis VK, et al
. Cigarette smoking and subtypes of bladder cancer. Int J Cancer 2012;130:896-901.
Zheng YL, Amr S, Doa'a AS, Dash C, Ezzat S, Mikhail NN, et al
. Urinary bladder cancer risk factors in Egypt: A multicenter case–control study. Cancer Epidemiol Prev Biomark 2012;21:537-46.
Bassett JC, Gore JL, Chi AC, Kwan L, McCarthy W, Chamie K, et al
. Impact of a bladder cancer diagnosis on smoking behavior. J Clin Oncol 2012;30:1871-8.
Laaksonen MA, MacInnis RJ, Canfell K, Giles GG, Hull P, Shaw JE, et al
. The future burden of kidney and bladder cancers preventable by behavior modification in Australia: A pooled cohort study. Int J Cancer 2020;146:874-83.
Lukas C, Selinski S, Prager HM, Blaszkewicz M, Hengstler JG, Golka K. Occupational bladder cancer: Polymorphisms of xenobiotic metabolizing enzymes, exposures, and prognosis. J Toxicol Environ Health A 2017;80:439-52.
Sun X, Hoadley KA, Kim WY, Furberg H, Olshan AF, Troester MA. Age at diagnosis, obesity, smoking, and molecular subtypes in muscle-invasive bladder cancer. Cancer Causes Control 2017;28:539-44.
Andrew AS, Mason RA, Kelsey KT, Schned AR, Marsit CJ, Nelson HH, et al
. DNA repair genotype interacts with arsenic exposure to increase bladder cancer risk. Toxicol Lett 2009;187:10-4.
Malhotra J, Borron C, Freedman ND, Abnet CC, Van Den Brandt PA, White E, et al
. Association between cigar or pipe smoking and cancer risk in men: A pooled analysis of five Cohort studies. Cancer Prev Res 2017;10:704-9.
Cumberbatch MG, Rota M, Catto JW, La Vecchia C. The role of tobacco smoke in bladder and kidney carcinogenesis: A comparison of exposures and meta-analysis of incidence and mortality risks. Eur Urol 2016;70:458-66.
McCormack VA, Agudo A, Dahm CC, Overvad K, Olsen A, Tjonneland A, et al
. Cigar and pipe smoking and cancer risk in the European Prospective Investigation into Cancer and Nutrition (EPIC). Int J Cancer 2010;127:2402-11.
Fuller TW, Acharya AP, Meyyappan T, Yu M, Bhaskar G, Little SR, et al
. Comparison of bladder carcinogens in the urine of e-cigarette users versus non e-cigarette using controls. Sci Rep 2018;8:507.
Letašiová S, Medve'ová A, Šovčíková A, Dušinská M, Volkovová K, Mosoiu C, et al
. Bladder cancer, a review of the environmental risk factors. Environ Health 2012;11 Suppl 1:S11.
Wu XR. Urothelial tumorigenesis: A tale of divergent pathways. Nat Rev Cancer 2005;5:713-25.
Zhao M, He XL, Teng XD. Understanding the molecular pathogenesis and prognostics of bladder cancer: An overview. Chin J Cancer Res 2016;28:92-8.
Audenet F, Attalla K, Sfakianos JP. The evolution of bladder cancer genomics: what have we learned and how can we use it? Urol Oncol 2018;36:313-20.
Cancer Genome Atlas Research Network. Comprehensive molecular characterization of urothelial bladder carcinoma. Nature 2014;507:315-22.
Foth M, Ahmad I, van Rhijn BW, van der Kwast T, Bergman AM, King L, et al
. Fibroblast growth factor receptor 3 activation plays a causative role in urothelial cancer pathogenesis in cooperation with Pten loss in mice. J Pathol 2014;233:148-58.
Waziry R, Jawad M, Ballout RA, Al Akel M, Akl EA. The effects of waterpipe tobacco smoking on health outcomes: An updated systematic review and meta-analysis. Int J Epidemiol 2017;46:32-43.
El-Setouhy M, Loffredo CA, Radwan G, Abdel RR, Mahfouz E, Israel E, et al
. Enotoxic effects of waterpipe smoking on the buccal mucosa cells. Mutat Res 2008;655:36-40.
Awan KH, Siddiqi K, Patil Sh, Hussain QA. Assessing the effect of waterpipe smoking on cancer outcome – A systematic review of current evidence. Asian Pac J Cancer Prev 2017;18:495-502.
Bourke L, Bauld L, Bullen C, Cumberbatch M, Giovannucci E, Islami F, et al
. E-cigarettes and urologic health: A collaborative review of toxicology, epidemiology, and potential risks. Eur Urol 2017;71:915-23.
Silverman DT, Devesa SS, Moore LE, Rothman N. Bladder cancer. In: Schottenfeld D, Fraumeni JF Jr., editors. Cancer Epidemiology and Prevention. 3rd
ed. New York, NY: Oxford University Press; 2006.
Yuge K, Kikuchi E, Hagiwara M, Asumizu Y, Tanaka N, Kosaka T, et al
. Nicotine induces tumor growth and chemoresistance through activation of the PI3K/Akt/mTOR pathway in bladder cancer. Mol Cancer Ther 2015;14:2112-20.
Yu V, Rahimy M, Korrapati A, Xuan Y, Zou AE, Krishnan AR, et al
. Electronic cigarettes induce DNA strand breaks and cell death independently of nicotine in cell lines. Oral Oncol 2016;52:58-65.
[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2], [Table 3], [Table 4]