Abstract
Introduction:
Research suggests that smokers of slim, long, or ultralong cigarettes may have a perception of reduced harm from their own brand. This study compared serum cotinine and urinary total 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanonol (NNAL) levels among smokers of regular-sized (68–72mm), king-sized (79–88mm), and long (94–101mm) or ultralong (110–121mm) cigarettes.
Methods:
Nationally representative data from the 2007–2008 and 2009–2010 National Health and Nutrition Examination Survey were analyzed for 3,699 current smokers aged ≥20 years. Biomarker levels were summarized using geometric means (GMs). Multivariate linear regression analyses were performed to assess the effect of cigarette rod length on log-transformed serum cotinine and creatinine-adjusted urinary total NNAL levels.
Results:
The GM of serum cotinine level was higher among smokers of long/ultralong cigarettes (263.15ng/ml) compared with smokers of regular-sized (173.13ng/ml) or king-sized (213.79ng/ml) cigarettes. Similarly, the GM of creatinine-adjusted NNAL levels was higher among smokers of long/ultralong cigarettes (0.48ng NNAL/mg of creatinine) compared with smokers of regular-sized (0.34ng NNAL/mg of creatinine) or king-sized (0.33ng NNAL/mg of creatinine) cigarettes. After adjusting for potential confounders, mean cotinine and NNAL levels were both significantly higher among smokers of long/ultralong cigarettes compared with levels observed in smokers of either regular-sized or king-sized cigarettes. However, no significant differences were observed between smokers of regular-sized and king-sized cigarettes in mean levels of cotinine or NNAL.
Conclusions:
Significantly elevated tobacco biomarker levels were observed among smokers of long/ultralong cigarettes compared with smokers of regular-sized or king-sized cigarettes. This underscores the need to educate the public about the dangers of all tobacco products.
INTRODUCTION
Cigarette design and engineering have evolved over the last several decades to keep up with changing social, psychological, health, and political climates. Apart from design features such as modifications of tobacco blend, filter, and vents, which were made to modify the quality and/or quantity of smoke yielded from the cigarette, the tobacco industry has also introduced other design features tailored to appeal to certain population niches. These include modifications in tipping color, packaging, flavoring, circumference, and changes in cigarette rod length (Bansal-Travers, Hammond, Smith, & Cummings, 2011; Carpenter, Wayne, & Connolly, 2005; Carpenter, Wayne, Pauly, Koh, & Connolly, 2005; Cook, Wayne, Keithly, & Connolly, 2003).
Within the United States, cigarette brands are sold in various cigarette rod length categories, namely regular-sized (68–72mm), king-sized (79–88mm), long (94–101mm), and ultralong (110–121mm) cigarettes (FTC, 2012). Several studies have assessed the effect of various physical attributes of cigarettes, such as vents, filters, menthol, and smoke yield on cotinine and tobacco-specific nitrosamines (Hecht et al., 2005; Jones, Apelberg, Tellez-Plaza, Samet, & Navas-Acien, 2013; Joseph et al., 2005; Melikian, Djordjevic, Chen, Richie, & Stellman, 2007; Sarkar, Wang, & Liang, 2012). However, to date, no study has assessed the effect of cigarette rod length on tobacco biomarker levels. This is important because design features such as length and circumference of cigarettes may influence perception of harm by smokers. A recent study showed that longer length cigarettes were often perceived by smokers to be attractive and of high quality. (Borland & Savvas, 2013).
Therefore, to fill this gap in knowledge, this study compared serum cotinine and urinary total 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanonol (NNAL) levels among smokers of regular-sized, king-sized, and long/ultralong cigarettes using nationally representative data from the 2007–2008 and 2009–2010 National Health and Nutrition Examination Surveys (NHANES) (CDC, 2007).
METHODS
Data Sources
We merged data from the NHANES 2007–2008 and 2009–2010 waves. NHANES is a household interview and examination survey that uses a complex, multistage probability sampling design to select participants from the noninstitutionalized U.S. population. Overall interview response rates were 78.4% (2007–2008) and 79.4% (2009–2010). Our analyses were restricted to respondents who were above 18 years old, were current smokers, and had provided information on the outcomes of interest, that is, length of cigarette currently smoked. Thus, our final analytic sample included 3,699 smokers aged ≥20 years.
Measures
All respondents who at the time of the survey reported smoking cigarettes everyday or on some days (including the past 5 days) were considered current smokers. Among smokers, the length of the cigarette currently smoked was asked. Categorical responses were “Regular (68–72mm)” (n = 588), “King (79–88mm)” (n = 1,855), “Long (94–101mm)” (n = 1214), or “Ultralong (110–121mm)” (n = 42). Within the analysis and throughout the article, long and ultralong cigarettes were merged into one category. Smokers were also asked the number of days in which they smoked during the past 30 days and the smoking intensity on the days they smoked (as measured by the number of cigarettes smoked per day or CPD). In addition, smokers were asked to indicate the time from awakening to taking their first cigarette.
Other covariates assessed included the following: age (18–24, 25–44, 45–64, and ≥65 years); gender (male or female); race/ethnicity (non-Hispanic White, non-Hispanic Black, Hispanic, or other race, including multiracial); educational attainment (<12 years, =12 years/General Educational Development Certificate, or >12 years); Poverty index ratio (<federal poverty level or ≥poverty level); body mass index (underweight: <18.5, normal weight: 18.5–24.9, overweight: 25–29.9, and obese: ≥30); presence of any smoker in household as proxy for secondhand smoke exposure (≥1 smoker vs. none); marital status (married or living with partner, widowed, divorced or separated, or never married), and tobacco use pattern (cigarette-only smokers vs. cigarette plus use of any other tobacco product such as pipes, cigars, snuff, or chewing tobacco products).
Serum Cotinine–Urinary Total NNAL
Serum cotinine, a major metabolite of nicotine and a valid marker for tobacco use (Benowitz, 1996), was measured by isotope dilution–high-performance liquid chromatography/atmospheric pressure chemical ionization tandem mass spectrometry (ID HPLC-APCI MS/MS).
NNAL, a metabolite of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanone and major component of tobacco and tobacco smoke (Hou et al., 2012), was measured by using liquid chromatography linked to tandem mass spectrometry (LC/MS/MS). Because urinary total NNAL was assayed with random urine samples and not 24-hr samples, correction for variability in urine output was made by adjusting urinary NNAL concentrations based on urinary creatinine levels (expressed as nanograms of urinary total NNAL per milligram of creatinine).
Statistical Methods
Tobacco use characteristics among smokers were assessed by cigarette rod length, including CPD, average number of cigarettes smoked in the past 30 days (product of CPD and average number of days in which respondent smoked cigarettes in the past 30 days), and level of nicotine dependence. Nicotine dependence was measured using the Heaviness of Smoking Index, a 6-point scale calculated from the number of cigarettes smoked per day (1–10, 11–20, 21–30, and >30 cigarettes) and the time to first cigarette after waking (≤5, 6–30, 31–60, and >60min) (Heatherton, Kozlowski, Frecker, Rickert, & Robinson, 1989). Scores of 0–1 were categorized as low nicotine dependence, 2–4 as moderate nicotine dependence, and 5–6 as high nicotine dependence.
Serum cotinine and urinary NNAL concentrations are presented using geometric means (GM) with 95% confidence intervals (95% CI) because of the skewness of the data. To assess the effect of cigarette rod length on cotinine and NNAL concentrations of smokers, multivariate linear regression models were fitted adjusting for age, sex, race/ethnicity, educational level, poverty index ratio, body mass index, presence of smoker in household, marital status, tobacco use pattern, and CPD. In the regression analyses, cotinine and NNAL were transformed to the natural log scale to assume a normal distribution. Results of the regression analysis are presented as unadjusted and adjusted β coefficients. The level of statistical significance was set at p < .05. All analysis were weighted and performed with STATA 11.0 (StataCorp., 2009).
RESULTS
Population Characteristics
Smokers of king-sized cigarettes represented slightly more than half (53.0%) of the overall smoker population, whereas smokers of long/ultralong cigarettes and regular-sized cigarettes constituted 31.5% and 15.4% of the smoker population, respectively. The distribution of the study population by selected sociodemographic characteristics and cigarette rod length is detailed in Table 1. A higher percentage of smokers in the ≤24 and 25–44 age groups were smokers of king-sized cigarettes (63.5% and 57.8%, respectively), with long/ultralong cigarettes used by 55% of the older respondents (≥65 years). Moreover, a higher percentage of females were smokers of long/ultralong cigarettes in comparison to males (40.8% vs. 23.4%, respectively, p < .001).
Table 1.
Distribution of Sociodemographic Characteristics of Smokers by Rod Length of the Cigarette Currently Smoked, NHANES 2007–2010 (N = 3,699)
| Characteristics | Number, n | Regular-sized cigarettes (68–72mm) | King-sized cigarettes (79–88mm) | Long (94–101mm)/ ultralong (110–121mm) cigarettes | p Value |
|---|---|---|---|---|---|
| % (n) | % (n) | % (n) | |||
| Age, years | |||||
| ≤24 | 403 | 18.8 | 63.5 | 17.6 | <.001 |
| 25–44 | 1,573 | 18.3 | 57.8 | 24.0 | |
| 45–64 | 1,334 | 11.8 | 46.2 | 42.0 | |
| ≥65 | 389 | 8.7 | 36.27 | 55.0 | |
| Sex | |||||
| Male | 2,020 | 18.9 | 57.7 | 23.4 | <.001 |
| Female | 1,679 | 11.6 | 47.6 | 40.8 | |
| Race/ethnicity | |||||
| White, non-Hispanic | 1,843 | 14.3 | 55.1 | 30.6 | <.001 |
| Black, non-Hispanic | 849 | 2.9 | 54.7 | 42.4 | |
| Hispanic | 846 | 34.5 | 43.0 | 22.4 | |
| Other race, non-Hispanic | 161 | 20.4 | 45.2 | 34.4 | |
| Education level | |||||
| <12 years | 1,375 | 17.9 | 47.7 | 34.4 | .110 |
| =12 years/General Educational Development Certificate | 1,091 | 14.6 | 54.9 | 30.4 | |
| >12 years | 1,231 | 14.2 | 55.5 | 30.3 | |
| Poverty index ratio | |||||
| Below federal poverty level | 1,141 | 16.7 | 47.4 | 35.9 | .096 |
| At or above federal poverty level | 2,208 | 14.4 | 55.0 | 30.7 | |
| Body mass index | |||||
| Underweight: <18.5 | 123 | 10.3 | 48.2 | 41.5 | .215 |
| Normal weight: 18.5–24.9 | 1,225 | 13.5 | 56.2 | 30.3 | |
| Overweight: 25–29.9 | 1,176 | 16.9 | 54.6 | 28.5 | |
| Obese: ≥30 | 1,140 | 16.6 | 48.1 | 35.3 | |
| Presence of smoker in household | |||||
| Yes | 2,104 | 11.0 | 48.4 | 40.5 | <.001 |
| No | 1,576 | 20.8 | 59.0 | 20.2 | |
| Marital status | |||||
| Married/Living with partner | 1,930 | 18.1 | 50.6 | 31.3 | .003 |
| Widowed/divorced/separated | 948 | 11.3 | 50.6 | 38.1 | |
| Never married | 818 | 13.0 | 61.3 | 25.7 | |
| Tobacco use patterns | |||||
| Cigarettes only | 3,597 | 14.9 | 53.1 | 31.9 | .024 |
| Cigarettes combined with any other tobacco product | 102 | 31.8 | 48.9 | 19.3 | |
| Cigarette smoked per day | |||||
| 1–10 | 2,138 | 18.2 | 54.4 | 27.4 | .080 |
| 11–20 | 1,162 | 12.4 | 51.9 | 35.7 | |
| 21–30 | 207 | 11.3 | 53.2 | 35.5 | |
| >30 | 165 | 10.3 | 48.8 | 40.9 | |
| Overall | 3,699 | 15.4 (588) | 53.0 (1,855) | 31.5 (1,256) | |
Note. All data were weighted to account for the complex survey design.
Tobacco Use Characteristics by Cigarette Rod Length
The proportion of low-nicotine-dependent smokers was lower among smokers of long/ultralong cigarettes (38.7%) compared with smokers of regular-sized (55.0%) or king-sized cigarettes, whereas a higher proportion of long/ultralong cigarette smokers had moderate or high nicotine dependence compared with either regular-sized or king-sized cigarette smokers (Table 2). Similarly, the proportion of daily smokers was significantly higher among long/ultralong cigarette smokers (92.1%) compared with smokers of regular-sized (72.7%) or king-sized (84.6%) cigarettes (Table 2).
Table 2.
Tobacco Use Characteristics by Cigarette Rod Length Among Adults Aged ≥20 Years, NHANES 2007–2010 (N = 3,699)
| Characteristics | Regular-sized cigarettes (68–72mm), n = 588 | King-sized cigarettes (79–88mm), n = 1,855 | Long (94–101mm) or ultralong cigarettes (110–121mm), n = 1,256 |
|---|---|---|---|
| Heaviness of smoking indexa, % (95% CI) | |||
| Low | 55.0 (42.6–67.5) | 49.9 (44.6–55.3) | 38.7 (34.4–42.9) |
| Moderate | 36.7 (26.6–46.8) | 41.2 (36.4–46.0) | 48.7 (43.9–53.4) |
| High | 8.3 (3.3–13.2) | 8.9 (5.7–12.0) | 12.7 (9.6–15.8) |
| Smoking frequency, % (95% CI) | |||
| Some days | 27.3 (19.6–35.0) | 15.4 (11.8–18.9) | 7.9 (5.0–10.7) |
| Daily | 72.7 (65.0–80.5) | 84.6 (81.1–88.2) | 92.1 (89.3–95.0) |
| Average number of cigarettes smoked per day | |||
| Mean (SD) | 11.4 (9.6) | 13.7 (10.8) | 15.4 (10.9) |
| Median (range) | 10.0 (1.0–50.0) | 10.0 (1.0–95.0) | 15.0 (1.0–95.0) |
| Average number of cigarettes smoked in the past 30 daysb | |||
| Mean (SD) | 314.8 (300.9) | 395.2 (333.5) | 452.7 (330.8) |
| Median (range) | 240.0 (1.0–1500.0) | 300.0 (1.0–2850.0) | 390.0 (1.0–2850.0) |
| Proportion of smokers concurrently using other non-cigarette tobacco productsc, % (95% CI) | 6.0 (3.1–9.0) | 2.7 (1.3–4.1) | 1.8 (0.8–2.8) |
Note. All data were weighted to account for the complex survey design. CI = confidence interval.
aA 6-point scale calculated from the number of cigarettes smoked per day (1–10, 11–20, 21–30, and >30 cigarettes) and the time to first cigarette after waking (≤5, 6–30, 31–60, and >60min). Scores of 0–1 are categorized as “low nicotine dependence,” 2–4 as “moderate,” and 5–6 as “high.”
bCalculated by multiplying the average number of cigarettes smoked per day by the self-reported number of days in which the respondent smoked cigarettes in the past 30 days.
cIncluding cigars, pipes, snuff, or chewing tobacco.
The mean CPD among long/ultralong cigarette smokers (15.4) was significantly higher compared with that among smokers of regular-sized (11.4) or king-sized cigarettes (13.7) (p < .05 for both). Similarly, the average number of cigarettes smoked in the past 30 days among long/ultralong cigarette smokers (452.7) was significantly higher compared with the number among smokers of regular-sized (314.8) or king-sized (395.2) cigarettes (p < .05 for both).
Cotinine/NNAL Associations With Cigarette Rod Length
Within the bivariate analyses, serum cotinine concentrations were higher among smokers of long/ultralong cigarettes (GM: 263.15ng/ml) compared with smokers of either regular-sized (GM: 173.13ng/ml) or king-sized (GM: 213.79ng/ml) cigarettes. Similarly, creatinine-adjusted urinary NNAL concentrations were higher among smokers of long/ultralong cigarettes (0.48ng NNAL/mg of creatinine) compared with those who smoked regular-sized (0.34 NNAL/mg of creatinine) or king-sized (0.33ng NNAL/mg of creatinine) cigarettes (Table 3). After adjusting for potential confounders within the linear regression analyses, serum cotinine concentrations were significantly elevated among smokers of long/ultralong cigarettes compared with levels observed in smokers of regular-sized (β = 0.60, p = .003) or king-sized cigarettes (β = 0.25; p < .001). Similarly, creatinine-adjusted urinary NNAL levels were significantly higher among smokers of long/ultralong cigarettes compared with levels observed in smokers of either regular-sized (β = 0.38, p = .006) or king-sized cigarettes (β = 0.26; p = .001) (Table 3). No significant differences in serum cotinine or urinary NNAL concentrations were noted between smokers of regular-sized and king-sized cigarettes.
Table 3.
Serum Cotinine and Urinary Total NNAL by Cigarette Rod Length and Other Selected Characteristics Among Adults Aged ≥20 Years, NHANES 2007–2010 (N = 3,699)
| Characteristics | Serum cotinine (ng/ml), geometric mean (95% CI) | Unadjusted urinary total NNAL (ng/ml), geometric mean (95% CI) | Creatinine-adjusted urinary total NNAL (ng NNAL/mg of creatinine), geometric mean (95% CI) |
|---|---|---|---|
| Cigarette length | |||
| Regular-sized cigarettes (68–72mm) | 173.13 (133.92–212.35) | 0.39 (0.26–0.51) | 0.34 (0.26–0.42) |
| King-sized cigarettes (79–88mm) | 213.79 (200.19–227.38) | 0.38 (0.33–0.42) | 0.33 (0.29–0.38) |
| Long (94–101mm) or ultralong (110–121mm) cigarettes | 263.15 (248.16–278.14) | 0.46 (0.42–0.5) | 0.48 (0.42–0.53) |
| Age, years | |||
| ≤24 | 171.93 (147.06–196.8) | 0.32 (0.24–0.39) | 0.23 (0.18–0.29) |
| 25–44 | 202.80 (182.58–223.02) | 0.41 (0.35–0.46) | 0.33 (0.28–0.38) |
| 45–64 | 269.05 (251.62–286.47) | 0.43 (0.39–0.47) | 0.48 (0.43–0.52) |
| ≥65 | 218.52 (197.01–240.02) | 0.40 (0.33–0.47) | 0.48 (0.38–0.58) |
| Sex | |||
| Male | 224.31 (206.16–242.45) | 0.42 (0.37–0.46) | 0.34 (0.3–0.38) |
| Female | 221.63 (205.53–237.73) | 0.39 (0.35–0.43) | 0.43 (0.38–0.48) |
| Race/ethnicity | |||
| White, non-Hispanic | 237.07 (222.49–251.65) | 0.45 (0.41–0.49) | 0.45 (0.4–0.5) |
| Black, non-Hispanic | 262.43 (244.87–280.00) | 0.35 (0.32–0.38) | 0.24 (0.22–0.27) |
| Hispanic | 118.90 (104.10–133.70) | 0.25 (0.22–0.29) | 0.20 (0.18–0.23) |
| Other race, non-Hispanic | 191.25 (157.43–225.07) | 0.32 (0.22–0.41) | 0.29 (0.2–0.37) |
| Education level | |||
| <12 years | 237.20 (215.79–258.57) | 0.46 (0.40–0.52) | 0.43 (0.37–0.50) |
| =12 years/GED | 232.31 (214.73–249.89) | 0.41 (0.35–0.47) | 0.38 (0.33–0.43) |
| >12 years | 205.12 (186.94–223.30) | 0.36 (0.31–0.41) | 0.34 (0.30–0.38) |
| Poverty index ratio | |||
| Below federal poverty level | 226.45 (200.51–252.39) | 0.45 (0.39–0.52) | 0.40 (0.34–0.45) |
| At or above federal poverty level | 224.26 (210.01–238.51) | 0.40 (0.36–0.43) | 0.38 (0.34–0.42) |
| Body mass index | |||
| Underweight: <18.5 | 300.56 (241.78–359.34) | 0.53 (0.38–0.68) | 0.53 (0.43–0.63) |
| Normal weight: 18.5–24.9 | 243.49 (223.69–263.29) | 0.39 (0.34–0.44) | 0.41 (0.35–0.46) |
| Overweight: 25–29.9 | 218.42 (204.11–232.72) | 0.38 (0.33–0.43) | 0.37 (0.32–0.41) |
| Obese: ≥30 | 194.48 (174.08–214.89) | 0.43 (0.35–0.51) | 0.34 (0.28–0.4) |
| Presence of smoker in household | |||
| Yes | 266.26 (252.42–280.1) | 0.49 (0.44–0.54) | 0.47 (0.41–0.52) |
| No | 169.38 (156.7–182.07) | 0.30 (0.27–0.33) | 0.27 (0.25–0.3) |
| Marital status | |||
| Married/living with partner | 223.65 (204.83–242.47) | 0.42 (0.37–0.47) | 0.39 (0.33–0.44) |
| Widowed/divorced/separated | 253.96 (234.41–273.52) | 0.44 (0.39–0.49) | 0.47 (0.42–0.52) |
| Never married | 189.86 (172.17–207.54) | 0.32 (0.27–0.37) | 0.27 (0.22–0.32) |
| Tobacco use patterns | |||
| Cigarettes only | 223.46 (208.81–238.12) | 0.39 (0.36–0.43) | 0.37 (0.33–0.42) |
| Cigarettes combined with any other tobacco producta | 211.15 (144.37–277.94) | 0.81 (0.4–1.22) | 0.51 (0.33–0.7) |
| Cigarettes smoked per day | |||
| 1–10 | 167.80 (154.30–181.20) | 0.29 (0.26–0.33) | 0.26 (0.22–0.30) |
| 11–20 | 274.80 (260.20–289.30) | 0.50 (0.46–0.53) | 0.47 (0.43–0.51) |
| 21–30 | 326.40 (296.50–356.30) | 0.57 (0.51–0.64) | 0.58 (0.52–0.64) |
| >30 | 318.50 (296.10–341.00) | 0.73 (0.58–0.88) | 0.73 (0.63–0.82) |
Note. All data were weighted to account for the complex survey design. CI = confidence interval
aIncluding cigars, pipes, snuff, or chewing tobacco.
Cotinine/NNAL Association With Dual Smokeless and Combustible Tobacco Use
Sensitivity analyses were performed to assess the relationship between tobacco biomarker levels and tobacco use patterns. Serum cotinine concentrations were higher among respondents who reported combined use of cigarette plus snuff or chewing tobacco (n = 40; GM = 279.2) compared with exclusive cigarette smokers (n = 3,597; GM = 223.46) or those who smoked cigarettes concurrently with cigars or pipes (n = 60; GM = 157.57). Similar results were observed for creatinine-adjusted NNAL levels among combined users of snuff or chewing tobacco plus cigarettes versus exclusive cigarette smokers versus concurrent smokers of cigarettes and cigars or pipes (0.75ng vs. 0.38 vs. 0.34ng NNAL/mg creatinine, respectively). After adjusting for potential confounders, average NNAL levels were significantly higher (p = .003) among combined cigarette plus snuff or chewing tobacco compared with exclusive cigarette smokers, whereas no significant differences were observed in mean cotinine levels between these groups.
Finally, although not a direct aim of our research, stratifying the analysis by sociodemographic characteristics indicated variations in measured cotinine and NNAL concentrations, with the later found to be higher among those older, White-non Hispanic, of lower educational status, and below the federal poverty level (Tables 3 and 4).
Table 4.
Linear Regression Analyses Assessing the Effect of Cigarette Rod Length on Cotinine and NNAL Concentrations Among Adults Aged ≥20 Years, NHANES 2007–2010 (N = 3,699)
| Characteristics | Cotinine, ng/ml (natural log) | Creatinine-adjusted NNAL, ng NNAL/mg of creatinine (natural log) | |||||||
|---|---|---|---|---|---|---|---|---|---|
| Crude coefficient | p Value | Adjusted coefficienta | p Value | Crude coefficient | p Value | Adjusted coefficienta | p Value | ||
| Cigarette length | Regular-sized (68–72mm) | Referent | |||||||
| King-sized (79–88mm) | 0.74 | .007 | 0.36 | .110 | 0.34 | .087 | 0.12 | .405 | |
| Long (94–101mm)/ultralong (110–121mm) | 1.21 | <.001 | 0.60 | .003 | 0.88 | <.001 | 0.38 | .006 | |
| Age, years | <24 | Referent | |||||||
| 25–44 | 0.16 | .171 | 0.02 | .866 | 0.33 | .010 | 0.20 | .086 | |
| 45–64 | 0.82 | <.001 | 0.32 | .019 | 1.03 | <.001 | 0.56 | <.001 | |
| ≥65 | 0.56 | <.001 | −0.05 | .692 | 0.91 | <.001 | 0.33 | .049 | |
| Sex | Male | Referent | |||||||
| Female | 0.02 | .827 | −0.12 | .066 | 0.35 | <.001 | 0.29 | <.001 | |
| Race/ Ethnicity | White, non-Hispanic | Referent | |||||||
| Black, non-Hispanic | 0.14 | .234 | 0.26 | .031 | −0.57 | <.001 | −0.41 | <.001 | |
| Hispanic | −1.44 | <.001 | −0.83 | <.001 | −1.22 | <.001 | −0.62 | <.001 | |
| Other race, non-Hispanic | −0.47 | .023 | −0.19 | .307 | −0.76 | .001 | −0.51 | .012 | |
| Education level | <12 years | Referent | |||||||
| =12 years | −0.02 | .873 | −0.05 | .563 | −0.05 | .636 | −0.03 | .658 | |
| >12 years | −0.30 | .020 | −0.19 | .076 | −0.34 | .006 | −0.24 | .012 | |
| Poverty index ratio | Below federal poverty level | Referent | |||||||
| At or above federal poverty level | −0.06 | .600 | −0.08 | .250 | −0.09 | .287 | −0.10 | .053 | |
| Body mass index | Underweight: <18.5 | Referent | |||||||
| Normal weight: 18.5–24.9 | −0.33 | .059 | −0.12 | .403 | −0.49 | .006 | −0.21 | .096 | |
| Overweight: 25–29.9 | −0.66 | .001 | −0.32 | .019 | −0.66 | .001 | −0.31 | .016 | |
| Obese: ≥30 | −0.77 | <.001 | −0.49 | .002 | −0.75 | <.001 | −0.44 | .004 | |
| Smoker in household | Yes | Referent | |||||||
| No | −0.99 | <.001 | −0.45 | <.001 | −0.92 | <.001 | −0.40 | <.001 | |
| Marital status | Married/living with partner | Referent | |||||||
| Widowed/divorced/separated | 0.36 | .006 | 0.15 | .071 | 0.40 | .001 | 0.12 | .090 | |
| Never married | −0.23 | .047 | −0.13 | .225 | −0.43 | <.001 | −0.19 | .041 | |
| Tobacco use patterns | Cigarettes only | Referent | |||||||
| Combined use with other tobaccob | −0.41 | .305 | −0.19 | .589 | 0.14 | .530 | 0.55 | .002 | |
| Cigarettes per day | 1–10 | Referent | |||||||
| 11–20 | 1.04 | <.001 | 0.74 | <.001 | 1.07 | <.001 | 0.74 | <.001 | |
| 21–30 | 1.25 | <.001 | 0.83 | <.001 | 1.35 | <.001 | 0.88 | <.001 | |
| >30 | 1.27 | <.001 | 0.69 | <.001 | 1.54 | <.001 | 0.99 | <.001 | |
Note. All data were weighted to account for the complex survey design.
aThe multivariate regression analyses had adjusted R 2 values of 24.6% (cotinine) and 33.0% (creatinine-adjusted NNAL) after adjusting for all factors listed in table.
bIncluding cigars, pipes, snuff, or chewing tobacco.
DISCUSSION
Analysis of the merged 2007–2010 NHANES datasets indicated that smokers of long/ultralong cigarettes had significantly higher levels of serum cotinine and urinary NNAL compared with smokers of either regular-sized or king-sized cigarettes. Several factors may account for these findings. First, the higher tobacco content in long/ultralong cigarettes—approximately 18% higher than king-sized cigarettes (American Tobacco, 1967)—may be associated with a correspondingly higher exposure to tobacco smoke under the assumption that the entire cigarette is smoked. Thus, smokers of long/ultralong cigarettes may be exposed to more nicotine and tobacco carcinogens, which may explain the higher levels of cotinine and NNAL observed in our study.
Research has also suggested that longer cigarette may be associated with a higher puff volume, which may result in the potential to inhale more smoke with increased exposure to many harmful constituents (Nemeth-Coslett & Griffiths, 1985). Nicotine boost has been shown to increase with higher puff volumes (Zacny, Stitzer, Brown, Yingling, & Griffiths, 1987), and this may account for the higher biomarker levels among smokers of long/ultralong cigarettes. Moreover, the more intense smoking behavior observed among smokers of long/ultralong cigarettes in our study may also contribute to higher exposure to tobacco smoke and increased levels of tobacco biomarkers including cotinine and NNAL (Joseph et al., 2005; Williams et al., 2011).
The fact that combined users of cigarettes plus smokeless tobacco products had significantly higher levels of NNAL compared with exclusive cigarette smokers demonstrates that persons who use multiple tobacco products may be at increased risk of tobacco-related morbidity and mortality. The high levels of NNAL among smokers who concurrently use smokeless tobacco products may be due to the direct swallowing of tobacco-heavy spittle associated with some smokeless tobacco products and the long duration in which habitual smokeless tobacco users put the tobacco products in their mouths (Hecht et al., 2007). Further research is needed to assess these hypotheses.
Variations in NNAL and cotinine levels were observed by several sociodemographic characteristics including race/ethnicity, sex, age, education level, poverty index ratio, body mass index, and presence of smoker in household. These variations may be due to differences in the pattern and duration of tobacco use or other consumption behaviors that were not assessed (Raunio & Rahnasto-Rilla, 2012; Upadhyaya, Carmella, Guengerich, & Hecht, 2000; Wood, Wewers, Groner, & Ahijevych, 2004). Moreover, the higher levels of NNAL and cotinine among respondents who had ≥1 smoker in the household may indicate an increased exposure to tobacco smoke through passive smoking (Bernert et al., 2010; Vardavas et al., 2013).
Our findings underscore the need for intensified efforts to educate the public through mass-media campaigns that all cigarettes, regardless of length, and all tobacco products are harmful. Other evidence-based interventions such as those outlined in the World Health Organization’s MPOWER package may help reduce use of all tobacco products. These interventions include increasing the price of tobacco products, implementing smoke-free laws in workplaces and public places, increasing access to help quitting, and enforcing restrictions on tobacco advertising, promotion, and sponsorship (WHO, 2008). The implementation of these strategies as part of sustained, adequately funded comprehensive tobacco control programs may lower all tobacco use and lead to reduced tobacco-related diseases and death (CDC, 2012).
The strength, and novelty, of this study is the use of a nationally representative dataset to assess the association between cigarette rod length and tobacco-specific carcinogen biomarkers among adult smokers. However, a number of limitations must be noted. First, these analyses did not account for cigarette rod diameter since only a small fraction of cigarettes (mostly ultralong cigarettes) were slim (i.e., 17.1–23.4 mm), whereas the majority were regular width cigarettes (23.5–27.1 mm). A longer, but smaller diameter rod with a longer filter length could yield relatively lower emissions (less tobacco to be consumed) than would be expected otherwise. Second, questionnaires were administered only in English and Spanish, which may have resulted in nonresponse or misresponse among persons who speak other languages. Finally, we limited our analyses to conventional cigarettes and did not include roll-your-own cigarettes or other tobacco products. Further research is needed to confirm the noted associations within case crossover experimental studies.
CONCLUSIONS
Our analyses indicated that smokers of long/ultralong cigarettes had significantly higher levels of serum cotinine and NNAL in comparison to smokers of either regular-sized or king-sized cigarettes. These findings suggest that cigarette rod length, a specific design characteristic, may be directly associated with tobacco-specific carcinogen concentrations among its consumers. This finding indicates the potential of taking cigarette rod length into account by the U.S. Food and Drug Administration under section 904 of the Family Smoking Prevention and Tobacco Control Act as a design characteristic that is directly related to tobacco carcinogen uptake.
FUNDING
National Cancer Institute grants 3R01 CA125224-03s1rev and 2R01 CA087477-09A2 funded the research for this study.
DECLARATION OF INTERESTS
None Declared.
ACKNOWLEDGMENTS
Dr. ITA initiated the reported research while affiliated with the Center for Global Tobacco Control at Harvard University. He is currently affiliated with the Centers for Disease Control and Prevention’s Office on Smoking and Health. The research in this report was completed and submitted outside of the official duties of his current position and does not reflect the official policies or positions of the Centers for Disease Control and Prevention. The National Cancer Institute had no role in the design and conduct of the study; in the collection, analysis, and interpretation of the data; or in the preparation, review, or approval of the manuscript.
REFERENCES
- American Tobacco (1967). Longer-than-king-size cigarette prices increase; equal time for the anti-smokers. Bates 94709 1186 Retrieved from http://legacy.library.ucsf.edu/tid/dsb80 a00/pdf?search=%22longer%20than%20king%20size%20cigarette%20prices%20increase%20equal%20time%20for%20the%20anti%20smokers%22
- Bansal-Travers M., Hammond D., Smith P., Cummings K. M. (2011). The impact of cigarette pack design, descriptors, and warning labels on risk perception in the U.S. American Journal of Preventive Medicine, 40, 674–682.10.1016/ j.amepre.2011.01.021 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Benowitz N. L. (1996). Cotinine as a biomarker of environmental tobacco smoke exposure. Epidemiologic Reviews, 18, 188–204 [DOI] [PubMed] [Google Scholar]
- Bernert J. T., Pirkle J. L., Xia Y., Jain R. B., Ashley D. L., Sampson E. J. (2010). Urine concentrations of a tobacco-specific nitrosamine carcinogen in the U.S. population from secondhand smoke exposure. Cancer Epidemiology, Biomarkers & Prevention: A Publication of the American Association for Cancer Research, Cosponsored by the American Society of Preventive Oncology, 19, 2969–2977.10.1158/1055–9965.EPI-10–0711; 10.1158/1055–9965.EPI-10–0711 [DOI] [PubMed] [Google Scholar]
- Borland R., Savvas S. (2013). Effects of stick design features on perceptions of characteristics of cigarettes. Tobacco Control, 22, 331–337.10.1136/tobaccocontrol-2011–050199 [DOI] [PubMed] [Google Scholar]
- Carpenter C. M., Wayne G. F., Connolly G. N. (2005). Designing cigarettes for women: New findings from the tobacco industry documents. Addiction (Abingdon, England), 100, 837–851.10.1111/j.1360-0443.2005.01072.x [DOI] [PubMed] [Google Scholar]
- Carpenter C. M., Wayne G. F., Pauly J. L., Koh H. K., Connolly G. N. (2005). New cigarette brands with flavors that appeal to youth: Tobacco marketing strategies. Health Affairs (Project Hope), 24, 1601–1610.10.1377/hlthaff.24.6.1601 [DOI] [PubMed] [Google Scholar]
- Centers for Disease Control and Prevention (CDC) (2007). National Center for Health Statistics (NCHS). National Health and Nutrition Examination Survey Data. Hyattsville, MD: U.S. Department of Health and Human Services, Centers for Disease Control and Prevention; Retrieved from www.cdc.gov/nchs/nhanes/nhanes2007-2008/nhanes07_08.htm [Google Scholar]
- Centers for Disease Control and Prevention (CDC) (2012). Current cigarette smoking among adults—United States, 2011. MMWR Morbidity and Mortality Weekly Report, 61, 889–894 [PubMed] [Google Scholar]
- Cook B. L., Wayne G. F., Keithly L., Connolly G. (2003). One size does not fit all: How the tobacco industry has altered cigarette design to target consumer groups with specific psychological and psychosocial needs. Addiction (Abingdon, England), 98, 1547–1561 [DOI] [PubMed] [Google Scholar]
- FTC (2012). Federal Trade Commission Cigarette Report for 2009 and 2010 Retrieved from www.ftc.gov/os/2012/09/120921cigarettereport.pdf
- Heatherton T. F., Kozlowski L. T., Frecker R. C., Rickert W., Robinson J. (1989). Measuring the Heaviness of smoking: Using self-reported time to the first cigarette of the day and number of cigarettes smoked per day. British Journal of Addiction, 84, 791–799 [DOI] [PubMed] [Google Scholar]
- Hecht S. S., Carmella S. G., Murphy S. E., Riley W. T., Le C., Luo X. … Hatsukami D. K. (2007). Similar exposure to a tobacco-specific carcinogen in smokeless tobacco users and cigarette smokers. Cancer Epidemiology, Biomarkers & Prevention: A Publication of the American Association for Cancer Research, Cosponsored by the American Society of Preventive Oncology, 16, 1567–1572.10.1158/1055–9965.EPI-07-0227 [DOI] [PubMed] [Google Scholar]
- Hecht S. S., Murphy S. E., Carmella S. G., Li S., Jensen J., Le C. … Hatsukami D. K. (2005). Similar uptake of lung carcinogens by smokers of regular, light, and ultralight cigarettes. Cancer Epidemiology, Biomarkers & Prevention: A Publication of the American Association for Cancer Research, Cosponsored by the American Society of Preventive Oncology, 14, 693–698.10.1158/1055–9965.EPI-04-0542 [DOI] [PubMed] [Google Scholar]
- Hou H., Zhang X., Tian Y., Tang G., Liu Y., Hu Q. (2012). Development of a method for the determination of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol in urine of nonsmokers and smokers using liquid chromatography/tandem mass spectrometry. Journal of Pharmaceutical and Biomedical Analysis, 63, 17–22.10.1016/j.jpba.2012.01.028; 10.1016/j.jpba.2012.01.028 [DOI] [PubMed] [Google Scholar]
- Jones M. R., Apelberg B. J., Tellez-Plaza M., Samet J. M., Navas-Acien A. (2013). Menthol cigarettes, race/ethnicity, and biomarkers of tobacco use in U.S. adults: the 1999-2010 National Health and Nutrition Examination Survey (NHANES). Cancer Epidemiology, Biomarkers & Prevention: A Publication of the American Association for Cancer Research, Cosponsored by the American Society of Preventive Oncology, 22, 224–232.10.1158/1055–9965.EPI-12–0912; 10.1158/1055–9965.EPI-12–0912 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Joseph A. M., Hecht S. S., Murphy S. E., Carmella S. G., Le C. T., Zhang Y. … Hatsukami D. K. (2005). Relationships between cigarette consumption and biomarkers of tobacco toxin exposure. Cancer Epidemiology, Biomarkers & Prevention: A Publication of the American Association for Cancer Research, Cosponsored by the American Society of Preventive Oncology, 14, 2963–2968.10.1158/1055–9965.EPI-04-0768 [DOI] [PubMed] [Google Scholar]
- Melikian A. A., Djordjevic M. V., Chen S., Richie J., Jr., Stellman S. D. (2007). Effect of delivered dosage of cigarette smoke toxins on the levels of urinary biomarkers of exposure. Cancer Epidemiology, Biomarkers & Prevention: A Publication of the American Association for Cancer Research, Cosponsored by the American Society of Preventive Oncology, 16, 1408–1415.10.1158/1055–9965.EPI-06-1097 [DOI] [PubMed] [Google Scholar]
- Nemeth-Coslett R., Griffiths R. R. (1985). Effects of cigarette rod length on puff volume and carbon monoxide delivery in cigarette smokers. Drug and Alcohol Dependence, 15, 1–13 [DOI] [PubMed] [Google Scholar]
- Raunio H., Rahnasto-Rilla M. (2012). CYP2A6: Genetics, structure, regulation, and function. Drug Metabolism and Drug Interactions, 27, 73–88.10.1515/dmdi-2012-0001; 10.1515/dmdi-2012-0001 [DOI] [PubMed] [Google Scholar]
- Sarkar M., Wang J., Liang Q. (2012). Metabolism of Nicotine and 4-(methylnitrosamino)-l-(3-pyridyl)-lbutanone (NNK) in menthol and non-menthol cigarette smokers. Drug Metabolism Letters, 6, 198–206 [DOI] [PubMed] [Google Scholar]
- Upadhyaya P., Carmella S. G., Guengerich F. P., Hecht S. S. (2000). Formation and metabolism of 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol enantiomers in vitro in mouse, rat and human tissues. Carcinogenesis, 21, 1233–1238 [PubMed] [Google Scholar]
- Vardavas C. I., Fthenou E., Patelarou E., Bagkeris E., Murphy S., Hecht S. S. … Kogevinas M. (2013). Exposure to different sources of second-hand smoke during pregnancy and its effect on urinary cotinine and tobacco-specific nitrosamine (NNAL) concentrations. Tobacco Control, 22, 194–200.10.1136/tobaccocontrol-2011-050144 [DOI] [PubMed] [Google Scholar]
- WHO (2008). WHO report on the global tobacco epidemic, 2008-The MPOWER Package Retrieved from www.who.int/tobacco/mpower/mpower_report_full_2008.pdf
- Williams J. M., Gandhi K. K., Lu S. E., Kumar S., Steinberg M. L., Cottler B., Benowitz N. L. (2011). Shorter interpuff interval is associated with higher nicotine intake in smokers with schizophrenia. Drug and Alcohol Dependence, 118, 313–319.10.1016/j.drugalcdep.2011.04.009; 10.1016/ j.drugalcdep.2011.04.009 [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wood T., Wewers M. E., Groner J., Ahijevych K. (2004). Smoke constituent exposure and smoking topography of adolescent daily cigarette smokers. Nicotine & Tobacco Research: Official Journal of the Society for Research on Nicotine and Tobacco, 6, 853–862 [DOI] [PubMed] [Google Scholar]
- Zacny J. P., Stitzer M. L., Brown F. J., Yingling J. E., Griffiths R. R. (1987). Human cigarette smoking: Effects of puff and inhalation parameters on smoke exposure. The Journal of Pharmacology and Experimental Therapeutics, 240, 554–564 [PubMed] [Google Scholar]