Biomarkers of Exposure among U.S. Cigar Smokers: An Analysis of 1999–2012 National Health and Nutrition Examination Survey (NHANES) Data

Jiping Chen; Anna Kettermann; Brian L. Rostron; Hannah R. Day

doi:10.1158/1055-9965.EPI-14-0849

DOI: 10.1158/1055-9965.EPI-14-0849 Published December 2014

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Figure 1.
Serum cotinine and urinary NNAL concentrations among daily and nondaily cigar and cigarette smokers. Each panel shows geometric mean concentrations and 95% CIs. Cotinine data were available for 1999–2012 NHANES participants. NNAL data were available for 2007–2012 NHANES participants. Serum cotinine concentrations for nondaily smokers (A); serum cotinine concentrations for daily smokers (B); urinary NNAL concentrations for nondaily smokers (C); and urinary NNAL concentrations for daily smokers (D).
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Figure 2.
Unweighted serum cotinine (A) and urinary NNAL (B) concentrations by average number of cigars smoked per day in the past 5 days. Cotinine data were available for 1999–2012 NHANES participants. NNAL data were available for 2007–2012 NHANES participants. Horizontal lines within boxes represent the median values. The bottom and top of the boxes are the 25th and the 75th percentiles. The distance between the top and bottom of the boxes represents the interquatile range (IQR). Top and bottom horizontal bars are the maximum and the minimum values without outliers. Solid circles are the outliers (i.e., biomarker values exceeding 1.5 times the IQR).

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Table 1.

Characteristics of NHANES participants by tobacco use status: United States, 1999–2012

		Nontobacco users^a	Primary cigar smokers^b	Secondary cigar smokers^c	Cigarette-only smokers^d	Dual cigar/cigarette smokers^e
Characteristics	N	(N = 17,711)	(N = 226)	(N = 183)	(N = 7,279)	(N = 123)
Age, y	25,522	45.7 (45.2–46.3)	39.1 (36.8–41.4)	49.4 (47.4–51.5)	41.9 (41.5–42.4)	38.5 (35.7–41.3)
Sex
Male	11,185	39.5 (38.6–40.4)	83.6 (76.8–90.4)	89.9 (83.9–95.9)	53.7 (52.3–55.1)	87.9 (81.2–94.6)
Female	14,337	60.5 (59.6–61.4)	16.4 (9.6–23.2)	10.1 (4.1–16.1)	46.3 (44.9–47.7)	12.1 (5.4–18.8)
Race/ethnicity	25,522
Mexican American	4,975	9.2 (7.8–10.6)	1.9 (0.4–3.5)	1.5 (0.1–2.8)	7.0 (5.7–8.2)	4.6 (0.8–8.4)
Other Hispanic	1,980	6.2 (4.9–7.5)	5.2 (1.3–9.1)	2.7 (0.0–5.3)	5.0 (3.6–6.4)	3.9 (1.5–6.3)
Non-Hispanic white	11,184	65.5 (62.9–68.2)	58.2(49.6–66.9)	83.1 (77.4–88.8)	70.2 (67.2–73.2)	60.0 (49.8–70.2)
Non-Hispanic black	5,665	11.9 (10.4–13.4)	33.7 (26.2–41.3)	8.5 (5.6–11.4)	12.5 (10.9–14.2)	26.8 (17.4–36.2)
Other	1,718	7.1 (6.1–8.1)	0.9 (0.0–2.0)	4.3 (0.6–8.0)	5.3 (4.4–6.3)	4.7 (0.0–10.1)
Education	25,488
Less than high school graduate or equivalent	7,545	16.1 (15.1–17.2)	13.2 (8.1–18.2)	10.6 (5.3–16.0)	27.9 (26.4–29.5)	29.3(20.5–38.0)
High school graduate or equivalent	5,971	21.1 (20.1–22.2)	26.0 (19.6–32.4)	27.7 (19.2–36.2)	31.3 (29.9–32.7)	27.3 (16.3–38.4)
More than high school graduate or equivalent	11,972	62.8 (61.3–64.3)	60.8 (53.9–67.8)	61.7 (53.3–70.0)	40.8 (38.9–42.6)	43.4 (31.8–55.1)
Body mass index (BMI), kg/m²	25,053	28.6 (28.4–28.8)	28.5 (27.5–29.4)	29.2 (28.3–30.0)	27.4 (27.2–27.6)	27.0 (25.8–28.2)
Cigarette smoking history (lifetime)
Age started smoking cigarettes regularly	7,358			17.6 (17.0–18.2)	17.7 (17.5–17.9)	18.0 (16.0–20.0)
Age stopped smoking cigarettes regularly	163			35.6 (33.5–37.8)
Years of cigarette smoking	7,340			18.5 (16.3–20.6)	24.3 (23.9–24.8)	20.5 (17.1–23.8)
Cigarette/cigar smoking history (past 5 days)
Number of days smoked cigarettes	6,413				4.6 (4.6–4.6)	4.3 (3.8–4.7)
Number of cigarettes smoked per day on days smoking cigarettes	6,409				14.8 (14.4–15.3)	10.4 (8.0–12.8)
Number of days smoked cigars	532		2.4 (2.1–2.6)	2.8 (2.5–3.2)		3.2 (2.8–3.6)
Number of cigars smoked per day on days smoking cigars	532		1.5 (1.3–1.7)	2.5 (1.9–3.1)		5.1 (2.9–7.3)

NOTE: Values represent weighted means (95% CI) for continuous variables, or weighted percentage distribution (95% CI) of these variables within tobacco use categories for categorical variables. ANOVA was used to compare study group characteristics for continuous variables and Pearson χ² or Fisher's exact test for categorical variables.

↵^aNontobacco users reported having smoked fewer than 100 cigarettes in their lifetime and not having used tobacco or nicotine products including cigarettes, pipes, cigars, chewing tobacco, snuff, or nicotine patches, nicotine gums, or any product containing nicotine in the past 5 days.
↵^bPrimary cigar smokers reported not having smoked at least 100 cigarettes in their lifetime and having smoked a cigar but not other tobacco or nicotine products in the past 5 days.
↵^cSecondary cigar smokers reported having smoked at least 100 cigarettes in their lifetime but currently not smoking cigarettes at all and reported having smoked a cigar but not other tobacco or nicotine products in the past 5 days.
↵^dCurrent cigarette-only smokers reported having smoked at least 100 cigarettes in their lifetime and currently smoked cigarettes every day or some days, but not having smoked a cigar or other tobacco or nicotine products other than cigarettes in the past 5 days.
↵^eDual cigarette and cigar smokers reported having smoked at least 100 cigarettes in their lifetime and currently smoked cigarettes every day or some days and reported having smoked a cigar but not other tobacco or nicotine products other than cigarettes in the past 5 days.

Table 2.

Geometric mean biomarker concentrations by tobacco use status, NHANES 1999–2012

Biomarkers of exposure	Nontobacco users	Primary cigar smokers	Secondary cigar smokers	Cigarette-only smokers	Dual cigar/cigarette smokers
Serum cotinine, ng/mL
Number of observations	16,990	221	178	7,017	119
Geometric mean (95% CI)	0.045 (0.043–0.048)	6.2 (4.2–9.2)	24.2 (14.9–39.3)	131.4 (123.1–140.1)	102.8 (77.5–136.5)
Urinary NNAL, pg/mg creatinine
Number of observations	8,117	102	78	3,259	77
Geometric mean (95% CI)	1.01 (0.95–1.07)	19.1 (10.6–34.3)	78.6 (40.8–151.7)	215.4 (191.6–242.2)	209.1 (147.1–297.1)
Blood cadmium, μg/L
Number of observations	17,277	222	179	7,097	122
Geometric mean (95% CI)	0.269 (0.264–0.275)	0.276 (0.245–0.311)	0.437 (0.379–0.503)	0.945 (0.921–0.970)	0.742 (0.638–0.863)
Blood lead, μg/dL
Number of observations	17,277	222	179	7,097	122
Geometric mean (95% CI)	1.18 (1.16–1.21)	1.42 (1.29–1.56)	1.91 (1.71–2.13)	1.75 (1.70–1.80)	1.90 (1.66–2.17)
Urinary arsenic, ng/mg creatinine
Number of observations	4,355	66	37	1,716	25
Geometric mean (95% CI)	9.7 (9.2–10.3)	7.3 (4.8–11.1)	11.1 (8.5–14.5)	7.8 (7.1–8.4)	8.4 (5.9–11.9)

NOTE: Urinary NNAL and arsenic concentrations were adjusted for creatinine. NNAL data were available for 2007–2012 NHANES participants and arsenic data were available for 2003–2012 NHANES participants.

Table 3.

Geometric mean concentrations of cotinine and NNAL among cigar or cigarette-only smokers by frequency of smoking, NHANES 1999–2012

		Primary cigar smokers		Secondary cigar smokers		Cigar-only smokers (primary and secondary cigar smokers combined)		Cigarette-only smokers
Biomarkers of exposure	Nontobacco users	Daily	Nondaily	Daily	Nondaily	Daily	Nondaily	Daily	Nondaily
Serum cotinine, ng/mL
Number of observations	16,990	44	177	54	124	98	301	5,834	1,183
Geometric mean (95% CI)	0.045 (0.043–0.048)	58.6 (31.2–109.9)	4.1 (2.8–5.8)	139.7 (103.1–189.2)	11.3 (6.4–20.0)	105.2 (78.5–141.0)	6.6 (4.6–9.4)	190.6 (184.0–197.4)	15.8 (12.7–19.8)
Urinary NNAL, pg/mg creatinine
Number of observations	8,117	26	76	24	54	50	130	2,709	550
Geometric mean (95% CI)	1.01 (0.95–1.07)	147.4 (76.0–285.9)	10.5 (6.3–17.5)	362.5 (221.0–594.6)	40.0 (22.5–71.0)	249.3 (161.2–385.6)	20.0 (12.3–32.6)	298.8(276.6–322.7)	36.8 (28.3–47.7)

NOTE: Urinary NNAL concentrations were adjusted for creatinine. NNAL data were available for 2007–2012 NHANES participants. “Daily” and “nondaily” were used to characterize cigar smoking pattern among cigar smokers, and cigarette smoking pattern among cigarette-only smokers. Primary and secondary cigar smokers were categorized as “daily cigar smokers” if they smoked cigars daily in the past 5 days and as “nondaily cigar smokers” if they smoked cigars on some days of the past 5 days. Current cigarette-only smokers were categorized as “daily cigarette smokers” if they smoked cigarettes every day, or “nondaily cigarette smokers” if they smoked cigarettes on some days.

Table 4.

Unadjusted and adjusted geometric mean ratios for biomarkers of exposure by tobacco use status, NHANES 1999–2012

Biomarkers of exposure	Tobacco use category	Unadjusted geometric mean ratio (95% Cl)	Adjusted geometric mean ratio (95% Cl)
Serum cotinine	Primary cigar smokers	137.3 (93.1–202.6)	92.2 (64.6–131.8)
	Secondary cigar smokers	535.4 (331.4–864.8)	485.7 (297.8–792.2)
	Cigarette only smokers	2,910.5 (2,694.4–3,143.9)	2,341.3 (2,146.7–2,553.5)
	Dual cigar/cigarette smokers	2,278.2 (1,716.9–3,023.1)	1,515.1 (1,143.5–2,007.5)
	Nontobacco users (Ref)	1.0	1.0
Urinary NNAL	Primary cigar smokers	26.6 (16.1–44.0)	19.0 (11.3–32.0)
	Secondary cigar smokers	92.8 (49.6–173.4)	82.3 (44.1–153.6)
	Cigarette only smokers	220.5 (198.5–244.9)	182.2 (164.5–201.8)
	Dual cigar/cigarette smokers	273.1 (196.0–380.3)	191.0 (139.0–262.4)
	Nontobacco users (Ref)	1.0	1.0
Blood cadmium	Primary cigar smokers	1.03 (0.91–1.16)	1.21 (1.08–1.36)
	Secondary cigar smokers	1.62 (1.41–1.87)	1.81 (1.58–2.08)
	Cigarette only smokers	3.51 (3.40–3.62)	3.68 (3.57–3.80)
	Dual cigar/cigarette smokers	2.76 (2.36–3.22)	3.20 (2.73–3.74)
	Nontobacco users (Ref)	1.0	1.0
Blood lead	Primary cigar smokers	1.20 (1.09–1.33)	1.13 (1.04–1.23)
	Secondary cigar smokers	1.61 (1.44–1.81)	1.31 (1.17–1.45)
	Cigarette only smokers	1.48 (1.44–1.52)	1.45 (1.42–1.48)
	Dual cigar/cigarette smokers	1.60 (1.40–1.83)	1.45 (1.30–1.62)
	Nontobacco users (Ref)	1.0	1.0
Urinary arsenic	Primary cigar smokers	1.18 (0.70–1.98)	0.85 (0.55–1.30)
	Secondary cigar smokers	1.45 (1.01–2.09)	1.33 (0.96–1.83)
	Cigarette only smokers	0.83 (0.75–0.92)	0.87 (0.80–0.95)
	Dual cigar/cigarette smokers	1.38 (1.02–1.85)	1.16 (0.79–1.69)
	Nontobacco users (Ref)	1.0	1.0

NOTE: NNAL data were available for 2007–2012 NHANES participants. Arsenic data were available for 2003–2012 NHANES participants. The adjusted geometric mean ratios were controlled for age, sex, race/ethnicity, educational attainment, and body mass index. For urinary NNAL and urinary arsenic, the adjusted ratios were further adjusted for creatinine. The unadjusted geometric mean ratios for urinary NNAL and urinary arsenic were not controlled for creatinine.