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. 2018 Jan 12;79(1):126–131. doi: 10.15288/jsad.2018.79.126

Nicotine Intake in Pregnant Smokers and a General Population of Smokers

Ivan Berlin a,*, Nelly Jacob a,✉, Stephen J Heishman b
PMCID: PMC9798487  PMID: 29227241

Abstract

Objective:

The purpose of this study was to assess whether pregnant smokers have the same nicotine intake from cigarettes as a general population of smokers and whether the known lower daily cigarette consumption among pregnant smokers is associated with higher nicotine intake among pregnant smokers.

Method:

The study was a cross-sectional comparison of pregnant smokers and a general population of smokers in smoking cessation clinics. Participants were treatment-seeking pregnant (n = 476), nonpregnant female (n = 116), and male (n = 195) smokers who participated in two independent smoking cessation trials. Nicotine intake was measured as saliva cotinine/cigarette/kg body weight ratio.

Results:

The mean saliva cotinine (μg/L)/cigarette/kg body weight (0.21, SD = 0.15) of pregnant smokers was similar to that of nonpregnant female smokers (0.24, SD = 0.14) and higher than that of male smokers (0.18, SD = 0.12, p = .002) despite a substantially lower number of cigarettes per day (pregnant smokers: 12, SD = 6; nonpregnant female smokers: 26.6, SD = 11.7; male smokers: 23.5, SD = 9.5, p < .001). Among pregnant smokers, saliva cotinine, as expected, increased in parallel with the number of cigarettes per day, but nicotine intake (cotinine/cigarette/kg body weight) was inversely associated with daily cigarette consumption (p < .001). No association between cigarettes per day and nicotine intake was observed in male and nonpregnant female smokers (p = .43).

Conclusions:

This secondary analysis showed that pregnant smokers’ nicotine intake was similar to that of a general population of smokers despite a lower cigarette consumption rate. Among pregnant smokers, lower daily cigarette consumption was associated with higher nicotine intake from cigarettes, suggesting compensatory smoking.

Plasma and saliva cotinine are widely used markers of nicotine exposure from tobacco (Jarvis et al., 1987). Intake of nicotine measured as serum or saliva cotinine concentration per cigarette ratio is a better indicator of nicotine exposure than the number of cigarettes smoked per day. For example, nicotine intake, expressed as cotinine per cigarette, increased from 12.4 to 17.6 over 25 years in the United States despite a reduction of the number of cigarettes per day from 17.3 to 12.3 (Jarvis et al., 2014). Thus, smokers likely compensate for reductions in cigarette consumption (Scherer, 1999) by increased nicotine extraction from cigarettes by increased puff volume or inhalation parameters (Zacny et al., 1987). Saliva cotinine concentrations show moderate to high stability within smokers despite a reduction of daily cigarette consumption (Fidler et al., 2011).

Cigarette consumption is usually lower among pregnant smokers than among nonpregnant female smokers (Haug et al., 1994, Ussher et al., 2012). Despite lower cigarette consumption and awareness of the health risks of smoking during pregnancy, pregnant smokers seem to have more difficulty quitting (Ingall & Cropley, 2010; Schneider & Schütz, 2008). A potential explanation is the increased metabolism of nicotine during pregnancy (Dempsey et al., 2002; Koren et al., 2008).

Our aim was to assess whether pregnant smokers have the same nicotine intake from cigarettes as a general population of smokers. We compared nicotine intake expressed as saliva cotinine per cigarette per body weight before a predefined quit date among pregnant smokers, nonpregnant female smokers, and male smokers participating in two smoking cessation trials. We also assessed nicotine intake according to the number of cigarettes smoked per day, assuming that nicotine intake can be stable and independent of the number of cigarettes smoked per day.

Method

We analyzed baseline pre-quit data from two previously published smoking cessation studies. Pregnant smokers were participants in the Study of Nicotine Patch in Pregnancy (SNIPP; Identifier: ClinicalTrials.gov NCT00507975) (Berlin et al., 2014), and male and nonpregnant female smokers were participants in the Adjustment of DOses of NIcotine in Smoking trial (ADONIS; ClinicalTrials.gov Identifier: NCT00235313) (Berlin et al., 2011). Research protocols for both studies were approved by the Ethics Committee of the Pitié-Salpêtrière Hospital, Paris, France. The SNIPP trial was a randomized, double-blind, placebo-controlled, parallel-group, multicenter study assessing the efficacy of 16-hour nicotine patches whose dose ranged from 10 to 30 mg/day based on individually adjusted saliva cotinine. Pregnant smokers who were older than 18 years, were between 12 and 20 weeks of gestation, and who smoked at least five cigarettes per day and scored 5 or higher on a scale of motivation to quit (range: 0–10) were included. The ADONIS trial enrolled a general population of smokers attending smoking cessation clinics in France (Berlin et al., 2011). In the ADONIS trial, women were included if they used an effective contraceptive method (hormonal contraception or intrauterine device) or were menopausal. Breastfeeding and pregnant women were excluded. The aim of this study was to compare nicotine replacement therapy efficacy when the nicotine replacement therapy daily dose was determined by progressive dose adaptation, based on saliva cotinine concentrations, to obtain 100% substitution and to compare to the standard monthly decreasing dose of nicotine replacement therapy without saliva cotinine determination. Included participants were 18 years old or older, smoked at least 10 cigarettes per day, intended to stop smoking in the coming weeks, and scored 5 or higher on a scale of motivation to quit (range: 0–10). All participants signed written consent forms before the study.

Saliva cotinine determination

The cotton roll from a Salivette® device (Sarstedt, Nümbrecht, Germany) was chewed for 1 minute, put back into the device, kept at 4 °C, and sent in less than 24 hours to the central biochemistry laboratory (Hôpital Pitié-Salpêtrière, Laboratoire de Biochimie, N. Jacob) for analysis. Cotinine concentration was determined using reversed-phase liquid chromatography and ultraviolet detection following extraction with an organic solvent from alkalinized and internal standard-spiked saliva samples. The cotinine standard solutions ranging from 5 to 800 μg/L were processed like unknown saliva samples, and the calibration curve was linear with R2 > .99. The long-term interassay precision was lower than 10% (Berlin et al., 2011; Jacob et al., 2015). The sampling methods for both saliva cotinine and expired air carbon monoxide (CO) were exactly the same in the SNIPP and ADONIS studies. The mean time to the last cigarette was 36 minutes (minimum = 1, maximum = 95) in the ADONIS study and 28 minutes (minimum = 1, maximum = 90) in the SNIPP study.

The mean gestational age at saliva cotinine sampling among pregnant smokers was 14.4 weeks (SD = 3.41).

Craving for tobacco was assessed in both studies by the 12-item French Tobacco Craving Questionnaire (FTCQ-12) (Berlin et al., 2010, 2015). The FTCQ-12 is a multidimensional 12-item self-report instrument that assesses four dimensions of tobacco craving [Emotionnalité (Emotionality), Attente (Expectancy), Compulsion (Compulsivity), and Anticipation (Purposefulness)]. Items are rated on an interval scale (1–7, strongly disagree to strongly agree). Four items are reverse-keyed to reduce acquiescence. In this study, the summary score of the four factor scores was used. Cigarette dependence was assessed by the Fagerström Test for Cigarette Dependence (FTCD; Fagerström, 2012).

Data analysis

We used cotinine/cigarette/body weight as the main index of nicotine intake. Analysis of variance or analysis of covariance was used to compare groups. Because pregnant smokers were younger and the body mass index of male smokers was higher than that of female smokers, data were adjusted for these covariables. Linear regression was used to assess the association between ln (natural logarithm) transformed saliva cotinine/cigarette/kg body weight with tobacco craving as measured by the FTCQ-12. Pearson’s r was used to assess correlations. Data are presented as means and standard deviations or standard errors for adjusted means. A two-tailed p value of .05 or less was considered as significant. Data were analyzed using SPSS Statistics for Windows, Version 18.0 (SPSS Inc., Chicago, IL).

Results

As expected, the general population of smokers was older than the pregnant smokers. The body mass index of male smokers was higher than that of female smokers. Pregnant smokers had significantly lower cigarettes-per-day consumption, expired air CO (carbon monoxide), and saliva cotinine concentrations than did the general population of smokers. These results can be attributed to the threshold number of cigarettes per day to enter the study being lower for pregnant smokers (at least 5 cigarettes/day) than it was for smoking nonpregnant women and men (at least 10 cigarettes/day). Nicotine intake expressed as saliva cotinine per cigarette was similar across the population samples, but saliva cotinine/cigarette/kg was higher among nonpregnant female smokers and pregnant smokers than among men (Table 1). Linear regression showed that nicotine intake (saliva cotinine/cigarette/kg) was associated positively with expired air CO (β = .222, t = 5.41, p < .001), and inversely with age (β = -.138, t = -3.32, p = .001) and tobacco craving (FTCQ-12) (β = -.09, t = -2.72, p = .007).

Table 1.

Comparison of sample characteristics

graphic file with name jsad.2018.79.126tbl1.jpg

Variable Male smokers (M) (n = 195) Non-pregnant female smokers (NP) (n = 116) Pregnant smokers (P) (n = 476) p Between-group comparisons
Age, in years 50.9 (9) 47.8 (10) 28.9 (5.8) <.001 M = NP > P
Body mass index (kg/m2) 26.48 (4.75) 24.33 (5.2) 24.93 (5.21) <.001 M > NP = P
FTCD 6.5 (2.2) 6.7 (1.8) 4.5 (2.1) <.001 M = NP > P
FTCQ-12 39 (9.9) 39.2 (9.9 33.3 (8.6) <.001 M = NP > P
Cigarettes per day 23.5 (9.5) 26.6 (11.7) 12 (6) <.001 M < NP; M > P; NP > P
Expired air carbon monoxide (ppm) 27.25 (12.22) 26.52 (12.16) 11.6 (6.91) <.001 M = NP > P
Saliva cotinine concentration (μg/L)a 312 (11) 300 (12) 148 (7) <.001 M = NP > P
Saliva cotinine/cigarette (μg/L/cigarette)a 13.67 (0.76) 13.8 (0.8) 13.43 (0.47) .943 –
Saliva cotinine/cigarette/body weightb (μg/L/cigarette/kg) 0.18 (0.12) 0.24 (0.14) 0.21 (0.15) .002 M < NP = P
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Notes: Data are means and standard deviations (or standard errors for adjusted means). FTCD = Fagerström Test for Cigarette Dependence; FTCQ-12 = 12-item French Tobacco Craving Questionnaire total score.

a

Adjusted for age and body mass index;

b

adjusted for age. a and b are analysis of covariance; all other variables are analysis of variance. All were calculated with Bonferroni’s correction for pairwise comparisons.

Among pregnant smokers, saliva cotinine concentration and expired air CO increased by the number of cigarettes smoked per day, as expected. However, nicotine intake (cotinine/cigarette/kg) showed the opposite trend; lower cigarette consumption was associated with higher nicotine intake (Table 2A). The gestational age at sampling was relatively narrow (M = 14.4 weeks, SD = 3.41, range: 9–20 weeks), and there was no association between gestational age at sampling and cotinine/cigarette/kg (r = -.073, p = .111). Cotinine/cigarette/kg was inversely associated with the number of cigarettes per day (r = -.307, p < .001). Partners’ smoking did not influence cotinine/cigarette/kg (nonsmoking partner: 0.22 [0.15], smoking partner: 0.21 [0.15], p = .476, mean μg/L/cigarette/kg [SD]). Table 2B shows data for male and nonpregnant female smokers. As among pregnant smokers, an increased smoking rate was associated with increased expired air CO and saliva cotinine but not with saliva cotinine/cigarette/body weight. No difference occurred between male and nonpregnant female smokers for any of the variables (p values for gender effect ranged from .228 to .907). Moreover, there was no correlation between cotinine/cigarette/kg and cigarettes-per-day consumption (r = .06, p = .288).

Table 2.

Saliva cotinine, saliva cotinine/cigarette, saliva cotinine/cigarette/kilogram body weight, and expired air carbon monoxide in (A) pregnant smokers and (B) male and nonpregnant female smokers by cigarettes smoked per day (CPD)

graphic file with name jsad.2018.79.126tbl2.jpg

A. Pregnant smokers 1–9 CPD (n = 155) 10–15 CPD (n = 236) >15 CPD (n = 85) p a
Expired air carbon monoxide (ppm) 9.3 (6.3) 12.4 (7) 13.7 (6.6) <.001
Saliva cotinine concentration (μg/L) 110.5 (71.3) 150.6 (70.5) 191.3 (86) <.001
Saliva cotinine/cigarette (μg/L/cigarette) 16.8 (10.8) 12.7 (6) 8.9 (4.1) <.001
Saliva cotinine/cigarette /body weight (μg/L/cigarette/kg) 0.27 (0.20) 0.20 (0.11) 0.13 (0.07) <.001
B. Male and female (non-pregnant) smokers 1–9 CPD (n.a.) 10–15 CPD (n = 57) >15 CPD (n = 253) p a
Expired air carbon monoxide (ppm) – 20.4 (11) 28.5 (12) <.001
Saliva cotinine concentration (μg/L) – 262 (138) 323 (152) .005
Saliva cotinine/cigarette (μg/L/cigarette) – 19.2 (10) 12.5 (6.5) <.001
Saliva cotinine/cigarette/body weight (μg/L/cigarette/kg) – 0.20 (0.16) 0.21 (0.15) .430
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Notes: Data are means and standard deviations. n.a. = not available.

a

From analysis of variance.

Discussion

Pregnant smokers usually have a reduced smoking rate and saliva cotinine concentration, but direct comparisons with other populations of smokers are surprisingly rare. We found that, although pregnant smokers smoked less, their nicotine intake expressed as cotinine/cigarette was similar to that of male or nonpregnant female smokers or higher if expressed as cotinine/cigarette/kg body weight, a more reliable expression of nicotine intake. Among pregnant smokers, cotinine/cigarette/kg body weight showed a strong and inverse association with cigarette consumption, but there was no such association among male and nonpregnant female smokers. These findings suggest compensatory smoking among pregnant smokers. Nicotine intake was inversely and strongly associated with craving for tobacco.

The clearance of nicotine is increased by 60% (and that of cotinine by 140%) during pregnancy compared with the postpartum time period (Dempsey et al., 2002), which might result in lower systemic exposure to nicotine in late pregnancy (Hukkanen et al., 2005b; Koren et al., 2008). The metabolism of nicotine as determined by the metabolite ratio cotinine/trans-3 -hydroxycotinine, progressively increases with gestational weeks and has been found to be faster during pregnancy than the postpartum time period (Bowker et al., 2015). The enhanced metabolism of nicotine has been attributed to sex hormonal induction of liver cytochrome 2A6 and flavin-containing monooxygenase 3 (Hukkanen et al., 2005a, 2005b). Increased nicotine clearance may contribute to an increased urge to smoke and withdrawal symptoms among pregnant smokers compared with the general population of smokers. In fact, we previously found, from the same sample, that after a predefined quit date during a 2-week period, craving for tobacco and withdrawal symptoms diminished less among pregnant smokers than among nonpregnant female smokers (Berlin et al., 2016). Therefore, one way to compensate for an increased urge to smoke can be to compensate for reduced cigarette consumption by increasing nicotine intake from cigarettes.

Because the clearance of nicotine may increase with gestational age, cotinine/cigarette/kg could have been increased by increasing gestational age. However, we found no association between gestational age and cotinine/cigarette/kg, but the sampling occurred between relatively narrow ranges of gestational age. Further studies might use sequentially measured cotinine/cigarette/kg during pregnancy to ascertain any association with gestational age.

Among other negative health outcomes, smoking during pregnancy restricts fetal growth, reduces birth weight, and increases risk for preterm delivery (U.S. Department of Health and Human Services, 2014). Although pregnant smokers might reduce their cigarette consumption, reduction has little or no benefit on negative pregnancy outcomes such as reduced birth weight (Benjamin-Garner & Stotts, 2013; Hebel et al., 1988; Li et al., 1993). The consequences of exposure to secondhand smoke during pregnancy on fetal health are similar to those of active smoking, although less pronounced (U.S. Department of Health and Human Services, 2006), indicating that even a small exposure can lead to negative health outcomes in the offspring.

The number of cigarettes smoked per day is not a reliable measure of direct smoke exposure or nicotine intake (Hughes & Carpenter, 2005). When the smoking rate is reduced, compensatory smoking may keep nicotine intake constant (Fidler et al., 2011; Scherer, 1999; Zacny et al., 1987). It is a likely way for pregnant smokers to reduce their increased craving or withdrawal symptoms that might occur with a reduced smoking rate. We analyzed data before smoking cessation or reduction occurred. Saliva cotinine/cigarette/kg body weight did not change with an increased number of cigarettes per day in male and female nonpregnant smokers but was inversely associated in pregnant smokers. This finding suggests that changes in saliva cotinine/cigarette/kg body weight by the number of cigarettes per day among pregnant smokers are more likely attributable to pregnancy and compensatory smoking.

We assessed the number of cigarettes per day before a smoking cessation attempt. Although pregnant smokers may underreport their smoking rate, this underreporting among pregnant women who smoke is about 3% compared with that estimated by their saliva cotinine (Owen & McNeill, 2001) and substantially lower than underreporting or nondisclosure of smoking during smoking cessation (13% to 25%; George et al., 2006). On the other hand, self-reported daily smoking has also been shown to be valid in early and late pregnancy (George et al., 2006). Although it cannot be excluded that underreporting contributed to the observed inverse association between cigarettes/day and cotinine/cigarette/kg body weight, this seems to be unlikely, given that the women were treatment-seeking pregnant smokers motivated to quit, and underreporting would have reduced their likelihood to be included in the study.

Limitations and strengths

Limitations.

We compared data of pregnant smokers with a historical comparison group; all participants were treatment-seeking smokers enrolled in smoking cessation clinical trials. Further studies should compare pregnant smokers with a matched control group of non–treatment-seeking smokers. Comparisons were cross sectional; further studies should compare sequential changes in nicotine intake during pregnancy to those of nonpregnant female smokers. Generality is further reduced by the fact that all individuals were French smokers mostly of European ancestry. Results need to be confirmed using independent samples from other countries and ethnicities.

Strengths.

We used saliva cotinine/cigarette/kg body weight as the measure of nicotine intake. This seems to be a more precise measure of nicotine intake than cotinine/cigarette because it takes into account body weight, and body weight is a proxy of volume of distribution. Pregnant, compared with nonpregnant, women have a larger blood volume and volume of distribution (Costantine, 2014). A higher volume of distribution of cotinine may be associated with a lower plasma cotinine concentration at the same level of nicotine intake/cigarette. In fact, Jain and Bernert (2010) found a strong inverse association between body mass index or total blood volume and serum cotinine concentration, supporting the notion that a person with a higher body mass index (or a larger blood volume), compared with a person with a lower body mass index (or a smaller blood volume), will have the same amount of cotinine distributed in a larger volume, leading to lower serum (or saliva) cotinine concentration. Further strength includes use of the same sampling method, determination of saliva cotinine in the same laboratory for all samples, and the use of a validated measure of tobacco craving.

In conclusion, this secondary analysis showed that pregnant smokers’ nicotine intake was similar to that of nonpregnant female smokers and higher than that of male smokers despite a lower cigarette consumption rate. Among pregnant smokers but not among nonpregnant female or male smokers, nicotine intake was inversely associated with daily cigarette consumption, suggesting compensatory smoking. This feature of smoking during pregnancy should be taken into account when health professionals help pregnant smokers quit smoking.

Conflict of Interest Statement

The authors declare no connection with the tobacco, alcohol, or gaming industries or any organization substantially funded by one of these organizations. They also declare no conflict of interest arising from involvement with organizations that seek to provide help with or promote recovery from addiction. The authors do not have contractual constraints on publishing imposed by the funders of the reported studies. Ivan Berlin reports having received occasional speakers’ honoraria and honoraria for participation in advisory boards from the pharmaceutical companies Pfizer and Novartis in the last 3 years. None of the authors was funded by these sources for the current research. Stephen J. Heishman is supported by the Intramural Research Program of the National Institute on Drug Abuse.

Footnotes

The ADONIS study was supported by the French Ministry of Health Programme Hospitalier de Recherche Clinique Loco-regional 2004 (AOR04001//P040406, registration number: 050558); by the Agence française de sécurité sanitaire des produits de santé, Convention Pharmacologie Clinique et Thçrapeutique 2003, RAF02020. The SNIPP study was funded by the Ministry of Health, France, Grant Number MA05 001050. The current work was not funded.

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