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Early Course of Nicotine Dependence in Adolescent

Smokers

WHAT’S KNOWN ON THIS SUBJECT: There is strong correlation between the occurrence of nicotine dependence symptoms and lifetime tobacco exposure. Symptoms of nicotine dependence occur soon after smoking initiation. Early symptoms of dependence typically precede the onset of daily smoking.

WHAT THIS STUDY ADDS: Smoking initiation triggers development of early symptoms of dependence, which in turn promotes smoking escalation. The sequence of evolution of dependence symptoms varies among individual youths. Early dependence symptoms often are not recognized as harbingers of addiction.

abstract

OBJECTIVE:The goal was to characterize the early course of nicotine dependence.

METHODS:Data were collected from 1246 sixth-graders in a 4-year (2002–2006) prospective study using 11 individual interviews. Subjects were monitored for 10 symptoms of dependence by using the Hooked on Nicotine Checklist. The bidirectional prospective relationship be-tween the intensity of dependence (number of symptoms) and smoking frequency was examined by using cross-lagged analyses.

RESULTS:Of the 370 subjects who had inhaled from a cigarette, 62% smoked at least once per month, 53% experienced dependence symp-toms, and 40% experienced escalation to daily smoking. Smoking fre-quency predicted the number of dependence symptoms at the next interview, and the number of symptoms predicted reciprocally the observed escalation in smoking frequency. Monthly smoking was a strong risk factor for the development of symptoms (adjusted hazard ratio: 9.9 [95% confidence interval: 6.6 –14.8]). A strong desire to smoke was the most common presenting symptom, typically followed by the appearance of symptoms of nicotine withdrawal, escalation to daily smoking, and then reports of feeling addicted or difficulty controlling smoking. The appearance of any dependence symptom increased the risk for daily smoking (hazard ratio: 6.81 [95% confidence interval: 4.4 –10.5]).

CONCLUSIONS:Nondaily tobacco use triggers the emergence of nico-tine dependence. Early dependence symptoms promote escalation in smoking frequency and, reciprocally, more-frequent smoking acceler-ates the appearance of additional symptoms of dependence. As this positive feedback progresses, the symptoms of nicotine dependence present in a typical sequence, with some individual variation. Pediatrics2010;125:1127–1133

AUTHORS:Chyke A. Doubeni, MD, MPH,a,bGeorge Reed,

PhD,cand Joseph R. DiFranza, MDa

aDepartment of Family Medicine and Community Health,bMeyers

Primary Care Institute, andcDivision of Preventive and

Behavioral Medicine, Department of Medicine, University of Massachusetts Medical School, Worcester, Massachusetts

KEY WORDS

nicotine, addiction, adolescent smoking, tobacco use/smoking

ABBREVIATIONS

HONC—Hooked on Nicotine Checklist HR— hazard ratio

CI— confidence interval

www.pediatrics.org/cgi/doi/10.1542/peds.2009-0238 doi:10.1542/peds.2009-0238

Accepted for publication Jan 28, 2010

Address correspondence to Chyke A. Doubeni, MD, MPH, Department of Family Medicine and Community Health, University of Massachusetts Medical School, 55 Lake Ave North, Worcester, MA 01655. E-mail: chyke.doubeni@umassmed.edu PEDIATRICS (ISSN Numbers: Print, 0031-4005; Online, 1098-4275). Copyright © 2010 by the American Academy of Pediatrics

FINANCIAL DISCLOSURE:The authors have indicated they have no financial relationships relevant to this article to disclose.

Funded by the National Institutes of Health (NIH).

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addicted, to progress to daily smoking, to continue smoking into adulthood, and to become heavier tobacco users as adults.1–4 Nicotine dependence

symptoms often develop soon after smoking initiation, generally before the onset of daily smoking.5–7The

ap-pearance of such symptoms was found to be a strong predictor of future smoking behavior in long-term longitu-dinal studies.5,8One study found that

the tobacco use trajectory of youths who went on to become heavy adult smokers diverged from that of youths who did not become heavy smokers at the point when they began smoking at a frequency of 2 cigarettes per week.9

The first Development and Assessment of Nicotine Dependence in Youth study, and subsequent published studies from other groups, described the or-der of presentation of nicotine depen-dence symptoms.5–8 Those studies

presented a consistent picture of symptoms emerging with minimal nondaily tobacco use, with craving for tobacco being the most common pre-senting symptom.7However, no

previ-ous studies examined the course of symptom development for individual smokers, to determine whether the typical sequence of symptom develop-ment applies to all individuals.

Furthermore, the strong correlation between the occurrence of depen-dence symptoms and lifetime tobacco use10suggests that the emergence of

dependence symptoms and escalation in smoking during the early phase of tobacco use proceed as parallel but reciprocal events. However, no previ-ous studies have assessed whether, among novice smokers, nicotine de-pendence drives the escalation of smoking and vice versa. In this pro-spective observational study, we exam-ined the sequence in which symptoms of dependence present, and we

as-dence over time.

METHODS

Study Design

The data for this report were obtained from the Development and Assess-ment of Nicotine Dependence in Youth 2 study, a 4-year prospective study of 1246 English-speaking students (age: median: 12 years [range: 11–13 years]) from 6 central Massachusetts communities that began when the stu-dents were in sixth grade. The details of the study, including methods for standardization of the interviews and the data collected, were fully de-scribed previously.5 In brief,

partici-pants underwent up to 11 cycles of standardized, confidential, in-person interviews, which were conducted in school at a frequency of 3 interviews per school year. The dates of the first puff on a cigarette, the appearance of each symptom of dependence, and the transitions in the frequency of tobacco use were recorded. To facilitate accu-rate recall of dates and events, inter-views were conducted with the aid of personal landmarks, bounded recall, decomposition, and a personalized cal-endar.11,12The study was approved by

the institutional review board of the University of Massachusetts Medical School.

Study Parameters

The main outcome measure for this study was the development of dimin-ished autonomy over tobacco use. The Diagnostic and Statistical Manual of Mental Disorders,Fourth Edition, pro-vides nomenclature for substance (in-cluding tobacco) use disorders.13

Un-like for other substances, there is no category for patients who have symp-toms but fall short of the number required for a diagnosis of nicotine dependence. Therefore, investigators

monly assessed diminished autonomy over tobacco, that is, the presence of any symptom that would be expected to make it more challenging to quit smoking.14 The Hooked on Nicotine

Checklist (HONC) (Table 1), which uses this approach for identifying nicotine dependence, has been extensively vali-dated.5,8,10Diminished autonomy is

de-fined by the appearance of any of the 10 symptoms on the HONC, and the symp-tom score (range: 0 –10) is the cumula-tive number of items endorsed.14 The

HONC differs from most other measures of dependence in that it does not include any direct or indirect measure of smok-ing frequency. This makes the HONC a particularly suitable measure for analy-sis of the interaction between depen-dence and smoking frequency.

We defined smoking frequency as the number of cigarettes smoked per 28 days, monthly smoking as smoking at least once during each of 2 consecu-tive 30-day periods, and daily smoking as smoking at least once daily for 30 days. Demographic data included date of birth, gender, and race/ethnicity, which was categorized as Hispanic, non-Hispanic white, or other.

Data Analyses

Event-time (or survival) analyses per-formed with Stata 11 (Stata, College Station, TX) were conducted from the date of the first puff on a cigarette. The time to the event of interest (ie, dimin-ished autonomy or smoking milestone of monthly or daily use) was tracked until the event occurred, the subject quit smoking, or the subject completed his or her last interview. Previous sim-ilar analyses assessed the time to the point at which 25% of those who expe-rienced a particular event had done so.6,7To maintain consistency with the

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focused on the time to 25% cumulative probability. Cox regression analyses adjusted for age, gender, and race/ ethnicity were used to determine whether monthly smoking increased the risk of symptom development and whether diminished autonomy pre-dicted progression to daily tobacco use.

To simplify the presentation of results, the 10 HONC symptoms were combined into 4 groups, as shown in Table 1. Three of these groups reflect diagnos-tic criteria for nicotine dependence (strong desire to smoke, withdrawal symptoms, and difficulty controlling tobacco use), leaving the item regard-ing feelregard-ing addicted as a separate cat-egory. These groupings do not repre-sent factors, because the HONC measures a single construct.15 The

date of onset for each symptom group

was determined on the basis of the date of the earliest symptom within that group. To assess the sequence of symptom development, we determined the rank order of appearance for each subject. When an individual reported

ⱖ2 symptoms at the same time, we ranked the tied symptoms for that in-dividual in the order of their appear-ance for the total cohort, as shown in Table 1.

We explored autoregressive latent tra-jectory models by using Mplus 5.2 (Mu-the´n & Mu(Mu-the´n, Los Angeles, CA), as described by Bollen and Curran,16,17to

assess whether HONC symptom scores predicted future smoking frequency (number of cigarettes per month) and, reciprocally, whether smoking fre-quency predicted future HONC scores. Autoregressive latent trajectory

analy-ses simultaneously control for the rate of change or growth over time in both symptom scores and smoking fre-quency. However, we used autoregres-sive (cross-lagged) model analyses alone for our analyses because autore-gressive latent trajectory models did fit the data well. Poisson models were used for HONC scores, and smoking frequency was logarithmically trans-formed and modeled as a continuous variable. Both processes were mod-eled from the date of the first puff on a cigarette. We used Bayesian informa-tion criteria to select a parsimonious model that included age at smoking initiation as a covariate. We restricted these analyses to the first 7 rounds af-ter smoking initiation and to subjects (n⫽229) who had been monitored for

ⱖ6 interviews after the first puff.

RESULTS

Study Subjects

Of the 370 subjects included in the analyses, 56% were female, 64% were non-Hispanic white, 23% Hispanic, and 13% of other racial/ethnic groups. The median age at first cigarette was 12 years (interquartile range: 4 years). The proportions of subjects reporting each HONC symptom and smoking milestone and the time to 25% cumula-tive probability are shown in Table 1. At least 1 HONC symptom (diminished autonomy) was reported by 33% of subjects who had ever puffed on a cigarette.

Course of Symptom Development Figure 1 shows variability in the order of symptom presentation on the basis of the symptom groups. In the entire co-hort, strong desire was the most com-mon presenting symptom type (re-ported by 88 [24%] of 370 subjects), and withdrawal symptoms were the

second most common presenting

symptom (n ⫽ 17 [5%]). Generally, symptoms appeared in the following TABLE 1 Time to 25% Cumulative Probability of HONC Symptoms and Smoking Frequency Among

Subjects Who Had Initiated Smoking

HONC Symptoms Proportion Reporting Symptom

(N⫽370), %a

Time to 25% Cumulative Probability, Estimate

(95% CI), mob Diminished autonomy (any symptom) 32.7 27.0 (21.0–37.0) Strong desire to smoke

Have you ever had strong cravings to smoke? 27.0 37.1 (30.6–55.5) Have you ever felt like you really needed a cigarette? 27.3 39.0 (28.2–53.8) Withdrawal symptoms

When you have tried to stop smoking or when you haven’t been able to smoke . . .

Did you feel a strong need or urge to smoke? 21.1 55.5 (35.0–83.9) Did you feel more irritable because you couldn’t

smoke?

18.1 76.9 (40.8–90.1)

Did you feel nervous, restless, or anxious because you couldn’t smoke?

16.8 73.7 (40.5–??)

Did you find it hard to concentrate because you couldn’t smoke?

15.4 86.4 (55.0–131.4)

Feeling addicted

Have you ever felt like you were addicted to tobacco? 19.7 63.6 (42.3–80.0) Difficulty controlling use

Have you ever tried to quit smoking but couldn’t? 14.3 83.2 (56.2–123.8) Do you smoke now because it is really hard to quit? 13.5 90.1 (56.0–??) Is it hard to keep from smoking in places where you

are not supposed to, like school?

10.0 ?? (74.1–??)

Symptom groups

Strong desire to smoke 30.8 30.6 (24.5–42.3) Withdrawal symptoms 25.1 43.6 (30.0–63.0) Feeling addicted 19.7 63.6 (42.3–80.0) Difficulty controlling use 18.9 57.2 (43.1–79.9) Smoking frequency

Monthly 37.0 23.8 (13.0–30.9)

Daily 24.6 50.5 (32.7–64.1)

aProportion of the cohort reporting each symptom. Each student could report1 symptom. bFor some outcomes, there were not enough events to estimate the 25% cumulative probability.

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order: strong desire, withdrawal symp-toms, feeling addicted, and difficulty controlling smoking.

Figure 2 compares the cumulative probability of onset of symptoms with the onset of monthly and daily

smok-ing. Diminished autonomy was re-ported by 4% of subjects within 1 month after the first cigarette, and

there was a progressive increase in the development of HONC symptoms over time. On the basis of the 25%

cu-1), monthly smoking typically pre-ceded all other measures, including the first HONC symptom of any type. Strong desire and withdrawal symp-toms typically preceded the onset of daily smoking, and feeling addicted and difficulty controlling tobacco use tended to appear at approximately the same time as one another and after the onset of daily smoking. Follow-up times beyond the 4 years of the study entail increasing periods of recall for subjects who initiated smoking before the initial study interview. Sensitivity analyses excluding subjects who had initiated smoking⬎4 months before the first interview (the average inter-val between interviews) produced sim-ilar results.

Relationship of Diminished Autonomy to Smoking Frequency Smoking at least once per month was reported by 92% of subjects who re-ported HONC symptoms but by only 10% (n⫽22) of those who did not re-port symptoms (P ⬍ .001). Approxi-mately 21% of the 121 subjects who ex-perienced diminished autonomy did so before monthly smoking, whereas the remaining 79% experienced dimin-ished autonomy coinciding with or fol-lowing the onset of monthly smoking. Symptoms of diminished autonomy were reported by 96% of daily smok-ers (n⫽87) and by 81% (n⫽111) of those who reported smoking at least monthly (including weekly and daily smokers). Compared with subjects who had not initiated daily smoking be-fore the development of HONC symp-toms (n ⫽ 53), subjects who began smoking daily before the onset of HONC symptoms (n ⫽ 38) reported symp-toms more rapidly (log-rank test,P⬍ .001).

In Cox proportional-hazards analyses that adjusted for gender, age, and FIGURE 1

Order of appearance of symptoms of diminished autonomy. The bars show how often (proportion) each symptom type appeared as the first, second, third, or fourth type of symptom to appear in 370 individuals who had ever puffed on a cigarette. Strong desire was the most common first symptom, withdrawal the most common second symptom, feeling addicted the most common third symptom, and difficulty controlling use (“can’t quit”) the most common fourth symptom.

FIGURE 2

Cumulative frequency distribution of development of symptoms of diminished autonomy and smoking frequency (N⫽370). The first symptom refers to the first symptom of any type. The upper border of the shaded area represents monthly smoking, and the lower border represents daily smoking. Log-rank tests of differences between curves yielded the following: strong desire versus withdrawal,P

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race/ethnicity, experiencing monthly smoking increased the risk for dimin-ished autonomy over tobacco use (ad-justed hazard ratio [HR]: 9.9 [95% confidence interval [CI]: 6.6 –14.8]). Ex-periencing any symptom of diminished autonomy increased the risk of pro-gressing to monthly smoking (HR: 3.7 [95% CI: 2.4 –5.5]) or daily smoking (HR: 6.8 [95% CI: 4.4 –10.5]).

Figure 3 depicts the results of the cross-lagged regression model analy-ses. Smoking frequency in rounds 1 to 3 predicted the number of HONC symp-toms in subsequent rounds (P⬍.01), and the number of HONC symptoms in rounds 2 to 4 predicted smoking fre-quency in subsequent rounds (P ⬍ .01). Neither factor was predictive of the other in subsequent rounds.

DISCUSSION

The traditional theoretical model de-scribing the onset of nicotine depen-dence holds that the sensory and so-cial rewards derived from smoking are the sole motivators of adolescent tobacco use for the first several years.18,19According to this model,

es-calation in tobacco use results from tolerance to the pleasure of smoking, and smokers develop dependence

when their pursuit of pleasure causes them to smoke at frequent intervals throughout the day.

The sensitization-homeostasis theory contradicts the traditional model.20It

proposes that symptoms of depen-dence that appear during nondaily smoking motivate continued tobacco use. According to this model, even smoking at monthly intervals entails a strong risk for developing depen-dence. Supporting this theory are 4 in-dependent studies showing that symp-toms of dependence develop during nondaily smoking, sometimes quite soon after the first cigarette.6–8,10The

findings of the current study, demon-strating that monthly smoking may in-crease the risk of developing depen-dence nearly 10-fold, support the sensitization-homeostasis theory.

The sensitization-homeostasis theory also posits that, once symptoms of craving and withdrawal appear, smok-ers experience symptoms whenever they go too long without smoking.20At

first, smoking intervals may be com-fortably spaced at intervals of days or weeks; as repeated exposures pro-mote tolerance, smokers must smoke at more-frequent intervals to keep

symptoms at bay. The theory asserts that early symptoms drive an escala-tion in the frequency of smoking to daily use. In this study, the early ap-pearance of dependence symptoms in-creased the risk of progression to daily smoking (HR: 6.8), and the number of symptoms predicted the magnitude of escalation in smoking frequency that oc-curred between interviews.

Previous studies found that depen-dence severity correlated with current smoking frequency and cumulative lifetime exposure,21–25but we think that

our study is the first to demonstrate that increased frequency of smoking puts youths at risk for more-rapid de-velopment and progression of depen-dence. This is important, because it suggests a dose-response effect of early nicotine exposure on the devel-opment of dependence.

Our findings suggest that the loss of autonomy over tobacco use proceeds in a typical sequence, with some indi-vidual variation. The order in which symptoms typically present is consis-tent with the mechanism described for the development of dependence under the sensitization-homeostasis theory. Among the symptoms assessed in this FIGURE 3

Relationship between loss of autonomy and smoking frequency over time. Shown are relative risk (RR) estimates with 95% CIs. The arrows denote the direction of the relationships modeled (eg, whether smoking frequency during round 1 increased the risk of symptoms in round 2). The relationship with frequency of smoking is expressed on a logarithmic scale. For instance, a 1-unit increase in the symptom score in round 2 increased by 6% the number of cigarettes smoked per month in round 3. Each 10-fold increase in the number of cigarettes smoked per month in round 2 increased by 20% the symptom score in round 3.

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withdrawal symptoms. These symp-toms typically develop before the onset of daily smoking. In previous studies, the early appearance of dependence symptoms was very strongly predic-tive of future smoking5,8 and

with-drawal symptoms predicted relapse among adolescent smokers, which in-dicated their clinical importance.21,26

Difficulty controlling use may not be re-ported until later in the course of symptom development, because re-fraining from smoking where it is not allowed may not be a problem when dependence can be satisfied by smok-ing less often than once per day.

The most important observation from our study is that the early course of nicotine dependence seems to involve a vicious cycle in which exposure to nicotine through smoking promotes the early development of craving and withdrawal, these symptoms drive an escalation in smoking frequency as tol-erance develops, and this escalation promotes the development of addi-tional symptoms of dependence. The strength of the reciprocal relationship between diminished autonomy and smoking frequency decreased over time. There are several potential expla-nations for this. A previous study found that the correlation between smoking frequency and levels of the nicotine metabolite cotinine decreased rapidly as consumption exceeded 4 or 5 ciga-rettes per day.27Therefore, at a certain

level of cigarette consumption, the dose of nicotine received may reach a physiological steady state with nico-tine requirement within individual per-sons. This suggests that the urge for escalating tobacco use diminishes once the dose of nicotine is sufficient to satisfy physiologic needs or to satu-rate receptor sites. Alternatively, at higher levels of consumption,

differ-levels of tolerance to nicotine that may be unrelated to dependence.28

In our study, some youths began smok-ing daily from their first cigarette, al-though they had no symptoms that would require them to do so. A possi-ble explanation for frequent smoking in the absence of symptoms is easy ac-cess to tobacco.29,30 Reducing the

ac-cessibility of cigarettes might slow the progression of dependence.

Our subjects typically did not report feeling addicted at the time when they experienced craving and withdrawal. Apparently, youths do not recognize strong craving and withdrawal as symptoms of addiction. Educating youths to recognize early symptoms of dependence may be a useful goal for secondary prevention programs, be-cause it might prompt earlier and more successful cessation efforts.

Our findings are consistent with a study by Gervais et al,7 which found

that craving typically precedes with-drawal and both symptoms typically precede daily smoking. However, our study found that feeling addicted was a late symptom, in contrast to the find-ings of Gervais et al,7 who reported

that self-diagnosed mental addiction typically preceded all other symptoms. This discordance may be attributable to differences in how these terms are interpreted by smokers.

Strengths of this study include the close, long-term, follow-up monitoring of novice smokers, with prospective data collection on symptom develop-ment and detailed records of smoking frequency, including dates for each event. The smoking prevalence in our cohort was comparable to that for the state of Massachusetts.31 A recent

study demonstrated that youths’ re-ports of symptoms of diminished au-tonomy are valid and is not merely the

other smokers.32

Study limitations include the limited number of subjects who had all 4 symptom types and the use of a geo-graphically limited convenience sam-ple. The results may not be applicable to individuals who initiate smoking af-ter adolescence. The earliest depen-dence symptom that was assessed in this study was strong craving. How-ever, a recent case series indicated that strong craving is not the initial symptom of dependence, because it may be preceded by recurrent want-ing, which is milder and less intrusive than craving.32 In this study, youths

were not asked about wanting and were not trained to recognize symptoms of de-pendence. If youths were taught to rec-ognize symptoms or were given the op-portunity to describe them in their own terms, they might report symptoms earlier. Between-subject variations in awareness and recognition of symp-toms could contribute to variations in the order of symptom reporting.

CONCLUSIONS

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Di-Franza JR. Screening adolescents for nico-tine dependence: the Hooked On Niconico-tine Checklist.J Adolesc Health. 2004;35(3): 225–230

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DOI: 10.1542/peds.2009-0238 originally published online May 3, 2010;

2010;125;1127

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DOI: 10.1542/peds.2009-0238 originally published online May 3, 2010;

2010;125;1127

Pediatrics

Chyke A. Doubeni, George Reed and Joseph R. DiFranza

Early Course of Nicotine Dependence in Adolescent Smokers

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Figure

TABLE 1 Time to 25% Cumulative Probability of HONC Symptoms and Smoking Frequency AmongSubjects Who Had Initiated Smoking
FIGURE 1Order of appearance of symptoms of diminished autonomy. The bars show how often (proportion)
FIGURE 3Relationship between loss of autonomy and smoking frequency over time. Shown are relative risk (RR) estimates with 95% CIs

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The capacity of SOCS2 to suppress the inhibitory effect of SOCS3 (and other SOCS family members) on cytokine signalling required the SOCS2 SOCS box, and SOCS2 was also shown to

Active psychiatric disorders are associated with daily smoking and progression to nicotine dependence.. (Breslau et

Active psychiatric disorders are associated with daily smoking and progression to nicotine dependence.. (Breslau et

V současné době roste vliv finančních trhů, nejen ve vyspělých ekonomikách, ale i v regionu střední Evropy, kde trhy prošly dlouhou ekonomickou transformací a vykazují

When a smoker stops smoking, the amount of dopamine in their body drops and they experience nicotine withdrawal symptoms.. These withdrawal symptoms include depressed mood,

See Smoke Free WA Health System Policy - Guidelines for the management of nicotine withdrawal and cessation support in nicotine dependent patients.. Smokers who are ready to