Nicotine & Tobacco Research, Volume 16, Number 7 (July 2014) 923–930

Original Investigation

Familial Aggregation of Tobacco Use Behaviors Among Amish Men Katie L. Nugent PhD1, Amber Million-Mrkva BA2, Joshua Backman BA2, Sarah H. Stephens PhD3, Robert M. Reed MD4, Peter Kochunov PhD1, Toni I. Pollin PhD3, Alan R. Shuldiner MD3, Braxton D. Mitchell PhD3,5, L. Elliot Hong MD1 1Maryland

Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, Baltimore, MD; Program in Epidemiology and Human Genetics, University of Maryland, Baltimore, MD; 3Division of Endocrinology, Diabetes, and Nutrition, University of Maryland School of Medicine, Baltimore, MD; 4Division of Pulmonary and Critical Care Medicine, University of Maryland School of Medicine, Baltimore, MD; 5Department of Veterans Affairs, Veterans Affairs Medical Center, Baltimore Geriatric Research Education and Clinical Center, Baltimore, MD 2Graduate

Received October 1, 2013; accepted January 13, 2014

Abstract Introduction: Tobacco use is a complex behavior. The Old Order Amish community offers unique advantages for the study of tobacco use because of homogenous ancestral background, sociocultural similarity, sex-specific social norms regarding tobacco use, and large family size. Tobacco use in the Old Order Amish community is almost exclusively confined to males. Methods: We examined characteristics of tobacco use and familial aggregation among 1,216 Amish males from cross-sectional prospectively collected data. Outcomes examined included ever using tobacco regularly, current use, quantity of use, duration of use, and frequency of use. Results: Sixteen percent of Amish men were current tobacco users, with the majority reporting cigar use only. Higher rates of tobacco use were found among sons of fathers who smoked compared with sons of fathers who did not smoke (46% vs. 22%, p < .001) as well as among brothers of index cases who smoked compared with brothers of index cases who did not smoke (61% vs. 29%, p < .001). After controlling for shared household effects and age, heritability accounted for 66% of the variance in ever smoking regularly (p = .045). Conclusions: The familial patterns of tobacco use observed among Amish men highlight the important role of family in propagating tobacco use and support the usefulness of this population for future genetic studies of nicotine addiction.

Introduction Smoking remains the leading cause of preventable medical illness and death in the United States (Danaei et  al., 2009; Mokdad, Marks, Stroup, & Gerberding, 2005). Smoking is a highly heritable behavior, estimated to account for 59% of the variance in persistent use (Li, Cheng, Ma, & Swan, 2003), yet tobacco use is also strongly influenced by environmental factors such as peer and family smoking, education level, racial group membership, socioeconomic status, exposure to advertising, and the price and availability of tobacco products (Bobo & Husten, 2000). The Old Order Amish community presents a useful population to study the environmental and genetic determinants of smoking behavior, due to their relatively homogeneous demographic and sociocultural practices and characteristics, their societal stance on tobacco use discouraging tobacco use in women, and the availability of

families with a large number of members. The Old Order Amish communities in the Lancaster, PA, area share a common ancestry with few founders. Amish place a high importance on family life and helping others; thus, there is less disparity in wealth across families. Amish life is greatly influenced by the Ordnung, which are sets of rules outlining behaviors permitted in the Amish community. Within the Amish communities, as dictated by the Ordnung, school is finished after the completion of 8th grade; therefore, there are minimal differences in education level. Many Amish farmers in Lancaster County grow tobacco as an economic crop, and sometimes smoke it as well. The Ordnung also includes rules pertaining to the use of tobacco. There is variation between church districts with use being more acceptable in Old Order versus New Order subgroups (Fuchs, Levinson, Stoddard, Mullet, & Jones, 1990), but most church leaders discourage tobacco use. Pipe and cigar smoking are more accepted than use of cigarettes, and use by

doi:10.1093/ntr/ntu006 Advance Access publication February 28, 2014 © The Author 2014. Published by Oxford University Press on behalf of the Society for Research on Nicotine and Tobacco. All rights reserved. For permissions, please e-mail: [email protected].

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Corresponding Author: Katie L. Nugent, PhD, Maryland Psychiatric Research Center, Department of Psychiatry, University of Maryland School of Medicine, PO Box 21247, Baltimore, MD 21228, USA. Telephone: 410-402-6859; Fax: 410-402-6023; E-mail: [email protected]

Familial aggregation of tobacco use behaviors among Amish men

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effects. We hypothesized that those who still use tobacco in this population may represent individuals who have a strong family-based predisposition to smoke, stemming from genetic and/or intrafamily social influences.

Methods Sample We examined data collected on 2,647 Amish individuals from Lancaster, PA, who had previously participated in health surveys carried out by researchers from the University of Maryland. Tobacco use behaviors were obtained by questionnaire from participants of seven studies of cardiovascular and metabolic health (Horenstein et al., 2013; Mitchell et al., 2008; Post et  al., 2007; Sorkin et  al., 2005; Zupancic et  al., 2012). These projects recruited participants through word of mouth, advertisements, community-wide mailings, referrals from local physicians, and from previous participation in one of the clinic’s studies. In each project, participants filled out a survey that characterized their tobacco use habits. Tobacco use in women is strongly discouraged among the Amish, and indeed, out of 1,431 females included in the sample, only 8 reported ever using tobacco regularly (0.6%). Therefore, all subsequent analyses included only the male participants. Tobacco Use Phenotypes Demographic information, including date of birth, sex, education, marital status, occupation, and body mass index (BMI) were collected from a uniform intake questionnaire across the seven studies. In the questionnaire, participants were also asked an initial question and then four follow-up questions about their use of tobacco: (a) “Since age 20, have you ever used tobacco regularly?”, (b) “How old were you or in what year did you start using tobacco?”, (c) “On average, how many cigarettes/cigars/or pipes did you smoke per day?”, (d) “Do you currently smoke?”, and (e) “In what year or how old were you when you stopped smoking?” Amish may use tobacco experimentally during Rumspringa (a period in an Amish person’s life following the completion of school and before baptism into the church). Thus, the initial question was worded to focus the investigation on regular tobacco use behavior after individuals have become regular members of the Amish community. Amount of cigarettes, cigars, and pipe bowls smoked was recorded individually. Based on the available information, we derived the following tobacco use phenotypes. Specifically, we examined: ever use (yes/no), age at first regular use, current use (yes/no), duration of use, cigarette per day equivalent used, and number of daily tobacco use sessions. Based on the number of cigarettes, cigars, and pipes participants reported using per week, we calculated a CPD Equivalent value. This was an attempt to match the highly variable types of tobacco use methods in the Amish to the currently accepted quantification for smoking addiction in the general population, the CPD. Assuming that a typical manufactured cigarette contains 11 mg of nicotine per cigarette (Tobacco Advisory Group of the Royal College of Physicians, 2007), the following values were utilized to convert small cigars and tobacco pipe bowls smoked into CPD equivalents. Typically small cigars contain, on average, 9.8 mg of nicotine; thus, 0.891 cigarettes is

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older men may be more accepted than use by younger men. Women are not allowed to smoke although it was occasionally overlooked for some older women as long as it was not done openly (Hostetler, 1993). Only a few small studies have reported on tobacco use among the Amish. A study of 134 Amish from Holmes County, Ohio, found current tobacco use rates to be 17.6% among men and 0% among women (Ferketich et  al., 2008). That study also measured a nicotine metabolite and found no discrepancy between self-report of tobacco use and biomarker confirmation. This supports the validity of self-report of tobacco use in the Amish. These rates are lower than the general U.S.  adult population, of which 34% of adult males are estimated to be current tobacco users (Falk, Yi, & Hiller-Sturmhofel, 2006). Genome-wide and candidate gene association studies have identified several genes associated with various measures of smoking behavior, such as age at initiation (Schlaepfer et al., 2008; Vink, Posthuma, Neale, Slagboom, & Boomsma, 2006), cigarettes per day (CPD; (Berrettini et  al., 2008; Caporaso et al., 2009; Saccone et al., 2010; Thorgeirsson et al., 2010), nicotine dependence (Broms et al., 2012; Greenbaum & Lerer, 2009; Li et al., 2007; Loukola et al., 2013; Sullivan et al., 2004), and severity of withdrawal (Swan et al., 2006). However, the variants of even the most robust candidates currently identified to be associated with smoking exhibit only small effects, explaining only a small fraction of the total variance of the behavioral trait. Given the high heritability of smoking, estimated to account for 59% of the variance in persistent smoking behavior in male adults (Li et al., 2003), much of the genetic variants contributing to this complex addiction phenotype have yet to be discovered. Shared environmental factors may play an important role. In terms of the effect of family, persistent smoking by parents is associated with greater frequency of use in children (Melchior, Chastang, Mackinnon, Galéra, & Fombonne, 2010). Children who observe parental tobacco use may come to view tobacco use as a normal and desirable behavior (Bantle & Haisken-DeNew, 2002; Laffert, 1998) and also may receive positive reinforcement for engaging in this behavior themselves (Bandura, 1977). Conversely, parental disapproval of smoking (even in the face of parental smoking) has been shown to influence initiation and quit behaviors (Jackson & Henriksen, 1997). Several twin studies of tobacco use have found that shared environmental factors contribute as much or even more to susceptibility to (or quantity of) tobacco use compared with genetic factors (Kendler & Gardner, 1998; Koopmans, Slutske, Heath, Neale, & Boomsma, 1999; Madden et  al., 1999). Within-family concordance is strongest for siblings less than 2  years apart in age, with older siblings having a greater influence on younger siblings (Boyle, Sanford, Szatmari, Merikangas, & Offord, 2001). These findings can in part be explained by genetics but are also highly suggestive of the influence of more similar familial environmental factors including access to tobacco, role modeling, and environmental pressures (Boyle et al., 2001). The Old Order Amish provide a unique opportunity to examine the importance of family in propagating tobacco use behaviors. The Amish are a very family-oriented community. Their limited contact with the non-Amish population minimizes outside influences on tobacco use. Additionally, their relatively uniform education and social background likely decrease the environmental influences on tobacco use behavior, perhaps increasing the likelihood of detecting family-based

Nicotine & Tobacco Research equivalent to one small cigar. Typically one pipe bowl contains, on average, 57.75 mg of nicotine (Wald, Idle, Boreham, Bailey, & Van Vunakis, 1984); therefore, 5.25 cigarettes is equivalent to one pipe bowl. We also examined daily smoking frequency as a means of quantifying use, recognizing that it is difficult to compare across cigars, pipes, and cigarettes due to variations in nicotine content and smoking style. Chewing tobacco was included in all analyses except those involving quantitative tobacco use as the amount used was not ascertained. Data Analyses

Smoking Behaviors Demographics including tobacco use are presented in Table 1. Among the 1,216 men in the sample, 42.7% reported ever having used any tobacco. Increasing age (p < .001) and greater BMI (p < .001) at the time of the interview were independently associated with ever use, whereas neither marital status nor occupation was associated with ever use. Of the 519 people who reported ever using tobacco, 442 were smokers of tobacco products and 77 used smokeless tobacco only. In multivariate analysis, increasing age at the time of the interview was significantly associated with lower odds of current use (Odds ratio = 0.91, 95% confidence interval [CI] = 0.85–0.97 for a 5-year change in age). Marital status, occupation, and BMI were not significantly associated with current use. While 41% of smokers who reported ever use remained current users, only 17% of persons who reported using only nonsmoking forms of tobacco continued to use (p 35)

aData

on current use was not ascertained for 4 smokers and 11 nonsmoking tobacco users; these 15 people were removed from the denominator when calculating current use. bData only available for 983 persons. *Significant difference in use by characteristic, p < .05.

Table 2.  Tobacco Use Characteristics in Males By Tobacco Product Used

Variable Proportion ever using specified type, n = 479 Proportion of ever users currently using, n = 468 Self-reported age at first regular use (years)a, n = 459 Duration of use (years)a, n = 412 CPD equivalent useda, n = 402 Number of daily tobacco use sessionsa, n = 479 aMean

Cigars only

Cigarettes only

Pipes only

Chewing tobacco only

More than one tobacco type

p value for difference between groups

48.2%

23.0%

5.0%

16.1%

7.7%



52.8%

28.2%

50%

15.2%

16.2%

17.4 (3.4)

16.8 (2.1)

17.2 (2.3)

18.4 (3.6)

16.1 (1.3)

Fisher p < .001 .002

27.2 (13.9) 2.8 (3.8) 3.2 (4.3)

17.9 (12.7) 11.2 (13.4) 11.2 (13.4)

31.5 (15.8) 18.7 (15.2) 3.6 (2.9)

18.4 (12.6) N/A N/A

24.9 (13.9) 18.7 (28.2) 13.0 (22.4)

Familial aggregation of tobacco use behaviors among Amish men.

Tobacco use is a complex behavior. The Old Order Amish community offers unique advantages for the study of tobacco use because of homogenous ancestral...
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