The genetic relationship between cannabis and tobacco cigarette use in European- and African-American female twins and siblings
Introduction
According to the most recent estimates from the National Survey of Drug Use and Health, 86.8% of lifetime cannabis users aged 12 and older reported a lifetime history of tobacco cigarette use while 61.7% of cigarette smokers also reported smoking cannabis during their lifetime (Substance Abuse and Mental Health Services Administration (SAMHSA), 2014). Adolescents reporting dual use are more likely to experience problems with both drugs, including rapid escalation to more involved stages of use and difficulty quitting (Agrawal et al., 2008, Peters et al., 2012, Timberlake et al., 2007).
Contributors to the co-occurring use of cannabis and cigarettes include risk and protective influences that shape a general liability to experimentation with multiple substances (Hawkins et al., 1992) as well as influences specific to cigarette and cannabis co-use (e.g., shared route of administration; (Agrawal et al., 2012)). Both genetic and environmental influences play a role in the shared vulnerability to cannabis and cigarette use (Agrawal et al., 2010, Han et al., 1999, Young et al., 2006). One study suggested a genetic correlation as high as 0.75 (Agrawal et al., 2010) between cannabis and cigarette use while another suggested a more modest overlap of r = 0.31 (Young et al., 2006). Environmental contributions on these early stages of substance use can be further parsed into those that make members of twin and sibling pairs similar to each other (i.e., shared environment) and those that are individual-specific, with more robust evidence for the shared influences being correlated than the non-shared (Young et al., 2006). However, a study using a subset of the data from this study showed that in African American (AA) women, the relationship between timing of onset of cigarette smoking and cannabis use was prominently attributable to overlapping individual-specific environmental factors (r = 0.95) (Sartor et al., 2009).
The strong evidence for the heritability of and the co-heritability between lifetime use of cannabis and cigarettes comes almost entirely from international research conducted in twin samples of European origin. In U.S. populations, this is particularly problematic given significant variations in the rates of cannabis and cigarette use across race/ethnicity (Garrett et al., 2008, Griesler and Kandel, 1998, Keyes et al., 2015, Wallace et al., 2003, Wu et al., 2014). Racial/ethnic differences are also particularly pronounced in females with AA adolescent girls and young adult women appearing to be less likely than their European American (EA) counterparts to use cigarettes and cannabis (Garrett et al., 2008, Keyes et al., 2015; SAMHSA, 2014; Wallace et al., 2003). In addition, although cigarette use typically predates cannabis use in EAs, reverse gateways (cannabis before cigarettes/alcohol) are somewhat more common in AAs than EAs (Sartor et al., 2013, Vaughn et al., 2008). Notably, these variations in prevalence and sequence may relate to differing societal attitudes towards cannabis and cigarette use, the relative availability and exposure opportunity of the two drugs as well as to putative differences in biological response to anticipation and receipt of drug-related rewards. For cigarette use, we are only aware of 3 studies, including two by us in the sample under study here, that show that additive genetic factors explain similar proportions of variance (40–50%) in AAs and EAs (Sartor et al., 2009, Sartor et al., 2015, Whitfield et al., 2007). However, in a recent study by our group (Sartor et al., 2015), the remainder of the variance in cigarette use was solely attributable to individual-specific environmental factors (44%) in AA twins while in EA twins, substantial influence of both individual-specific (10%) and shared environmental factors (34%) was noted for cigarette use. Likewise, we have previously reported that timing to cannabis use is heritable in AA female twins (0.52) and that the role of shared environment is limited (Sartor et al., 2009). However, no study to date has examined the bivariate relationship between lifetime use of cannabis and cigarettes in AA and EA twins.
In the current study, we utilize a large, general population sample of adult female twins and non-twin siblings of self-described AA (n = 956) and EA (n = 3557) ancestry to examine the role of additive genetic, shared environmental and individual-specific environmental influences on the covariance between lifetime cigarette and cannabis use and the extent to which the magnitude of their contribution varies across race/ethnicity.
We leveraged a sample of females who are notably understudied in addiction research. Importantly, AA females appear to be at low risk for both cannabis and cigarette involvement, relative to EA females, both during adolescence (Keyes et al., 2015, Wallace et al., 2003) and adulthood (SAMHSA, 2014). Thus, access to related individuals of AA ancestry is a unique aspect of the present study – we are also not aware of other datasets of this magnitude with AA twins. Further, by utilizing a young adult sample, we circumvented concerns regarding lack of adequate opportunity for experimentation with cannabis (Wagner and Anthony 2002).
Section snippets
Participants
The sample was composed of female twins who completed the fourth wave of data collection for the Missouri Adolescent Female Twin Study MOAFTS and female participants from the Missouri Family Study (MOFAM). Data on male twins were not collected in MOAFTS, although male siblings did participate in MOFAM but were not included in the present study.
Substance use
Cigarette use was more common in EAs (75.3%) relative to AAs (64.2%) while cannabis use was marginally, but significantly, more commonly reported by the AA (55.5%) than the EA (52.4%) participants. Cigarette use (mean age at onset ∼14 years) typically preceded cannabis use (mean age at onset ∼17 years) in both racial/ethnic groups (see Table 1). As shown in Table 1, 50.3 and 46.4% of EA and AA participants respectively reported using both substances. While a fair proportion of women reported
Discussion
To our knowledge, this is the first study to examine the role of genetic and environmental influences on cannabis use, and on covariation between cannabis use and cigarette use, separately in EA and AA women. Our study also includes the largest number of AA twins currently available for the study of substance use. We broadly replicated existing racial/ethnic trends in cannabis and cigarette use with one exception in that rates of cannabis use in our sample were comparable, if not marginally
Conflict of interest
AA received peer-reviewed funding and a travel honorarium from ABMRF/Foundation for Alcohol Research prior to 12/31/12. Other authors have no interests to declare.
Role of funding source
This study was funded by grants DA23668and DA32573from the National Institute on Drug Abuse, grants AA017921, AA023549, AA12640, AA017688from the National Institute on Alcohol Abuse and Alcoholism, grant HD049024from the National Institute of Child Health and Human Development, and a grant from the Robert E. Leet and Clara Guthrie Patterson Trust. There are no contractual constraints on publishing the research being reported. Funding sources were not involved in any aspect of this submission.
Contributors
AA, JDG and CS conceived of analyses, conduct all analyses and prepared the first and all revised drafts. MTL provided critical feedback on cannabis data and PAFM provided similar feedback on tobacco data. KKB and ACH, along with PAFM collected MOAFTS and MOFAM data. ACH consulted on analyses. KKB provide key insights into study of ethnic variation for substance use. All authors have participated in manuscript preparation and approved the final submission.
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