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Apr 25, 2012 - Secondhand smoke exposure and osteoporosis in never-smoking postmenopausal women: the Fourth Korea National Health and Nutrition ...
Osteoporos Int (2013) 24:523–532 DOI 10.1007/s00198-012-1987-9

ORIGINAL ARTICLE

Secondhand smoke exposure and osteoporosis in never-smoking postmenopausal women: the Fourth Korea National Health and Nutrition Examination Survey K. H. Kim & C. M. Lee & S. M. Park & B. Cho & Y. Chang & S. G. Park & K. Lee

Received: 6 October 2011 / Accepted: 26 March 2012 / Published online: 25 April 2012 # International Osteoporosis Foundation and National Osteoporosis Foundation 2012

Y. Chang Department of Family Medicine, Seoul Red Cross Hospital, Seoul, South Korea

Introduction This study aimed to assess the association between SHS and postmenopausal osteoporosis. Methods Of 2,067 postmenopausal women (age, ≥55 years) participating in the Fourth Korea National Health and Nutrition Examination Survey, 925 never-smokers identified through interviews and urinary cotinine level verification were enrolled. Cross-sectional relationships between self-reported SHS exposure and osteoporosis of the lumbar vertebrae and femoral neck (defined using the World Health Organization T-score criteria) were investigated by bone densitometry. Results Participants having actively smoking family members showed increased adjusted odds ratio (aOR) for femoral neck osteoporosis compared with participants not exposed to SHS (aOR, 3.68; 95 % confidence interval [CI], 1.23–10.92). Participants whose cohabitant smokers consumed any number of cigarettes per day showed increased occurrences for lumbar and femoral neck osteoporosis compared with the nonexposed group. Participants whose cohabitant smokers consumed ≥20 cigarettes/ day showed increased aORs for lumbar (aOR, 5.40; 95 % CI, 1.04–28.04) and femoral neck (aOR, 4.35; 95 % CI, 1.07–17.68) osteoporosis compared with participants not exposed to SHS. Conclusions In postmenopausal never-smoking Korean women, exposure to SHS was positively associated with osteoporosis. This finding further emphasizes a need to identify vulnerable groups exposed to SHS to increase bone health.

S. G. Park Department of Family Medicine, Haeundae Paik Hospital, Inje University College of Medicine, Pusan, South Korea

Keywords Bone mineral density . Environmental smoke . Osteoporosis . Passive smoking . Postmenopause . Secondhand smoke

Abstract Summary The association between secondhand smoke (SHS) exposure and lumbar and femoral neck osteoporosis was assessed in postmenopausal never-smoking Korean women. The presence of family members who actively smoked was associated with femoral neck osteoporosis. The number of cigarettes consumed by cohabitant smokers was positively associated with lumbar and femoral neck osteoporosis.

K. H. Kim and C. H. Lee contributed equally to this work as first authors. K. H. Kim : S. M. Park : B. Cho Department of Family Medicine, Seoul National University Hospital, Seoul National University College of Medicine, Seoul, South Korea C. M. Lee Department of Family Medicine, Healthcare System Gangnam Center, Seoul National University Hospital, Seoul National University College of Medicine, Seoul, South Korea

K. Lee (*) Department of Family Medicine, Seoul National University Bundang Hospital, Seoul National University College of Medicine, 82, Gumi-ro 173beon-gil, Bundang-gu, Seongnam-si, Gyeonggi-do 463-707, South Korea e-mail: [email protected]

Introduction Many epidemiological and biological studies have found that active smoking or firsthand smoking is one of the major

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behavioral risk factors for osteoporosis. Active smokers display not only a 4 % reduction in bone mineral density (BMD) compared with nonsmokers [1] but also a BMDindependent increased risk for fractures [2]. Nicotine, the most characteristic component of tobacco, is known to inhibit the formation of bone [3], and polycyclic aromatic hydrocarbons, benzopyrene, and 7,12-dimethylbenzanthracene are known to decrease bone mass and strength [4]. From an endocrinological perspective, tobacco smoke is reported to have antiestrogenic effects [5] and is also associated with low serum 25-OH vitamin D3 levels and low calcium absorption [6]. Furthermore, menopause in female smokers has been reported to occur up to 2 years earlier than that in nonsmokers [7]. Secondhand tobacco smoke (SHS) can be defined as “the smoke emitted from the burning end of a cigarette or from other tobacco products usually in combination with the smoke exhaled by the smoker” [8]. According to several toxicological reports, inhaled sidestream smoke, the main component of SHS, is approximately three times more toxic and two to six times more carcinogenic per gram than mainstream smoke [9]. Although SHS exposure has been shown to be associated with a multitude of diseases worldwide [10], including certain cancers [11, 12], cardiovascular diseases [13], and respiratory diseases [14], little is known about the effect of SHS on bone metabolism. One animal study demonstrated that SHS-exposed rats had small osteocytes, fewer osteoblasts and marrow cells, and black carbon dust-like substances in their bones [15]; another animal study found that SHS inhibited bone formation and increased bone resorption [16]. Some cross-sectional human studies have found an association between SHS exposure and decreased BMD [17, 18]. One of these studies included active smokers, however, and though the authors controlled for multiple risk factors, including smoking habits, the inclusion of active smokers could be a possible confounder [17]. Furthermore, these studies used questionnaire responses instead of biomarkers to distinguish neversmokers from active smokers, and the daily exposure duration or intensity of SHS was not thoroughly evaluated [17, 18]. Thus, to evaluate the effect of SHS exposure on BMD without potential confounding by active smoking, our study included only neversmokers who were verified through both interviews and urinary cotinine concentration—the gold standard measure [19]. We then investigated the association between SHS exposure and lumbar and femoral neck BMD in postmenopausal women using data from the Fourth Korea National Health and Nutrition Examination Survey (KNHANES IV).

Osteoporos Int (2013) 24:523–532

Korean general population and included comprehensive information on the health status, health behaviors, and sociodemographic characteristics of 20,277 individuals in 600 national districts. A stratified multistage probability sampling design was used. The population was selected via proportional allocation based on the 2005 Korean Population and Housing Census using multistage stratified cluster random sampling procedures stratified to gender, age, regional area, and type of residential area. The KNHANES survey consisted of four stages: (1) selection and recruitment of a representative sample of civilians, (2) performance of the Health Interview Survey and Health Examination Survey at mobile examination centers (MECs), (3) performance of the Health Nutrition Survey within 2 weeks after the completion of the Health Examination Survey, and (4) mailing the test results to the subjects within 2 weeks after the end of the survey. The KNHANES IV Health Interview Survey, including the survey of SHS exposure, was conducted through face-to-face interviews at MECs by trained interviewers and the Health Nutrition Survey, including the survey of dietary calcium intake, was also conducted by trained nutritionists using face-to-face interviews at the homes of the subjects. Informed consent was given by each participant before inclusion in the study [20]. The unit nonresponse rate of the KNHANES survey was 22.2 % in 2008 and 17.2 % in 2009. The item nonresponse rates of the SHS exposure survey and the BMD test were 1.39 and 3.14 % in 2008 and 0.40 and 3.36 % in 2009, respectively [21]. Initial candidates for this study included 2,067 postmenopausal women. We selected women aged ≥55 years because physiologic menopause occurs around age 50 for women in Korea [22] and postmenopausal bone loss is known to occur largely during the first 5 years of menopause [23]. The initial candidates included subjects who had completed the SHS survey and had complete BMD and urinary cotinine concentration measurements. We excluded current and past smokers, who were identified through interviews, and suspected current smokers, who were those with a urinary cotinine concentration above 100 ng/mL [19, 24]. To reduce the number of confounders that might influence BMD, we excluded participants who were taking medications for the treatment of osteoporosis. Finally, a total of 925 subjects were included in this study. As the survey data analyzed are publicly available, this study was exempt from review by the Institutional Review Board. Self-reported SHS exposure and urinary cotinine measurements

Materials and methods Study population Eligible participants are shown in Fig. 1. The KNHANES IV (2008–2009) was a nationwide survey representing the

At MECs, trained interviewers administered a standardized questionnaire. The education and quality control of the interviewers have been reported elsewhere [20]. Interviewers asked subjects about active and passive smoking status. Lifetime never-smokers were defined by the World

Osteoporos Int (2013) 24:523–532 Fig. 1 Flow diagram of inclusion or exclusion of study participants. Asterisks defined using the WHO criteria. KNHANES IV Fourth Korea National Health and Nutrition Examination Survey

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Health Interview Survey and Health Examination Survey of KHANES IV N = 20277

Men (N = 9213) Not in postmenopausal status (N = 8491) Age < 55 years (N = 506)

N = 2067

Participants who did not receive a dualenergy x-ray absorptiometry scan (N = 61) Participants who did not respond to the secondhand smoke interview (N = 9) Participants whose urinary cotinine was not measured (N = 395)

N = 1602

Current smokers (N = 56)* Suspected current smokers with a urinary cotinine level of ≥100 ng/mL (N = 13) Past smokers (N = 74)*

N = 1459

Participants using anti-osteoporotic medications (N = 534)

Study population N = 925

*Defined using World Health Organization criteria. KNHANES IV, Fourth Korea National Health and Nutrition Examination Survey.

Health Organization (WHO) as those who had not smoked more than 100 cigarettes nor used any other tobacco products in their lifetimes. Current smokers were defined as those who had smoked at least 100 cigarettes in their lifetimes and who currently smoked, and past smokers were defined as those who had smoked at least 100 cigarettes and had ceased smoking prior to the interview [20]. Both current and past smokers were excluded. Self-reported SHS status was assessed among lifetime never-smokers. Interview questions included the duration of workplace exposure over 1 day (0, >0 to 0 to 0 to 0 to