Tobacco Use, Women, Gender, and Chronic Obstructive Pulmonary Disease Are the Connections Being Adequately Made? Lorraine J. Greaves1 and Lindsay A. Richardson1 1

British Columbia Centre of Excellence for Women’s Health, Vancouver, British Columbia, Canada

This article reflects on a multidisciplinary workshop addressing the evidence pertaining to tobacco use, sex, gender, and chronic obstructive pulmonary disease (COPD). In preparation, a literature review was conducted that examined the academic and gray literature on tobacco, COPD, and gender and women, with a view to assessing if and how these literatures spoke to each other. These materials were discussed in a sponsored workshop (Toward a Research Agenda on Gender and Chronic Obstructive Pulmonary Disease) held in Vancouver, Canada, in 2007, engaging a variety of scientists and stakeholders in assessing the issues and emergent questions. The goal of this workshop was to foster the advancement of a research agenda that more tightly links tobacco, COPD, and lung health and that reflects and investigates sex and gender issues, especially in reference to the growing rates of COPD among women. A research agenda for consideration by researchers in the fields of women’s health, medicine, tobacco use, COPD, and related fields is offered. Keywords: respiratory disease; gender; women; tobacco use

It is projected that the rates of chronic obstructive pulmonary disease (COPD) among women will surpass those of men in about 10 years (1). Because tobacco use is a key cause of COPD and because women’s rates of tobacco use have typically lagged behind and peaked later than men’s, it is not surprising that we are now seeing higher rates of COPD among women. In addition, COPD often takes some years to emerge, delaying the obvious impact of women’s increased tobacco use on the emergence and rates of COPD. There are, however, sex and gender patterns that reflect important differences in the size of the problem of COPD in women and its particular characteristics. Although the terms ‘‘sex’’ and ‘‘gender’’ may at times be incorrectly used interchangeably or used differently by different disciplines (2), they have distinct meanings. Sex refers to biologically based characteristics, factors, and processes such as metabolism, physiological processes, hormones, or anatomic characteristics, whereas gender refers to social, cultural, and economic factors that differentially affect females and males, such as income adequacy, caregiving responsibilities, interpersonal power dynamics, occupational roles, or domestic responsibilities. Although distinguishing between these concepts is understood to enhance all health research (3), it is especially relevant to the study of COPD given the mix of factors affecting the etiology and progress of COPD. Notwithstanding the

(Received in original form June 27, 2007; accepted in final form August 16, 2007) Supported by Canadian Institutes for Health Research (CIHR) through the ICEBERGS group and by the Canadian Tobacco Control Research Initiative (CTCRI), Health Canada. Correspondence and requests for reprints should be addressed to Lorraine Greaves, Ph.D., British Columbia Centre of Excellence for Women’s Health, E311-4500 Oak Street, Box 48, Vancouver, BC V6H 3N1, Canada. E-mail: [email protected] Proc Am Thorac Soc Vol 4. pp 675–679, 2007 DOI: 10.1513/pats.200706-079SD Internet address: www.atsjournals.org

progress in understanding the respective importance and impact of sex and gender, there remain considerable challenges in measurement (3), particularly with respect to accurately assessing the impact of gender (4). Despite these challenges, it is important to approach the examination of COPD using these concepts. For example, not only is the highest rate of increase in hospitalizations and deaths from COPD among women, but women are more likely to develop COPD at an earlier age and to have a more severe expression of the disease than men (8). Precise reasons for these differences are unknown. Further, the extent to which they reflect the interaction of sex differences (biological, genetic, and/or physiological characteristics) and gender influences (social, cultural, or economic issues) is also largely unexplored. For these reasons, improving research, treatment, health information, and policy development with respect to COPD and making sure all of these initiatives and activities are sex and gender informed and sensitive is of critical importance if we are to better understand and respond to the growing problem of COPD in women.

BACKGROUND COPD is a set of respiratory diseases that are often tobacco related and characterized by a gradual but relentless increase in breathing difficulty and severe disability. Active cigarette smoking is the primary cause of COPD (6), and passive smoking may also be an important cause of COPD (7). COPD is the fourth leading cause of death in Canada and is expected to become the third leading cause in the next decade (5). Tobacco use represents the single largest preventable cause of death and disease in Canada. The 2004 U.S. Surgeon General’s report (6) identifies more than 20 diseases and adverse health effects for which smoking is identified as a cause, including cancers, reproductive effects, cardiovascular diseases, and respiratory diseases. There are numerous sex and gender issues connected to the study of COPD and tobacco use. One of the key findings reported is that, given the same amount of exposure to tobacco smoke, women are more likely to develop severe, early-onset COPD than men (8). However, gender-related issues in the development, diagnosis, and treatment of COPD are likely to be confounding factors in these studies (9–11). For example, historical differences in the type of cigarettes smoked by women (12) and women’s exposure to passive smoke may be factors in their development of lung diseases and conditions. Within the vast body of literature on tobacco and the growing evidence regarding sex and gender issues in the development of smoking-related diseases such as COPD, there are relatively few studies that focus on the specific intersections between and among COPD, gender, and tobacco. The reasons for this are not clear, but this gap likely has had an impact on the gray literature (reports and non–peer-reviewed materials often produced by nongovernmental agencies or health charities) in the COPD and tobacco arenas. In this sense, a gap in the academic literature will have an ongoing influence on the

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knowledge transfer to clinicians or patients and to tobacco policy and program designers and their constituents. This gave rise to several questions that this article addresses and that focused our review and discussion: (1) What does the academic literature say about COPD, tobacco/smoking, and sex and gender? (2) What does the COPD gray literature say about tobacco/smoking and gender? and (3) What does the tobacco policy documentation (especially in Canada) say about COPD and gender? This article reflects on the findings of a literature review that examined academic and gray literature on tobacco, COPD, gender, and women, with a view to assessing if and how these literatures spoke to each other. These materials were discussed in a sponsored workshop engaging a variety of scientists and stakeholders in assessing these issues, results, and emerging questions. The goal of this workshop was to foster the advancement of a research agenda that more tightly links tobacco, COPD, and lung health that reflects and investigates sex and gender issues. The results of these discussions are offered here in the form of a research agenda for consideration by researchers in the fields of women’s health, medicine, tobacco use, COPD, and related fields, with some additional policy recommendations that emerged from workshop discussions.

WHAT DOES THE ACADEMIC LITERATURE SAY ABOUT COPD, TOBACCO/SMOKING, AND SEX AND GENDER? Sex, gender, and tobacco use influence the pathology of COPD (8, 13). The rise in prevalence rates among women has been largely attributed to increases in smoking (8), which reflects the differences in smoking patterns and trends between males and females (5). It seems that these differences can be attributed to sex-based characteristics (14) and gender influences. Further complicating the situation is the fact that gender and sex interact to influence the development of lung disease (15, 16). There is some research on sex differences in the development of COPD related to tobacco use (8, 13). One of the key findings reported is that, given the same amount of exposure to tobacco smoke, women are more likely than men to develop severe, early-onset COPD (8). The impact of tobacco depends on biological (e.g., sex, age, and genetics) and behavioral (e.g., mode of smoking and intake of other toxins) factors (17). Women’s lungs are smaller than men’s and require less exposure to nicotine to produce negative effects (17). Due to underlying sex differences in lung anatomy and physiology, women experience different development of lung disease than men (14). Gender may interact with underlying sex differences in lung anatomy and physiology, and these sex differences may influence the development of lung disease (14–16). For example, girls and boys of the same age may be at different stages of physical maturation and express different vulnerabilities to exposures. Thus, early smoking may have a greater negative impact on the growth of lung function among girls (19). These sex and gender issues need to be considered before concluding that women are more susceptible to COPD than men. Gender-related issues in the development, diagnosis, and treatment of COPD are likely to be confounding factors in these studies (9, 10). For example, historical differences in the type of cigarettes smoked by women and women’s exposure to passive smoke may be factors in their development of lung diseases and conditions (20). There is a possibility that gendered products, such as the ‘‘light’’ cigarettes developed and marketed specifically to women (21), are more deeply inhaled and smoked more intensely, have higher yields of nitrosamines, and are responsible for the increase in lung cancer in women (20).

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Passive smoking (or environmental tobacco smoke) endangers women’s health and is a possible link to COPD (7). This is particularly pertinent for women in developing countries where women’s rates of smoking have traditionally been low and may still be low (22) and where women are exposed to biomass fuels in the course of preparing meals (23). These are additional factors that need to be taken into consideration in teasing apart the influence of sex and gender on women’s development of COPD along with the influence of secondhand smoke and/or active smoking and/or exposure to biomass fuels. Lower socioeconomic (SES) individuals (women and men) are more likely to smoke and to live in areas with higher air and water pollution, which has been suggested to contribute to the development of COPD (24). However, more women than men are low SES, generally having lower income adequacy than men, so low SES is a gendered influence on smoking and exposure to pollution, particularly, but not only, in developed countries. There has been research focusing specifically on gender and COPD with respect to diagnostics, lived experience, and smoking behavior. There is a gender bias in diagnosis of the disease (23), with men more likely to be diagnosed with COPD than women with the same symptoms. Other studies have also explored the gender differences in men’s and women’s experience of the disease because women diagnosed with COPD tend to experience a lower quality of life (25–27) and are less likely to present at emergency departments after the exacerbation of symptoms (28). There are also some studies that focus on the effect of a COPD diagnosis on men’s and women’s smoking patterns (29) and the importance of tailoring smoking cessation interventions by gender for men and women at risk of COPD (30). As outlined by Joseph and colleagues (29), men are more likely to reduce cigarette consumption after diagnosis than women. However, women were more likely to reduce cigarette consumption on their own. Some studies have explored the forms of discrimination that people with COPD regularly experience. Physicians do not administer spirometric tests as readily to women as they do to men (31). Doctors fail to take ‘‘smokers cough’’ seriously; some physicians and pulmonologists tend to see COPD as a ‘‘selfinflicted’’ disease wherein people have brought their ill health upon themselves by smoking (31–33). Aside from physiological sex differences that might give rise to COPD, patterns of tobacco use are also strongly gendered. In countries such as Canada, Australia, the United States, and the United Kingdom, smoking patterns are influenced by a variety of factors including gender norms and responsibilities, gendered reasons for smoking, and tobacco marketing practices, all ultimately contributing to the development of COPD. Traditional gender roles create expectations about genderappropriate behavior, which can influence smoking uptake, maintenance, and cessation (34, 35). For example, as Amos and Bostock (36) note, a wide range of factors influence why young people start and continue to smoke. Personal characteristics (e.g., attitudes, beliefs, and self-esteem); interpersonal relationships (e.g., family and friends who smoke); and the wider social, cultural, and environmental environment (e.g., social norms, tobacco marketing, and access to cigarettes) all have an influence. However, these factors are also gendered. Concerns about body image, weight management, self-esteem, and affect management are particularly influential among girls (36). Gender differences in smoking patterns carry on into adulthood. According to Greaves (37), women smoke to organize social relationships, create an image, or control emotions. Moreover, women state that smoking is a source of support, predictability, and control: smoking is seen as a something that

Greaves and Richardson: Tobacco, Gender, and COPD

is reliable and consistent. On the other hand, men’s tobacco use may signify and reflect their independence, physical resilience to harmful substances, and capacity to endure risk-taking (38). It is also noted that men smoke for the enjoyment of the habit and because it provides them with something to do (39). They are less likely to smoke as a result of stress, depression, or anxiety (36, 39). Berlin and colleagues (40) highlight many of these differences in their study examining gender smoking patterns and dependence.

WHAT DOES THE COPD GRAY LITERATURE SAY ABOUT TOBACCO/SMOKING AND GENDER? We examined two Canadian reports and one Australian report to determine how COPD as a women’s health issue is addressed in the gray literature. The Canadian Lung Association’s COPD: A National Report Card (31) provides no further discussion of gender- or sex-related issues in tobacco use and/or the experience of COPD. Two other reports, one from Canada and one from Australia, discuss tobacco use and gender. The key report Respiratory Disease in Canada (1) acknowledges that tobacco use is the most important preventable risk factor for chronic respiratory diseases but also provides a more detailed discussion of the gender and sex differences in tobacco use and COPD. The report suggests that the earlier diagnosis of females may be due to sex differences in the response to the harmful components of tobacco smoke and gender influences that influence women’s and men’s health-seeking behaviors. The report also posits that the increase in smoking among women after World War II may be partly responsible for the growing number of diagnoses among women of middle age. The report discusses differences in mortality and morbidity among men and women and the growing numbers of women hospitalized with COPD, which again is attributed to historical changes in gendered smoking patterns over the course of the 20th century. The report recognizes that given the increase in COPD diagnoses among women, because a higher proportion of older women live alone, ‘‘the need for home care, supportive housing and other community services will increase’’ in the future (p. 54). A report on COPD produced by the Australian Lung Foundation (41) briefly considered the gender implications of the increase in COPD diagnoses among women. It recognizes that the increasing prevalence of COPD in women who are widowed means that the burden of care is falling increasingly on extended family or community services. In short, the gray literature focused on COPD is inconsistent in its approach and emphasis on naming tobacco use, and specifically women’s tobacco use and/or sex and gender issues, as key to understanding the current trends in COPD.

WHAT DOES THE TOBACCO POLICY DOCUMENTATION SAY ABOUT COPD AND GENDER? Despite the fact that tobacco use is the primary cause of COPD and despite the important gender- and sex-related differences in COPD and tobacco use, these facts are rarely considered in tobacco control policies and policy documentation. Three Canadian strategies and the key U.K. and U.S. tobacco documents were examined as a case in point. In Canada, the federal Tobacco Control Strategy: A Framework for Action (42), with its four pillars of protection, prevention, cessation, and harm reduction, does not mention sex or gender, nor are the specific health effects of tobacco use discussed. The national strategy outlined in New Directions for Tobacco Control in Canada (43) is similarly based on four

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pillars, although a slightly different four: prevention, cessation, protection, and denormalization. Denormalization seeks to encourage the view that tobacco use is an antisocial and an undesirable behavior (44). The national strategy also outlines the health effects of tobacco use, although it focuses on ischemic heart disease and cancers, with ‘‘respiratory diseases’’ mentioned only in passing. However, unlike the federal strategy, it recognizes gender and other differences in tobacco use, particularly the high rates of tobacco use among teenage girls and aboriginal people. Although the strategy highlights the importance of tailoring interventions for aboriginal people, the importance of gender-appropriate interventions is not discussed. The First Nations and Inuit Tobacco Control Strategy (45) identifies the need for aboriginal population–specific tobacco control strategies, with gender mentioned only as it pertains to pregnant women. Pregnant women and youth are identified as the target populations who will be given special emphasis; however, despite the extremely high rates of smoking among aboriginal teenage girls, a specific gender focus in not mentioned in relation to the targeted youth. Two key tobacco-focused documents on the health effects of cigarette smoking and environmental tobacco smoke similarly fail to discuss COPD or sex and gender. A key U.K. report produced by the Scientific Committee on Tobacco and Health (46) does not discuss COPD or the role that sex and gender play in any aspect of tobacco-related disease. Although the U.S. Surgeon General’s report (7) highlights the connection between smoking, passive smoking, and COPD, it indicates only that the rate of COPD is higher in women than in men and describes the link between COPD and low SES. There is no further discussion of the implications of these findings. The other portion of the discussion of COPD focuses on the different ways COPD can be measured (e.g., self-reports via symptoms and physician’s diagnosis, physician diagnosis via hospitalization and mortality, and spirometric criteria). Despite the growing body of evidence that women are underdiagnosed with COPD, there is no discussion on this point. This section of the report concludes with an assertion of the need for further research, which lies in examining ‘‘the types and magnitude of risk for adverse respiratory health effects caused by exposure to secondhand smoke’’ (p. 563). Although this recommendation does not include mention of any other population health indicators, such as sex or gender, it does leave the areas of further study open to include other significant factors in its reference to ‘‘the types and magnitude of risk.’’

DISCUSSION Despite the fact that tobacco use is the primary cause of COPD and despite the important gender- and sex-related characteristics affecting COPD and tobacco use, these factors are rarely considered concurrently in the academic or gray literature. This lack of intersection and interaction emerges as a key theme in our analysis of these bodies of literature, policy documents, and strategies. This creates gaps in the knowledge bank regarding women, tobacco, and COPD, which contributes to a lack of direction or support for tackling these three components in a coordinated and evidence-based fashion. We speculate that this creates deficiencies not only in treatment and research but also in the quality of the information made available for patients, women, and the general public. When these materials were digested by the workshop participants, discussion focused on developing a more progressive research framework and identified some key priorities for action to fill this knowledge vacuum. Participants also contributed their own views and impressions of the intersections of

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gender, sex, tobacco, and COPD, especially as it pertains to women. A key theme of these contributors was a perception that the denormalization of smoking had led to increased stigma for the remaining smokers in the population and less empathy for those with smoking-related diseases. There was speculation on the level of internalization of these feelings by smokers with COPD and how this may or may not contribute to treatmentseeking delays and other consequences. First, a framework for researching COPD, women, and tobacco was developed. The development of enhanced measures of a variety of factors ranging from accurately assessing nicotine dependence in a sex-specific manner to measuring and documenting ethical issues in negative diagnostic practices or practitioner attitudes was identified as a critical need. Enhanced methods were suggested as a key shift in the research on these issues. Qualitative and quantitative methods were recommended to improve the data collection and measurement of the interactivity between sex, gender, tobacco, and COPD. In addition, research into ethical practices was suggested to further illuminate the clinical and other responses to the growing population of women with COPD. Methods of involving patients in research, including action research (i.e, research with the goal of bringing together action and reflection, theory, and practice in participation with others [47]), narrative and ethnographic research, and related approaches were suggested to more fully contextualize the situation of women with smoking histories who have COPD, focusing more closely on their lived experience. Transdisciplinary research was suggested as a more appropriate framework for addressing the constellation of sex, gender, tobacco use, and COPD. The development of common approaches, collaborative teams, and a common language for addressing these issues and enhanced communication between disciplines was encouraged. In terms of specific research topics, the group recommended a research agenda that focuses on Health Care Practitioners, Patient Voice and Experience, Specific Sub-Populations, Language/ Discourse, and Denormalization of Tobacco. Participants were asked to rank the areas of research in order of importance for inclusion in a future research agenda. The areas of research are presented in order, starting with the ones ranked as highest in importance by the participants. The subheadings are examples of specific areas of research that could be done in each theme area. Health Care Practitioners d

d

d d d

d d

Delays to diagnosis of COPD z delayed referrals for spirometry: What are the causes of these delays? Ethics of not providing smoking cessation resources to smokers of low income Gendered patterns of referral to rehabilitation The impact of doctor workload on diagnosis and care Doctor attitude as it relates to diagnostic procedure, gender, and referrals—a probability sample stratified by workload (could also consider doctor’s gender) Integration of smoking cessation into practice The quality and effect of the patient–doctor relationship

Patient Voice and Experience d

d d

d

Experiences of consumer groups demanding change, such as people with COPD demanding better services How do smokers with COPD manage their disability? What experiences do patients with COPD have as smokers or former smokers? Experiences of patients with COPD during a hospital stay

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Research with Some Specific Subpopulations d

d

d

Examine the impact of SES, ethnicity, and geography with respect to COPD patient access to health care. Conduct all future research with a sex and gender analysis and with the integration of sex and gender considerations in design. Examine the impact of engagement of patients with COPD in online communities and self-help groups.

Language and Discourse d

Examine the use of slang associated with patients with COPD by clinicians (e.g., ‘‘blue bloaters or pink puffers’’).

Denormalization d

d

Examine the experiences of shame for patients with COPD who are or have histories of smoking. Examine the effects of tobacco denormalization on patients with COPD.

CONCLUSIONS Active smoking is a major cause of COPD, and passive smoking may also be a significant cause of COPD. The highest rate of increase in hospitalizations and deaths from COPD is among women. Women are more likely to develop COPD at an earlier age and to have a more severe expression of the disease than men. Reasons for these differences are unknown, and the extent to which they reflect the contributions and interactions of sex differences and gender influences is also largely unexplored. Within the vast body of literature on tobacco and the growing evidence regarding sex and gender issues in the development of smoking-related diseases such as COPD, there are relatively few studies that focus on the intersections between them. Available research studies tend to focus on COPD and tobacco use or COPD and sex/gender, rarely drawing these three strands together. Furthermore, within tobacco policy documents and strategies, there is little mention of the issues of gender and COPD. Given gendered smoking patterns that lead to a growing risk of COPD among women and the existence of possible sex differences in susceptibility to the disease, it is crucial that further research be conducted in this area. It is recommended that this research be performed in a transdisciplinary manner, using methods that engage COPD patients in a respectful manner and fully integrate sex and gender considerations in design and analysis. It is also recommended that the development of more effective measures of sex and gender be developed that would assist in enhancing health research in general but would have direct applicability to improving our understanding of COPD. All of these approaches will begin to address the knowledge gap in understanding the intersections between sex, gender, tobacco, and COPD and will contribute to enhanced understanding or etiology, treatment, and the experiences of living with COPD. Conflict of Interest Statement: Neither author has a financial relationship with a commercial entity that has an interest in the subject of this manuscript. Acknowledgments: The authors thank the workshop participants for their contributions to the research agenda described in this paper and Kirsten Bell and Kamala Sproule for their research assistance, which supported the materials for the workshop.

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