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American Journal of Epidemiology Advance Access published online on September 4, 2007
American Journal of Epidemiology, doi:10.1093/aje/kwm235
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American Journal of Epidemiology © The Author 2007. Published by the Johns Hopkins Bloomberg School of Public Health. All rights reserved. For permissions, please e-mail: journals.permissions@oxfordjournals.org.

Original Contribution

Prospective Study of Cured Meats Consumption and Risk of Chronic Obstructive Pulmonary Disease in Men

Raphaëlle Varraso1, Rui Jiang2, R. Graham Barr2,3,4, Walter C. Willett1,4,5 and Carlos A. Camargo, Jr.4,5,6

1 Department of Nutrition, Harvard School of Public Health, Boston, MA
2 Division of General Medicine, Department of Medicine, College of Physicians and Surgeons, Columbia University, New York, NY
3 Department of Epidemiology, Mailman School of Public Health, Columbia University, New York, NY
4 Channing Laboratory, Department of Medicine, Brigham and Women's Hospital, Harvard Medical School, Boston, MA
5 Department of Epidemiology, Harvard School of Public Health, Boston, MA
6 Department of Emergency Medicine, Massachusetts General Hospital, Harvard Medical School, Boston, MA

Correspondence to Dr. Raphaëlle Varraso, 16 avenue Paul Vaillant Couturier, 94807 Villejuif, France (e-mail: varraso{at}vjf.inserm.fr).

Received for publication February 12, 2007. Accepted for publication July 26, 2007.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Cured meats are high in nitrites. Nitrites generate reactive nitrogen species that may cause damage to the lung. The objective is to assess the relation between frequent consumption of cured meats and the risk of newly diagnosed chronic obstructive pulmonary disease (COPD). Between 1986 and 1998, the authors identified 111 self-reported cases of newly diagnosed COPD among 42,915 men from the Health Professionals Follow-up Study. The cumulative average intake of cured meats consumption (processed meats, bacon, hot dogs) was calculated from food frequency questionnaires administrated in 1986, 1990, and 1994 and divided according to servings per week (never/almost never, <1 serving/week, 1–3 servings/week, 4–6 servings/week, at least once/day). After adjustment for age, smoking status, pack-years, pack-years squared, energy intake, race/ethnicity, US region, body mass index, and physical activity, the consumption of cured meats was positively associated with the risk of newly diagnosed COPD (for highest vs. lowest intake: relative risk = 2.64, 95% confidence interval: 1.39, 5.00; ptrend = 0.002). In contrast to these findings, the consumption of cured meats was not associated with the risk of adult-onset asthma. These data suggest that cured meat may worsen the adverse effects of smoking on risk of COPD.

diet; meat; men; nitrites; pulmonary disease; chronic obstructive

Abbreviations: CI, confidence interval; COPD, chronic obstructive pulmonary disease; FEV1, forced expiratory volume in 1 second; RR, relative risk


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Cured meats contain various compounds added to meat products as preservatives and color fixatives (1), among which the most important are nitrites (2). Nitrites generate reactive nitrogen species that can amplify inflammatory processes in the airways and lung parenchyma causing DNA damage, inhibition of mitochondrial respiration, and nitrosative stress (3). The long-term persistence of nitrosative stress may contribute to the progressive deterioration of pulmonary function and may be implicated in the pathogenesis of chronic obstructive pulmonary disease (COPD) (4).

Currently, COPD is the fourth leading cause of mortality in Europe and in the United States (5). With the increase in cigarette smoking in developing countries, COPD is expected to become the third leading cause of death worldwide by 2020 (6). Cigarette smoking is the most important risk factor for COPD in developed nations (7), but not all smokers develop COPD (8)—an observation that suggests that other factors also are involved. In the last decade, there has been a growing interest to identify foods related to the level of lung function or COPD symptoms (9). Most investigations have focused on foods with antioxidant properties and not foods with a potential deleterious effect.

Two recent studies have tested the hypothesis that frequent consumption of cured meats increases the risk of COPD: a cross-sectional study of more than 7,000 men and women (10) and a longitudinal study of more than 71,000 women (11). Both reported a positive association between the frequent consumption of cured meats and an increased risk of COPD. Gender differences in the manifestations and diagnosis of obstructive airway disease over the human life span (12), as well as gender differences in food choices and energy intake (13), provide a compelling rationale to study the relation between cured meat and COPD among men as well. We therefore examined the association between cured meats consumption and risk of newly diagnosed COPD in a prospective cohort of more than 40,000 men.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Study population
The Health Professionals Follow-up Study, a prospective cohort study, began in 1986 when 51,529 US health professionals (dentists, optometrists, pharmacists, podiatrists, and veterinarians) aged 40–75 years answered a detailed mailed questionnaire that included a diet survey and items on lifestyle practice and medical history. Follow-up questionnaires were sent every 2 years thereafter to update information on smoking habits, physical activity, weight, and other risk factors and to ascertain newly diagnosed medical conditions. Dietary intake data were collected in 1986 and every 4 years thereafter with a 131-item food frequency questionnaire. The study is being conducted according to the ethical guidelines of Brigham and Women's Hospital (Boston, Massachusetts).

Men who did not satisfy a reported daily energy intake between 3.3 and 17.6 MJ (800 and 4,200 kcal) or who left blank more than 70 of a total of 131 food items on the diet questionnaire were excluded. We further excluded 232 men with confirmed COPD at baseline or missing date of diagnoses, 1,834 with reported asthma, and 272 with unconfirmed COPD at baseline or during the follow-up. The final baseline population included 42,915 men.

Consumption of cured meats
Cured meats consumption was defined as the total consumption of processed meats, bacon, and hot dogs, which was asked as three separate questions: "How often on average have you used the amount specified during the past year: 1) processed meats, e.g., sausage, salami, bologna, ... (slice); 2) bacon (two slices); 3) hot dogs?" (1). Participants indicated their average frequency of consumption over the past year in terms of the specified serving size by checking one of nine frequency categories ranging from "almost never" to "≥6 times/day." The selected frequency category for each food item was converted to a daily intake. Cured meats consumption was identified from food frequency questionnaires administrated in 1986, 1990, and 1994. To reduce measurement errors and to represent long-term dietary intake, we calculated the cumulative average of cured meats consumption, which was then divided into five categories according to the number of servings per week: never/almost never, <1 serving/week, 1–3 servings/week, 4–6 servings/week, and at least once/day. The cumulative average incorporated repeated measures of diet (14). With this approach, the 1986 cured meats consumption was used to predict newly diagnosed COPD in 1986–1990; an average of the 1986 and 1990 cured meats consumption was used to predict COPD in 1991–1994; and the average of the 1986, 1990, and 1994 cured meats consumption was used to predict COPD from 1995 to 1998. The individual associations with processed meats, bacon, and hot dogs were also investigated in relation to newly diagnosed COPD. The cumulative average was calculated for each one of these cured meats and then divided into three categories according to the number of servings per week (never/almost never, <1 serving/week, and at least once/week).

Assessment of respiratory phenotypes
Because the Health Professionals Follow-up Study includes many participants dispersed throughout the United States and is conducted by mail, the diagnosis of COPD was assessed by questionnaire and did not include spirometry. Supplemental questionnaires were sent in 1998 and 2000 to all participants who reported chronic bronchitis or emphysema on the biennial questionnaires. Self-reported COPD was defined by the affirmative response to physician-diagnosed chronic bronchitis or emphysema on the biennial questionnaires and by confirmation of chronic bronchitis, emphysema, or COPD on the supplemental COPD questionnaire, plus report of a diagnostic test at diagnosis (pulmonary function testing, chest radiograph, or chest computed tomography). This epidemiologic definition was validated in a random sample of another cohort of health professionals (15). Between 1986 and 1998, 111 cases of newly diagnosed COPD that were reported met these criteria.

Asthma was also self-reported and was defined by a new physician diagnosis of asthma on the biennial questionnaires and by confirmation on the supplemental asthma questionnaire, plus use of medication for asthma in the 12 months preceding the supplemental questionnaire. Between 1986 and 1998, 212 new cases of adult-onset asthma were reported.

Assessment of other variables
Total calorie intake was estimated through the food frequency questionnaire, expressed in kilocalories per day. Information on smoking status included the categories never smokers, former smokers, and current smokers. We further characterized smokers using their lifetime pack-years of smoking and pack-years squared; prior analyses have demonstrated that including both measures optimally controls for the association between smoking and COPD risk. Data on race/ethnicity and region also were collected. Race/ethnicity was categorized in two classes (White, non-White), and US region was categorized in three classes (East, South, Central; Mountain; and other regions). Body mass index, physical activity, and multivitamin use were assessed every 2 years by self-reported questionnaires. Body mass index was calculated as weight (kg)/height (m)2 and was categorized into four classes: <20.0, 20.0–24.9, 25.0–29.9, and ≥30.0 kg/m2. Men also reported physical activity, including a variety of activities such as walking, bicycle riding, swimming, or tennis. Physical activity was measured in metabolic equivalent hours per week, where 1 metabolic equivalent was equal to the energy expended at the basal metabolic rate or at rest.

Previously, in this cohort of men, a strong association between dietary patterns and the risk of newly diagnosed COPD was reported (16). The "prudent pattern" was loaded by a high consumption of fruits, vegetables, fish, and whole grains and was negatively associated with newly diagnosed COPD, whereas the "Western pattern" was loaded by a high intake of refined grains, cured and red meats, desserts and sweets, and French fries and was positively associated with newly diagnosed COPD. Because cured meats are a food group included in the Western pattern, we derived a new Western pattern without contribution from cured meats, and we termed this the "modified Western pattern."

Statistical analysis
Statistical analyses included chi-squared, analysis of variance, linear regression, and Cox proportional hazards regression models. Cox proportional hazards models were adjusted for age and energy intake and then for seven variables (smoking status, pack-years, pack-years squared, race/ethnicity, US region, body mass index, and physical activity). We intensively adjusted for smoking (smoking status, pack-years, pack-years squared), because it is the main risk factor for COPD and because smokers tend to have a different diet than do nonsmokers (17). We also adjusted for race/ethnicity, because death rates from COPD are rising faster in African Americans than in Whites (18) and because diet is highly related to racial/ethnic identity. To take into account geographic disparities in COPD and diet across the United States, we also adjusted for US region. The adjustment for body mass index and physical activity was motivated by the strong interrelations among diet, body mass index, and physical activity. Furthermore, low body mass index is highly related to COPD (19), and it has been reported that physical activity is associated with lower risk of COPD (20).

In a subsequent analysis, we also adjusted for the prudent dietary pattern and the "modified Western pattern" to better assess the individual effect of cured meat intake and to control for the other potential deleterious effects of the Western diet. All analyses were conducted using SAS, version 9, software (SAS Institute, Inc., Cary, North Carolina).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
The characteristics of the cohort, according to the consumption of cured meats, are presented in table 1. Compared with men eating the most cured meats (≥1 serving/day), men with the lowest intake of cured meats (never/almost never) were more physically active, were less likely to be current smokers, and had a lower body mass index. Men with the highest consumption of cured meats were more likely to eat processed meats than to eat bacon or hot dogs. At baseline, 27 percent of men reported that they never ate processed meat, while 51 percent ate less than one serving per week, and 22 percent ate at least one serving per week. The comparable analysis for bacon yielded 38 percent never, 50 percent less than one serving per week, and 12 percent at least one serving per week. Likewise, the results for hot dogs were 44 percent never, 51 percent less than once per week, and 5 percent at least once per week. The consumption of cured meats was positively associated with the risk of newly diagnosed COPD in age-adjusted analysis (for highest vs. lowest consumption of cured meats: relative risk (RR) = 4.09, 95 percent confidence interval (CI): 2.32, 7.22; ptrend < 0.001) and even after adjustment for age and energy intake (table 2). After controlling for smoking status, pack-years, and pack-years squared, the positive association between cured meats and the risk of newly diagnosed COPD remained. Further adjustments for race/ethnicity, US region, body mass index, and physical activity revealed the same significant positive association (table 2). Further adjustment for the prudent diet led to similar results (for highest vs. lowest consumption of cured meats: RR = 2.43, 95 percent CI: 1.26, 4.68; ptrend = 0.006). Adjustment for the "modified Western pattern" led to a borderline significant association (for highest vs. lowest consumption of cured meats: RR = 1.88, 95 percent CI: 0.96, 3.69; ptrend = 0.06). The "modified Western pattern" remained highly related to the risk of newly diagnosed COPD after adjustment for cured meats (for highest vs. lowest quintile of the "modified Western pattern": RR = 4.49, 95 percent CI: 1.67, 12.07; ptrend = 0.001).


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  		TABLE 1. Age-standardized baseline characteristics in 42,915 men, according to consumption of cured meats in 1986, Health Professionals Follow-up Study, United States, 1986–1998

 

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  		TABLE 2. Association between consumption of the cumulative average of cured meats and newly diagnosed chronic obstructive pulmonary disease, Health Professionals Follow-up Study, United States, 1986–1998 (n = 42,915 men)

 
When the population was restricted to men without cancer or cardiovascular disease at baseline (n = 35,284), similar associations were found. The consumption of cured meats was positively associated with the risk of newly diagnosed COPD after adjustment for age and energy intake (for highest vs. lowest consumption of cured meats: RR = 3.56, 95 percent CI: 1.46, 8.66; ptrend < 0.001). Further adjustment for smoking status, pack-years, pack-years squared, race/ethnicity, US region, body mass index, and physical activity led to similar results (highest vs. lowest consumption of cured meats: RR = 1.81, 95 percent CI: 0.88, 4.76; ptrend = 0.01).

Of the three individual cured meats (processed meats, bacon, hot dogs), only the consumption of processed meats was significantly associated with the risk of newly diagnosed COPD (for highest vs. lowest consumption of processed meats: RR = 1.93, 95 percent CI: 1.13, 3.28; ptrend = 0.02). A significant association was found for the consumption of bacon (for highest vs. lowest consumption of bacon: RR = 1.79, 95 percent CI: 0.99, 3.22; ptrend = 0.03), and no relation was found for hot dog consumption (ptrend = 0.43).

On average over the study period, among the 111 cases of COPD, about 86 percent reported a history of cigarette smoking. Considering different time periods, the cases occurring between 1990 and 1992 (n = 12) had the highest proportion of smokers: 67 percent were smokers and 12 percent were former smokers. Considering "ever smoker" (n = 96 cases), the age-adjusted relative risk for ever smokers versus never smokers was 3.90 (95 percent CI: 2.26, 6.72) (p < 0.001). Because smoking is the main risk factor for COPD, we conducted additional analyses excluding never smokers. This analysis was performed among 27,755 men with a history of cigarette smoking (96 cases), and we found that the consumption of cured meats was strongly and positively associated with the risk of newly diagnosed COPD (table 3).


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  		TABLE 3. Association between consumption of the cumulative average of cured meats and newly diagnosed chronic obstructive pulmonary disease in former and current smokers, Health Professionals Follow-up Study, United States, 1986–1998 (n = 27,755 men)

 
To examine whether smoking status modifies the relation between cured meat consumption and COPD risk, we conducted multivariate analyses stratified according to smoking status (table 4). We combined the two highest categories of cured meats consumption because of the small number of cases. After adjustment for age, energy intake, smoking status, pack-years, and pack-years squared, the relative risk comparing the highest vs. the lowest categories of cured meats consumption was 2.39 (95 percent CI: 0.91, 6.27) (ptrend = 0.07) in past smokers and 2.69 (95 percent CI: 1.11, 6.56) (ptrend = 0.03) in current smokers.


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  		TABLE 4. Association between consumption of the cumulative average of cured meats and newly diagnosed chronic obstructive pulmonary disease according to smoking, Health Professionals Follow-up Study, United States, 1986–1998

 
Although the primary outcome of this study was newly diagnosed COPD, we also examined the relation between cured meats and adult-onset asthma, because of the potential overlap between the diagnoses of COPD and asthma (table 5). In contrast with the risk of newly diagnosed COPD, no association was found between the consumption of cured meats and the risk of adult-onset asthma.


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  		TABLE 5. Association between consumption of the cumulative average of cured meats and adult-onset asthma in men, Health Professionals Follow-up Study, United States, 1986–1998

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
In this large prospective cohort of US men during 12 years of follow-up, the risk of newly diagnosed COPD increased with a greater consumption of cured meats after adjustment for many important confounders. Among the individual cured meats, consumption of processed meats was significantly associated with the risk of newly diagnosed COPD, and a borderline significant association was found for bacon. In contrast to the COPD findings, there was no association between consumption of cured meats and risk of adult-onset asthma.

The sodium salts of nitrate (NaNO3) and nitrite (NaNO2) are used in the curing and preserving of processed meats. They are used for three purposes: to preserve color, especially the pink color for hot dogs and other cured meats; to enhance flavor by inhibiting rancidity; and to protect against bacterial growth (2). Regulations controlling the use of curing agents were established in the United States in 1926, and the same rules are in effect at present, with slight modification. The critical feature of these rules is that a maximum-use level of sodium nitrite is defined: No more than one-fourth ounce (7.1 g) may be used per 100 pounds (45.4 kg) of meat. Bacon has been a focus of special attention. Because it is so widely consumed and the risk of infection with anerobic Clostridium botulinum is relatively high (2), the regulations were changed for bacon with ingoing nitrite targeted at 200 ppm. A similar regulation was applied to other cured meats, such as ham, sausages, and corned beef.

In an inflammatory microenvironment, exaggerated production of nitric oxide in the presence of "oxidative stress" may produce the formation of strong oxidizing reactive nitrogen species, such as peroxynitrite, leading to nitration that provokes DNA damage, inhibition of mitochondrial respiration, protein dysfunction, and cell damage ("nitrosative stress") (21, 22). Reactive nitrogen species have been implicated in the pathogenesis of COPD (4). The level of nitrotyrosine immunoreactivity, a marker or production of reactive nitrogen species, was higher in COPD patients than in healthy subjects (23) and correlated with the level of obstruction in COPD patients (24), suggesting that nitrosative stress might be involved in both the risk of COPD and the progression of the disease. These findings are also consistent with animal studies reporting that rats drinking water enriched with sodium nitrite for 2 years developed pulmonary emphysema (25).

The hypothesis that frequent consumption of cured meats might be associated with increased risk of COPD was first tested in a cross-sectional study of 7,432 men and women in the Third National Health and Nutrition Examination Survey (10). Jiang et al. (11) reported that frequent consumption of cured meats was associated with low lung function (forced expiratory volume in 1 second (FEV1)) and with an increased risk of COPD. To address a possible reverse causation due to the cross-sectional design, Jiang et al. then tested the association in a longitudinal study from 1984 to 2000 of more than 71,000 US women. The longitudinal analysis supported the hypothesis that frequent consumption of cured meats was positively associated with the risk of newly diagnosed COPD in women.

Prior epidemiologic studies suggested a beneficial association between foods rich in antioxidants and COPD status or FEV1 level (9). Most of these epidemiologic studies are cross-sectional (26–29), but the few longitudinal studies also have reported a negative association between intake of fruits, vegetables, and vitamin C and the decline of FEV1 (30–32). Previously in this male cohort, a strong association between the prudent dietary pattern and the risk of newly diagnosed COPD was reported (16). Adjustment for this "protective" diet did not affect our finding of a strong, independent, positive association between cured meat consumption and COPD risk. Also previously reported was a strong positive association between the Western dietary pattern and COPD risk (16). Because the Western pattern was highly loaded by the cured meats food group, a new pattern was derived in the present analysis to exclude this food group. The association between cured meat and the risk of newly diagnosed COPD remained, although with wider confidence intervals and marginal significance, after taking into account the "modified Western pattern." The Western pattern was also loaded by refined grains, red meats, desserts and sweets, and French fries and, among all these food groups, only cured meats increased the risk of COPD. We also note that the "modified Western pattern" remained strongly associated with the risk of newly diagnosed COPD after adjustment for cured meats and that both the "modified Western diet" and cured meat contributed independently to the risk of COPD.

The study has several potential limitations. First, we acknowledge that the association between cured meats and newly diagnosed COPD may be due, in part, to a residual confounding by cigarette smoking. To minimize this possibility, multivariate models were adjusted with multiple measures of tobacco exposure (smoking habits, pack-years, and pack-years squared) and, despite the small numbers of cases, stratified analysis according to smoking status yielded comparable results. Nevertheless, the residual confounding effect by smoking remains an issue. Furthermore, we were not able to adjust for environmental tobacco smoke, which remains an important risk factor for COPD (33). Nevertheless, adjustment of cured meats and COPD analyses in the Nurses' Health Study for environmental tobacco smoke did not attenuate the association (11).

Second, newly diagnosed COPD was defined by a self-reported physician diagnosis of COPD, and no lung function results were available. Nevertheless, validation of an identical, questionnaire-based definition of newly diagnosed COPD in a similar study of female health professionals showed that 80 percent of a random sample of cases meeting this definition had medical record documentation of COPD, and the mean FEV1 among those with available spirometry reports was 50 percent of predicted (15). In addition, since the main source of misclassification of COPD reported by health professionals was misdiagnosis with asthma, we examined the association of cured meats and the risk of adult-onset asthma. The complete lack of association of cured meat intake with asthma suggests that our findings are unlikely to be due to misclassification with asthma. While we acknowledge the potential for some misclassifications, the Health Professionals Follow-up Study data allowed us to investigate the relation between cured meats and COPD in a very large population, with repeated measurements of both diet and COPD status.

Even if diet is assessed every 4 years with accurate food frequency questionnaires, we lacked a specific measure of nitrite intake to more specifically examine the biologic mechanism that we believe explains our results. However, cured meats contain thousands of biologically active phytochemicals other than nitrites, and it remains possible that they too might be involved in the increased risk of COPD. For example, cured meats are rich in sodium, and experimental studies suggest that a high intake of sodium may increase bronchial hyperresponsiveness, although the association with other respiratory endpoints such as medication use and lung function was not consistent (34).

In summary, the consumption of cured meats was positively associated with the risk of newly diagnosed COPD. Although several compounds may be responsible for this finding, we believe that nitrites provide a very plausible biologic mechanism. Because of emerging evidence regarding the deleterious effect of cured meats in other diseases (e.g., cancer (35) and diabetes (36)), we recommended reduced daily intake of cured meats. For COPD prevention, the most important public health message remains smoking cessation, but our data suggest that diet, another modifiable risk factor, might influence COPD risk. Future studies of actual levels of nitrite intake and COPD risk would be useful, as well as the examination of this novel association in other data sets.


   ACKNOWLEDGMENTS
 
Supported by research grants CA55075 and HL60712 from the National Institutes of Health (Bethesda, Maryland). R. V. was supported by grants from the Société de Pneumologie de Langue Française (Paris, France) and the Société Française de Nutrition (Paris, France).

Conflict of interest: none declared.


   References
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

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