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(Chest. 2006;129:879-885.)
© 2006 American College of Chest Physicians

Seven-Year Cumulative Incidence of COPD in an Age-Stratified General Population Sample*

Anne Lindberg, MD, PhD; Berne Eriksson, MD; Lars-Gunnar Larsson, MD, PhD; Eva Rönmark, PhD; Thomas Sandström, MD, PhD and Bo Lundbäck, MD, PhD

* From the The OLIN Studies (Drs. Lindberg, Eriksson, Larsson, Rönmark, and Lundbäck), Sunderby Central Hospital of Norrbotten, Luleå, Sweden; and Lung and Allergy Research (Dr. Sandström), National Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden; Lung and Allergy Research, National Institute of Environmental Medicine, Karolinska Institutet, Stockholm, Sweden (Dr. Lundbäck) and Department of Respiratory Medicine and Allergy, Umea University, Umea, Sweden (Dr. Sandström).

Correspondence to: Anne Lindberg, MD, PhD, Senior Consultant, Division of Respiratory Medicine and Allergy, Department of Medicine, Sunderby Central Hospital of Norrbotten, SE-971 80 Luleå, Sweden; e-mail: anne.lindberg{at}algmed.se

Abstract

Aim: To estimate the cumulative incidence of COPD and risk factors related to the development of COPD, including evaluation of the relationship between Global Initiative for Chronic Obstructive Lung Disease (GOLD) stage 0 (ie, respiratory symptoms and normal lung function) and the development of COPD, in an age-stratified general population sample of middle-aged and elderly individuals.

Method: The third survey of the Obstructive Lung Disease in Northern Sweden studies cohort I (three age strata born in 1919 to 1920, 1934 to 1935, and 1949 to 1950) was performed in 1996, and 5,189 subjects (88%) responded to the postal questionnaire. Of the responders, a random sample (1,500 subjects) was invited to an examination in 1996 and in 2003. A total of 963 subjects performed spirometry on both occasions. COPD was defined according to the spirometric criteria of the GOLD. Two levels of disease severity, grade I and higher (GOLD criteria, FEV1/FVC ratio of < 0.70) and also grade II and higher (GOLD II criteria, FEV1/FVC ratio of < 0.70 and FEV1 <80% predicted).

Results: The 7-year cumulative incidence of COPD was 11.0% and 4.9%, respectively, according to GOLD and GOLD II, and was significantly related to smoking (smokers, 18.8% and 10.6%, respectively; ex-smokers, 10.5% and 5.2%, respectively; non-smokers, 7.6% and 1.6%, respectively). Incident COPD according to GOLD, but not according to GOLD II, was significantly associated with increasing age. Most respiratory symptoms at study entry were markers of increased risk for incident COPD when analyzed in a multivariate model adjusting for confounders.

Conclusion: The GOLD criteria yielded a higher cumulative incidence (11.0%) compared to the GOLD II (4.9%). Smoking, but not gender, was associated with incident COPD. Most respiratory symptoms at the beginning of the observation period marked an increased risk for developing COPD, thus the classification GOLD stage 0 seems relevant among middle-aged and elderly persons.

Key Words: COPD • epidemiology • spirometry

There have been several reports1234 on the prevalence of COPD in the general population, most of which were in the range of 4 to 10%. It is well-established that the age distribution and smoking habits of the studied populations, as well as the spirometric criteria of COPD, will influence the prevalence.56 Cross-sectional studies have also provided data on other factors associated with COPD, including socioeconomic group, occupational airborne exposure, chronic productive cough, and other respiratory symptoms.7

There have been only a few reports891011 about the incidence of COPD in the literature. Only one of them, a report from the Copenhagen City Heart Study,10 use currently accepted spirometric criteria of COPD (ie, the criteria of the Global Initiative for Chronic Obstructive Lung Disease [GOLD] guidelines1213) to assess the incidence of COPD in a general population sample. Smoking and age were associated with development of COPD in the Danish report. The GOLD guidelines and the standards defined by the European Respiratory Society (ERS) and American Thoracic Society (ATS),14 define also a population that is "at risk" for COPD (ie, subjects with normal lung function and respiratory symptoms). Currently, there are limited data to support the relationship between the development of COPD and the subpopulation defined as "at risk for COPD." In contrast, according to the Danish report10 GOLD stage 0 did not predict the development of COPD. However, there is also a recent publication11 supporting the classification of GOLD stage 0 (at risk for COPD), in that respiratory symptoms were found to mark an increased risk for the development of COPD in a symptomatic cohort, and also when adjusted for possible confounders. Besides these data, there have been only a few reports891011 based on longitudinal studies about risk factors associated with the development of COPD. There is a need for further longitudinal epidemiologic studies with a focus on COPD concerning the incidence and risk factors for the development of COPD. Furthermore, in longitudinal studies the course of the disease, including early clinical signs, can be explored, which is an area in which at present there are scarce data.

The aim of this study was to estimate the cumulative incidence of COPD during a 7-year follow-up of an age-stratified general population sample and to evaluate the risk factors associated with incident disease. Further aims were to evaluate the impact of different spirometric criteria of COPD in relation to age and to determine to what extent respiratory symptoms preceded the development of COPD. We used the spirometric criteria of the GOLD guidelines1213 at two different cutoff levels of disease severity to illustrate different spirometric definitions of COPD, as follows: GOLD stage I and higher (FEV1/FVC ratio of < 0.70); and GOLD stage II and higher (FEV1/FVC ratio of < 0.70 and FEV1 of < 80% predicted).

Materials and Methods

Study Population
The Obstructive Lung Disease in Northern Sweden (OLIN) studies have collected epidemiologic data since 1985 to 1986 with a focus on allergy and obstructive lung disease (OLD).415161718 This study is a follow-up of the first OLIN cohort that was recruited in 1985 to 1986, when a postal questionnaire was sent to all 6,610 subjects born in 1919 to 1920 (age group I), 1934 to 1935 (age group II), and 1949 to 1950 (age group III) in eight representative areas of northern Sweden.16 In 1996, the cohort comprised 5,933 subjects, and 5,892 were traced for a follow-up with a postal questionnaire, for which the response rate was 88%.18 A random sample of the responders, 1,500 subjects, were invited to a structured interview and spirometry, of whom 1,282 subjects (85%) participated and 1,237 performed a spirometry maneuver with acceptable technique.4 All participants from the 1996 examination were invited to a second examination in 2003, of whom 1,009 subjects (85%) participated and 979 performed an adequate lung function test.

The study sample consists of the 963 subjects who performed a technically adequate spirometry maneuver in both 1996 and 2003. Basic characteristics of the study sample are shown in Table 1 . The 274 subjects participating in 1996 but not in 2003 had a lower lung function compared with those attending at the follow-up (mean FEV1, 89.17% vs 97.45% predicted, respectively; p < 0.001). A significant difference remained also after excluding the prevalent cases of COPD in 1996.


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  		Table 1.. Basic Characteristics Study Population at Entry by Age, Smoking Habits, Lung Function, and Reported Symptoms*

 
Methods
The postal questionnaire and the interview questionnaire developed from the British Medical Research Council questionnaire19 have previously been described.1518 Both questionnaires have been used in several studies in Sweden, Finland, and Estonia.41516171820 The spirometry was performed according to ATS recommendations.21 No reversibility test was performed. Swedish reference values for FEV1 were used,22 conforming well with the adult population in Norrbotten.16 The study was approved by the Regional Committee for Ethics at the Umeå University.

Definitions
Spirometric Criteria of COPD: The GOLD guidelines1213 define the spirometric criteria for COPD (FEV1/FVC ratio of < 0.70) and disease severity is classified by level of FEV1 into four stages. The GOLD classification also includes a population at risk for COPD (ie, in GOLD stage 0), subjects with respiratory symptoms as cough and sputum production but normal lung function.

Disease severity classified according to GOLD is as follows:

GOLD stage I (mild disease): FEV1/FVC ratio of < 0.70 and FEV1 ≥ 80% predicted;
GOLD stage II (moderate disease): FEV1/FVC ratio of < 0.70 and FEV1 < 80% and ≥ 50% predicted;
GOLD stage III (severe disease): FEV1/FVC ratio of < 0.70 and FEV1 < 50% and ≥ 30% predicted; and
GOLD stage IV (very severe disease): FEV1/FVC ratio of < 0.70 and FEV1 < 30% predicted.

The GOLD criteria refer to spirometry after bronchodilatation. In the article, the following two levels of disease severity have been used: the term GOLD refers to GOLD stage I to IV (FEV1/FVC ratio of < 0.70); and the term GOLD II refers to GOLD stage II and higher (FEV1/FVC ratio if < 0.70 and FEV1 < 80% predicted). A reversibility test was not performed, thus a modified GOLD criterion was used. The GOLD criteria have been used in a similar modified manner in other studies.1023 The guidelines do not clearly exclude asthma as a cause of chronic obstructive lung function impairment, thus subjects reporting asthma were not excluded.

Cumulative Incidence: The cumulative incidence is defined as the proportion of a disease-free population (population at risk) that develops disease during a specified time period (in this study, 7 years). An incident case is a subject who develops disease (in this study, COPD according to the GOLD criteria: GOLD I and GOLD II) during the observation period.

Smoking Habits: Smoking habits were classified according to the answers given at the interview in 1996, as follows: non-smokers; ex-smokers (ie, those who had stopped smoking for at least 1 year); and smokers.

Socioeconomic Classification
The Swedish socioeconomic classification by occupation was used24 as follows: (1) professionals and executives; (2) assistant nonmanual employees; (3) manual workers in industry; (4) manual workers in service; (5) self-employed nonprofessionals; (6) housewives; and (7) occupation unknown.

Statistical Analysis
A statistical software package (SPSS, version 10.0; SPSS; Chicago, IL) was used for statistical analysis. The {chi}2 test was used for bivariate analyses and for tests for trend. The t test was used for comparing means. A multiple logistic regression model was created with the two definitions of incident COPD (ie, GOLD and GOLD II) as dependent variables, and gender, family history of OLD, age group, and smoking habits as independent variables. To the model were singly added the symptoms cough ("usually have cough"), sputum production ("usually have phlegm"), chronic productive cough ("phlegm when coughing, or phlegm which is difficult to bring up, most days during periods of at least 3 months, during at least the 2 last years"), recurrent wheeze, and dyspnea (corresponding to British Medical Research Council dyspnea scale grade II, dyspnea when hurrying walking on level ground). Socioeconomic classification was also added to the model. The 95% significance level (p < 0.05) and 95% confidence intervals (CIs) were used.

Results

Incidence of COPD
During the observation period of 7 years, COPD developed in 45 subjects (25 women) according to the GOLD II criteria and in 91 subjects (52 women) according to the GOLD criteria, which corresponds to a cumulative incidence of 4.9% (95% CI, 3.6 to 6.5) and 11.0% (95% CI, 9.0 to 13.4), respectively. The cumulative incidence was significantly associated with smoking. The cumulative incidence of COPD (GOLD II criteria) was more than six times higher among smokers (10.8%) compared to nonsmokers (1.6%). When tested for trend, incident COPD according to GOLD criteria but not according to GOLD II criteria, was significantly associated with increasing age (Table 2 ).


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  		Table 2.. The 7-Year Cumulative Incidence of COPD According to the Spirometric Criteria of GOLD I and Higher and GOLD II and Higher at Study Entry*

 
The incident cases of COPD reported significantly more respiratory symptoms at the start of the observation period compared to the subjects not developing COPD (incident GOLD II criteria, 88.9% vs not 59.2%, respectively [p < 0.001]; incident GOLD criteria, 75.6% vs not 57.5%, respectively [p = 0.001]) [Table 3 ]. The most common symptoms preceding the development of COPD were sputum production and recurrent wheeze. Male and female patients with incident cases of COPD reported respiratory symptoms at study entry to the same extent, besides dyspnea, which was more commonly reported by women developing COPD according to GOLD criteria (women, 53.8%; men, 23.1%; p = 0.003). All patients with incident cases of COPD according to GOLD II criteria between 76 and 77 years of age reported respiratory symptoms, while the corresponding proportion among the oldest patients with incident cases of COPD according to GOLD criteria was 85.7%.


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  		Table 3.. Proportion of the Population at Risk Reporting Respiratory Symptoms at Study Entry Comparing Subject Who Did Not Develop COPD to Those Who Developed COPD According to GOLD and GOLD II Criteria*

 
Multivariate Analyses
In a multivariate regression model, smoking was a significant risk factor for incident COPD when adjusted for age, gender, and family history of OLD. Higher age was a significant risk factor for incident COPD according to GOLD criteria, while the risk for incident COPD according to GOLD II criteria was increased among subjects aged 61 to 62 years, but not significantly higher among the oldest subjects (age 76 to 77 years) when compared to subject in the youngest age group (age 46 to 47 years) at study entry. The respiratory symptoms were singly added to the model, and most of the symptoms were significant, or close to significant, as markers of increased risk for developing COPD (Table 4 ). The other risk factors in the multivariate model remained on a similar level when the respiratory symptoms were added. Socioeconomic group was not significantly associated with incident COPD when added to the same multivariate model (data not shown).


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  		Table 4.. Risk Factor Analysis for Development of COPD According to the GOLD II and GOLD Criteria, Multiple Logistic Regression Model, including Gender, Family History of OLD, Age Group and Smoking Habits and Also Respiratory Symptoms One at a Time*

 
Discussion

The 7-year cumulative incidence of COPD was estimated at 4.9% and 11.0%, respectively, according to the spirometric criteria of GOLD II and GOLD, and was strongly associated with smoking but not gender. The cumulative incidence of COPD according to GOLD criteria, but not according to GOLD II criteria, was associated with increasing age. The cumulative incidence of COPD according to GOLD II criteria corresponds to an annual incidence rate of 7 per 1,000 persons per year in the total population, while it was 15 per 1,000 persons per year in smokers and 2 per 1,000 persons per year in nonsmokers (GOLD criteria, 16 per 1,000, 27 per 1,000, and 11 per 1,000 persons per year, respectively).

It has been reported that the prevalence of COPD is higher in men compared to women.35 However, since the very start of the OLIN studies in northern Sweden we have found no major gender differences with regard to bronchitic symptoms, chronic bronchitis, or the prevalence of COPD.41115 Thus, the lack of significant gender difference in the incidence of COPD in the current study is not surprising. One explanation is that the main risk factor for COPD, namely, smoking, has become more common in women and has been comparable to smoking rates for men in Sweden for many years.

We have found only one published report10 on the incidence of COPD in general population using modern spirometric criteria for COPD. The data were based on three surveys in the Copenhagen City Heart Study and included subjects from 20 years of age at entry. At a follow-up of a general population sample without COPD at study entry, COPD developed in 9.7% of subjects (smokers, 11.6%) and 13.2% of subjects (smokers, 18.5%) according to GOLD criteria after 5 and 15 years, respectively.10

We made an approximate estimate of the annual incidence rate of COPD based on the data in the Danish report,10 which yielded incidences of 19 per 1,000 persons per year and 9 per 1,000 persons per year, respectively, based on the 5-years and 15-year follow-up, while in smokers the results were 23 per 1,000 persons per year and 12 per 1,000 persons per year, respectively. In an earlier Finnish report8 of a 20-year follow-up of subjects aged 40 to 64 years at study entry, the annual incidence rate of an FEV1/FVC ratio of < 0.60 was estimated in the population at risk to be 2 per 1,000 persons per year and in smokers 10 per 1,000 persons per year. Longitudinal data from a Polish study9 based on a 14-year follow-up showed an annual incidence rate of an FEV1 of < 0.65 at 5 per 1,000 persons per year in subjects aged 19 to 70 years at study entry. The different demographic data of the studied populations and the different spirometric criteria complicate comparisons between studies. However, the incidence of COPD in the Danish study seems to be higher and less smoking-dependent compared with the incidence in earlier studies and also in our study.

Respiratory symptoms are related to impaired lung function on a population level,16 and an association with respiratory symptoms such as chronic productive cough and increased decline in lung function has been reported.25 In our study, respiratory symptoms were associated with the development of COPD. The most commonly reported symptoms prior to the development of COPD were sputum production and recurrent wheeze. Dyspnea was more common in women in whom COPD developed according to GOLD criteria; otherwise the expression of symptoms preceding COPD was similar in men and women.

The GOLD guidelines classify subjects who are at risk for developing COPD (subjects with respiratory symptoms and normal lung function1213), and a similar definition of subjects who are at risk for COPD is included also in the published ATS/ERS standards.14 According to our results, the classification of subjects who are at risk seems relevant in middle-aged and elderly persons. Respiratory symptoms preceded and were markers of an increased risk for COPD developing in this age-stratified general population sample. We have found similar results when following up a cohort with respiratory symptoms; most respiratory symptoms singly marked an increased risk for the development of COPD over a 10-year observation time, and also when adjusted for possible confounders.11 In that respect, our results were contrary to the Danish report,10 in which the authors concluded that the classification of GOLD stage 0 (at risk) did not predict the development of COPD, even though it was associated with an excess decline in FEV1. One possible explanation given was that GOLD stage 0 was not a stable condition. One report26 on the benefits of smoking cessation on the remission of respiratory symptoms on a population level suggested that smoking habits may interfere with the results. The study population in the Danish report10 included subjects from the age of 20 years, while our studies were performed in the age strata of ≥ 36 years (the symptomatic cohort11) and the age strata of ≥ 45 years (the general population sample of the current study) [ie, higher ages in which COPD are known to be more common]. The differences in age distribution may contribute to the contradictory results regarding the relationship between respiratory symptoms and the development of COPD in our studies and in the Danish study.10

Incident COPD according to GOLD criteria, but not GOLD II criteria, was associated with increasing age. Incident COPD according to the GOLD II criteria was most common in the age group 61 to 62 years, while it was less common in the youngest and the oldest age groups (46 to 47 years and 76 to 77 years) at study entry. All incident cases of COPD according to the GOLD II criteria in the oldest age group (76 to 77 years of age at entry) reported respiratory symptoms and were ex-smokers or smokers prior to the development of COPD. The associations among smoking habits, respiratory symptoms, and incident COPD according to GOLD criteria in the oldest age group were somewhat weaker. An earlier published report27 concluded that the GOLD criteria overestimated the prevalence of COPD in elderly persons, as many subjects were found to be healthy non-smokers without respiratory symptoms. This overestimation seems to be applicable also for incident COPD according to GOLD criteria in elderly persons.

It has been suggested that GOLD stage II (FEV1/FVC ratio of < 0.70 and FEV1 of < 80% predicted) is a threshold for symptomatic and possibly clinically relevant COPD.6 According to our results, this can be expected to be true also in elderly persons (76 to 77 years of age at entry) as the subjects with incident cases identified by GOLD II criteria were all symptomatic and had a history of smoking. For further comparison, those criteria were similar for moderate COPD according to the published ATS/ERS standards,14 COPD according to the British National Institute of Clinical Excellence criteria28 and the British Thoracic Society guidelines.29 According to the guidelines, asthma was not excluded as a cause of chronic obstructive airflow limitation. Consequently, some cases of asthma may contribute to the incident cases of COPD, but asthma and COPD may also coexist in the same subject.

Socioeconomic factors have been reported3031 to be associated with COPD, but socioeconomic group was not significantly associated with incident COPD in our study. The retirement age in Sweden is usually 63 to 65 years of age. Thus, nearly half of the study population had already retired in 1996 or retired during the observation period, which may have affected the results. The Swedish classification of socioeconomic group by occupation25 was used, and indexes of socioeconomic group determined by other than by former occupational title may be more relevant in elderly persons.

The analysis of longitudinal data in the present study illustrates the development of COPD in a defined healthy population (with respect to lung function). In contrast, the prevalence data on COPD may include subjects with impaired lung function since early adulthood, which may have predisposed the patient to the development of COPD despite a normal decline in lung function, such as that in subjects not reaching expected maximal adult lung function. The prevalence of COPD is dependent on the spirometric criteria of COPD5 and may change fourfold.6 The spirometric criteria also affect the incidence of COPD, first as a discriminator of the population at risk, and second when identifying the incident cases. To date, there are very limited longitudinal data on COPD and incidence estimates. The choice to use two different spirometric criteria in this study was made in order to illustrate the difference in incidence related to different spirometric criteria, but it will also increase the possibilities for comparison with future studies. Further, we also made an attempt to evaluate the possible clinical relevance of incident disease by different criteria in middle-aged and elderly subjects.

The original cohort is an age-stratified general population sample with three age groups that were recruited between 1985 and 1986.15 The participation in the following surveys has been high (≥ 85%),419 and the cohort is considered to be representative of the general population in current ages, which supports the validity of the results. Due to the age distribution and time of follow-up, the number of subjects lost to follow-up was, as expected, greatest in the oldest age group. A healthy survivor effect must be included when interpreting the results. In an earlier report,11 we found that subjects not participating in a 10-year follow-up had lower lung function at baseline and also a higher mortality rate. The subjects lost to follow-up in the current study were also characterized by lower lung function at baseline, and consequently we can assume that they had higher mortality and morbidity rates than those participating at follow-up. Low lung function itself is a known predictor of mortality.32 Thus, the healthy survivor effect indicates that the cumulative incidence underestimates the number of subjects affected by COPD.

In conclusion, the 7-year cumulative incidence of COPD was estimated at 4.9% and 11.0%, respectively, according to GOLD II and GOLD spirometric criteria. The incidence of COPD was strongly associated with smoking. Respiratory symptoms at the beginning of the observation period were markers of an increased risk for developing COPD. Thus, the classification of subjects at risk for COPD according to the GOLD criteria and published ATS/ERS standards14 seems relevant in middle-aged and elderly persons. However, the GOLD II spirometric criteria, excluding subjects with an FEV1 ≥ 80% predicted appear to be more reliable than the GOLD criteria in identifying incident COPD that is of possible clinical relevance among elderly patients.

Acknowledgements

The research assistants Linnea Hedman, Ann-Christin Jonsson, and Sigrid Sundberg, and statistician Ola Bernhoff are acknowledged for collecting and entering the data into the computerized database.

Footnotes

Abbreviations: ATS = American Thoracic Society; CI = confidence interval; ERS = European Respiratory Society; GOLD = Global Initiative for Chronic Obstructive Lung Disease; OLD = obstructive lung disease; OLIN = Obstructive Lung Disease in Northern Sweden

This research was supported by The Swedish Heart-Lung Foundation and the Norrbotten's Health Care Authority. The GlaxoSmithKline R&D department is acknowledged for additional financial support.

Received for publication May 24, 2005. Accepted for publication October 20, 2005.

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