COPD: Journal of Chronic Obstructive Pulmonary Disease

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Adherence to a Mediterranean-like
Diet as a Protective Factor Against
COPD: A Nested Case-Control Study

Alexandra Fischer, Ingegerd Johansson, Anders

Blomberg & Björn Sundström

To cite this article: Alexandra Fischer, Ingegerd Johansson, Anders Blomberg & Björn Sundström
(2019): Adherence to a Mediterranean-like Diet as a Protective Factor Against COPD: A
Nested Case-Control Study, COPD: Journal of Chronic Obstructive Pulmonary Disease, DOI:
10.1080/15412555.2019.1634039
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COPD: JOURNAL OF CHRONIC OBSTRUCTIVE PULMONARY DISEASE
https://doi.org/10.1080/15412555.2019.1634039

Adherence to a Mediterranean-like Diet as a Protective Factor Against COPD:

A Nested Case-Control Study
Alexandra Fischera, Ingegerd Johanssonb, Anders Blomberga, and Bjorn€ Sundstrom€a
aDepartment of Public Health and Clinical Medicine, Section of Medicine, Umeå University, Umeå, Sweden; bDepartment
of Odontology, Cariology, Umeå University, Umeå, Sweden

ABSTRACT ARTICLE HISTORY

A diet rich in nutrients has been suggested to have protective effects against the development of Received 8 April 2019
chronic obstructive pulmonary disease (COPD). Since the traditional Mediterranean diet is high in Accepted 15 June 2019
nutrients, including antioxidants, vitamins, and minerals, it is of interest to study as a protective
factor against COPD. Our aim was therefore to study its associations with development of COPD KEYWORDS
COPD; dietary habit;
using population-based prospective data from the Vasterbotten€ Intervention Programme (VIP) Mediterranean diet;
cohort. Data on diet from 370 individuals, who later visited the Department of Medicine at the nutrients
University Hospital, Umeå, Sweden, with a diagnosis of COPD, were compared to 1432 controls.
Adherence to a Mediterranean diet was assessed by a modified version of the Mediterranean diet
score (MDS). Cases were diagnosed with COPD 11.1 years (mean) (standard deviation [SD] 4.5
years) after first stating their dietary habits in the VIP at a mean age of 55.5 years (SD 6.6 years).
Higher MDS was associated with a higher level of education and not living alone. After adjustment
for co-habiting and education level, individuals with an intermediate MDS and those with the highest
MDS had a lower odds of developing COPD (odds ratio [OR] 0.73, 95% confidence interval [CI]
0.56–0.95; OR 0.56, 95% CI 0.37–0.86, respectively). These results remained also after adjust-ment
for smoking intensity, i.e., numbers of cigarettes smoked per day (OR 0.73, 95% CI 0.53–0.99; OR
0.59, 95% CI 0.35–0.97), respectively). To conclude, adherence to a Mediterranean-like diet seems
to be inversely associated with the development of COPD.

Introduction
According to the Global Initiative for Chronic Obstructive
Lung Disease (GOLD), chronic obstructive pulmonary dis-
ease (COPD) is estimated to become the third leading cause of
mortality by 2030 (1). Whilst there are genetic predisposi-
tions to develop COPD, the most well-known is the a1-anti-
trypsin deficiency, which affects between 0.02% and 0.05% of
the population, smoking or exposure to other hazardous
fumes, and dust are the major risk factors for COPD (2,3).
Approximately 50% of the smokers develop COPD (4), but
since not everyone exposed to smoking or hazardous fumes/
dust develop COPD, protective factors related to lifestyle,
such as diet, may exist. Previous studies on diet have focused
mainly on specific dietary micro- and macronu-trients,
including antioxidants, vitamins, fatty acids, meat, dietary
fibers, fruit, and vegetables. Although the results of these
studies differ, it appears that consuming a diet high in
antioxidants, vitamins, omega-3 fatty acids, fiber, fruits, and
vegetables and low in processed meat offers some protection
against developing COPD (5–11).
Recently, there has been a shift toward studying the effect
of diet on diseases by examining dietary patterns instead of
isolated nutrients, due to the complexity of diet-ary habits
(12). The traditional Mediterranean diet is espe-cially
interesting, as it is characterized by a high intake of
vegetables, legumes, fruits and nuts, unrefined cereals, olive
oil, and fish as well as a low intake of saturated fats, meat, and
poultry and a low-to-moderate intake of dairy products (13).
The Mediterranean diet concept was first brought to light by
Ancel Keys and The Seven Countries Study of cardiovascular
disease (14) and has been proven to reduce both morbidity and
mortality in numerous dis-eases (15). However, to our
knowledge, no study has been performed to investigate
whether a Mediterranean diet may be a preventive factor
against the development of COPD.
Our aim was, therefore, to investigate if a Mediterranean-
style dietary pattern is associated with the development of
COPD in the large cohort of the V€asterbotten Intervention
Program (VIP) in northern Sweden.

CONTACT Bj€orn Sundstr€om bjorn.sundstrom@umu.se Department of Public Health and Clinical Medicine, Section of Medicine,
Umeå University, SE-90185,
Umeå, Sweden.
Supplemental data for this article can be accessed at https://doi.org/10.1080/15412555.2019.1634039
2019 The Author(s). Published with license by Taylor and Francis Group, LLC
This is an Open Access article distributed under the terms of the Creative Commons Attribution-NonCommercial-NoDerivatives License
(http://creativecommons.org/licenses/by-nc-nd/4. 0/), which permits non-commercial re-use, distribution, and reproduction in any medium, provided the original work is
properly cited, and is not altered, transformed, or built upon in any way.
2 A. FISCHER ET AL.
Methods
Study area and settings
Due to a high incidence of cardiovascular diseases in the
V€asterbotten County in northern Sweden, with approxi-
mately 260,000 citizens, a health-screening and intervention
project was started in 1985 (16) and gradually extended to the
V€asterbotten Intervention Programme (VIP). Since 1991, the
program invited all citizens aged 30, 40, 50, and 60 years
throughout the county; individuals aged 30 years were not
included after 1996. The participation rate for the VIP var-ied
between 48% and 57% of the target population during the first
years; however, it gradually increased to 72% in recent years
(17). By the end of 2011, approximately 30% of the studied
individuals had participated in the VIP more than once (18).
As part of the VIP, background data, such as education and
marital status, and data on lifestyle, such as smoking and
dietary habits, are investigated through the use of
questionnaires. In addition, participants are given the
opportunity to donate their data to the Northern Sweden
Health and Disease Study (NSHDS) for future research
purposes.
Identification of cases and controls
Cases were identified through registered visits with a diag-
nosis of COPD at the Department of Medicine, Division of
Respiratory Medicine and Allergy, University Hospital, Umeå,
between 2007 and 2013, using International Classification of
Diseases (ICD)-codes J44.0, J44.1, and J44.9 according to
clinical practice. The use of J44.x for epidemio-logical studies
of COPD in a Swedish context has been vali-dated with
acceptable validity for epidemiological research (19). The
resulting cases were searched in the NSHDS for visits in the
VIP before their first registered diagnosis at the University
Hospital during 1991–2013. For each case found, five controls
matched for smoking, age, sex, place of resi-dence, time of
examination in the VIP (±2.5 years), and ver-sion of
questionnaires used were selected using a sampling scheme
with replacement (WR scheme).
Study variables and handling of data
Smoking habits in the VIP questionnaires were labeled as
never smoker, current daily smoker, current occasional
smoker, previous daily smoker, and previous occasional
smoker; these were also used as matching variables. In some
versions of the questionnaires used in the VIP, additional
quantitative data on smoking were requested (i.e., number of
cigarettes smoked per day), thereby providing data on
smoking intensity. Education level was evaluated as a
dichotomous variable with higher education defined as stud-
ies at college or university. Participants were classified as
either living alone or cohabitating; the former was grouped as
unmarried, widow/widower, or divorced/separated, and the
latter as married, cohabitating, or remarried.
Dietary habits were assessed through the use of a semi-
quantitative food frequency questionnaire (FFQ). Until 1996,
the form consisted of 84 questions, but since 1997, the ques-
tions have been merged to range between 64 and 66 ques-
tions. The longer version of the FFQ has been validated, (20)
and comparisons between the versions have shown that
ranking is similar, although absolute levels tend to be slightly
lower when using the shorter version (21). The FFQ assesses
the intake frequency of different foodstuffs on a nine-level
scale ranging from never to four or more times per day and
contains examples of portion sizes. These fre-quencies and
portion sizes were used to calculate daily energy and
nutritional intake based on the reference data-bases of the
Swedish National Food Administration (22). Nutritional
intake was adjusted with regard to energy intake using the
residual method (23).
For cases and controls, a food intake level (FIL) was cal-
culated as energy intake divided by basal metabolic rate, the
latter according to Schofield (24). Individuals who did not
state portion size in the FFQ (n ¼ 320; 92 cases and 228
controls), thereby rendering calculations of energy intake
impossible, were excluded. Furthermore, individuals with a
FIL below the bottom 1st and above the upper 99th percen-
tiles in the total VIP population were classified as unreliable
under and over-reporters and were also excluded from the
study. Individuals who stated that they were occasional or
previous occasional smokers were excluded due to issues with
the classification of their exposure, i.e., only cases and
controls who stated that they were current smokers, ex-
smokers, or never smokers were included in the study. If cases
had several visits in the VIP before their diagnosis of COPD
(n ¼ 65), the visit closest to the mean time between the VIP
and the diagnosis of COPD for the total cohort was used to
decrease the heterogenicity of the studied group. After
selection according to the criteria above, the final cohort
consisted of 370 cases and 1432 controls.
Definition of the Mediterranean diet
Adherence to a Mediterranean dietary pattern was scored
based on the Mediterranean diet score (MDS) established by
Trichopoulou et al. (13,25) with modifications by Tognon et
al. (26). The modified MDS is based on food components
typical of a Mediterranean diet, where a favorable gender-
specific intake above or below the median was scored one
point, together with a favorable intake of alcohol.
The following components were scored one point each: (1)
a ratio between intake of mono-/polyunsaturated and saturated
fats above the median; (2) intake of vegetables and potatoes
above the median; (3) intake of fruit above the median; (4)
intake of wholegrain cereals above the median; (5) intake of
fish above the median; (6) intake of meat and meat products
below the median; (7) intake of dairy prod-ucts below the
median; and (8) an intake of alcohol between 5–25 g/day for
women and 10–50 g/day for men. The gen-der-specific
median intake of the components is presented in
Supplementary Table S1. Since the shorter version of the FFQ
tends to yield slightly lower intake levels (21), the above
scoring system was not only gender-specific but also specific
to the version of FFQ used. The final modified MDS

Table 1. Descriptive data for 370 individuals who developed COPD and 1432 controls matched for age, sex, and smoking habit. a
Variable
Age at screening, years, mean (min–max)
Time to first visit to Respiratory Department, Umeå, mean (SD)
Female, n (%)
Current smokers, n (%)
Ex-smokers, n (%)
Never smokers, n (%)
Body mass index, kg/m2, mean (SD)
Higher education, n (%)
Living alone, n (%)
Low adherence to MDS, n (%)
Medium adherence to MDS, n (%)
High adherence to MDS, n (%)
aSmoking status was defined at the time of examination in the V€asterbotten Intervention Programme.
bUnadjusted OR with 95% CI for the development of chronic obstructive lung disease calculated using conditional logistic regression analyses.
OR: odds ratio; CI: confidence interval; SD: standard deviation; MDS: Mediterranean diet score.
score ranged from 0 to 8, with a higher score indicating
greater adherence to a Mediterranean-like diet.
Statistical method
Odds ratios (ORs) for developing COPD were estimated using
conditional logistic regression analysis with 95% confi-dence
intervals (CIs). ORs were calculated by adherence to a
Mediterranean diet using a three-grade scale as in the study
by Sjogren€ et al. (27), categorizing individuals as low-adher-
ent (0–2 points), medium-adherent (3–5 points), and high-
adherent (6–8 points). In the calculation of ORs, the lowest
adherence was used as the reference. Adjustments were made
to models based on a scientific and clinical rationale. To
evaluate the importance of the different food compo-nents
contained in the modified MDS, ORs were calculated based
on the scoring of each component, i.e., above or below the
median intake using conditional logistic regres-sion. In a
sensitivity analysis, the dietary habits stated at the first
available visit in the VIP at least 10 years before the diagnosis
of COPD were analyzed. All final statistical calcu-lations were
performed using Stata (version 13.1, StataCorp, Lakeway, TX,
USA), and significance was set at a p-value <0.05. All study
participants provided informed consent through the original
data collection in the VIP cohort, and the procedures of this
study were approved by the Regional Ethical Review Board at
the University Hospital, Umeå, in accordance with the
Declaration of Helsinki and the Swedish Law on personal data
act (PuL).
Results
Descriptive data for the 370 individuals who later visited the
Department of Medicine, University Hospital, Umeå with a
diagnosis of COPD (referred to as cases) and the 1432
matched controls are presented in Table 1. Data from the VIP
were collected on average 11.1 years (SD 6.6 years) before the
first registered medical visit. There was a signifi-cant
difference between the cases and controls with respect to
education level as well as living arrangements (p ¼ 0.001 and
p < 0.001, respectively).
Individuals with higher education scored higher on the
modified MDS (mean [standard deviation (SD)] 4.2 [1.5])
COPD: JOURNAL OF CHRONIC OBSTRUCTIVE PULMONARY DISEASE 3
Cases (n ¼ 370) Controls (n ¼ 1432) OR (95% CI)b
55 (30–61) 55 (30–61)
11.1 (4.5)
213 (58) 817 (57)
269 (73) 1040 (73)
83 (22) 322 (22)
18 (5) 70 (5)
25.7 (4.9) 26.0 (3.9) 0.98 (0.95–1.01)
42 (11) 258 (18) 0.56 (0.39–0.80)
86 (23) 224 (16) 1.69 (1.26–2.26)
116 (31) 327 (23) –
216 (58) 896 (63) –
38 (10) 209 (15) –
than those with a lower education level (3.6 [1.6];
p < 0.001). Individuals living alone scored lower on the
modified MDS (mean [SD] 3.5 [1.6]) than those living with
someone (3.7 [1.6]; p < 0.05).
In unadjusted analyses, individuals with medium and high
adherence to the modified MDS exhibited significant lower
ORs in a dose-response manner to develop COPD than those
with low adherence (Table 2). The significance and dose-
response relationship remained in differently adjusted models.
In the sensitivity analysis restricted to the first available visit
in the VIP at least 10 years (243 cases; mean time between
assessment of dietary habits and diagno-sis 14.4 years; range
10.0–21.8 years) before the diagnosis of COPD, similar
findings were observed (Supplementary Table S2).
In the analysis of the individual scores for food items
comprising the modified MDS and the odds to develop COPD,
significant effects could only be observed for the consumption
of fruit (Table 3).
Discussion
In this study, adherence to a Mediterranean-like diet was
shown to be inversely associated with the development of
COPD. Moreover, a higher adherence was associated with a
lower odds for developing COPD. Adherence to a
Mediterranean diet was associated with higher education and
not living alone. Our findings also highlight the import-ance
of studying the diet as a whole, since only fruit had a
significant effect on the odds when analyzing individual
components contained in the modified MDS score in this
population.
Previous prospective studies examining dietary patterns and
the risk of developing COPD have focused on either
prudent/healthy or Western diets (9,10,28,29). In these stud-
ies, a prudent/healthy diet lowered the risk of developing
COPD, whereas a Western diet increased the risk. In a meta-
analysis on this topic, a healthy/prudent diet was con-cluded to
decrease the risk of developing COPD (OR 0.55, 95% CI
0.46–0.66), whereas a Western diet increased the risk (OR
2.12, 95% CI 1.64–2.74) (30). Since healthy/prudent dietary
patterns have characteristics partly overlapping with a
Mediterranean diet (12,31), our results concur with the
4 A. FISCHER ET AL.

Table 2. Mediterranean diet score (MDS) and odds ratios (95% confidence interval) for developing chronic obstructive pulmonary disease among
370 cases and 1431 controls matched for age, sex, and smoking habit.a
Crude Adjusted, model 1b Adjusted, model 2c Adjusted, model 3d Adjusted, model 4e
Cases (n) 370 370 367 286 284
Modified MDS
Low adherence 0–2 1 (reference) 1 (reference) 1 (reference) 1 (reference) 1 (reference)
Medium adherence 3–5 0.68 (0.53–0.88) 0.71 (0.55–0.92) 0.73 (0.56–0.95) 0.67 (0.50–0.91) 0.73 (0.53–0.99)
High adherence 6–8 0.50 (0.33–0.76) 0.54 (0.36–0.82) 0.56 (0.37–0.86) 0.52 (0.31–0.87) 0.59 (0.35–0.97)
a
Smoking status was defined at the time of examination in the V€asterbotten Intervention Programme.
b
Adjusted for higher education.
cAdjusted for higher education and living alone.
dAdjusted for numbers of cigarettes smoked per day.
e
Adjusted for higher education, living alone and numbers of cigarettes smoked per day.
Bold font indicate statistically significant result p<0.05.

Table 3. Consumption of different food groups and odds ratios (95% confi-
dence intervals) for developing chronic obstructive pulmonary disease.
Single MDS component OR (95% CI)
Intake above the median
(MUFA þ PUFA): SFA 0.81 (0.64–1.03)
Vegetables and potatoes 0.81 (0.64–1.02)
Fruit 0.71 (0.57–0.90)
Wholegrain cereals 0.88 (0.70–1.11)
Fish 0.88 (0.70–1.10)
Intake below the median
Meat and meat products 0.94 (0.75–1.18)
Dairy 0.88 (0.70–1.11)
Intake within limits
Alcohol 0.84 (0.62–1.15)
MUFA: monounsaturated fat; PUFA: polyunsaturated fat; SFA: saturated fat; OR:
odds ratio; CI: confidence interval.
Bold font indicate statistically significant result p<0.05.
findings of these studies. In the analyses of individual com-
ponents contained in the modified MDS score, only fruit
intake was significantly associated with a decreased odds of
developing COPD. This finding highlights the complexity of
assessing dietary habits and the value of studying the effect of
the diet beyond isolated nutrients. The phenomenon of
observing effects from the resulting MDS and not from iso-
lated components of the score was previously described by
Trichopoulou et al. in the original MDS in 1995 (13).
As described by Romieu and Trenga (32), there might be
several explanatory theories regarding the effects of diet on
the development of COPD. For example, the highly oxida-tive
environment of the lung could be protected by antioxi-dants
provided by diet. Moreover, the anti-inflammatory properties
of omega-3 fatty acids, as well as the pro-inflam-matory
properties of omega-6 fatty acids, might be of importance,
since inflammation plays an important role in COPD (33).
Vegetables and fruits are high in antioxidants, and fish and
nuts are high in omega-3 fatty acids, whereas red meat is high
in omega-6 fatty acids. The protective effect of vegetables,
fruits, and fish and the deleterious effect of red meat in the
development of COPD have been demon-strated in several
studies (5,6,11,34–40). The effect of proc-essed meat such as
sausage and cured meat has also garnered attention due to
their high content of food addi-tives such as nitrites, and it has
been proposed that these additives may cause oxidative stress
in the lung (39). In a recent meta-analysis, it was concluded
that each 50 grams of increase in the intake of processed meat
per week was asso-ciated with an 8% increased risk of
developing COPD (41).
The main strength of this study is the use of comprehensive
and validated prospective data collected equally among thor-
oughly matched controls and cases in the VIP cohort. Although
the diagnosis of COPD when using ICD coding for identification
of the cases was not verified by spirometry, individuals with
COPD who visit a specialist care unit usually suffer from
advanced disease, mainly spirometric grade GOLD 3 or 4,
according to the GOLD criteria (1). A misdiagnosis of the cases
is therefore unlikely, but it may introduce a bias toward a more
severe disease among the cases. Another limita-tion with the lack
of spirometry in the studied population is that it cannot be ruled
out that there are controls that do have COPD. However, this
should mainly introduce a statistical type-II error and will
decrease the power and possibilities to find a real difference.
Since COPD is a slowly progressing disease, and patients are
most often not diagnosed until symp-toms are evident, slowly
emerging symptoms may have already affected the individuals’
lifestyle, including dietary habits, at the time of participation in
the VIP examinations. Nonetheless, we were able to verify our
findings in the sensitivity analyses, which were restricted to
dietary habits more than 10 years before the diagnosis. Last,
although we have adjusted for education level and living alone,
we cannot rule out that there still is residual confounding, or
other unmeasured factors related to lifestyle that may contribute
to the results.
Conclusion
Among the population of the V€asterbotten County, a
Mediterranean-like diet is inversely associated with the
development of COPD, defined as a visit to a specialist
health-care clinic with a registered diagnosis code for COPD.
Adherence to this diet was associated with higher education
level and not living alone. Taken together, the present study
suggests that healthy dietary habits might be of value to
investigate further as a protective factor against the
development of COPD, especially among individuals with
lower education and those living alone.
Acknowledgments
We gratefully acknowledge the Northern Sweden Medical Research
Bank and V€asterbotten County for collecting and providing access to
the data. Construction of the diet database has been supported by the
Swedish Research Council for Health, Working Life and Welfare
(FORTE) and The Swedish Research Council.

Declaration of interest
The authors report no conflict of interest.
ORCID
Bj€orn Sundstrom€ http://orcid.org/0000-0001-7226-0969
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