nutrients

Review
Diet and Asthma: Is It Time to Adapt Our Message?
Laurent Guilleminault 1 ID , Evan J. Williams 1 ID
, Hayley A. Scott 1 , Bronwyn S. Berthon 1 ID
,
Megan Jensen 2 ID and Lisa G. Wood 1,2, * ID
1 Priority Research Centre for Healthy Lungs, Hunter Medical Research Institute, University of Newcastle,
Callaghan, NSW 2308, Australia; guillel@free.fr (L.G.); evan.j.williams@uon.edu.au (E.J.W.);
hayley.scott@newcastle.edu.au (H.A.S.); bronwyn.berthon@newcastle.edu.au (B.S.B.)
2 Priority Research Centre Grow Up Well, Hunter Medical Research Institute, University of Newcastle,
Callaghan, NSW 2308, Australia; megan.jensen@newcastle.edu.au
* Correspondence: lisa.wood@newcastle.edu.au; Tel.: +61-240-420-147; Fax: +61-249-855-850

Received: 13 September 2017; Accepted: 6 November 2017; Published: 8 November 2017

Abstract: Asthma is a chronic respiratory disorder which is associated with airway inflammation.
Environmental factors, in association with genetic susceptibility, play a critical role in asthma
pathophysiology. Inhaled allergens, smoke exposure, indoor and outdoor air pollution are common
triggers of asthma symptoms. Although the role of diet has clearly established mechanisms in diseases
such as cardiovascular disease, type 2 diabetes, and cancer, it is not commonly identified as a causal
factor in asthma. However, some dietary patterns, such as the Western diet, which includes a high
intake of refined grains, processed and red meats, and desserts, have pro-inflammatory effects. On the
contrary, the Mediterranean diet, with high intake of fruits and vegetables has anti-inflammatory
properties. The influence of food on asthma outcomes is of growing interest, but dietary habits
of asthma patients are not commonly investigated in clinical practice. In this review, we focus on
the impact of diet on asthma risk and asthma control. We also detail the influence of diet on obese
patients with asthma.

Keywords: diet; asthma; inflammation; obesity

1. Introduction
Eating is an essential part of life. Beyond the concept of survival, it is well known that food
plays an important role in preserving health [1]. The famous Hippocrates’s quote “let food be thy
medicine” introduced the idea of the potential impact of food on health. Nowadays, the role of food in
chronic diseases, including cardiovascular disease, type 2 diabetes, metabolic syndrome, and cancer,
is undisputed [2], and dietary interventions are an important component in managing numerous
chronic diseases [3]. The role of diet as a key factor influencing the development of allergic diseases
has been described [4]. The direct influence of food on asthma outcomes regardless of allergic status
has emerged more recently [5], with dietary factors showing the potential to be directly involved in
asthma pathogenesis [6,7]. Obese asthmatics have a distinct phenotype with a unique pathophysiology
(low eosinophilic inflammation, low allergen sensitization) [8,9]. The specific role of diet on asthma
outcomes in obese patients is also of growing interest due to their limited responsiveness to inhaled
corticosteroids, as well as other difficulties faced when managing these patients [10,11]. The key
question for clinicians is to know whether changes in the diet could benefit patients with asthma in
routine practice. In this review, we will describe the impact of diet on asthma, and identify messages
that can be used in asthma management. Given that obese asthmatic patients represent a particular
group in terms of inflammation and clinical management, we will also focus on the effect of diet on
asthma patients with obesity.

Nutrients 2017, 9, 1227; doi:10.3390/nu9111227 www.mdpi.com/journal/nutrients

Nutrients 2017, 9, 1227 2 of 25

2. Dietary Patterns
Nutrients 2017, 9, 1227 2 of 25
The literature examining the effect of dietary intake on asthma risk and progression examines
2. Dietary Patterns
both individual nutrients and dietary patterns. Dietary patterns describe the overall habitual intake of
food and food The literature
groups by examining the effect
individuals andof dietary
groups, intake
withonconsideration
asthma risk andgiven progression
to theexamines
combination,
both individual nutrients and dietary patterns. Dietary patterns describe
frequency, quantity, and variety [12]. Dietary pattern analysis provides several advantages the overall habitual intake in
of food and food groups by individuals and groups, with consideration given to the combination,
examining the relationship between dietary intake and health outcomes: foods or nutrients are not
frequency, quantity, and variety [12]. Dietary pattern analysis provides several advantages in
eaten inexamining
isolation,the andrelationship
considerable interactions
between and synergistic
dietary intake effects exist
and health outcomes: foodswith common
or nutrients arenutrients
not in
foods [13].
eatenTwo commonly
in isolation, investigated
and considerable dietary patterns
interactions are the
and synergistic Mediterranean
effects exist with common diet (Med-diet)
nutrients and
the Western diet.
in foods [13]. Two commonly investigated dietary patterns are the Mediterranean diet (Med-diet)
and the Western
The Mediterranean diet.dietary pattern was identified in the 1950’s and 1960’s along the coastal
The Mediterranean dietary pattern was identified in the 1950’s and 1960’s along the coastal
regions of southern European countries, including Italy and Greece, and was associated with a lower
regions of southern European countries, including Italy and Greece, and was associated with a lower
mortality rate from coronary heart disease [14]. Current recommendations for the Med-diet promote
mortality rate from coronary heart disease [14]. Current recommendations for the Med-diet promote
meals based
meals on a variety
based of fruits,
on a variety vegetables
of fruits, vegetablesand and wholegrain cereals
wholegrain cereals [15].[15]. In contrast,
In contrast, the Western
the Western
diet, prevalent in developed
diet, prevalent in developedcountries,
countries,isisdominated
dominated by byconvenience
convenience and andhighlyhighly processed
processed foods, foods,
resulting
resulting in highinintakes
high intakes of refined
of refined grains,
grains, processed and
processed andred
redmeats,
meats, desserts
dessertsand and
sweets, fried foods,
sweets, fried foods,
and high-fat dairy products, with low intake of fruits and vegetables (Figure
and high-fat dairy products, with low intake of fruits and vegetables (Figure 1) [12]. 1) [12].

Figure 1. Characteristics
Figure of Mediterranean
1. Characteristics of Mediterranean and Western
and Western diets.
diets. The The Mediterranean
Mediterranean dietaryispattern
dietary pattern
is basedbased
on aon a variety
variety of fruits,
of fruits, vegetables and
vegetables and wholegrain
wholegrain cereals. In contrast,
cereals. the Western
In contrast, diet is diet is
the Western
dominated by convenience and highly processed foods, and includes a high intake of
dominated by convenience and highly processed foods, and includes a high intake of refined grains, refined grains,
processed and red meats, desserts and sweets, fried foods, and high-fat dairy products, with a low intake
processed and red meats, desserts and sweets, fried foods, and high-fat dairy products, with a low
of fruits and vegetables.
intake of fruits and vegetables.
One of the key differences between the Med-diet and Western diet, is the amount of fruits and
One vegetables
of the keythat are consumed.between
differences Increasedtheintakes of fruit and
Med-diet and vegetables
Western are recommended
diet, for the
is the amount of fruits
general population due to their abundance of vitamins, minerals, fibre and non-nutritive
and vegetables that are consumed. Increased intakes of fruit and vegetables are recommended
phytochemicals such as antioxidants, polyphenols, flavonoids and carotenoids, and low energy
for the content
general[16].
population due to their abundance of vitamins, minerals, fibre and non-nutritive
Fruits and vegetables feature prominently in the dietary guidelines for many countries,
phytochemicals such as [17],
including Australia antioxidants,
Canada [18],polyphenols,
USA [19], United flavonoids andFrance,
Kingdom [20], carotenoids,
Germany and low energy
and Spain
content [21],
[16]. with
Fruits and vegetablesranging
recommendations featurefrom
prominently
5–7 servesinpertheday.
dietary guidelines
However, for many
the intake in manycountries,
includingWesternised
Australiacountries is inadequate
[17], Canada [18], USA with mean
[19], national
United intakes [20],
Kingdom meeting recommended
France, Germanytargets in
and Spain [21],
only 0.4% of the global population for fruits and vegetables [22].
with recommendations ranging from 5–7 serves per day. However, the intake in many Westernised
Another key difference between the Med-diet and Western diet, is the amount of seafood
countries is inadequate with mean national intakes meeting recommended targets in only 0.4% of the
consumed. Seafood is the primary food source of long-chain omega-3 (LC n-3) polyunsaturated fatty
global population
acids (PUFA), fordocosahexaenoic
fruits and vegetables [22].eicosapentaenoic acid (EPA), and docosapentaenoic
acid (DHA),
Another key difference between the Med-diet and Western diet, is the amount of seafood
consumed. Seafood is the primary food source of long-chain omega-3 (LC n-3) polyunsaturated
fatty acids (PUFA), docosahexaenoic acid (DHA), eicosapentaenoic acid (EPA), and docosapentaenoic
acid (DPA), with fatty fish such as salmon, mackerel, and sardines providing higher levels
Nutrients 2017, 9, 1227 3 of 25

(1.7–2.2 g/100 g) [23]. Western populations are estimated to have a low intake of LC n-3 [23] with few
reaching the targets for chronic disease reduction of 0.6 g/day for men and 0.4 g/day for women [17],
which can be achieved by consuming the recommended two or more serves of (preferably oily) fish
per week [24]. Fish oil supplements contain approximately 30–60% EPA/DHA, and are often used to
achieve higher LC n-3 intakes [23].
In general, the Med-diet is believed to have health benefits, largely attributed to the content of
fibre, antioxidants, protein, and moderate amounts of fat-predominantly from mono-unsaturated
(MUFA) and omega-3 PUFA. On the other hand, consumption of a Western diet is believed to
have detrimental consequences, due to the excess consumption of total energy, saturated fat and
omega-6 PUFA, sugar and sodium, combined with the low intakes of omega-3 PUFAs, protein, fibre,
micronutrients (including folate and magnesium), antioxidants, and phytochemicals (e.g., carotenoids,
flavonoids) [25].

3. Diet and Inflammation

3.1. Diet and Systemic Inflammation

Systemic inflammation can be a feature of asthma, particularly in the neutrophilic inflammatory
phenotype [26,27], and is associated with worse disease outcomes, such as poorer lung function [28–30],
increased frequency of exacerbations [31,32] and increased airway inflammation [26,31].
Dietary intake has been shown to modify systemic inflammation (Figure 2). The Western diet has
been thought to promote a pro-inflammatory environment due to factors such as lack of antioxidants,
which increases susceptibility to oxidative stress, and abundance of saturated fatty acids, which can
lead to innate immune activation, via activation of receptors such as toll like receptor 4 (TLR4),
which stimulates the NF-κB inflammatory cascade [33–35]. In contrast, the Med-diet is thought
to promote an anti-inflammatory environment [36,37], due to the presence of anti-inflammatory
nutrients such as unsaturated fatty acids e.g., MUFA, omega-3 PUFA and antioxidants [36,37].
These anti-inflammatory effects have been shown in a recent meta-analysis noting significant decreases
in plasma C-reactive protein (CRP), IL-6 and intracellular adhesion molecule-1 (ICAM-1) in healthy
individuals following a Med-diet [38].

3.2. Diet and Airway Inflammation

Chronic inflammation of the airways is a key component of asthma [39], which may be modulated
by dietary intake [40–44]. High fat intake, a characteristic of the Western diet, can cause an increase
in airway inflammation. Consumption of a high-fat mixed meal has been shown to increase sputum
neutrophils 4 h post-meal in patients with asthma [40], as well as activation of a number of genes
in sputum involved in “immune system processes”, such as TLR4, indicating an increase in airway
inflammation [44]. Reduction of dietary saturated fat intake was associated with a reduction in
neutrophilic airway inflammation in asthmatics [45]. In adults with severe asthma, higher fat and
lower fibre intakes have been associated with increased eosinophilic airway inflammation [42].
In contrast, fruits, vegetables and their antioxidants may lower airway inflammation [41,43].
Fruit and vegetable intake was inversely associated with IL-8 protein in nasal lavage of asthmatic
children [43]. In asthmatic adults, intake of tomato juice, which is abundant in the antioxidant lycopene,
reduced airway neutrophil influx and sputum neutrophil elastase activity after just seven days of
supplementation [41]. The link between systemic inflammation and airway inflammation induced by
diet is still unknown.
Nutrients 2017, 9, 1227
Nutrients 2017, 9, 1227 4 of 25 4 of 25

Figure 2. Figure 2. Systemic

Systemic and airway
and airway effects
effects ofofdietary
dietary patterns
patterns onon
asthma. The Western
asthma. diet promotes
The Western a
diet promotes a
pro-inflammatory environment and causes an increase in airway inflammation. Fruit and vegetable
pro-inflammatory environment and causes an increase in airway inflammation. Fruit and vegetable
consumption has systemic anti-inflammatory properties, with a decrease of pro-inflammatory
consumption hasinsystemic
cytokines anti-inflammatory
plasma. Fruit and vegetables are alsoproperties, with
associated with lowera airway
decrease of pro-inflammatory
inflammation and a
cytokines reduction
in plasma. Fruit andinvegetables
of neutrophils aremicrobiota
asthmatics. Gut also associated with
plays a role lower airway
in immune response inflammation
to diet in and
asthma. Metabolites such as short-chain fatty acids (SCFA) (including ω-3 fatty
a reduction of neutrophils in asthmatics. Gut microbiota plays a role in immune response to diet acids) that have
immunomodulatory effects are produced in high amounts after fruit and vegetable intake. The
in asthma. Metabolites such as short-chain fatty acids (SCFA) (including ω-3 fatty acids) that have
western diet altered microbiota composition and potentiate inflammation.
immunomodulatory effects are produced in high amounts after fruit and vegetable intake. The western
diet altered
3.3. Dietmicrobiota composition and potentiate inflammation.
and Gut Microbiota
The gut microbiome is responsible for the production of some of the most important
3.3. Diet and Gut Microbiota
metabolites that impact on immune and metabolic responses and can be modulated by different
dietary patterns [46]. Fruit and vegetables are a rich source of dietary fibre, which is fermented by
The gut microbiome
gut bacteria, is responsible
to produce for the
metabolites such production
as short-chain fattyofacids
some of theThese
(SCFA). most important
metabolites havemetabolites
that impact on immune and
immunomodulatory metabolic
mechanisms, such responses
as activationand can be modulated
of metabolite-sensing by different dietary
G-protein-coupled
receptors
patterns [46]. (GPCRs),
Fruit and and epigenetic are
vegetables and gene
a richtranscription
source of modulation
dietary and havewhich
fibre, been shown to affect
is fermented by gut
airway inflammation and airway reactivity in animal models of allergic airways disease [47–49].
bacteria, to produce metabolites such as short-chain fatty acids (SCFA). These
High fibre diets have been shown to protect against airway allergic responses, associated with
metabolites have
immunomodulatory mechanisms, such as activation of metabolite-sensing
increased colonic Bacteroidetes and Actinobacteria species, and decreased Firmicutes and G-protein-coupled receptors
(GPCRs), Proteobacteria
and epigenetic andIngene
[50,51]. mice, transcription modulation
a high dietary fibre intake during andpregnancy
have been shown
protects to affect
against the airway
development of airway disease in the offspring, with marked effects on the composition
inflammation and airway reactivity in animal models of allergic airways disease [47–49]. High fibre of the gut
microbiota [52].
diets have been shown to protect against airway allergic responses, associated with increased colonic
A high-fat diet also alters gut microbiota composition, particularly the expansion and
Bacteroidetes and Actinobacteria
colonization species,reduction
of invasive bacteria, and decreased Firmicutes
in protective andand
bacteria, Proteobacteria
reduction in [50,51].
SCFA In mice,
a high dietary fibre intake
concentrations, duringa pregnancy
supporting potential roleprotects against
in inflammation andthe development
immune of airway
response [53–55]. disease in the
The role
offspring,ofwith
highmarked
fat diets on gut microbiota
effects and asthmatic immune
on the composition of the responses is unknown.
gut microbiota [52].
A high-fat diet also alters gut microbiota composition, particularly the expansion and colonization
of invasive bacteria, reduction in protective bacteria, and reduction in SCFA concentrations, supporting
a potential role in inflammation and immune response [53–55]. The role of high fat diets on gut
microbiota and asthmatic immune responses is unknown.

4. Diet and Risk of Asthma

The influence of dietary intake on asthma risk has been examined in many studies over the last
two decades. Mediterranean diets and Western diets, whole foods and individual nutrients, have been
found to have an influence on asthma risk, at various stages of the life cycle (Table 1).
 Nutrients 2017, 9, 1227 5 of 25

4. Diet and Risk of Asthma

The influence of dietary intake on asthma risk has been examined in many studies over the last
two decades. Mediterranean diets and Western diets, whole foods and individual nutrients, 5have
Nutrients 2017, 9, 1227 of 25
been found to have an influence on asthma risk, at various stages of the life cycle (Table 1).

Table 1.1. Diet and

Table and risk
risk of
of asthma
asthma or or wheezing.
wheezing. Beneficial
Beneficial effect; negative effect; No
No
effect; ?? =
= no data. Very Very strong evidence defined as
evidence is defined as data
data obtained
obtained inin meta-analysis
meta-analysis of of randomized
randomized
controlled
controlled trials
trials(RCTs);
(RCTs);Strong
Strong evidence
evidenceis defined as data
is defined as obtained in individual
data obtained RCT; Low
in individual evidence
RCT; Low
is defined as
evidence is data
definedobtained
as datain individual
obtained prospective
in individualstudies or meta-analysis
prospective studiesoforprospective
meta-analysisstudies;
of
Very low evidence
prospective studies;isVery
defined
lowas data obtained
evidence in individual
is defined cross-sectional
as data obtained or case-control
in individual studies,
cross-sectional or
or meta-analysis
case-control of cross-sectional
studies, or meta-analysis or case-control studies.or
of cross-sectional Incase-control
case of conflicting results
studies. between
In case studies,
of conflicting
data from
results the studies
between withdata
studies, the from
most therobust methodology
studies are used
with the most to define
robust the effectare
methodology of diet
usedon toasthma
define
risk. * One
theNutrients
effect ofMeta-analysis
2017, diet
9, 1227on asthma found
risk. a* One
negative association
Meta-analysis with aasthma
found negativeor association
wheeze and 25one asthma
5 ofwith found noor
association;
wheeze and**one conflicting
found no results in cross-sectional
association; studies;
** conflicting *** from
results diet but not from
in cross-sectional supplementation.
studies; *** from diet
ts 2017, 9, 1227 Nutrients 2017,Risk
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5 of 25 5 of 25 5 of 25
but not from supplementation.
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et and Risk of Asthma 4. Diet and Risk of Asthma
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and individual nutrients, have Adulthood
Nutrients 2017, 9, 1227
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Nutrients 2017, 9, 1227 6 of 25

[61,63,74–77]. In cross sectional studies, fast food consumption at least three times a week during
pregnancy increased the odds of childhood wheeze by 2.17–3.96, compared to a consumption less
than once a week [60,86,87]. In contrast, cohort studies found no association between the Western diet
or a high intake of fast food consumption during pregnancy and childhood wheeze [63,91–93]. In a
meta-analysis, no association was found between meat intake during pregnancy and childhood wheeze
and asthma, but one cohort study found that high intakes of ‘processed’ meat during pregnancy were
associated with an increased risk of wheeze in the first year of life with an odd ratio (OR) of 1.18
(95% confidence interval (CI) 1.02–1.37) [62,101].
Given the inconclusive data, no message can be clearly delivered to pregnant women regarding
dietary patterns or nutrients other than the current dietary guidelines.

4.1.2. Vitamin D and E and Fish Oil: Beneficial

Individually, intake of vitamins A (and carotenoids), B, or C during pregnancy are not associated
with wheeze and/or asthma in childhood [75,114–116,119–122]. However, vitamin D intake during
pregnancy was associated with a reduction in childhood wheeze (OR ranged from 0.58, 95% CI
0.38–0.88 to 0.81; 95% CI, 0.67–0.98) in meta-analyses [101,123]. A similar effect has been observed with
vitamin E (OR 0.54, 95% CI 0.41–0.71) [75,101,121,122,127]. However, no effect of vitamin D or E on
risk of childhood asthma has been found [75,101,115,124,125,127]. Although no guidelines have been
published on the necessity of vitamin supplementation in pregnant women for decreasing asthma risk,
general guidelines used for vitamin D supplementation during pregnancy should be applied in all
pregnant women by respiratory medicine physicians [144].
No link has been observed between fish intake during pregnancy and wheeze and/or asthma in
childhood in most studies, nor in a meta-analysis [74,77,92,102–108]. However, fish oil supplementation
during pregnancy has been shown to decrease wheeze or asthma in childhood [130–132]. In an RCT,
fish oil supplementation (2.7 g/day) during pregnancy, containing LC n-3 PUFA, reduced the risk
of asthma development in the offspring by 63% (95% CI: 8–85%) and this protection appears to be
maintained into adulthood [130,131]. Latest evidence from an RCT also found a reduction in asthma
or wheeze in children from mothers using fish oil supplements (2.4 g/day) during pregnancy [132].

4.2. Children

4.2.1. Breastfeeding: Beneficial

The World Health Organization and the American Academy of Paediatrics emphasize the
value of breastfeeding for infant health. The strong protective effect of breastfeeding on asthma
development is clearly established. This effect is particularly observed at age 0–2, and decreases over
time but is maintained after seven years of age [56]. Compared to no breastfeeding, any duration of
breastfeeding was inversely associated with asthma in children aged 0–2 years, 3–6 years, and older
than 7 years, with an OR of 0.65 (95% CI 0.51–0.82), 0.79 (95% CI 0.68–0.91) and 0.86 (95% CI 0.77–0.96),
respectively [56].

4.2.2. Fruit and Vegetables: Beneficial

Fruit and vegetable intake in childhood appears to have a beneficial effect on wheeze and asthma
risk. In a meta-analysis, fruit intake had an inverse association with wheeze and asthma with a relative
risk (RR) of 0.81 (95% CI: 0.74–0.88) and 0.90 (95% CI: 0.86–0.94) respectively [78]. Vegetable intake
was also inversely associated with wheeze and asthma with a RR of 0.88 (95% CI: 0.79–0.97) and
0.91 (95% CI: 0.82–1.00), respectively [78]. Our group reported a beneficial effect of fruits or vegetables
on asthma [80]. In the only cohort study included in this meta-analysis, fresh fruit consumption at
early age and long-term fruit intake, but not vegetable intake, was associated with reduced asthma
symptoms (OR = 0.93, 95% CI 0.85–1.00 and 0.90, 95% CI: 0.82–0.99) [79]. Another cohort study that
was subsequently published confirmed the protective effect impact of fruit and vegetable consumption
Nutrients 2017, 9, 1227 7 of 25

on asthma [81]. In order to decrease the risk of childhood asthma, fruit and vegetable intake should be
encouraged particularly for the youngest children.

4.2.3. Dietary Patterns: Med-Diet–No Effect, Western Diet–Detrimental

A protective effect of the Med-diet has been observed only in cross-sectional studies [59,64–68].
A prospective study did not find an association between the Med-diet and current wheezing at 1.5 and
four years of age [63]. The majority of data from prospective and cohort studies describe a protective
effect of fish consumption on asthma or wheeze [95,105,109–112]. Of two meta-analyses assessing the
effect of fish consumption on asthma, one found a protective effect of childhood intake of fish [108,113].
In Western society, children have high intakes of ‘fast food’, and this increases further in
adolescence. However, fast food and western diets should be limited because of their negative impact
on asthma risk [88]. Consumption of fast food and meat at least three times a week is significantly
associated with wheeze at four years of age [63]. In addition, fast food consumption in childhood
may decrease the protective effect of breastfeeding on asthma risk [89]. More generally, a Western
diet that is high in fat and processed foods has been shown to increase the risk of asthma or wheeze
in childhood [94,95]. Recently, two studies have found an association between sugar-containing
beverages (fruit drinks and soda) and asthma [96,97].

4.2.4. Vitamins and Fish Oil: Inconclusive Data

In early childhood, two RCTs have shown that fish oil intake had no effect on asthma risk [133,134],
while one RCT found a protective effect of fish oil on wheeze [134]. In the most recent meta-analysis,
PUFA consumption was not found to have any beneficial effect on asthma [135].
Although antioxidant and vitamin deficiency has been found in asthmatic children, β-carotene
(vitamin A) or vitamin D supplementation does not appear to reduce the risk of asthma or
wheeze [117,118,126]. Vitamin C consumption has been described as protective for childhood wheeze,
but the results were extrapolated from fruit rich in vitamin C [145,146].

4.3. Adults
Understanding the link between dietary intake and asthma risk in adults is difficult, due to the
multitude of clinical and inflammatory phenotypes that the disease encompasses and considering
disease modifying effects of diet in terms of prevention versus management of established disease.

4.3.1. Breastfeeding: No Effect

The effect of breastfeeding in childhood does not appear to be sustained in adulthood. In one
cohort study with a follow-up from birth to 20 years, breastfeeding was not associated with a reduction
in adult asthma [57].

4.3.2. Fruits and Vegetables: Beneficial

Although the level of evidence is low, fruit and vegetable consumption seems to decrease
asthma risk. Indeed, fruit is inversely associated with asthma in cohort studies and the strongest
association has been observed with intake of apples and oranges [69,82,83]. The positive effect
of vegetables on asthma has indirectly been suggested in a cohort study analysing the effect of
flavonoids [83], and also in several cross-sectional studies [84,85], while other studies have found
no association [70]. To our knowledge, no studies have specifically evaluated the effect of the
Med-diet on asthma development in adults but one cross-sectional and two cohort studies found
no association between fish and fruit and/or vegetable intake and adult asthma [69–71]. A recent
review did not find evidence to support an association between a Western diet and incident adult
asthma [90]. However, sugar-sweetened beverage intake at least two times per day was associated
with adult asthma in three cross-sectional studies with an OR ranging from 1.26 (95% CI: 1.01–1.58) to
 Nutrients 2017, 9, 1227 8 of 25

1.66 (95% CI: 1.39–1.99) [98–100]. The dichotomy between Western diet and Med-diet does not reflect
the complexity of dietary intake. The dietary may be radically different from one day to another.
A French study analysed the composite score Alternate Healthy Eating Index 2010 (AHEI-2010) that
measures the diet quality in asthma control [147]. The investigators observed an asthma control
improvement with an improvement in AHEI-2010.

4.3.3. Vitamins and Fish Oil Supplementation: Inconclusive Data

Although vitamin A, C and E deficiency has been suggested to increase the risk of asthma
in adults [148–150], the effects of supplementation are not conclusive due to a low evidence level.
One case control and one prospective study found a potential beneficial effect of vitamin E from dietary
sources, while vitamin E supplementation was not protective [128,129].
A meta-analysis, published in 2013, found no association between fish or fish LC n-3 PUFAs
and the risk of asthma [113]. However, the analysis was based on only two studies: a case control
study and a prospective study [136,137]. Although the case-control study (525 subjects) observed no
association between LC n-3 PUFAs and asthma risk [136], the prospective study (4162 subjects with
446 incident cases of asthma) found that the highest quintile of LC n-3 PUFAs intake was inversely
associated with the risk of asthma (HR 0.46, 95% CI: 0.33–0.64) [137]. Other studies are warranted to
form definitive advice in this area.

5. Diet and Asthma Control

According to the Global Initiative for Asthma (GINA), asthma control has two domains:
symptom control and future risk of adverse outcomes (such as exacerbations and lung function
Nutrients
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**
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but not from supplementation.
[60,63,86,87] Pregnancy “Western”
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[63]
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[90] Adulthood
[90,98–100]
[90] [88,94–97] Very
Lowlow [90,98–100]
[90] Low
Very [63,88,89]
Very
Very [60,63,86,87] [63,88,89]
85]
Nutrients 2017, 9, 1227 9 of 25

5.1. Pregnancy: Studies Are Needed

The scientific evidence for a benefit of dietary interventions on asthma control in pregnancy
is limited. In a cross-sectional study of 180 asthmatic pregnant women, those with uncontrolled
asthma had higher energy-adjusted intakes of saturated fat, total carbohydrate, and sugar compared
with women with controlled asthma; notably, they also had higher intakes of MUFA and fibre [152].
Further studies on the impact of diet on asthma in pregnant women are warranted.

5.2. Children

5.2.1. Med-Diet, Fruit and Vegetables: Beneficial

In a prospective study performed in children 1–5 years of age, a nutritional education programme
based on the Med-diet recommendations led to a significant reduction in asthma exacerbations after
1 year compared to the previous year and decreased use of asthma medications (inhaled corticosteroids
and short acting bronchodilators) [153]. Another study found that adherence to the Med-diet was
inversely associated with asthma symptoms [154]. The direct effect of fruit and vegetable intake on
asthma control in children has not been adequately studied. Providing free fruit at school did not have
a significant impact on asthma control, however this is not surprising as fresh fruit intake increased
marginally from 1.3 to two servings per day [155]. In a multicentre cross-sectional study, fruit intake
at least three times a week was associated with a reduction in current wheeze and severe symptoms
of asthma (OR 0.87 (95% CI 0.80–0.95) and 0.86 (95% CI 0.76–0.97), respectively), in children aged
6–7 years [156]. A similar association was observed for vegetable intake. The positive impact of fruits
and vegetables was also observed in adolescents. RCTs are warranted to elucidate the direct effects of
the Med-diet and fruit and vegetable intake on asthma control. A combination of fruit plus vegetable
concentrate, fish oil and probiotics has demonstrated promising results in asthmatic children aged
10–12 years with an improvement in pulmonary function parameters and reduction in the use of
short-acting inhaled bronchodilators and inhaled corticosteroids [157].
Key features of the Western diet have been associated with negative asthma outcomes. Salty-snack
(foods high in salt and fat and low in vitamins and antioxidants) and fast food consumption ≥3 times
a week has been associated with the presence of asthma symptoms, even after adjustment for sex and
body mass index (BMI) [156,158,159].

5.2.2. PUFA: Conflicting Data

Findings from studies describing the role of fish oil LC n-3 PUFA on asthma control in children
are inconsistent. A significant reduction in wheeze, bronchodilator use and nocturnal coughing has
been observed in children aged 18 months, who have the highest blood concentrations of omega-3
PUFAs [160]. However, in a 2002 meta-analysis, fish oil supplementation did not have any effect on
asthma control [161]. More recently, a significant 10% reduction in the prevalence of cough was found in
atopic children, younger than three years, who were given omega-3 fatty acid supplements compared
to children who were given placebo [162]. Another trial using daily consumption of a nutritional
formula enriched in EPA (3 g/day), gamma-linolenic (GL) acid (1.6 g/day) and antioxidants showed
improvement in asthma symptom-free days, but there was no difference compared with placebo [163].

5.2.3. Vitamin C and D: Possible Benefit

The role of vitamins on asthma control is still debated in children. Although folate deficiency
appears to be associated with severe exacerbations, no clinical study has assessed the efficacy of folate
supplementation in improving asthma control [164,165]. Vitamin C supplementation (0.2 mg/day) has
been shown to provide small improvements in asthma control in a cross-over trial, hence a definitive
RCT is warranted to confirm this result [166]. In an RCT, monthly doses of 60,000 intravenous units (IU)
vitamin D significantly reduced the number of exacerbations, requirement for steroids and emergency
visits in school-aged children compared to placebo [167]. In this study, asthma control was achieved
Nutrients 2017, 9, 1227 10 of 25

earlier in subjects who received monthly vitamin D compared, with those who received placebo.
However, vitamin D supplementation does not seem to have a significant effect on subjective asthma
control and oral steroid intake in preschool-aged children; however, larger adequately powered trials
are required [168,169].

5.3. Adults

5.3.1. Fruit and Vegetables: Beneficial

Although a case-control study suggested that high adherence to the traditional Med-diet increased
the likelihood of well controlled asthma, a small RCT of 38 patients concluded that multiple
consultation sessions with a nutritionist had no impact on asthma control despite an increase in
the Med-diet score [170,171]. On the other hand, high intakes of raw vegetables (>5 units/week) and
fruit (particularly citrus fruit) has been associated with well controlled asthma [172,173]. In an RCT,
high fruit and vegetable intake (≥5 servings vegetable and two servings fruit daily for 14 weeks)
was associated with fewer exacerbations and improved asthma control compared with low fruit and
vegetable intake (≤5 servings vegetable and two servings fruit daily) [174]. Therefore current evidence
suggests that fruit and vegetable intake can have a significant effect on asthma control in adults,
thus increased consumption should be encouraged in patients with asthma.

5.3.2. Vitamins or Fish Oil Supplementation: No Effect

Conversely, there is a paucity of evidence supporting an effect of individual antioxidants on
asthma control. Although folate deficiency appears to be related to asthma control, being associated
with a significant increase in episodes of shortness of breath in adult asthmatics [175], the effect of
folate supplements is still unknown. RCTs have failed to demonstrate an effect of vitamin C, D, or E
supplements on asthma control [176–178], despite beneficial effects on other asthma outcomes. In an
open-label study, a combination of vitamins A, B6, C and E, fish oil, calcium, zinc, and selenium
increased asthma control and health-related quality of life at the end of the study [7].
Fish oil alone does not seem to have a significant impact on asthma control in adult
asthmatics [161]. However, EFF1009, a medical food emulsion containing GL acid and EPA, leads to
improved quality of life and asthma control and decreased reliance on rescue medication [179,180].

5.3.3. Western Diet: Detrimental

A number of studies demonstrate that a Western diet has a negative impact on asthma
control [181–183]. A high intake of pizza/salty pies, dessert and cured meats has been associated with
an increased risk of frequent asthma attacks (OR 1.79, 95% CI 1.11–3.73) [181]. In a French prospective
study, cured meat intake was associated with worsening asthma symptoms [182]. A link between fast
food consumption and breathlessness has also been observed [183].

6. Diet and Lung Function in Asthma Patients

6.1. Children

6.1.1. The Impact of Breast Feeding on Lung Function Is Low

As demonstrated in a recent systematic review, breastfeeding has a protective effect on forced
expiratory volume in 1 s (FEV1 ) and forced vital capacity (FVC) in healthy children [184]. However,
the evidence of a potential effect of breastfeeding on lung function in asthmatic children is still low.
No association has been observed between breastfeeding and bronchial hyperresponsiveness (BHR)
in children [185,186]. A study found an increase in the FEV1 /FVC ratio in breastfed children with
asthma compared to non-breastfed children with asthma [187]. This lack of association may be due to
Nutrients 2017, 9, 1227 11 of 25

technical issues, as the effect of breastfeeding on lung function in children aged less than four years is
hard to assess and after this age, the effect of breastfeeding may diminish or disappear.

6.1.2. Med-Diet and Lung Function: Beneficial Effect

Research regarding the impact of the Med-diet on lung function in children is conflicting [43,188].
Although a cross-sectional study found no effect of the Med-diet on FEV1 , lung function parameters
(FVC, FEV1 ) were improved with the Med-diet [43,188]. No specific effect on lung function has been
found for fruit or vegetable intake in children, although the level of evidence is low (Table 3) [43].
Interestingly, in a RCT performed in asthmatic children, the improvement in FEV1 was significantly
better in those who were given a supplement containing fruit and vegetable concentrate, fish oil and
probiotics than those who received a placebo (107 mL vs. 40 mL) [157]. However, the specific effect of
each component contained within the combination remains unknown.

6.1.3. Vitamin C and E and Lung Function: A Low Beneficial Effect

Vitamin A supplementation has not shown an association with lung function in asthma
patients [118]. In asthmatic children the effect of vitamin C supplementation, on FEV1 may be
age dependent [166]. However, the methodology of the RCTs was poor and insufficient to draw
a conclusion [189]. Although vitamin D deficiency is correlated with pulmonary function deficit
in childhood asthma, intervention with vitamin D supplementation does not seem to have a
beneficial impact on lung function [190–192]. In a meta-analysis published in 2014, no evidence
for a positive effect of vitamin E on lung function was observed. This meta-analysis did not include
an RCT, published the same year, that found that FEV1 and FEV1 /FVC improved significantly after
supplementation with vitamin E (50 mg/day) but not after placebo in children with mild to moderate
asthma [193]. In a meta-analysis, n-3 LCPUFA supplementation does not have an impact on lung
function, except for exercise-induced asthma, but the studies included had small sample sizes [194].

6.2. Adults

6.2.1. Fruit and Vegetable Intake: Beneficial

The Med-diet has no effect on lung function in asthmatic adults [43,170,171,188]. In a RCT
performed on adults with asthma, a high fruit and vegetable diet for 14 days led to an improvement
in FEV1 and FVC, whereas no change was observed in patients following a low fruit and vegetable
diet [174]. A cross-sectional study reported that adults with severe asthma had lower fibre intakes
than healthy controls, which were related to lower lung function [42]. In asthmatic adults, a beneficial
effect on lung function has been suggested for soy genistein in a cross-sectional study [195], while a
soy isoflavone supplement had no effect on lung function in a RCT [196].

6.2.2. Vitamins and Lung Function: A Low Positive Impact with Vitamin C
Vitamin B supplementation has not shown an association with lung function in asthma
patients [175]. A meta-analysis of observational studies found a very small effect of vitamin C
supplementation on FEV1 in adult asthmatics [197]. Similarly to children, vitamin D supplementation
does not seem to have a beneficial impact on lung function in adults [190,191,198].

6.2.3. Meat and Lung Function: No Impact

In a European study, a diet high in meat and potatoes had no impact on lung function in
adult asthmatics [71]. However, a single high-fat meal has been shown to negatively influence
post-bronchodilator FEV1 in adults with asthma [40].
 Nutrients 2017, 9, 1227 Nutrients 2017, 9, 1227 5 of 25 5 of 25

4. Diet and Risk of 4. Diet and Risk of Asthma

Asthma
The influence
The influence of dietary intake onof dietaryrisk
asthma intake on asthma
has been risk has
examined been studies
in many examined in the
over many
laststudies over the last
two decades.
two decades. Mediterranean dietsMediterranean
Nutrients 2017, 9, 1227 and Western diets
diets, and
wholeWestern
foods diets,
and whole
individualfoods and individual
nutrients, have nutrients,
12 ofhave
25
been found to have been found toon
an influence have an influence
asthma on asthma
risk, at various risk,
stages of at
thevarious stages
life cycle of the
(Table 1). life cycle (Table 1).

Table 1. Diet and Table Table

risk of 1. Diet
3. asthma
Diet andorand risk
wheezing.
lung of asthma
function or wheezing.
Beneficial
in asthma effect;
patients. Beneficial effect;
negative effect;
Beneficial effect; negative
No
No effect; ?effect;
= no data.No
effect; ? = no data. Very strong
effect; ? =evidence
strong no data. is
evidence isdefined
Very strong
defined as data
dataobtained
asevidence ininmeta-analysis
is defined
obtained ofofRCTs,
as data obtained
meta-analysis Strong evidence
in meta-analysis
randomized of is defined
randomized
as data
controlled trials (RCTs); obtained
controlled
Strong in individual
trials (RCTs);
evidence RCT; Low
Strong
is defined as evidence
evidence is is
data obtained defined
defined as data obtained
in as
individual RCT; inLow
obtained inindividual
individual prospective
RCT; Low
evidence is defined studies or meta-analysis
evidence
as data is definedinas
obtained ofindividual
prospective
data obtained 25 studies; Very
in individual
5 of prospective low evidence
studies prospective is defined
or meta-analysis studiesofasordata obtained in of
meta-analysis
trients
7, prospective
2017,
9, 1227 individual
prospectivecross-sectional
studies; Veryor case-control
low evidence studies,
is or
defined meta-analysis
as data
9, 1227 studies; Very low evidence is defined as data obtained in individual cross-sectional of
obtained cross-sectional
in
5 of 25 individual
or 25
5 of or case-control
cross-sectional or
case-control studies,studies. In casestudies,
case-control
or meta-analysis of of
conflicting resultsorbetween
or meta-analysis
cross-sectional studies,
of cross-sectional
case-control data
studies. from
orIn casethe
case-control studies with
studies.
of conflicting Inthe
casemost robust
of conflicting
Nutrients 2017, 9, 1227 5 of 25 5 of 25
dDiet results
Riskand between
Risk
of Asthma methodology
results
studies,
of Asthma fromarethe
databetween used to define
studies,
studies withthe
data theeffect
from most of diet on
the studies
robust lung
with thefunction.
methodology most are
robust
usedmethodology
to define are used to define
sthma risk has been examined in many
Nutrients 2017,studies
9, 1227 over the last
5 of 25 5 of 25
the 4.
the effect of diet on asthmaeffect ofand
risk.
Diet *diet
One on
Risk asthma risk. found
Meta-analysis
of Asthma * One aMeta-analysis found a with
negative association negative association
asthma or with asthma or
Western
Thewheeze
nfluence diets,
influencewhole
of dietaryof foods
dietary
intake on and
intake individual
asthma on asthma
risk has nutrients,
risk
been has have
been
examined examined
in many
Childhood in many
studies studies
over the over
last the last
Adulthood
and one found wheeze and one found
no association; no association;
** conflicting results ** cross-sectional
in conflicting results in cross-sectional
studies; *** from diet studies; *** from diet
ma
sthmarisk,
o decades.
es. at various
Mediterranean
risk has beenstages
Mediterranean
diets and
examined 4.Western
Diet
of diets
the life
in The and
cycle
and
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(Table
Western
diets,
influence
studies ofdiets,
Asthma
1).
whole
of whole
foods
dietary
over the foods
and
intake
last onand
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nutrients, have in many studies over the last
haveexamined
been
but not from supplementation.
but not from supplementation. Effect Evidence Effect Evidence
d7,
ento9,found
1227
have tohas
an have
influenceanexamined
influence
on asthma on asthma
risk, risk,
atstudies
various at various
stages ofstages
the life of the
cycle life cycle
(Table 1).(Table 5 of
1).25examined
Western
sthma riskdiets, whole
been foods two
and in decades.
individual
The
many influence Mediterranean
nutrients,
of
over thehave
dietary diets
intake
last and
on Western
asthma riskdiets,
has whole
been foods and in individual
many studies nutrients,
over thehavelast
New born Breast feeding Diet During Life Stages Low Diet During Life Stages ? ?
wheezing.
ma risk,Dietat variousBeneficial
stages effect; been
ofDiet
the lifenegative
found
cycleto effect;
have
(Table 1). No
[185–187]
anPregnancy
influence on and
asthma risk, at various stages of the life cycle (Table 1).
Western
d isRisk diets,
of Asthma whole foods two
and decades.
individual
Pregnancy Mediterranean
nutrients, have diets
Childhood Western diets, whole
Childhood foods
Adulthood and individual
Adulthood nutrients, have
defined asDietdataandobtained inormeta-analysis
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ma 1. Table
Diet at
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asthma
stages asthma
ofEffect
been
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found
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Effect
Evidence
have
(Table Beneficial
effect;
[43,188]
an influence
1). effect;
Effecton negative
Evidence
asthmaEvidencenegative
effect;Effect
risk, effect;
at various No Effect No of
[43,170,171,188]
Evidence
stages the lifeEffect
Evidence cycle (Table Evidence
1).
nce
7,
? 9,
=
nfluencenois
1227 defined
Post-natal
effect; ?
data.
of = no
Very
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data.
strongVery
intake obtained
Post-natal
strong
evidence
on in
is
asthma individual
evidence
defined
Fruit
Table risk is defined
as
has
1. Diet RCT;
data
been as Low
data
obtained
effect;and riskexamined obtained
in in
meta-analysis
in many meta-analysis
Very
of asthma or wheezing. of
studies
low randomized
over of the5 of
randomized25
last
Beneficial Strong
wheezing. Beneficial effect; negative No [56]
[43] Very strong
[56] [172–174]
[57] Veryeffect;
strong
Low negative
[57] effect;Low No
breast feeding breast feeding
dtrients
lled
es. in individual
controlled
trials (RCTs);
Mediterranean prospective
trials (RCTs);
Strong
diets studies
Strong
evidence
and Western ordefined
evidence
is2017, meta-analysis
israndomized
defined
as data of
asstrong
data
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inindividual in
individual individual
RCT;asLow RCT; Low5 ofin25meta-analysis
wheezing. 2017, 9,
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Vegetables
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negative
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Very
No
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Beneficial
Low[59,63–68] [174] effect; Strong of
negative randomized
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nce
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in trials
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=various
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of studies
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[69,82,83]
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ma Risk
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aternal
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Nutrients 2017, 9, 1227 13 of 25

weight loss of 14.5% (vs. 0.3% in control group) and demonstrated significant improvements in lung
function, dyspnoea, and rescue medication use in the intervention vs. control group [208].
Although the small trials available to date provide promising results, larger clinical trials with
longer follow-up are needed to investigate the ideal dietary intervention to improve asthma outcomes
in obese adults and children with asthma.

8. How to Change the Patients’ Behaviour?

Given the potential impact of healthy food on general health and asthma outcomes in asthmatic
patients, a message about diet should be delivered to the patient. However is this enough to
change the patients’ behaviour regarding diet? As patient education is used to improve therapeutic
adherence, a structured intervention is needed to change patients’ diets and physical activity levels.
Behavioural therapy is likely to be a necessary component of such interventions, as lifestyle changes are
difficult to adopt and maintain. The dietary approach to stop hypertension (DASH) is a dietary pattern
characterised by an emphasis on healthy food, with key dietary goals including: consumption of 7–12
servings of fruit and vegetables, as well as two to four servings of low-fat/fat-free dairy products,
total fat grams at 27% of estimated energy needs and ≤2300 mg of sodium per day [209]. Adoption of
the DASH diet in a 6-month intervention (3-month intensive stage and 3-month maintenance stage
with support by behavioural coaches who were dietitians) was feasible and acceptable to adults with
uncontrolled asthma [210] and led to small improvements in diet quality and asthma control [211].
In children, to durably change dietary behaviours, the child or adolescent should be actively involved.
The I Can Control Asthma and Nutrition Now (ICAN) program, based on nutrition and weight
management education, as well as asthma education, has demonstrated promising preliminary results
in improving nutrition and asthma health outcomes in high school students [212]. School-based
nutrition programs should be assessed in asthmatic children [213]. Incorporation of a multi-disciplinary
team including dietitians and exercise physiologists into asthma clinics and services may be a
positive strategy to facilitate the adoption and maintenance of beneficial eating and exercise habits in
asthma patients.

9. Conclusions
In conclusion, higher intakes of fruits and vegetables may have a positive impact on asthma risk
and asthma control. In a recent overview, the European Academy of Allergy and Clinical Immunology
(EAACI) concluded that the literature supports recommendation in clinical practice to increase the net
intake of fruits and vegetables as a way of reducing the risk of asthma, particularly in children [214].
The effect on asthma control is also promising, but well-designed RCTs are warranted to formulate
official guidelines. Western diets likely have a negative impact on asthma but the level of evidence
is still low. The synergistic effect of a healthy diet and exercise could be an effective way to improve
asthma outcomes, and the combination of these two non-pharmacological interventions needs to
be thoroughly evaluated. Dietary intervention, based on evidence-based guidelines, should be
incorporated into the routine clinical management of patients with asthma, in order to achieve overall
health benefits and disease management.

Acknowledgments: We would like to acknowledge “le fond de Recherche en Santé Respiratoire” and
“la Fondation du Souffle” for their support of Laurent Guilleminault’s project on asthma and obesity.
Author Contributions: L.G., E.J.W., H.A.S., B.S.B., M.J. and L.G.W. conceived and designed the review; L.G. wrote
the introduction, the paragraphs on diet and asthma (risk, control and lung function) and the conclusion;
E.J.W. wrote the paragraphs on diet and inflammation; B.S.B. and M.J. wrote the paragraphs on the dietary
patterns; H.A.S. and L.G.W. wrote the paragraphs on diet and obese-asthma phenotype. All the authors have
approved the final version of the manuscript.
Conflicts of Interest: All the other co-authors declare no conflicts of interest.
Nutrients 2017, 9, 1227 14 of 25

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