Respiratory Allergy to Conifers

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Respiratory Allergy to Conifers
Denis Charpin, Hélène Sénéchal, Pascal Poncet
To cite this version:
Denis Charpin, Hélène Sénéchal, Pascal Poncet. Respiratory Allergy to Conifers. Ana Cristina
Gonçalves. Conifers - Recent Advances, IntechOpen, 2022, 978-1-83969-778-4 (ebook). �10.5772/inte-
chopen.101217�. �pasteur-03718500�


Chapter
Respiratory Allergy to Conifers
DenisCharpin, HélèneSénéchal and PascalPoncet
Abstract
The conifers, from the latin meaning “cone carrier,” include about 650 species
distributed in seven families. They are found all over the world, and the most
known conifers are the cypresses, the junipers, the yews, the larches, the firs, or the
pines. The most allergenic pollen is emitted by the Cupressaceae/Taxaceae family
with mainly five different genera: Cupressus, Hesperocyparis, Juniperus, Cryptomeria,
and Chamaecyparis. The symptomatic period starts in November and ends in April.
In Mediterranean areas, Cupressus sempervirens is the most common pollinating
species. Five main cypress allergens have been thoroughly described. Depending on
the geographic area and the studied population, the prevalence of cypress allergy
in the general population ranges from 0.6% to 3%, and 9–65% of outpatients
consulting an allergist are sensitized to cypress pollen. This prevalence is increas-
ing likely to be due to the modifications of the environment. Rhinitis is the most
prevalent clinical symptom, while conjunctivitis is the most disabling. Clear-cut
improvements of the quality of life are observed upon an effective and safe specific
immunotherapy. Associations with food allergy based on molecular allergen cross-
reactivities were described resulting in sometimes severe symptoms. Pollens from
Pinaceae family, especially pines or firs, although abundant, do not demonstrate a
significant clinical impact.
Keywords: cypress pollen, pine pollen, allergens, aerobiology, epidemiology, botanic,
clinic
. Introduction
Respiratory allergic diseases are among the most prevalent chronic disease,
affecting 20–25% of the general population. Allergy reactions at large encompass
several mechanisms, but allergy reactions to pollen are considered as a “ type-1 ”
or “ immediate-type ” or “ IgE-dependent ” hypersensitivity reaction involving
mast cells and basophiles as effectors cells. Those cells are responsible for releas-
ing inflammatory and immune mediators leading to ocular, nasal, and bronchial
symptoms. Pathophysiology of these reactions allows the use of skin tests and/or
measurement of serum specific IgE as powerful diagnostic tools.
The prevalence of allergy is increasing whatever is the allergenic source, pol-
len, food, animals. Pollen grains are the main inducers of respiratory allergies, and
conifers play a major role around the Mediterranean basin, in North America, or in
Japan. According to a phylogenetical classification, the conifers consist of one class,
Pinopsida, and seven families have been described: Araucariaceae, Podocarpaceae,
Sciadopityaceae, Cupressaceae/Cephalotaxaceae/Taxaceae, and Pinaceae. No
extensive studies were reported on the allergenicity of the pollen grains from
Araucariaceae and Sciadopityaceae, but a huge amount of data are published for

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Cupressaceae/Taxaceae (also reviewed in [1]) and Pinaceae pollen (see below).
Cephalotaxaceae are sometimes included in Taxaceae and Araucariaceae and might
be assimilated to pine because of the Wollemi pine discovered in Australia. A few
data are available on the allergenicity of Podocarpaceae pollen [2, 3].
This review provides an update on various aspects of the highly allergenic family
of conifer, i.e., Cupressaceae (Chapter 2) with, first, a botanical and palynological
presentation of cypress followed by the various cypress pollen allergens involved;
second, data on epidemiology; and third, the clinical aspects together with the
management of cypress pollen allergy. Chapter 3 is devoted to the poorly allergenic
conifer family, Pinaceae.
. Cupressaceae
. Trees, pollen, and allergens
.. Trees
Cupressaceae corresponds to a family of the order Pinales. According to a
phylogenetical classification, the family includes about 140–160 species with 27–30
genera. Cupressaceae is the most widely distributed conifer worldwide, except
Antarctica devoid of any trees (Figure ). Cupressaceae, commonly named cypress,
is the most well-known gymnosperm family that produces allergenic pollen. Two
main contributors to cypress pollen allergies belong to Cupressoideae by species
from the Cupressus, Juniperus, and Thuja genera and to Taxodioideae by species
from Cryptomeria and Taxodium genera [4] (see below the description of the
respective allergens in the section “Allergens”).
Besides botanical and phylogenetical classification, a classification was proposed
based on the functional and structural aspects of allergens (Table ) [4, 5]. These
allergens in different species exhibit a high degree of homology, up to 97% between
Hesperocyparis arizonica (Cup a 1) and Cupressus sempervirens (Cup s 1), although
molecular studies led to a split of the two species into two different genera,
C. arizonica being assigned to the newly created Hesperocyparis genus [6]. Botanical
proximity is responsible for cross-reactivities. The same molecular-type allergen
produced by botanically distant plants appears very limited [7, 8] .
Figure 1.
Worldwide distribution of reported Cupressaceae pollen allergy (orange dots).

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Groups Proteins Cupressus
sempervirens
Hesperocyparis
arizonica
Cryptomeria
japonica
Juniperus Chamaecyparis
obtusa
Taxodium
disticum
Thuja
ashei other
Italian
cypress
Arizona
cypress
Japanese
cedar
Mountain
cedar
Japanese
cypress
Bald
cypress
cedar
Group 1 Pectate lyase
(40-45 kDa)
Cup s 1* Cup a 1* Cry j 1* Jun a 1* Jun c 1, o 1,
v 1*
Cha o 1* Thu p 1
Group 2 Polygalacturonase
(43-60 kDa)
Cup s 2* Cup a 2 Cry j 2* Jun a 2* Cha o 2* Tax d 2
Group 3 Thaumatin-like protein
PR-5 (24-34 kDa)
Cup s 3* Cup a 3 Cry j 3 Jun a 3* Jun r 3, v 3* Thu oc 3
Group 4 Ca-Binding protein
(17-29 kDa)
Cup a 4 Cry j 4 Jun o 4*, v 4
Group 5 Gibberellin-regulated
protein (8kDa)
Cup s 7 * Cup a 7 Cry j 7* Jun a 7*
OTHER ß-galactosidase
46-50 kDa
ß-galactosidase
46-50 kDa
Chitinase
27 kDa
Cha o 3*
63 kDa
Profilin (Cup s 8)
14 kDa
LTP
14 kDa
CJP8 (LTP)
17 kDa
Phenylcoumaran
reductase
33 kDa
Isoflavone
reductase
35 kDa
Rab-like protein
18 kDa
Aspartic protease
42 kDa
Sigma factor
regulation
protein
29 kDa
Serine protease
subtilisin-like
79 kDa

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Groups Proteins Cupressus
sempervirens
Hesperocyparis
arizonica
Cryptomeria
japonica
Juniperus Chamaecyparis
obtusa
Taxodium
disticum
Thuja
ashei other
Italian
cypress
Arizona
cypress
Japanese
cedar
Mountain
cedar
Japanese
cypress
Bald
cypress
cedar
Cytochrome c
12 kDa
SOD
15 kDa
Lactoyl glutathione
lyase
32 kDa
Malate
dehydrogenase
31 kDa
Triosephosphate
isomerase
33 kDa
Glucanase
37 kDa
HSP104
104 kDa
*referenced in IUIS/WHO database; Jun c: Juniperus communis (Common juniper) ; Jun o: Juniperus oxycedrus (Prickly juniper); Jun r: Juniperus rigida (Temple juniper); Jun v: Juniperus virginiana
(Eastern red cedar); Thu p: Thuja plicata (Western red cedar); Thu oc: Thuja occidentalis (Eastern white cedar); SOD: Superoxide dismutase; LTP: Lipid transfer protein; HSP: Heat shock protein.
Table 1.
Cupressaceae allergens. Name, protein function, and molecular masses (kDa) are indicated.

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.. Pollen
... Pollination: phenology and pollen features
Within a species, the pollination period is usually short. However, because of the
different species in Cupressaceae, the pollination periods do not overlap, and this
contributes to extend the exposition duration to Cupressaceae pollen from autumn
to spring. In Mediterranean regions, pollen from early pollinating species (e.g.,
Juniperus oxycedrus) is produced in October or November [9–11], while pollination
by late pollinating species (e.g., C. sempervirens) can occur up to late April or May
[12]. Belmonte et al reported the diversity, floral phenology, and distribution of the
Cupressaceae species in the Iberian Peninsula in 1999 [13].
All Cupressaceae species produce spherical pollen grains very similar in appear-
ance (Figure A) [14]. In the Cupressus genus, the mean size of hydrated pollen
grains varies from 25 to 40 micrometers (Figure B). However some variations can
occur. Pollen grains are small for Mediterranean species (except for C. dupreziana,
which produces diploid pollen [16], intermediate for New World species, and larger
for Asian species [17]. The Cupressaceae pollen is inaperturate, although a faint
circular pore blocked with a bulge can be seen in fresh material. The exine (outer
membrane) is very thin and covered with scattered granules or orbicules (Ubish
bodies, 300–600nm) (Figure A). The intine (inner membrane) is very thick, and
hydration unblocks the bulge leading to the swelling of the intine until the exine
cracks (Figure B).
Cupressaceae trees are anemophilous, and pollen grains can be wind-
transported over long distances because of their small size. Cupressaceae species
generally produce huge quantities of pollen. The number of pollen grains per
male inflorescence average 400,000, and production by individual trees has been
estimated to be 276,000 million [18, 19]. Cupressaceae pollen predominates in the
winter period, but can also be present all year long (Figure ). In Mediterranean
regions, Cupressus, together with Olea, produces the largest amount of allergenic
tree pollen [20]. Cupressaceae/Taxaceae pollen is one of the 12 most abundant aero-
allergenic pollens in Europe [21]. Cupressus pollen can account as much as 40% of
the total annual pollen counts in Marseille, in Southern France [22], 38% in Antalya
[23], and 35% in Istanbul, Turkey [24], 25% in Thessaloniki, Greece [25], 23%
and 24% in Toledo and Cuenca, Spain [9, 26], 18% in Nicosia, Cyprus [27], 17% in
Figure 2.
A: Hesperocyparis arizonica pollen grains (scanning electron microscopy from Shahali et al. [14]) collected
in Tehran, Iran. (2225x magnification). The arrow shows the presence of a bulge on the external surface of
the exine serving as a valve for regulating the entrance of fluids at the beginning of pollen hydration [15].
Numerous submicronic orbicules (300–600nm) are visible on the pollen surface. B: Hesperocyparis arizonica
pollen hydrated for 5min in phosphate buffer saline. Optical light microscopy observation after viable trypan
blue staining (100x magnification). The various elements are indicated.

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Figure 3.
Cupressaceae pollen dynamics over the course of the year in the Mediterranean area: Barcelona (Spain);
Aix-En-Provence (France); Vielha, (Spain); Mornag (Tunisia); Thessaloniki (Greece); Madrid (Spain) and
outside Mediterranean area: Paris (France); and Gümüshane (Turkey). Mean daily (thick black line) and
maximum daily (thin black line) pollen concentrations are indicated for the period.
Palma de Mallorca, Balearic Islands, Spain [10], and 14% in Nerja, southern Spain
[11]. Cupressaceae pollen is also abundant or present outside of the Mediterranean
region: Northern Europe, 8% for Cupressaceae and Taxaceae in Munster, Germany
[28], South America, 30% in Bahia Blanca, Argentina [29], North America, 18%
in Mexico [30], 5–10% on the east coast of the United States [31, 32], and up to
3872 pollen grains/m3 in January in Tulsa, Oklahoma, central United States where
Juniperus ashei is predominant [33, 34], Asia, 19% in Yunnan, China [35], and 60%
in Japan because of the huge presence of Cryptomeria japonica [36], and finally 3%
in Santa Cruz de Tenerife, Canary Islands, Spain [37].
... Aerobiology
Comparative sampling methods developed during the last decades of the twen-
tieth century showed that concentrations of airborne pollen diversity have steadily
progressed [36–39].
At least four indices exist to characterize the dynamics and patterns of airborne
pollen: (a): the mean daily pollen concentration, expressed as the number of pollen
grains per cubic meter of air (P/m3); (b): the annual pollen index (API), which

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corresponds to the sum of the mean daily pollen concentration for each year); (c):
the dates corresponding to the beginning and end of the pollination; and finally (d):
the duration of the pollen season.
In the case of cypress pollen, the pollination period (except in mountainous
and in very cold sites) begins in autumn and lasts until the end of the following
spring. However, in the Mediterranean area, days without any cypress pollen
are rare. Therefore a percentage method was proposed. The season is considered
to begin when 2.5% of the API has been reached and finished when 97.5% was
reached. This method is not totally satisfactory because of substantial year-to-year
variations of API.
Using pollen collectors mainly located in urban areas, the Cupressaceae API
showed increasing trends in Mediterranean countries. This was shown in Southern
France with an early pollination onset [40], in Greece [41] or in Catalonia (NE
Iberian Peninsula). Two of these API trends, for Barcelona and Vielha, are shown
in Figure  together with the trends in other localities around the Mediterranean.
These trends were confirmed for 23 taxa from 13 European countries (97 sites) [42].
Authors did not find any correlation with variation of temperature and rather pro-
posed, as an explanation, the extensive use of Cupressaceae as ornamental plants in
the cities. Ariano et al. [43] have, however, attributed to climate change a possible
role in variations in pollen seasons and allergic sensitizations.
The daily pollen concentration threshold levels required to elicit allergic symp-
toms in patients remain a crucial question, and no general agreement has been
reached. For instance, in Israel, the threshold is considered to be between 10 and
50 pollen grains/m3, whereas in France, different thresholds of symptom risk have
been established for the Mediterranean area (designated as low, when 7–13 pollen
grains/m3, moderate when 14–141 pollen grains/m3, and high >141 pollen grains/
m3, respectively), and for the north and center of France (designated as low when
70–141 pollen grains/m3 and moderate when >141 pollen grains/m3 [44]). The
Catalan Network of Aerobiology defined the risk of allergy as being low when con-
centrations are <20 pollen grains/m3, moderate for 20–50 pollen grains/m3, high for
50–100 pollen grains/m3, and very high when >100 pollen grains/m3. Furthermore
the risk to develop allergy symptoms was shown to be increased by airborne pollut-
ants, especially PM2.5 and suspended particulate matter [45].
... Allergenicity of cypress pollen
The cypress pollen is considered to be highly allergenic (see, for instance,
the website of the French National Network of Aerobiological Surveillance,
RNSA,“Réseau National de Surveillance Aérobiologique”, www.pollens.fr). The
allergenic potential of specific pollen depends on the following:
• the degree of exposure, related to the total pollen amount released in the
atmosphere (from intact or fragmented grains);
• the phenological conditions in the considered area;
• temperature, hygrometry, photoperiod, …;
• air pollution.
The exposure to cypress pollen is high because of an abundant production of
pollen (see pollen chapter), making of this pollen the most represented in the
atmosphere (up to 40% of total pollen counts around Marseille in the south of

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Figure 4.
Cupressaceae annual pollen index (API) and trends at the localities with the longest continuous data series.
Madrid (Spain), Barcelona (Spain), Vielha, (Spain), Aix-En-Provence (France), Paris (France), Thessaloniki
(Greece), and Ankara (Turkey).
France). Not only is the load high but also the spreading, since rather small pol-
len, can be wind-transported. Moreover, the pollen grain carries sub-micronic
particles named orbicules on its surface (Figure A). These orbicules were shown
to contain allergens from the groups 1 and 2 [46–50] (see below for the definition
of groups of allergens) and to be easily released upon rainfall and an experimental
in vitro treatment of cypress pollen grains with NO2, a gas frequently found in
gaseous pollutants [46, 51]. Because of their small size (300–600nm), orbicules
might be able to penetrate deeper in the bronchial tract and sensitize individuals to
induce asthma, as was shown in a rat model [52]. However, free airborne orbicules
have never been evaluated; therefore such an orbicule-sensitizing mechanism, in
real conditions, was not as yet demonstrated. Besides these characteristics, and

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in addition to protein allergens, some biogenic intrinsic adjuvant molecules may
contribute to the allergenicity of cypress pollen [53–55] by favoring Th2 immune
responses and/or triggering innate immune responses. For instance, NADPH
oxidase, an enzyme that generates reactive oxygen species, is reported to be
involved in inflammation [56, 57]. This enzyme, required for pollen tube growth,
is intrinsically expressed at different levels in the pollen grain of various plant
species [58, 59]. Cypress pollen is one of the tree pollens containing the highest
level of redox activity as compared with other pollen and in particular to the poorly
allergenic pine pollen, which expresses the lowest redox activity. Moreover, other
biogenic cofactors, pollen-associated lipid mediators (PALMs), play a role in pollen
allergenicity. Studies performed on cypress pollen show that lipids of the pollen
membrane interact with CD1+ dendritic cells to activate CD1-restricted T cells
with the Th0/Th2 phenotype [54]. PALMs are also able to activate eosinophils and
neutrophils and decrease IL12 production from dendritic cells, therefore, favoring
Th2-biased immune responses [60–64].
.. Allergens
... Cypress pollen allergens
C. japonica was the first cypress pollen studied at the level of allergen content,
and in 1983 Cry j 1 (previously called SBP, for Sugi Basic Protein) was reported to be
its major allergen [65]. Several other allergens were then described in C. sempervi-
rens and Hesperocyparis arizonica [66–68]. All research groups deciphering allergens
from the various cypress species reported a cross-reactive 42–43kDa protein as
being the major cypress allergen: Cry j 1 for C. japonica, Cup a 1 for Hesperocyparis
arizonica, Cup s 1 for C. sempervirens, etc... (see Table ). As compared with grass,
olive, or ragweed pollen, the extraction of proteins from cypress pollen is difficult,
yielding few proteins. This particularity may be related to the high sugar content
of the intine quickly swelling when the pollen grain is hydrated; this might delay
or prevent the release of proteins [15] (Figure B). One way to circumvent this
difficulty is to grind the pollen in suspension with silica microbeads.
Up to now, five groups of allergens have been described in cypress pollen,
although all allergen members for each species have yet to be referenced in
the International Union of Immunological Societies (IUIS) allergen data bank
(www.allergen.org): group 1: pectase lyase, group 2: polygalacturonase, group 3:
thaumatin-like protein, group 4: Ca-binding protein, group 5: Gibberellin-regulated
protein. Furthermore, about 20 additional allergens have been reported in the three
most studied pollens, C. japonica, Hesperocyparis arizonica, and C. sempervirens
(Table ). More details on cypress allergens are reported in Charpin et al. [1] and
Poncet et al. [69].
... Cross-reactivities
• Pollen/pollen
Cross-reactivities between pollen are common because proteins may belong to
families of panallergens, such as Ca++-binding proteins or profilins. Some cross-
reactivities were observed with Podocarpus gracilior of the Pinales order [70],
although other authors did not find any cross-reactivity of C. sempervirens with
pine pollen [71]. Parietaria judaica, Lolium perenne, and Olea europaea pollens were
shown to exhibit some degree of cross-reactivity [72] although the nature of the
involved allergens remains unknown.

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• Pollen/food
Like for pollen from birch, mugwort, grass, ragweed, olive, plane, cypress
pollen sensitization was shown to be associated to food allergies. In general, up to
60% of food allergies are associated with an inhalant allergy [73]. A pollen food
allergy syndrome (PFAS) has been described, including mainly an oral allergy
syndrome. As soon as 2000, Ishida et al reported PFAS in patients allergic to
Japanese cedar pollen following consumption of specific vegetables and fresh
fruits (e.g., melon, apple, peach, and kiwi) [74]. The cypress/peach syndrome was
mostly studied [75, 76]. Symptoms might, in some conditions, with cofactors, be
more severe than an oral syndrome, up to an anaphylactic shock [77]. An unchar-
acterized (putative Cup s 1 or Cup s 2) allergen of 45kDa was proposed to be the
cross-reactive allergen [76], and more recently the allergens from the Gibberellin-
regulated protein family (group 5 allergens) were shown to be cross-reactive with
peach, Japanese apricot, citrus, and pomegranate [77–80]. Prevalence of sensitiza-
tion to Pru p 7, the GRP from peach, coincides with the prevalence of sensitization
to cypress pollen in France [81].
. Epidemiology of cypress pollen allergy
Cypress pollen allergy was reported for the first time in 1929 in the United
States (Texas and New Mexico) [82] and in the early 1960s in Europe [83]. Cypress
pollinosis is also reported in several locations worldwide: Japan [84], Australia [85],
Iran [86], South Africa [87], the United States, and with special emphasis around
the Mediterranean basin [88–94] (Figure ).
.. Prevalence of sensitization and allergy to cypress pollen in non-selected
populations
There are consistent correlations between exposure to Cupressaceae/Taxaceae
pollen and the presence of sensitization and allergy [95]. Studies performed in the
general population are scare. In southern France and in Italy, two studies performed
in children [96, 97] and one study in young adults [98] concluded that around
2–4% might suffer from cypress pollen allergy. A study performed in Japan led to a
number of Cryptomeria pollen allergy of 13% [97–99].
.. Prevalence of sensitization and allergy to cypress pollen in outpatients
In surveys performed in Mediterranean countries, 14–32% of patients attending
an allergy clinic had an allergy to cypress pollen [1]. In a larger Italian study from
Rome, 23,077 outpatient sera were studied. The presence of specific IgEs against 75
allergens was investigated, and 42.7% of the subjects exhibited specific IgEs against
cypress pollen. In this survey, cypress allergy was the leading cause of sensitization
in adults over 35years of age (in children, house-dust mite allergy was the leading
cause) [100]. In Montpellier, a cross-sectional study performed in 400 outpatients
concluded that cypress pollen sensitization (20.7%) ranked third, after sensitiza-
tion to Dermatophagoides farinae (37%) and pteronyssinus (43%) allergens [101].
.. Increase in the prevalence of cypress pollen allergy
Several cross-sectional surveys carried out repeatedly over time showed an
increase in the proportion of cypress allergy among outpatients consulting for
allergic rhinitis: rising from 9.9% in 1991 to 24.5% in 1993, then to 35.4% in 1994

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in central Italy [102], from 9.3 to 30.4% between 1994 and 1999 in the area around
Rome [103], and from 7.2 to 22.0% between 1995 and 1998 in Italy’s Latium area
[104]. A recent study in the southern region of Italy showed that cypress pollen
sensitization almost doubled from 2005 (17%) to 2010 (29%) [105]. Eighteen were
sensitized to cypress or Taxodiaceae pollen in an Italian survey of 3057 outpatients
selected in 12 study centers [106]. The sensitization rate was higher in southern
Italy (20.1%) and central Italy (28.2%) than in northern Italy (9.2%). In a more
recent survey, the geographical hierarchy was unchanged, but the prevalence
figures went up to 32.7%, 62.9%, and 16.1%, respectively [107]. A study performed
in western Liguria demonstrated an upward trend, whereas pollen counts remained
unchanged [108, 109]. This study, like the one by Mari et al., suggests that con-
founding factors, such as the quality of allergenic extracts, might at least partially
explain these discordances [102]. On the other hand, a gradual increase in pollen
load, pollen allergenicity [1, 110], and interaction in the patient between air pollut-
ants and cypress allergens [95] are clear indications of a genuine increase.
The rationale for such a rapid increase in prevalence mainly lies with the
fact that:
• millions of cypresses were planted in the 1970s and 1980s in the suburbs
and around private houses and blocks of flats to offer a degree of privacy.
Therefore the proximity of pollen sources has drastically changed: whereas
Cupressaceae were traditionally planted in agricultural zones, away from
dwellings, nowadays they are planted as hedges to as visual barriers.
• at the same time, a decrease in farming allowed for the extensive proliferation
of Juniperus in the countryside.
• lastly, in urban areas, air pollution interacts with pollen to increase the
allergenicity [51] (see below).
.. Risk factors for developing cypress pollen allergy
... Repeated and heavy exposure
In contrast to other respiratory allergic diseases, part of cypress pollen aller-
gic patients have no personal or familial history of allergic diseases, and in this
subgroup, the onset of symptoms occurs at an older age [111, 112]. Therefore,
even non-atopic individuals repeatedly and heavily exposed during many years
to cypress pollens can develop this allergic condition. In high exposure areas, the
general population may become allergic to this pollen.
... Air pollution
Ishizaki et al. first noticed in the 1980s the association between Cupressaceae
pollen allergy and air pollutants [84]. They found that living near Japanese cedar
trees in urban areas tended to increase the allergy risk compared with living near
these trees in rural areas. Concomitantly in Japan, Muranaka et al. demonstrated
the adjuvant effect of diesel exhaust particles on IgE reactivity to Japanese cedar
pollen in mice [113]. The rising prevalence of these pollen allergies observed
between 1987 and 1991 (from 17 to 25%) in Japanese mountainous areas could then
be partly explained by a drastic increase in the diesel vehicle fleet [114]. Japanese
cedar pollen grains in urban areas may adsorb major urban gaseous pollutants such
as NO2, SO2, and NH3. Besides, Japanese studies also demonstrated that, on the

Conifers - Recent Advances

exine surface, pollutants may be attached, thereby modifying the morphology and
ionic composition of pollen grains [115, 116]. This phenomenon could facilitate
the release and dispersion of pollen-derived particles smaller than pollen into the
atmosphere [46]. During the Japanese cedar pollination period, the level of particle
matter (PM2.5) and suspended particle matter is therefore increased [117], which
induce a negative impacts of this increase on the respiratory health of allergic
patients [45].
Since then, Cupressaceae pollen grains have frequently been used as a model
to study the interrelationship between air pollutants and pollen allergies [51,
118]. The effects of pollution on the molecular and developmental biology of
Cupressaceae pollen has been exemplified by several studies. In polluted areas, the
accumulation of numerous inorganic elements such as sulfur, copper, aluminum,
and iron on pollen grains and the acidification of pollen surfaces by the adsorption
of acid gases such as nitric and citric acids were demonstrated. The natural expo-
sure of Arizona cypress pollen to air pollutants in Barcelona and Madrid promotes
the production and release of an allergenic protein (Cup a 3) of the pathogenesis-
related family 5 (PR-5 protein) [110, 119]. Therefore, the allergenic content of
cypress pollen grains could be modified by urban air pollution. Interestingly,
levels of adsorption of gaseous pollutants vary greatly, in in vitro exposure stud-
ies, among different plant species, and cypress pollen seems to be one of the most
impacted. The kinetics of NO2 uptake by cypress pollen is two and six times that
of grass and birch pollen, respectively [120]. Furthermore, allergen-carrying free
orbicules are generated following exposure of cypress pollen to NO2 [51]. More
comprehensive and experimentally designed studies on the interrelationship
between pollen, air pollution, and respiratory allergies should derive from these
recent physicochemical experiments.
. Clinical and management aspects
.. Symptoms and diagnosis
According to the Japanese survey [99], and a subsequent study from Europe,
rhinitis is more common than conjunctivitis. The latter is, however, the most
disabling symptom, occurring in 72% of patients allergic to cypress pollen, versus
26% of patients allergic to grass pollen [111]. In this study, the occurrence of a
chronic cough was much more frequent with cypress pollen allergy, whereas asthma
symptoms during the pollen season were equally prevalent in patients allergic to
grass and cypress pollens. Besides, allergy to cypress pollen was more disabling
than other pollen allergies, according to a visual analog scale used by 4025 patients
visiting their general practitioner for allergic rhinitis [121].
The diagnosis of cypress pollen allergy mostly relies on the clinical history,
which is usually highly suggestive because most cypresses pollinate in winter-
time when no other airborne pollens are present. The diagnosis is supported by
skin tests, using either a mixture of C. sempervirens and Hesperocyparis arizonica
or extracts from J. ashei. However, in a few cases, despite the convincing medi-
cal history, skin tests are negative. [122]. The allergist can ask for specific IgE
measurement. Measurement of specific IgE to J. ashei has proven to be more
sensitive than IgE directed toward Cupressus allergens [123]. In few cases, the
patient is indeed sensitized to cypress pollen, but the relevance of this sensitiza-
tion in the clinical picture is questionable. Then, measurement of serum recom-
binant Cup a 1, which evaluates antibodies directed to the major allergen, can be
useful [122].

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Respiratory Allergy to Conifers
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.. Management of cypress allergic patients
... Pharmacological treatment
Compared with other allergic diseases, no specific pharmacologic treatments are
given for this condition.
... Immunotherapy
Although they only included a limited number of patients, several clinical
trials have addressed this issue [1]. A benefit in terms of symptoms, quality of life,
on-demand medications, late cutaneous response to allergen, and specific nasal
hyperactivity was demonstrated in all trials. Clearly, larger clinical trials including
longer treatments and longer follow-up periods are required.
... Individual avoidance procedures
While all of these procedures are based on common sense, they have not been
clinically validated [124]. This paper demonstrated that four recommendations are
provided by most scientific committees and organizations: avoiding outdoor activi-
ties, consulting pollen forecasts, avoiding drying laundry outdoors, and wearing
pollen protective glasses and mask when outdoors. All these pieces of advice are
applicable when the taxon to which an individual is sensitized is present.
... Collective strategies
Integrated strategies have to be developed to prevent cypress pollen allergy, in
addition to medical care and desensitization. The reduction in individual exposure
to pollen is the upstream component of this strategy. Pollinosis is more frequent in
urban areas, although airborne pollen concentrations should be lower than in rural
areas [125]. Therefore, the allergenic features of ornamental plants that are used
in urban green spaces, parks, and gardens should be taken into account in future
urban planning [126]. Should be chosen over allergenic wind-pollinated species
non-allergenic species and/or insect-pollinated species the use of the latter species
should be reduced in order not to aggravate their impact on allergy sufferers, even if
cultural and historical reasons often make this a difficult choice.
A “Database of Urban Tree Potential Allergenic Values,” integrating the different
components of the allergenicity risk (e.g., tree size, type of pollen dispersal type,
flowering period, etc.), has been generated for all of the individual trees producing
an estimate of the allergenicity of Urban Green Zones [127, 128].
People with pollen allergies could limit their exposure to pollen through consult-
ing forecast of pollen emissions based on phenological modeling of pollination.
They should avoid spending time in areas with high densities of Cupressaceae taxa.
Because pollen penetration in summer was estimated to be one hundred times
higher than in winter and although pollen is much more abundant in winter, the
penetration of pollen into dwellings must also be minimized by avoiding the open-
ing of doors and windows in the summer time [129]. This is all the more true that
cypress pollen allergenic potency was shown to last over at least a 10-month period
in an indoor environment [130].
Trimming of isolated trees or hedges before pollination represent a comple-
mentary strategy to reduce the amount of pollen produced by Cupressaceae trees.
It can significantly reduce pollen production [131]. An efficient medium- to

Conifers - Recent Advances

long-term way to reduce atmospheric pollen loads without the need to eradicate
the Cupressaceae species in urban areas could be to select low pollen producing
varieties. Female cultivars are preferable for the few monoecious species. Low
pollen cultivars should be selected for other species, either in natural populations or
breeding populations, as for C. japonica [132]. For this latter species, an approach to
prevent pollen dispersal lies in the use of pollen-specific fungal infection [133]. For
Cupressus, sterile cultivars can be produced through the production of haploid lines
from C. dupreziana surrogate mothers [134].
. Pinaceae
As stated in the introduction, Cupressaceae/Taxaceae and Pinaceae are the three
families of conifers studied at an allergy point of view. Pinaceae is mentioned as
poorly allergenic in the RNSA data bank despite a huge amount of pollen produced.
Eleven genera were described distributed in four subfamilies and 220–240 species.
Two genera are presented below, Pinus and Abies.
. Pinus
From the family Pinaceae, the genus Pinus includes about 120 species. The
main species studied at an allergy point of view are Pinus pinea, halepensis, radiata,
sylvestris, and nigra.
.. Trees and pollen
Pine trees are evergreen, conifer trees with leaves as needles bundled in clusters
called fascicles. Pines are mostly with male and female cones on the same tree. The
male cones are mainly present in spring, falling after pollen shedding. The female
cones have numerous spirally arranged scales, with two seeds per scale. Some pine
seeds (pine nuts) are edible and have been reported to induce allergies. Pine pollen
grains are 40–80μm diameter, are heavy, and harbor a waxy hydrophobic coat.
They are easily distinguishable under microscope observation because of two bal-
loons filled with air. This particularity does not help the pollen to float in the air but
rather to float on a water surface. The tree is anemophilous, and pollination is abun-
dant generating the so-called “sulfur rain” during pollinating season [135, 136].
.. Allergenicity
Despite the sometimes widespread pine forest and the abundance of pollen
grains, the allergenicity of pine pollen was considered very poor if not nonexistent
by some authors [137–144]. The involvement of pine pollen in seasonal allergic
reactions has been evaluated in some studies and has generally been considered of
little clinical significance. For example, Harris and German, in 1985, evaluated 200
patients during the pine pollen season [145]. Among them, only five had a positive
skin test to pine pollen (Pinus radiata), i.e., about 2%. Kalliel and Settipane reported
6% using Pinus strobus pollen [146], and Armentia et al described three cases with P.
pinea including one patient also sensitized to pine nuts [147]. Cross-reactions were
reported with ray-grass, but some genuine sensitization to pine pollen could also be
demonstrated in P. radiata [71, 148, 149]. In another study involving 826 patients in
northern Arizona [150], only 12 (1.5%) had a positive skin test to pine pollen (Pinus
ponderosa). Among them, eight reported a rhino-conjunctivitis during the pollen
season while four had perennial symptoms. However, a paper originating from an


Respiratory Allergy to Conifers
DOI: http://dx.doi.org/10.5772/intechopen.101217
area with high exposure to pine trees (north-west of Spain) described a series of 10
patients sensitized to pine pollen (Pinus pinaster and radiata) with symptoms dur-
ing the pine-pollen season, among whom eight were mono-sensitized [151]. As well,
in Canada, an increase in pollen from Pinaceae (pine, fir, spruce), Tsuga (hemlock),
and Larix (larch, tamarack) was shown to play a role in increase of daily hospital-
ization for asthma [152]. These studies did not result in the description of specific
pine pollen allergens. Allergens were only reported in pine nuts and correspond to
storage proteins, 7S vicilin, 2S albumin, and a 17kDa protein [153–155].
.. Hypotheses for low allergenicity
There are several hypotheses to account for this low apparent clinical signifi-
cance, which is at variance with the heavy pollen exposure in areas densely covered
with pines. Firstly, there might be an underestimation of the sensitization rate
because protein extraction from pine pollen is difficult [156]. In comparison to
classical extraction protocols such as soft incubation in aqueous solution, grinding
of the pollen grains together with 1mm silica beads results in 20–50 times more
extracted proteins amount (Figure ) [157]. The improvement of the extraction is
not only quantitative but also qualitative. Interestingly Pasaribu et al, using adapted
extractions protocols showed sequence homologies between oleosins from pine
nuts and pine pollen [158]. Oleosins have been reported to be allergenic in sesame,
peanut, and hazelnut, but classical protocols do not allow the extractions of these
hydrophobic proteins. Secondly, the pine pollen might have a low allergenic potency
because intrinsic compounds, which have been shown to play a role in enhancing a
Th2 immune response via innate immunity, are deficient. For instance, the enzyme
NADPH oxidase, proteases, and PALM (pollen-associated lipid mediators) contents
are low in pine pollen [56, 159, 160]. NADPH oxidase leads to generation of reac-
tive oxygen species, and PALM boosts Th2-type allergic reactions [161]. Finally,
similarly to other airborne allergenic sources, pollution and climatic change have
an impact on the allergenicity of pollen grain, and allergenicity of pine pollen was
indeed shown to be affected by O3 [162].
. Abies
.. Trees and pollen
From the family Pinaceae, the genus Abies includes 46 species. They originated
from temperate and north hemisphere, and fir is the most represented. They are
Figure 5.
Pine pollen (Pinus halepensis) observed under optical light microscopy, (200x magnification) from Brazdova
et al. [157]. A: Intact pollen grains. B: Grinded pollen using a multidirectional grinder (fast-prep 24-5G,
cool prep, MPBiomedicals) in the presence of 1mm silica beads. The disruption of pollen grains results in
qualitative and quantitative enriched protein extraction.

Conifers - Recent Advances

found in North and Central America, Europe, Asia, and North Africa, occurring
mostly in mountains. They are large trees, reaching heights of 10–80m tall when
mature. Firs can be distinguished from other members of the pine family by the
way in which their needle-like leaves are attached singly to the branches with a base
resembling a suction cup and by their cones, which stand upright on the branches
like candles and disintegrate at maturity. The leaves are significantly flattened with
an upper surface uniformly green and shiny. Fir trees produce very large amounts of
pollen annually in the spring and early summer. The pollen grains are large (160μm)
and similar to the pine pollen grains exhibiting two balloons filled with air.
.. Allergenicity
Abies pollen is considered barely allergenic, and only one study mentioning fir
pollen together with other Pinaceae pollen has been carried out so far in Canada
(see above [152]). No prevalence is reported and no allergens are described.
Fir is present in many homes during Christmas time, and there are a few reports
of rhinitis and conjunctivitis occurring during and following Christmas tree
exposure [163]. However, authors concluded that these symptoms were not pollen-
dependent but rather caused by volatile organic compounds emitted by the tree
since fir pollen grains have disappeared at Christmas time. One of these compounds
was identified as colophonium shown to be able to sensitize allergic patient to
induce dermatitis [164]. Another confounding and misleading factor could be mold
spores contaminating the Christmas tree [165]. Mold spores such as Aspergillus or
Cladosporium are well-known allergenic sources.
. Conclusion
Out of the seven families described in conifers, obviously the Cupressaceae/
Taxaceae was the most studied precisely because its wide distribution and the
powerful allergenic potential of its pollen giving rise to a high prevalence where
Cupressaceae/Taxaceae is implanted. Furthermore numerous associations with
food allergy were reported inducing not only respiratory but also food allergy
symptoms from the oral syndrome to more severe outputs such as systemic anaphy-
laxis or urticaria. Sensitization can occur lately, in non-atopic individuals and thus,
represents a public health threat. However, compared with ragweed or grass pollen
allergy, Cupressaceae trees rarely spontaneously reproduce, and their expansion
could then be controlled by policymakers.
Pinaceae pollen allergy was also studied, though to a lower extent, because
pollination is huge despite a very low prevalence. Therefore it does not repre-
sent an important health issue. The question of food cross-reactivity was also
addressed, especially with the edible pine seeds, but no convincing data were
published.
However, the climatic change and polluted environment might result in a general
trend to increase allergenicity of airborne allergenic sources, including pollen.
Therefore an immunosurveillance and health monitoring should be maintained for
all pollen species.
Funding
A part of the work on aerobiology was funded by the ICTA “Unit of Excellence”
(MinECo, MDM2015-0552).


Respiratory Allergy to Conifers
DOI: http://dx.doi.org/10.5772/intechopen.101217
Author details
DenisCharpin1*, HélèneSénéchal2 and PascalPoncet3
1 French Clean Air Association, Aix-Marseille University, Marseille, France
2 Armand Trousseau Children Hospital, APHP, Paris, France
3 Immunology Department and Armand Trousseau Children Hospital, APHP,
Institut Pasteur, Paris, France
*Address all correspondence to: charpindenis27@gmail.com
A part of the work on allergen identification was supported by the program
Hubert Curien-Barrande 2015-2016 (France and Czech Republic scientific
exchanges).
Conflict of interest
The authors declare that they have no conflict of interest concerning this article.
© 2021 The Author(s). Licensee IntechOpen. This chapter is distributed under the terms
of the Creative Commons Attribution License (http://creativecommons.org/licenses/
by/3.0), which permits unrestricted use, distribution, and reproduction in any medium,
provided the original work is properly cited.


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