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available at http://dx.doi.org/10.1289/ehp.124-A70.

Pollen Overload
Seasonal Allergies in a Changing Climate
Several intertwined factors influence how a plant grows and how much pollen it produces. Projected rises in two of
theseregional temperatures and atmospheric CO2 levelscould mean an increase in the number of people affected by
seasonal allergies. Joe Petersburger/Getty

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Focus | Seasonal Allergies in a Changing Climate

W
atery red eyes, runny nose, sneezing, symptoms in most cases dont trigger emergency room
coughingthese familiar symptoms visits or other types of medical care.
mean spring is in the air. Millions There is evidence suggesting that hay fever prevalence
of people suffer from seasonal aller- is rising in many parts of the world, particularly in urban
gies triggered by airborne pollen areas, although some of the most recently published stud-
not just in spring but in summer and fall, tooand now ies date back to the late 1990s.7,8,9 A newer report from
evidence suggests their numbers will rise in a changing Frances Rhne-Alpes Center of Epidemiology and Health
climate. The evidence so far is preliminary, but it points Prevention shows that hay fever prevalence rose from 8%
to a confluence of factors that favor longer growing sea- of the local population in 2004 to 12% in 2015.10 Michel
sons for the noxious weeds and other plants that trigger Thiboudon, director of the French National Aerobio-
seasonal allergies and asthma attacks. Carbon dioxide logical Monitoring Network, attributes the rising preva-
(CO2), in addition to being the lence to increased exposures
principal global warming gas, to highly allergenic ragweed.
can also be thought of as plant Climate change has been pro-
foodits the source of carbon jected to accelerate ragweeds
needed to make sugars during spread throughout the Euro-
photosynthesis.1 When exposed pean continent.11
to warmer temperatures and Bielory says its likely that
higher levels of CO2 , plants other environmental factors,
grow more vigorously and pro- such as changing diets and bet-
duce more pollen than they ter hygiene, contribute to the
otherwise would.1,2 prevalence of asthma and hay
Physicians who treat aller- fever by limiting early expo-
gic airway diseases are already sure to allergens and altering
reporting an uptick in symp- the immune systems normal
toms that they attribute to cli- development. However, much
mate change. 3 In a statement remains unknown about the
published last year, the World relationship between aeroaller-
Allergy Organization, compris- gens and exacerbation of asth-
ing 97 medical societies from ma, especially less severe attacks
around the world, opined that that arent reflected in hospital
climate change will affect the visit data.12
start, duration, and intensity Seasonal allergies in North
of the pollen season and exac- Pollen (gold spheres) is produced by the sta- America generally begin in
erbate the synergistic effects mens (gray), which are the male reproductive spring, when trees begin to
of pollutants and respiratory organ of flowering plants. Pollen grains are flower and disperse their aller-
infections on asthma.4 covered in proteins that assist in reproduction genic pollen into the airthey
Were seeing increases in but also trigger allergic reactions in sensitized include, among others, oak
both the number of people with people. Martin Oeggerli /Science Source and birch in the South and
allergies and what theyre aller- Northeast and mountain cedar
gic to, says Leonard Bielory, a professor and allergy spe- in the West. Late spring and early summer bring the
cialist at the Rutgers University Center of Environmental emergence of various allergenic grasses and weeds, such
Prediction and attending physician at Robert Wood John- as mugwort and nettle, which introduces another round
son University Hospital. Should warming continue, he of symptoms. The ragweed season comes last, starting in
says, then more people will be exposed to seasonal aller- late summer and persisting until the plants die with the
gens with subsequent effects on public health. first frost.13 A resurgence in grass pollen also occurs in
early fall, Bielory says.
Allergies on the Rise Pollen grains contain the male gametes (sperm cells)
Seasonal allergies and asthma impose significant health of the flowering plant; they are covered in proteins that
burdens, with an estimated 1030% of the global female gametes of the same species will recognize. Its
population afflicted by allergic rhinitis (or hay fever) and those same coating proteins that trigger allergic reac-
300 million people worldwide affected by asthma.5 Trend tions in sensitized people, with the degree of sensitization
data suggest that the prevalence of asthma, including varying among individuals. According to Lewis Ziska,
forms of the disease triggered by pollen, mold, and other a research plant physiologist with the U.S. Department
allergenic substances, is on the rise. Childhood asthma of Agriculture (USDA), the intensity of an allergic reac-
rates in the United States, for instance, doubled from tion depends on three interrelated factors: how much
1980 to 1995 before slowing to a more gradual (albeit pollen a given species emits into the air, the duration of
ongoing) increase. 6 Kate Weinberger, a postdoctoral exposure, and the allergenicity of the pollen. In ragweed
associate at Brown University, says trends in seasonal these factors coalesce in a perfect storm of allergic misery.
allergy prevalence are more difficult to track because Whats unique about ragweed is that it produces so much

Environmental Health Perspectives volume 124 | number 4 | April 2016 A71


Focus | Seasonal Allergies in a Changing Climate

with greater increases the farther north they


looked.13
During a more recent study published
in 2014, Bielory and colleagues reached a
similar conclusion. This team studied pollen
measures taken from 50 sampling stations
across the contiguous United States between
1994 and 2010. They reported that pollen
seasons for allergenic species were lengthen-
ing more in the north than in the south, and
that total counts of daily airborne pollen
were getting larger. As Ziskas research also
showed, the lengths of the southern pollen
seasons were either unchanged or had actu-
ally shortened with time.2
That finding goes to the heart of the
geographic complexities underlying climate
change and its inf luence on biological
systems. Ziska explains that CO 2 and
atmospheric water vapor exert competing
inf luences on warming trendswater
vapor suppresses warming in wetter, rainier
southern latitudes, in part by boosting cloud
cover, while CO2 accelerates warming in
dryer regions farther from the equator.
temperatures. He grew ragweed in chambers The implications of these phenomena
containing up to 600 ppm ambient CO2. are consistent with the health data.
Thats the atmospheric concentration that Jonathan Silverberg, an assistant professor
the Intergovernmental Panel on Climate at Northwestern University Feinberg School
Change predicts by the year 2050, assum- of Medicine, and his colleagues studied rates
ing no changes in current emissions.14 (At of childhood hay fever in relation to pollen
present, the atmospheric concentration level counts and weather conditions throughout
is just over 400 ppm.15) Ziska found that the United States, and found they were
the size of the experimental ragweed plants lowest in wetter areas with higher humidity
and their pollen output increased in tandem levels.19
with rising CO2.16 Meanwhile, in Europe ragweed has dra-
Ziska then modeled future climate con- matically expanded its range since it was
ditions using a novel surrogate: He and his first introduced to the continent in the
colleagues compared how ragweed grew in 1800s, 20 and scientists anticipate its spread
urban and rural locations. Their rationale will accelerate further with climate change.
was that cities are heat sinks (because theyre Modeling by the French Climate and
Top: Seasonal allergies in North America paved in dark surfaces that absorb and later Environment Sciences Laboratory predicts a
begin in the spring, when trees such re-radiate solar heat) as well as sources of four-fold jump in levels of airborne ragweed
as birch (shown), oak, and mountain
CO2 (from traffic and industrial emissions). pollen by 2050, with the biggest increases
cedar begin to bloom. The inconspicuous
flowers of plants like these are designed
Ziskas team planted ragweed in urban Bal- occurring in northern and eastern parts of
not to attract pollinators but to release timore, where measured CO2 levels were Europe.11 Apart from ongoing seed disper-
their pollen into the air, where it is carried 30% higher and temperatures 3.5F hotter sal, the models estimate higher CO2 levels
by the wind. Marcus Lindstrom/Getty on average than they were outside the city. and warmer temperatures will help lengthen
Inset: Certain grasses and weeds Their findings showed that urban ragweed ragweeds pollen season.
(such as Bermuda grass, shown here plants grew faster, flowered earlier, and pro- A study published in 2014 showed that
magnified) trigger further allergies into duced more pollen than those grown outside pollen seasons have already become longer
the summer. Flowers that are barely the city.17 in western Poland. 21 The authors focused
visible to the naked eye can pack a Climate changerelated warming is on allergenic species other than ragweed
major allergenic punch. Susan M. Booker anticipated to increase as one moves up in namely, nettle, sorrel, broad-leaf dock, and
latitude.18 To assess the effect of warming various grasses. According to their sam-
pollenroughly a billion grains per plant, temperatures on the length of ragweeds pling results, species-specific pollen seasons
Ziska says. And the Amb a 1 protein [con- flowering season, Ziskas team, including lengthened by 2 to nearly 4 days between
tained in the ragweed pollen coat] is also Bielory, studied measures of airborne pol- 1996 and 2011, a trend the authors attribut-
highly reactive with the immune system. len collected from 10 sampling stations ed mainly to warmer summer temperatures
extending from east Texas to Saskatoon, and later pollen season end dates.
Regional Differences 2,200 kilometers to the north. The results,
Ziska conducted studies in the 1990s to though not unexpected, were remarkable: Accessing Pollen Data
explore potential links between pollen pro- Between 1995 and 2009, they found the European pollen databases are more accessi-
duction, rising CO2 levels, and warming pollen seasons lengthened by 1327 days, ble and widespread than those in the United

A72 volume 124 | number 4 | April 2016 Environmental Health Perspectives


Focus | Seasonal Allergies in a Changing Climate

a CHIMERE c CHIMERE e CHIMERE

b RegCM d RegCM f RegCM

0 50 100 500 1,000 2,500 5,000 7,500 10,000 12,500 15,000 20,000 25,000

Using two different climate models, researchers modeled historical levels of ragweed
States, says Richard Flagan, a professor pollen in Europe (frames a/b), then projected increases by 2050 (frames c/d and e/f).
of environmental science and engineering Some areas saw a projected fourfold jump. Source: Hamaoui-Laguel et al. (2015)11
at the California Institute of Technology.
He says thats chiefly because European
national weather agencies take responsibil- Flagan describes his efforts to access The Council of State and Territorial Epi-
ity for sampling and organizing the infor- NAB data as an exercise in frustration demiologists, a professional association for
mation in ways that scientists can use for that was frequently met with unanswered public health epidemiologists, has proposed
research. phone calls and e-mails. Moreover, the way such a system in a draft white paper that
By contrast, pollen sampling in the these stations collect data isnt compatible it plans to finalize at its June 2016 annual
United States is performed by a constella- with science, he says. We have at best a conference.
tion of agencies and allergy clinics. Cur- semi-qualitative historical record supplied
rently 84 of these sampling stations submit by people who do not focus on the statistics Lab Results Hint at
their data to a volunteer organization called of the measurementthat record has some Possibilities
the National Allergy Bureau (NAB), scientific value, but you have to look at it Even as researchers grapple with limited
which is organized by the American Acad- with a big grain of salt. In reality, the pollen field data, they continue to produce
emy of Allergy, Asthma & Immunology database in the United States is abysmal. compelling results in climate-controlled
(AAAAI).22 Bielory says the AAAAI pro- The USDAs Ziska says the NAB has chambers that predict future effects on
vides quality control in the form of training become more cooperative and responsive allergenic species. In her research at the
and certification for contributors on how to to the needs of outside researchers. But he University of Massachusetts Amherst,
sample airborne pollen. adds that since NAB sampling stations use Kristina Stinson, an assistant professor
The NAB provides daily pollen counts different tools and methodologies to collect of environmental conservation, grows
to local media outlets, but it wont release pollen, rather than one uniform system, ragweed in greenhouses containing CO2
any data for research without the consent their data can be difficult to aggregate and at levels ranging from 360 ppmjust
of the sampling stations that collected it. compare. under the current ambient concentration
To access those data, scientists have to Bielory, who contributes to the NAB, to 720 ppm. Stinson says higher CO 2
submit formal requests describing their agrees on the need for a national monitor- levels could force evolutionary changes
research plans.23 The NAB passes approved ing system that collects, stores, analyzes, in ragweed. A study she published in
requests to the appropriate member sta- and shares pollen data for the purpose of 2011 showed that genotypes that are
tions, which have 30 days to respond. advancing science and health policy issues. suppressed at current CO2 levels devoted

Environmental Health Perspectives volume 124 | number 4 | April 2016 A73


Focus | Seasonal Allergies in a Changing Climate

Protection Agency, shes now collaborating


+27 days with David Foster, director of the 3,750-
acre Harvard Forest, on a project to map
ragweed hot spots in New England. Their
field studies so far, which have been sub-
+22 days mitted for publication, show that ragweed
plants from urban and rural areas differ in
the extent and timing of flower production
and in their responses to CO2.
+19 days Among other research questions, Stin-
+21 days son hopes to explore spatial patterns in how
people experience the effects of climate
+15 days change on pollen production. We may
find that urban populations from a par-
+13 days
ticular demographic might be dispropor-
tionately affected by how climate change
+10 days affects allergenicity, she says.

Connecting the Dots on Health


+18 days Stinson says that connecting climate-
induced trends in allergenicity with public
health impacts could be challenging. It will
require that scientists have better access to
+10 days pollen data than they currently do in addi-
+1 day tion to health outcomes data that might be
correlated with rising pollen exposure levels.
Weinberger, of Brown University, has
studied the relationship between daily
spring pollen counts and health outcomes
in New York City. Results published
-1 day last year showed that mid-spring peaks
in tree pollen were associated with over-
the-counter allergy medication sales and
emergency room visits for asthma attacks,
Warming is expected to increase with increasing distance from the equator. One especially among children. 28 By contrast,
multiyear study in North America found that pollen seasons lengthened incrementally unpublished research shes conducted
with increasing northern latitudeby up to 4 weekswhile decreasing slightly in the
showed no similar relationship between
southernmost monitoring location. Source: U.S. EPA, based on data from Ziska et al. (2011)13
allergy drug sales and peak exposures to
ragweed pollen in the fall. Weinberger
more resources to reproduction as CO2 precursor pollutants also continue rising.26 says thats possibly because allergy medica-
levels rose. 24 In other words, she says, Albertines study didnt reveal any growth- tion purchased in the spring might last
more genotypes overall were f lowering. limiting effect of ozone on grasses raised for months; in the absence of sales data,
Stinson says that while she didnt measure in elevated CO2. But she did find that researchers wouldnt be able to detect a
pollen output directly, we do note that the grasses responded to higher ozone relationship to symptoms.
more vigorous flowering and higher pollen levels by making less of their allergenic Despite the data gaps that remain, many
production are usually correlated. protein (Phl p 5). However, any reduction healthcare professionals believe the trend is
Her colleague Jennifer Albertine, a in the plants allergenic protein content, real, as evidenced by surveys of physicians
postdoctoral researcher at the University Albertine predicted, would be offset by who treat seasonal allergies. One survey
of Massachusetts Amherst, generated com- a corresponding increase in pollen involved members of the American Thoracic
parable results with timothy grass, a wide- production, for a net boost in allergenic Society, including pulmonologists, critical
spread perennial in North America and threat.25 (Similarly, Ziskas research showed care clinicians, pediatricians, and other spe-
Europe and a major cause of early summer that when raised in greenhouses containing cialists. Over half the participants queried
allergies. Albertine studied the effects of up to 600 ppm CO 2, ragweed plants in the survey reported increases in allergic
CO2 at both 400 and 800 ppm. She found produced 6080% more of their allergenic symptoms among their own patients that
that timothy grass exposed to 800 ppm protein, Amb a 1.27) the doctors believed were related to climate
CO2 produced roughly twice as much pol- Stinson acknowledges that, although change.3 A survey of AAAAI members, cur-
len as the lower-exposed grass.25 greenhouses allow for a controlled assess- rently in press, reached a similar conclusion:
Albertine also tested the effects of ment of how atmospheric conditions affect In this case, specialists were asked [How]
boosting ground-level ozone, which allergenic plants, they dont replicate the do you think your patients are being affect-
ordinarily slows plant growth by inducing real world, where other pollutants, humid- ed by climate change or might be affected
oxidative damage. Coupled climate/ ity, rainfall, and additional soil nutrients in the next 1020 years? Nearly two-thirds
tropospheric chemistry modeling indicates especially nitrogenalso influence plant reported seeing increased care for allergic
ozone levels could rise significantly by growth and pollination patterns. With sensitization and symptoms of exposure to
the end of the century as emissions of funding from the U.S. Environmental plants or mold.29

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Focus | Seasonal Allergies in a Changing Climate

Mona Sarfaty, director of the Program


on Climate and Health at George Mason
University, led both those surveys. She says
that to her surprise, neither study detected
regional difference in physician responses.
Instead, greater allergy symptoms seemed to
be showing up across the country, she says,
with only the symptoms themselves varying
by location. So a doctor in Michigan who
ordinarily sees relief from mold allergies with
the arrival of cold weather might see them
persisting later into the year, she explains,
while a doctor in Southern California might
be reporting grass allergies all year round.
Sarfaty says that doctors who claimed not to
believe in climate change were less likely to
report these trends.
Kim Knowlton, a senior scientist with
the Natural Resources Defense Council, who
also holds a faculty post at the Columbia
University Mailman School of Public Health,
acknowledges the need for more research.
What we have to do is tease out the chain Clim Change 5(8):766771 (2015), doi:10.1038/
nclimate2652.
of events starting with higher temperatures 12. Schmier JK, Ebi KL. The impact of climate change
and CO2 levels, to effects on allergenicity, and aeroallergens on childrens health. Allergy
Asthma Proc 30(3):229237 (2009), doi:10.2500/
to human health symptoms, she says. The aap.2009.30.3229
studies so far are compelling, but we need 13. Ziska L, et al. Recent warming by latitude associated
with increased length of ragweed pollen season
more comprehensive studies at larger scales. in central North America. Proc Natl Acad Sci
USA 108(10):42484251 (2011), doi:10.1073/
For the tens of millions who have allergies pnas.1014107108.
and asthma, this is more than an inconve- 14. IPCC. Carbon Dioxide: Projected Emissions
and Concentrations [website]. Geneva,
nience, she saysThose illnesses can keep Switzerland:Intergovernmental Panel on Climate
you out of school and work, and for some Change (updated 4 April 2014). Available:http://
www.ipcc-data.org/observ/ddc_co2.html[accessed
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15. CO2. Earth [website]. Victoria, British Columbia,
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Available: https://www.co2.earth/ [accessed
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research journals, and websites. artemisiifolia L.), a known allergy-inducing species:
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