temporal and geographic variation in aeroallergen

Temporal and geographic variation in aeroallergen

measurements across four Canadian cities from

2008-2012

by

Cecilia Sierra Heredia

M.A., University of British Columbia, 2004

B. Psych. (Hons.), Universidad Nacional Autónoma de México, 2001

Thesis Submitted in Partial Fulfillment of the

Requirements for the Degree of

Master of Science

in the

Master of Science Program

Faculty of Health Sciences

© Cecilia Sierra Heredia 2019

SIMON FRASER UNIVERSITY

Spring 2019

Copyright in this work rests with the author. Please ensure that any reproduction or re-use is done in accordance with the relevant national copyright legislation.

ii

Approval

Name: Cecilia Sierra Heredia

Degree: Master of Science (Health Sciences)

Title: Temporal and geographic variation in aeroallergen measurements across four Canadian cities from 2008-2012

Examining Committee: Chair: Anne-Marie Nicol Associate Professor

Timothy Takaro Senior Supervisor Professor

Ryan Allen Supervisor Associate Professor

Sarah Henderson Supervisor Associate Professor, School of Population and Public Health, University of British Columbia

Robert Schellenberg External Examiner Professor, Faculty of Medicine University of British Columbia

Date Defended/Approved: March 11, 2019

iii

Ethics Statement

iv

Abstract

Fungal spores and pollen from trees, grasses, and weeds are associated with outdoor

environmental allergies in Canada. These aeroallergens typically have a distinct

temporal pattern across geographical regions. This study describes seasonal and

geographic variation in aeroallergens from 2008-2012 in the Canadian cities of

Vancouver, Edmonton, Winnipeg, and Toronto. The study period and study locations

were chosen to characterize the potential aeroallergen exposures of participants in the

Canadian Healthy Infant Longitudinal Development (CHILD) birth cohort. Seasonal

exposures in Vancouver were the longest for every group of aeroallergens, except

grasses. Vancouver was also the highest for the trees pollen. Total fungal spore

concentrations were higher in Edmonton, Winnipeg, and Toronto than in Vancouver.

The differences recorded in this study across geographical regions may be significant for

the CHILD participants if they lead to distinct and clinically important windows of

exposure for infant immune response and subsequent differential risk of allergenic

disease.

Keywords: Aeroallergens; pollen; spores; Canada; asthma, allergies.

v

Dedication

To Rodrigo, Natalia and Gerardo: Whose smiles infused me with fortitude from Heaven.1

1 The Tempest, 1.2.263.

vi

Acknowledgements

To Tim Takaro: For your steady support, in every possible way, at each step of

this process.

To Ryan Allen and Sarah Henderson: For your valuable insights and keen

attention to detail.

To the members of the Childhood Asthma, Climate Change and Health Impacts

group: Jordan Brubacher, Shadi Mahmoodi, Bhimal Chhetri, Jaclyn Parks and Sally

Maguet. For generously sharing your hard-earned expertise and for all the different ways

you helped me along the way.

To my coauthors, Michelle North, Jeff Brook, Christina Daly, Anne K. Ellis, Dave

Henderson and Éric Lavigne.

To Frances Coates and everyone at Aerobiology Research Laboratories.

To Nikolas Krstic: For compiling the Landsat images included in Figure 7.

To the people at the Faculty of Health Sciences: Your everyday acts of kindness

were always noted and much appreciated.

To SFU Library’s Research Commons and each of their consultants: For the

invaluable services they provide through the Read-Ahead, R, and Thesis Template

Consultations, and the Thesis Boot Camp.

To SFU’s Graduate Student Society, Teaching Support Staff Union and Big Data

Initiative: For the KEY Graduate scholarship, Professional Development Grant, Childcare

Benefits and many other ways you supported my time as a graduate student.

To the CHILD community: participants, families, research associates and study

investigators: I am honored to have worked with you through your data.

To my friends and family (here, there and everywhere): Just as it takes a village

to raise a child, it took a village to complete my studies and I would not have been able

to do it without your help.

vii

Table of Contents

Approval .......................................................................................................................... ii

Ethics Statement ............................................................................................................ iii

Abstract .......................................................................................................................... iv

Dedication ....................................................................................................................... v

Acknowledgements ........................................................................................................ vi

Table of Contents .......................................................................................................... vii

List of Tables .................................................................................................................. ix

List of Figures.................................................................................................................. x

List of Acronyms ............................................................................................................. xi

Chapter 1. Introduction .............................................................................................. 1

Chapter 2. Background .............................................................................................. 3

2.1. Plant Pollen ........................................................................................................... 3

2.2. Fungal Aeroallergens ............................................................................................ 5

2.3. Canadian Distribution of Plant-Derived Aeroallergens ........................................... 6

2.4. The Impact of Aeroallergens on Humans: .............................................................. 8

2.4.1. Immune System ............................................................................................. 8

2.4.2. Respiratory System ....................................................................................... 9

2.4.3. Asthma ........................................................................................................ 10

2.5. The Role of Aeroallergens and the Development of Respiratory Disease ............ 10

2.5.1. The Relationship Between Allergies and Asthma ......................................... 10

2.5.2. Thresholds of Effect ..................................................................................... 12

2.5.3. The Priming Effect ....................................................................................... 12

2.5.4. Effect Modifiers ............................................................................................ 13

Effect Modifier: Weather ......................................................................................... 14

Effect Modifier: Seasonality .................................................................................... 14

Effect Modifier: Urbanization .................................................................................. 15

Effect Modifier: Air Pollution ................................................................................... 15

2.6. Effects of Climate Change on Aeroallergens ....................................................... 16

2.7. Knowledge Gaps and Challenges ........................................................................ 18

Chapter 3. Methods .................................................................................................. 19

3.1. Study Setting ....................................................................................................... 19

3.2. Data Collection .................................................................................................... 20

3.3. Data Analysis ...................................................................................................... 24

Chapter 4. Results .................................................................................................... 26

4.1. Within-Station Differences for Pollen ................................................................... 28

4.2. Between-Station Differences for Pollen ............................................................... 35

4.3. Within-Station Differences for Fungal Spores ...................................................... 38

4.4. Between-Station Differences for Fungal Spores .................................................. 45

viii

Chapter 5. Discussion .............................................................................................. 48

5.1. Limitations ........................................................................................................... 49

5.2. Strengths ............................................................................................................. 50

5.3. Recommendations ............................................................................................... 51

Chapter 6. Conclusion ............................................................................................. 54

References ................................................................................................................... 56

Appendix. Allergenic pollen reported by country .............................................. 77

ix

List of Tables

Table 1. List of aeroallergen stations and years of data collection. ....................... 21

Table 2. Family, genus and species analyzed ...................................................... 21

Table 3. Peak values and peak dates for pollen ................................................... 28

Table 4. 5-year mean and range of pollen cumulative concentrations (grains / m3 in hundreds). .......................................................................................... 38

Table 5. 5-year mean and range of pollen season length between cities (number of days). ..................................................................................................... 38

Table 6. Peak values and peak days for spores ................................................... 39

Table 7. 5-year mean and range of spore cumulative concentrations (spores / m3 in hundreds). .......................................................................................... 46

Table 8. 5-year mean and range of spore season length between cities (number of days). ..................................................................................................... 47

x

List of Figures

Figure 1. The aerobiology pathway of pollen ........................................................... 4

Figure 2. Ecological zones of Canada. .................................................................... 7

Figure 3. Adverse immune response in the airway. ................................................. 8

Figure 4. Effects of climate change on aeroallergens ............................................ 17

Figure 5. Location of the four Canadian Healthy Infant Longitudinal Development (CHILD) birth cohort cities and the aeroallergen stations. ....................... 19

Figure 6. Month of birth of the participants from the Canadian Healthy Infant Longitudinal Development (CHILD) birth cohort. .................................... 20

Figure 7. Ground coverage at 20km resolution from Landsat satellite data. .......... 27

Figure 8. Weekly pollen concentrations 2008-2012 in Vancouver with Mean and Standard Deviation (SD). ....................................................................... 30

Figure 9. Weekly pollen concentrations 2008-2012 in Edmonton with Mean and Standard Deviation (SD). ....................................................................... 31

Figure 10. Weekly pollen concentrations 2008-2012 in Winnipeg with Mean and Standard Deviation (SD). ....................................................................... 33

Figure 11. Weekly pollen concentrations 2008-2012 in Toronto with Mean and

Standard Deviation (SD). ....................................................................... 34

Figure 12. Weekly aggregates of coniferous and deciduous tree pollen concentrations, average of 2008-2012 in the CHILD cities. .................... 36

Figure 13. Weekly aggregates of grass and weed pollen concentrations, average of 2008-2012 in the CHILD cities. ............................................................... 37

Figure 14. Weekly spore concentrations 2008-2012 in Vancouver with Mean and Standard Deviation (SD). ....................................................................... 41

Figure 15. Weekly spore concentrations 2008-2012 in Edmonton with Mean and Standard Deviation (SD). ....................................................................... 42

Figure 16. Weekly spore concentrations 2008-2012 in Winnipeg with Mean and Standard Deviation (SD). ....................................................................... 43

Figure 17. Weekly spore concentrations 2008-2012 in Toronto with Mean and Standard Deviation (SD). ....................................................................... 44

Figure 18. Weekly aggregates of Ascomycetes, Basydomicetes and Fungi Imperfecti spores concentrations, average of 2008-2012 in the CHILD cities. ........ 46

xi

List of Acronyms

ARL Aerobiology Research Laboratories

CHILD Canadian Healthy Infant Longitudinal Development (birth cohort)

CO2 Carbon Dioxide

ETS Environmental Tobacco Smoke

GST Glutathione-S-Transferase

H2O2 Hydrogen Peroxide

IgE Immunoglobulin E

ILC2 Innate Lymphoid cells 2

iNKT Invariant Natural Killer T Cells

NO2 Nitrogen Dioxide

PM Particulate Matter

SD Standard Deviation

SO2 Sulfur Dioxide

VOCs Volatile Organic Compounds

1

Chapter 1. Introduction

Over the past 70 years, the prevalence of allergic conditions has increased in

high-income countries affecting as much as 40% of the population in regions of

Australia, New Zealand, and the United States, and becoming widely recognized as a

public health concern (1,2). Studies in countries such as Germany (3), Japan (4),

Morocco (5), Hungary (6), Mexico (7), and Australia (8) report rapid increases in the

prevalence of allergic conditions that cannot be explained by genetic changes only (9–

12). Aeroallergens and air pollutants have been hypothesized as potential causes for the

steep increase in allergic conditions, because the nature of these environmental

exposures has changed during a similar time period (13).

Environmental factors play a key role in defining the type of sensitization and the

kind of atopic disease in genetically at-risk individuals. While heredity regulates the

intergenerational transmission of the susceptibility to different phenotypes of atopic

responsiveness, environmental exposure is a crucial factor in the development of atopic

disease. Common aeroallergens (e.g., pollen or mold spores) and air pollution, such as

particulate matter (PM) or environmental tobacco smoke (ETS); and other environmental

exposures have been associated with increased risk of atopic conditions (14).

Pollen grains and fungal spores are widely dispersed in the air so that the

respiratory system is the first point of contact between the human body and the proteins

they contain (15); therefore, the immune response (adverse immune response) to these

proteins starts in this system (16). Aeroallergens (i.e. pollen grains and fungi) carry non-

infectious proteins, so exposure to aeroallergens is an innocuous event for most

individuals because for them, these proteins do not trigger an infectious disease (17).

For others, however, the exposure to aeroallergens’ proteins triggers an allergic immune

response and the related symptoms. Allergic reactions to aeroallergens represent the

most frequent type I hypersensitivity, affecting up to 30% of the population in high-

income countries (18).

Previous research has indicated that certain pollen grains are highly allergenic

(e.g., ragweed a.k.a. Ambrosia) and exist at relatively high concentrations in some parts

of Canada (19). Spores from fungi are also important aeroallergens that have been

2

linked to allergic reactions (20,21) and in some studies potentially also to the risk of

asthma development (22). This combination of allergenicity and prevalence makes

pollen such as ragweed problematic, because the number of sensitized individuals is

increasing (23). This exposure and the physical symptoms of the immune response have

a direct impact on the everyday lives of patients who develop allergic conditions.

Researchers such as de Weger et al. (16) and von Mutius (24) acknowledge the

diversity of factors that influence the health impacts of aeroallergens and call for better

understanding of extrinsic influences, such as differences in temporal and geographical

patterns, which contribute to the new onset of the allergic conditions associated with

aeroallergen exposures. In this project, I describe the seasonal and geographic patterns

for the most common aeroallergens in four Canadian cities: Vancouver, Edmonton,

Winnipeg and Toronto, between 2008-2012.

3

Chapter 2. Background

2.1. Plant Pollen

Pollen grains are defined as “multinucleate reproductive microgametophytes of

plants” (25, p.2); they function as a container for the male gametophytes of plants (26).

The essential reproductive event among higher plants is achieved only when the pollen

grain is successfully transferred from the floral anther to the recipient stigma. However,

this transfer is not easily accomplished and successful pollination involves many steps.

Plants are classified into two categories according to the strategies they use for pollen

transfer (27):

1) Entomophilous plants depend on organisms such as insects or hummingbirds

to carry larger, stickier pollen grains to their receptors.

2) Anemophilous plants release large quantities of pollen grains to be blown in

the wind to their receptors.

When anemophilous plants release pollen, a number of environmental factors

affect when and how many grains reach their final destination (28). Many of these

factors are affected by shifting climatic conditions (29,30). The aerobiology pathway of

pollen illustrates how pollen grains can travel from their source to interact with humans

and potentially affect health (Figure 1).

4

Figure 1. The aerobiology pathway of pollen Adapted from (31).

Because inhalation is the predominant type of exposure for humans, the

respiratory system is the first point of impact for aeroallergens. The exact point of impact

on the respiratory system depends on the size of the inhaled pollen. Pollen size can vary

from less than 10m to more than 100m; pollen grains from trees, weeds or grass or

spores from the fungus Alternaria, that are larger than 5m, deposit in the ocular

conjunctiva and nasal mucosa and have the potential to trigger allergic reactions such as

conjunctivitis or allergic rhinitis (32). Smaller particles (<5m), like spores of moulds

such as Penicillium or Aspergillus (33), can reach the lungs and have been linked to

asthma onset or exacerbation (34).

Because anemophilous plants are present in almost every location inhabited by

humans, humans are exposed to anemophilous pollens and our bodies have the

potential to develop adverse immune responses to those pollen. Currently, more than

150 pollen allergens are curated by the International Union of Immunological Societies

(18). Each geographical region has their own list of pollen of particular interest due to

5

their abundance in the atmosphere (35) and allergenic potency (36), (p.10). In Canada,

birch and grasses are more abundant than ragweed, which is found mostly in Ontario

and Quebec (19).

The concentrations of outdoor aeroallergens are determined by sampling the

outdoor air, and largely based on microscopic examination to identify pollen and spores

based on morphologic pattern recognition (37,38). Because aeroallergens must still be

collected and manually counted, it is currently impossible to offer real-time data using

conventional methods. Furthermore, due to the large amount of resources required for

aeroallergen measurements, it is not yet feasible to routinely make measurements at

high spatial or temporal resolution, although bi-hourly values are occasionally reported in

research (39).

2.2. Fungal Aeroallergens

Fungi are eukaryotic organisms that grow all over the world, in the presence of

moisture and carbohydrates (21,40). Fungi produce spores on maturity, through both

sexual and asexual mechanisms (41,42). The asexual spores produced by mitosis

appear to be the most allergenic (20,21). In addition to molecules on the surfaces of

spores, fungi also secrete enzymes into their environment that can act as allergens in

sensitized individuals, triggering detectable IgE levels (21,43). Like pollen grains, fungi

spores have low mass and can remain suspended in the air for varying periods of time

depending on the weather, with proteins (from their secreted enzymes) in both live and

dead fungi products causing symptoms in humans (15); in some zones of North America

they can be found in the air year-round (44).

Currently, fungi are organized into eight phyla, some of which produce important

aeroallergens, such as Ascomycota, Basidiomycota and Deuteromycetes (previously

labelled Fungi Imperfecti) (21,45,46). Outdoor airborne fungi such as Cladosporium,

Alternaria, Penicillium, and Aspergillus can trigger allergic responses in sensitized

individuals (47) and were traditionally grouped in the taxa of Fungi Imperfecti if they

lacked an obvious sexual stage (21). Advances in the classification of fungi through DNA

sequencing have opened the possibility of reorganizing and relabeling this taxa (as

Zygomycota, (21), but for health-based reporting spore concentrations are still grouped

6

in the traditional three categories: Ascomycota, Basidiomycota and Fungi Imperfecti

(Personal communication, Aerobiology Research Laboratories).

2.3. Canadian Distribution of Plant-Derived Aeroallergens

The environmental factors involved in pollen dispersion, including precipitation,

soil composition and moisture, and average high and low temperature (Figure 1) also

affect the geographical distribution of plant species (19).

A climate-based classification for local climate or ecological zones shows 15

different terrestrial ecozones in Canada (Figure 2); the cities from the Canadian Healthy

Infant Longitudinal Development (CHILD) birth cohort are located in three different

ecozones: Vancouver in the Pacific Maritime, Edmonton and Winnipeg in the Prairies,

and Toronto in the Mixedwood plains. Ecological zones are defined as areas of the

Earth’s surface with uniform cover, structure, material, and human activity. Each zone is

characterized by interactive and adjusting abiotic and biotic factors that span hundreds

of meters to several kilometers in horizontal scale (48,49). Aeroallergens are one of the

biotic factors that characterize each ecological zone. These include (a) a thermal factor,

as a metric for climate-dependent ecological processes involving vegetation, and (b) a

moisture factor, to quantify the wetness of the environment corresponding with the

distribution of natural vegetation (50). The major allergenic plants that grow in each of

the Canadian ecological zones are widely varied.

7

Figure 2. Ecological zones of Canada.

(51)

Local factors can also affect spatial variation within a region (52). Examples of

these are (a) tree canopy, defined as the types of trees planted in the geographical area

of interest (53), and (b) level of urbanization, defined considering street network

coverage and quantity of vegetation (54). The amount of pollen in the air at a particular

location also depends on the proximity to and number of source plants in the area,

atmospheric conditions, and plant physiological factors such as the number of

accumulated degree days (a temperature threshold for that species) at which their pollen

are released (55). Pollen grains can break open to release submicronic pollen-derived

bioaerosols that contain allergenic proteins, particularly when the grains have been aloft

for some time and/or become wet (56–59), especially during thunderstorms. Some

increased exposure to aeroallergens is also due to human activities, such as

landscaping practices, that create niches favoring the growth of weeds such as ragweed

(55).

8

2.4. The Impact of Aeroallergens on Humans:

2.4.1. Immune System

In humans, aeroallergens can lead to both immunosuppression or a heightened

immune response (i.e., allergies) (60), with a biologically appropriate response in the

middle of these extremes (i.e. appropriate recognition and response to harmful

pathogens) (17). Pollen grains carry cytoplasmic granules that release different proteins

and glycoproteins when they are exposed to water or airborne pollutants. These proteins

instigate the adverse immune response in sensitized individuals (Figure 3) (25,61–63).

In addition, single and repeated exposures to pollen in allergic individuals have been

shown to induce epigenetic changes, both in the blood and the nasal tissue (64).

Figure 3. Adverse immune response in the airway.

Adapted from (65).

Environmental exposures to aeroallergens produce a specific imbalance in the

immune system (66) that triggers the heightened immune response. There are two types

of T helper immune cells (Th1 and Th2) that appear imbalanced in allergic conditions

(67), with a higher proportion of the Th2 cell population (68). The hygiene hypothesis is

also considered as one of the reasons for the specific imbalance in the immune system

9

(69). This hypothesis attributes a reduced exposure to infectious agents at key times of

immune system development to the Th2 predominance. This skewed microbial exposure

may be due to improved hygiene and sanitation, and increased use of disinfectants,

vaccines, and antibiotics (70). When an individual has this type of imbalanced immune

system, repeated exposures to a myriad of specific proteins (e.g., pollen, certain molds,

dust mite feces, eggs, peanuts) can induce the creation of IgE antibodies (71). The initial

exposures to the proteins produce a sensitization to these specific molecules, and

subsequent exposures will trigger symptoms each time (71,72). Allergy symptoms in

response to pollen and fungal spores are driven by IgE that is specific to proteins found

in these spores (73). The allergenicity of pollen spores refers to the concentration of

protein epitopes in each spore, to which specific IgE molecules produced by the plasma

cells of allergic individuals may bind (74).

2.4.2. Respiratory System

Trees, grasses, and ragweed are the most common allergens associated with

outdoor allergies across Canada (75,76). There is substantial clinical cross-reactivity

between tree and grass allergenic species (76). Additionally, short ragweed is highly

cross-reactive with all other ragweed species, as well as sage and mugwort (75,77–80).

For example, individuals allergic to birch pollen in Northern Sweden have also been

sensitized to beech pollen (Fagus), although that species does not grow in the region

(81). For seasonal allergic rhinitis, grass and tree pollen are the most common allergens

(82).

The impact of aeroallergens has been documented in every section of the

airway. Due to the many similarities between the nasal and bronchial mucosa and their

reactions to aeroallergens, the “one airway, one disease” concept has been proposed for

allergic rhinitis and allergic asthma (83). The nasal passage is the first point of contact

with aeroallergens, and the histamine released due to interaction with aeroallergens

increases tissue swelling and permeability, causing rhinitis and rhinorrhea (84). Rhinitis

is a risk factor for the development of asthma (82) and allergic rhinitis is most commonly

due to pollen allergy (85). Approximately 80% of patients with allergic asthma also have

allergic rhinitis symptoms upon exposure to aeroallergens, but not all people with allergic

rhinitis experience asthma symptoms (83,86,87). Sensitization to aeroallergens is a

major contributing factor to this discrepancy (88).

10

2.4.3. Asthma

Among respiratory conditions, asthma is one of the major non-communicable

chronic diseases. Globally, approximately 235 million people currently suffer from

asthma (89). In high-income countries such as Canada, prevalence rose for many years

from the early 1960s to 2000 (29,61) and recently seems to have reached a plateau

(90,91).

Asthma is one of the most severe expressions of an adverse immune response

in the respiratory system (60,92). This condition falls into the category of allergic disease

because it involves the specific IgE-mediated hypersensitivity and the subsequent

inflammatory processes in the airways (93). The hyper-responsiveness of the airways

and subsequent constriction following allergen exposure are distinctive clinical findings

in asthma (94–96). Constriction is due to inflammatory processes and airway

remodeling. The reversibility of the inflammation (over time or by medication) is also

considered in asthma diagnosis (24). Wheeze, cough, and paroxysmal dyspnea are less

specific clinical signs of asthma. Persistent symptoms, triggered by the Th2 and IgE

interactions, lead to structural changes and remodeling of the airway (97).

2.5. The Role of Aeroallergens and the Development of Respiratory Disease

2.5.1. The Relationship Between Allergies and Asthma

A link between sensitization to outdoor pollen of local plants has been reported in

many countries between 1990 and 2016 on almost every continent (complete list in

Appendix “Allergenic pollen reported by country”, p. 75). Approximately two-thirds of

people with asthma are allergic to aeroallergens, and these allergens act as triggers for

asthma exacerbations (23). In Canada, approximately 7.7 million were affected by

aeroallergens in 2016 (98), and allergic rhinitis is highly prevalent, affecting

approximately 20–25% of the population (99). Asthma is estimated to affect about three

million Canadians, and between 12% (100) to 25% of Canadian children (101–103).

Asthma is a complex disease that can be understood as a syndrome, because different

pathways can result in diverse phenotypes (24). Several clinical phenotypes of asthma

display differences in severity, inflammatory pattern, and comorbidity with allergic

11

diseases (since not all asthma is atopic) (104). Reversible bronchoconstriction, either

spontaneously or after bronchodilator treatment, remains a common process in all the

phenotypes (97).

In many children with asthma, the appearance of different allergic conditions

follows a sequence that has been labelled the “atopic march” (105). This sequence

connects the different expressions of allergic diseases that vary with age, which often

have transient symptoms. Typically, a large exposure to a potential allergen is followed

by sensitization, according to the order in which infants are exposed to a predominant

allergen: first food allergens (e.g., egg), then indoor allergens (e.g., dust mites), and

finally outdoor allergens (e.g., local anemopilous pollen) (11). This sequence of

exposures and sensitizations generally precedes the sequence of atopic symptoms that

begins with food allergy and associated gastrointestinal disorders, continues with atopic

dermatitis, and progresses to respiratory allergies (106).

Because the first symptoms of the allergic conditions involved in the “atopic

march” often emerge during the first year of life, the first possible window for the

environmental exposures responsible for these cases of atopy and asthma is likely to be

open during gestation and the first months of life. This window is calculated considering

two factors: (1) that only exposures preceding the first symptoms of an illness “can

influence its inception” (9) (p. 2231); and (2) that antigens and air components can cross

the placental barrier (107).

In other cases, such as pollen-related later-onset symptoms, allergies and

asthma appear later in life when individuals are exposed to:

- new varieties of pollen through immigration to a new location (108,109), or

through the appearance of botanical species in new geographical zones other

than their native zones (110);

- higher than normal exposures to pollen, including in jobs that require long

periods of contact with plants (111). Occupational allergies and bronchial asthma

have been reported in agricultural populations (112–114), florists (115),

floriculturists (116), carpenters (117) who are in contact with plants such as

saffron (112), ragweed (118) or the Brassica oleracea species (i.e broccoli,

cauliflower), (114).

12

2.5.2. Thresholds of Effect

A critical question for both pollen and fungi allergy is: how much aeroallergen

exposure is needed for an allergic person to develop sensitization, or to exacerbate

existing disease? Most studies of exacerbation have found non-linear responses to

indoor and outdoor allergens, potentially signaling a minimum threshold level

(40,119,120). In addition to a threshold for clinical symptoms, threshold exposure levels

have also been described for the release of biological and inflammatory mediators (121).

The threshold values for fungi spores are generally higher than those for pollen grains,

ranging from ≥100 spores/m3 for Alternaria to ≥3000 spores/m3 for Cladosporium (122–

125); a relevant consideration here is that the proteins in the spores are the active

immunologic agent, not the spore itself, so fragmented molecules might not be counted

but still affect the immunological response in humans due to their proteins.

Although individuals vary widely in their reactivity to allergens, one proposed

threshold for outdoor ragweed levels in the United States was 10 to 20 grains/m3 for a

period of at least 15 minutes (40). During peak ragweed season, daily concentrations in

North America can reach 250 grains/m3, and they remain above 100 grains/m3 for most

of the season (126); likewise, with tree pollen in Ontario, where mean in-season daily

values of 300 grains/m3 were recorded, with daily peaks reaching even higher (127).

Peaks reported for grass are somewhat lower, between 70 and 110 grains/m3 to

precipitate symptoms (128).

2.5.3. The Priming Effect

The priming effect is another important phenomenon involved in our

understanding of the induction of allergic symptoms. The priming effect describes the

transition from a state of minimal symptoms out of season to noticeable/bothersome

symptoms after sufficient exposure to an allergen. It is formally defined as an increase in

reactivity of the nasal membrane following repeated exposure (129). Individuals who are

already experiencing symptoms due to a perennial allergen (dust, pets, etc.) (130) or to

high levels of air pollution (131) are more sensitive to subsequent exposure to

aeroallergens. Conversely, when individuals with multiple sensitizations are ‘primed’ by

an ongoing pollen season, they react more readily to other allergens found in the home

environment, such as dust (71,132). The priming effect is relevant to consider when

13

developing pollen warning or forecasting systems in conjunction with existing systems

for outdoor air pollutants. It demonstrates that, for those who suffer from seasonal

allergies, the option to initiate short-term treatment (such as antihistamines or sublingual

immunotherapy) within the first 3–5 days of the season could potentially, block the

development of severe symptoms. However, those who are already suffering from poorly

controlled allergic rhinitis or asthma are in danger of reacting severely and almost

immediately upon the arrival of pollen season due to priming (133).

2.5.4. Effect Modifiers

The most promising mechanism that explains the development of allergies

involves interactions between individual genetic susceptibility and environmental

exposures (94). For example, gene–environment interactions have been demonstrated

with changes in microRNA (134) and bronchial epithelial DNA methylation, after

exposures to diesel exhaust (135). For individuals with atopy-prone or immune

modulated genotypes, environmental exposures play a role in the onset of an allergic

disorder (136), including exposures to aeroallergens (137,138). However, the

environmental effect may be either detrimental or protective: Tovey et al. (120) found a

non-linear relationship between mite allergen exposure and sensitization and asthma,

with children on the lowest and highest quintile of exposure less likely to have both

sensitization and asthma compared with the middle range of exposures.

In the study of the development of health conditions in humans, an environmental

exposure can be considered as a protective factor if it is linked to decreased risk of the

development of a specific condition (136). Early exposure to animals and breastfeeding

are linked to decreased risk for the development of allergies to pollen and spores. To

consider an environmental component as a risk factor, it is necessary to demonstrate

that increased exposure to it is associated to an increase in the incidence of atopy (139).

Interactions between pollen and other environmental conditions such as weather,

seasons, urban environments and high concentrations of air pollution have been studied

and linked to increased risk for the development of an allergic condition. The interactions

between these environmental conditions and aeroallergens also happen at the

atmospheric level and could impact aeroallergen concentration. In this way, the

environmental conditions could be understood as effect modifiers: “a variable that

modifies the effect of the exposure of interest… through an interaction between the

14

effect modifier and the exposure.” (p.212) (140). These effect modifiers are described in

the following sections:

Effect Modifier: Weather

In northern climates such as Canada, pollen production, dispersal, and airborne

lifespan are highly dependent on the weather. In general, trees bloom in the early spring,

grasses bloom late spring to early summer, and weeds pollinate in the fall (40).

Ragweed is in late August until the first frost, and thus ragweed season can be cut short

by an early frost (52,141). The weather in the current year has less effect on the intensity

of the tree pollen season than the weather in the previous year, because trees produce

pollen in the summer and fall, and release them when a sufficient number of warm days

occur in the following spring (52,141).

Diurnal changes in pollen levels have also been observed. Because ragweed

pollen is released in the morning, peak concentrations are reached around noon in the

absence of high winds or rain (142). Depending on the temperature, humidity, and wind

conditions, the counts may drop at night or remain elevated (40,143). Mature pollen

grains tend to be released when the relative humidity drops, and they remain airborne

longer at low humidity, low wind speeds, and high atmospheric pressure (142).

Meteorological conditions also affect fungi sporulation, as many grow well when

conditions are wet and they produce spores as a survival mechanism when conditions

are dry (40,142).

Thunderstorms can be associated with asthma exacerbations, with steep

increases in the use of emergency services and increased mortality (144–146).

Thunderstorms during pollen season are known to carry whole and ruptured pollen

grains at the ground level where wind outflows distribute them with larger geographic

coverage than under normal conditions (90). Climate change has been linked to an

increase in frequency of thunderstorms in some areas (147).

Effect Modifier: Seasonality

The division of the year into four seasons (spring, summer, fall, and winter) takes

into consideration variables that undergo yearly cyclical changes, such as day length,

temperature, and humidity. The influence of these factors on aeroallergens can be direct

and indirect (61), and all have been associated with allergic respiratory morbidity (148–

15

150) and mortality (151,152). There is some indication of an association between

season of birth on the development of asthma and allergies (153). If an individual is

exposed to high aeroallergen counts in utero and/or during the sensitive immune system

development period of the first months of life, there may be at risk of atopic disease later

in life (154–156).

Effect Modifier: Urbanization

Living in urban areas, as opposed to rural and semi-rural areas, is a known risk

factor for the development of aeroallergen-induced respiratory allergy (61,157). There is

evidence that highly allergenic species of fungi are present at higher levels in the

outdoor air in cities compared with rural environments (158). Differences between

aeroallergen counts (higher in rural areas) and species diversity (lower in urban areas)

may drive some of the differences between rural and urban influence on the onset of

allergies and asthma (159). Additionally, the higher levels of air pollutants in urban areas

can interact with airborne pollen grains, which is likely to exacerbate allergic conditions

and respiratory distress (61). Two thirds of the global population will live in urban areas

by 2020, and an increased risk for aeroallergen-induced respiratory allergy is expected

(147).

Effect Modifier: Air Pollution

Population based studies support the hypothesis that air pollution contributes to

the etiology of respiratory allergies (160,161). Epidemiological and clinical research

have documented the chronic, adverse effects of air pollution on the pulmonary

development of children and also the relevance of the timing of exposure for the

development of asthma (162,163).

The interactions between air pollution and aeroallergens are complex and occur

both in the atmosphere and in the airways (161). Ziska et al. (164) have demonstrated

that outdoor air pollution can prompt an increase in pollen production by certain

herbaceous species, similar to the effects seen with increased CO2. A number of studies

have also shown that air pollution may increase the allergenicity of pollen and/or fungi,

because air pollutants can attach to their surfaces and can alter their allergenic potential

and morphology by making the surface coating more fragile (61,165,166). Co-

occurrence of exposure is important, and the simultaneous release of pollen grains

16

and/or fungal spores and increased air pollution episodes appears to be the most

harmful in terms of increased allergenicity (167–170).

In the airway, oxidative stress has been identified as a major biologic pathway for

the effects of most of the air pollutants (171,172). Air pollutants allow for easier

penetration of pollen and spore allergens because they trigger damage to the airway

mucociliary clearance mechanisms (61,161). Particulate matter smaller than 2.5 μm

(PM2.5) reaches deeply in the lungs and acts as an adjuvant that increases production of

IgE (134,173,174). Furthermore, exposure to diesel exhaust is known to impact DNA

methylation and impaired regulatory T-cell functions, two mechanisms relevant for the

immune response (135). Decrements in lung function (measured through changes in

FEV1) following allergen exposure and controlled diesel exhaust exposure have also

been modified by the presence of the GST genotype, in a gene–environment interaction

manner (174).

2.6. Effects of Climate Change on Aeroallergens

In addition to its negative effects on human health, air pollution also shapes the

anthropogenic climate change that has been documented for several decades (175).

Atmospheric concentrations of greenhouse gases (GHG) have contributed to increasing

global temperatures, and it has been acknowledged that further increases are inevitable

(REF). Drawing on over 29,000 longitudinal data sets, the findings from an international

group of experts show that human-led activities have contributed to a global increase in

temperature and other long-term shifts in weather conditions (176–178).

Climate-related changes in the local ecosystems will present specific threats for

their human populations (179). Among the areas of human life affected by climate

change, health is prominent. The incidence, range, and seasonality of many existing

disorders will certainly be altered due to fluctuations in the average climate conditions,

the climatic variability, and other noninfectious drivers of health (180,181). Levels of

some specific aeroallergens are on the rise in particular regions (182), and some of this

increase has been linked to anthropogenic climate change (183). The increasing

planetary temperatures affect plant biology through the timing and length of the growing

seasons (184), increased production and allergenicity of pollen, and shifts in range of

species (Figure 4) (183,185).

17

Figure 4. Effects of climate change on aeroallergens

Due to the warmer temperatures, pollen seasons will start earlier and end later

(25,157,186,187). Warming by latitude has been associated with longer ragweed pollen

seasons in North America, increasing by 27 days between 1995 and 2009 (171). Earlier

seasonal starts have also been found for Juniperus, Ulmus, and Morus (110). In

Western Europe, spring events have advanced by six days (187) and changes in birch

pollen season (188) and Artemisia have been described (189). Changes in season

length will lead to changes in human exposure (190) and also in sensitization and

symptoms of allergic conditions (137,185,191).

Increased pollen counts have been associated with the current levels of CO2,

when compared with CO2 levels of the previous century (192) or even between different

decades (2004 and 2013) (183,193). Increases in the atmospheric concentrations of

CO2 impact the reproductive processes in plants, leading them to produce more pollen

(8,194,195) with significantly stronger allergenicity (110,189,196). This increased

allergenicity is due to more diversity in the heterogeneity of the antigenic proteins in

pollen grains (32).

Climate change affects many meteorological variables that participate in the

dispersal and deposition of aeroallergens (i.e., humidity, precipitation, and temperature)

(147). Changes in dispersion, both region- and species-specific, can potentially expose

18

(and sensitize) populations to novel allergens (161). These changes will also impact

plant distribution, as species that could not survive in previously hostile environments

can potentially thrive in changing temperature and precipitation regimes (189).

Alternatively, native species or species with limited adaptive capacity might not survive

the hotter and drier conditions forecasted (177). The proliferation of anemophilous plants

where those species were not previously prevalent exposes atopy-prone individuals to

new pollens (197).

2.7. Knowledge Gaps and Challenges

With the documented changes over time in environmental factors, it is expected

that pollen concentrations in different locations within Canada will display differences in

temporal and geographical patterns. More research is needed in order to understand

these differences (171) and to contribute to better understanding of basic environment-

health associations (198). The Canadian Healthy Infant Longitudinal Development

(CHILD) birth cohort aims to increase our understanding of the environment-health

interactions that occur during the prenatal and early childhood windows of development

for allergic conditions (199). In this study, I describe the temporal and geographic

variations for the most common aeroallergens (1) during the years in which the CHILD

participants were born (i.e. 2008-2012) and (2) in the four cities where they live:

Vancouver, Edmonton, Winnipeg and Toronto. The exposure data will support

subsequent epidemiologic analyses of allergic disease outcomes.

19

Chapter 3. Methods

3.1. Study Setting

I used pollen and spore concentration data collected in the four CHILD cities,

from 2008 through 2012 (Figure 5). These cities are located in different ecological zones

in Canada: Vancouver is in the Pacific Maritime, Edmonton and Winnipeg are in the

Prairies, and Toronto is in the Mixedwood plains.

Figure 5. Location of the four Canadian Healthy Infant Longitudinal Development (CHILD) birth cohort cities and the aeroallergen stations.

Aeroallergen stations: One station in Edmonton and Toronto, and two stations in Vancouver (one active in 2008 and 2009 and a second active from 2010 through 2012) and Winnipeg (one active in 2011 and a second active from 2008 through 2010 and 2012).

20

3.2. Data Collection

I obtained and analyzed data collected between January 1, 2008 and December

31, 2012 during the period of pregnancies and deliveries in the CHILD birth cohort

(Figure 6).

Figure 6. Month of birth of the participants from the Canadian Healthy Infant Longitudinal Development (CHILD) birth cohort.

Pollen and fungi concentrations were measured by Aerobiology Research

Laboratories (ARL) at one station in Edmonton and Toronto and at two stations in

Vancouver (one for 2008 and 2009 and a second for 2010 through 2012) and Winnipeg

(one for 2011 and a second for 2008 through 2010 and 2012; Figure 5 and Table 1).

Aeroallergen samplers are located in neighborhoods that have been identified by ARL to

be representative of the biota in an approximate 50-mile (80 km) radius (Personal

communication, ARL May 2018). Samplers are located at approximately 6-7 feet above

the ground, a height chosen to be representative of human breathing zones (127). All

samplers are located away from structures and as far away as possible from the local

21

trees in order to allow atmospheric mixing to make the collections more representative of

the flora present in the location (137). Private residences are often used for the

collection stations where the samplers are installed so the exact coordinates are

confidential.

Rotation impaction samplers (Model GRIPST 2009) were used to collect pollen

grains and fungal spores. These samplers are considered suitable for the collection of

pollen and spores as small as 2-3m (200). Sampling was conducted on a 10% duty

cycle over each 24-hr period (Personal communication, ARL). Pollen grains and fungal

spores: (1) adhered to the silicon grease-coated sample rods of the samplers, (2) were

identified by trained palynologists with microscopic morphology, (3) grouped according

to taxa, and (4) counted to establish the number of particles per cubic meter of air

sampled.

Table 1. List of aeroallergen stations and years of data collection.

Station Province Years

E Vancouver BC 2008 - 2009

W Vancouver BC 2010-2012

Edmonton AB 2008-2012

N Winnipeg MB 2008-2010, 2012

S Winnipeg MB 2011

Toronto ON 2008-2012

Pollen season is defined as the days in which pollen is measurable in the air

(201). Daily aeroallergen concentrations for each taxon were collected by ARL after

measurable counts of pollen were recorded for five consecutive days and until

measurable pollen counts were not recorded for five consecutive days (131). The peak

value was defined as the maximum concentration in each year, and the date when that

concentration was reached was defined as peak date (202). Each specie of pollen grains

and fungal spores was grouped in a genus and a family (Table 2).

Table 2. Family, genus and species analyzed

Family Genus Species

Pollen

Deciduous trees Acer Boxelder, Maple

Aesculus Buckeye, Horse Chestnut

ALNUS (Alder)

22


BETULA (Birch)

Birch Look-a-likes Hornbeam, Hop-Hornbeam

Carya Hickory

CORYLUS (Hazelnut)

Fagus (Beech)

Fraxinus (Ash)

Juglans Walnut

Morus Mulberry

Oleaceae (Ligustrum, Syringa)

Platanus Sycamore

Populus Aspen, Poplar

Prunus, Malus, Crataegus Apple, Plum, Pear, Hawthorn

Quercus Oak

Salix Willow

Sambucus Elderberry

Tilia Basswood, Linden

Ulmus Elm

Castanea Chestnut

Coniferous trees Cupressaceae Cedar, Cypress, Juniper, Thuja

Larix Larch, Tamarak, Pseudotsuga

Pinaceae Pine, Fir, Spruce

Tsuga Canadensis / Tsuga Heterophylla

Hemlock

Weeds Ambrosia Ragweed

Artemisia Sagebrush, Wormwood

Chenopodiaceae, Amaranthaceae (Amaranthaceae Family)

Cruciferae family (Mustards)

Plantago Plantain

Rumex Dock, Rhubarb, Sorrel

SALSOLA PESTIFER (Russian Thistle)

Solidago (Goldenrod)

Typha (Cattail)

Urticaceae Family Nettles & Pellitory

Grasses Cyperaceae (Sedge family) Gramineae (True grasses)

Spores

Ascomycetes

Ascobolus

Caloplaca, Xanthoria

Chaetomium

Diatrypaceae

Didymella

Leptosphaeria and Look-a-likes

Massaria

23


Massarina

Misc. Ascospores

Oospora Powdery mildew

Peronospora Downey mildew

Pleospora

Sordaria

Venturia

Basidiomycetes

Boletus, Leccinum, Melanogaster

Calvatia

Coprinus, Coprinellus

Ganoderma

Misc. Basidiospores

Panaeolus, Psathyrella, Parasola

Uredinales Rusts

Ustilaginales Smuts

Fungi Imperfecti Alternaria

Arthrinium

Aspergillus, Penicillium

Botrytis

Cercospora

Cladosporium

Curvularia

Drechslera, Bipolaris, Exosporium, Sporidesmium, Exserohilum

Epicoccum

Fusarium

Fusicladium

Helicomyces

Misc. Fungi Imperfecti

Nigrospora

Periconia

Pithomyces

Polythrincium

Stemphylium

Tetraploa

Torula

Ulocladium

24

3.3. Data Analysis

Because of the diversity in specific allergenic plants that grow in each floristic

zone in Canada, I analyzed pollen and spores by taxa in order to have adequate

concentrations and variation. For example, a preliminary analysis of a single genus

(Ragweed, Ambrosia) showed high levels in some cities (Toronto and Winnipeg) and

extremely low levels in others (Vancouver and Edmonton), prohibiting the comparative

analysis of this genus in all four cities. Spores considered highly allergenic such as

Alternaria, Aspergillus and Cladosporium were grouped by ARL in the taxa of Fungi

Imperfecti. The analysis was done with the following categories: Deciduous trees pollen,

Coniferous trees pollen, Weeds pollen, Grasses pollen; and Ascomycetes,

Basydiomicetes and Fungi Imperfecti spores (Table 2).

The data manipulation and descriptive statistical analyses were performed in R

(203) and RStudio (Version 1.0.143) using the plyr (204), broom (205), dplyr (206),

ggplot2 (207), zoo (208), and lubridate (209) packages.

When data were missing for periods of less than four days, I used the R package

zoo (208) to interpolate the missing data with the approx function. This function uses

linear interpolation with the contiguous existing values to fill in the missing data. In

Vancouver, Edmonton, Winnipeg and Toronto I interpolated 11, 10, 56, and 10 days of

non-consecutive data, respectively. Winnipeg has two long periods of 16 days and nine

consecutive days during which samples were not readable or the sampler

malfunctioned. Data were not interpolated for those two time periods.

I used satellite images from Landsat 5 and Landsat 7 to visualize seasonal

variations in vegetation in the 20 km surrounding the pollen measurement stations in

each city. Landsat images are space-based moderate-resolution land remote sensing

data, collected by the U.S. Geological Survey (USGS) and the National Aeronautics and

Space Administration (NASA) (210). Landsat images are considered useful for capturing

seasonal and annual changes in vegetation type that alter pollen production (211). A

figure displaying Landsat imagery for 20km around the monitoring locations throughout

the year was included in order to show the differences in greenness between the cities

going through the seasons (Figure 7).

25

Descriptive statistics were calculated for both within-station (seasonal) and

between-station (geographical) differences, data were expressed as: average

cumulative concentrations (and minimum and maximum values for the five-year period,

tables 4 and 7); average number of days in the season (also with minimum and

maximum values for the five-year period, tables 5 and 8); and peak values and dates

(Tables 3 and 6). Cumulative concentrations were chosen in order to reflect both the

level of grains and spores and the seasons length. Within-station differences were

described with one graph per city that displayed the weekly aggregates of the daily

concentrations, as well as the mean and standard deviation, for each taxon for pollen

(figures 8-11) and spores (figures 14-17) per year.

Between-station differences were described with a plot that grouped the four

cities and displayed the average of the five-years weekly aggregates for: 1) the

coniferous and deciduous pollen (figure 12), 2) the grass and weeds pollen (figure 13)

and 3) the spore taxa (figure 18). Further details were provided for:

1) Cumulative concentrations: Average and range for the five years in each city

is listed separately for pollen (table 4) and spore taxa (table 7).

2) Season length: Average and range for the five years in each city is listed

separately for pollen (table 5) and spores taxa (table 8).

With the data provided by ARL, which had one start and end date for all the taxa,

I used two definitions of the aeroallergen seasons for each taxa, which yielded different

season lengths (Tables 5 and 8):

a) the period between the days when the 5% and the 95% of the total pollen

was collected, and

b) the period between the days when the 1% and the 99% of the total pollen

was collected.

26

Chapter 4. Results

Consistent with the more moderate climates, Vancouver had a longer season for

every group of pollen but grass, where Toronto had the longest season. Toronto also

had the second longest season for weeds, deciduous and coniferous pollen (Table 5).

Vancouver had the highest average values for the cumulative concentrations for

coniferous and deciduous trees, with over ten times more than Edmonton for coniferous

pollen (Table 4).

The distinctive patterns of the seasons lengths for the aeroallergens studied for

each city are consistent with the differences in greenness and snow coverage observed

in the Landsat images of the four participant cities (Figure 7), and to the ecological

zones where each city is located (Figure 5).

27

Figure 7. Ground coverage at 20km resolution from Landsat satellite data. Jagged edges mark the edge of the image from the satellite. Approximate location of the aeroallergen samplers is depicted with red dots: One station in Edmonton and Toronto, and two stations in Vancouver (one active during 2008 and 2009 and one active for 2010 through 2012) and Winnipeg (one active during 2011 and a second active from 2008 through 2010 and 2012).

28

4.1. Within-Station Differences for Pollen

The pollen levels for coniferous and deciduous trees, grasses, and weeds

showed yearly variations in the four cities and peak concentrations were highly varied

across the time periods studied (Figures 8-11, Table 3).

Table 3. Peak values and peak dates for pollen

Vancouver

Coniferous Deciduous Grass Weeds

Date: 2008 February 25 March 6 June 12 August 3

grains / m3 1104 591 54 40

Date: 2009 April 21 March 20 June 13 June 04

grains / m3 3427 1721 70 28

Date: 2010 February 23 March 1st July 7 May 24

grains / m3 1305 4509 81 23

Date: 2011 March 10 March 24 June 21 June 8

grains / m3 1006 5155 96 48

Date: 2012 March 3 March 23 June 20 July 1

grains / m3 1254 3060 96 19

Edmonton


Date: 2008 May 31 May 15 July 12 July 11

grains / m3 149 533 312 129

Date: 2009 June 17 May 5 July 21 August 29

grains / m3 435 1096 74 108

Date: 2010 June 28 April 21 July 18 July 31

grains / m3 96 616 64 100

Date: 2011 June 28 May 09 July 15 July 20

grains / m3 257 319 286 240

Date: 2012 July 8 May 4 June 21 July 14

grains / m3 131 503 235 58

Winnipeg


Date: 2008 June 10 May 23 June 9 August 30

grains / m3 597 1117 249 250

Date: 2009 June 15 May 6 June 24 September 2

grains / m3 910 748 108 155

Date: 2010 May 22 April 19 July 3 August 22

grains / m3 997 2724 54 218

Date: 2011 April 24 May 20 June 18 August 12

grains / m3 794 2355 140 126

Date: 2012 March 18 March 31 June 3 August 23

grains / m3 274 858 30 99

29

Toronto


Date: 2008 April 20 April 20 June 7 August 31

grains / m3 388 1426 110 244

Date: 2009 June 24 April 25 June 22 August 21

grains / m3 395 902 44 126

Date: 2010 March 25 April 3 May 30 September 1

grains / m3 320 1296 86 300

Date: 2011 April 12 May 12 June 8 September 2

grains / m3 1470 1624 70 133

Date: 2012 March 22 March 22 May 25 August 31

grains / m3 129 720 55 209

In Vancouver, coniferous trees and deciduous trees showed similar values for

the five-year mean of the cumulative concentrations (21026 and 21830 grains / m3,

respectively, Table 4) and these were the highest concentrations for the pollen taxa in

this city; however, the season length for coniferous trees was longer (98 days for the 5-

95% values and 151 days for the 1-99% values, Table 5) than for deciduous trees (58

days for the 5-95% values and 96 days for the 1-99% values, table 5. Both coniferous

and deciduous trees concentrations reached peak values before May (Figure 8),

although only the concentrations for coniferous trees display two peaks each year (with

the second before July).

For grass pollen, the five-year mean of the cumulative concentrations was 1497

grains / m3 (Table 4). Season length for grass pollen lasted on average 75 days (for the

5-95% values) and 124 days (for the 1-99% values, Table 5). Grass pollen

concentrations reached peak values later in the year (between June and July) compared

with the trees pollen (Figure 8, Table 3).

Weeds pollen had a five-year mean of the cumulative concentrations of 821

grains / m3 (Table 4), the lowest values of all the pollen taxa for Vancouver. Season

length for weeds pollen lasted on average 103 days (for the 5-95% definition) and 130

days (for the 1-99% definition, Table 5). The months for peak values for weeds pollen

concentration are between May and August (Figure 8, Table 3).

30

Figure 8. Weekly pollen concentrations 2008-2012 in Vancouver with Mean and Standard Deviation (SD).

In Edmonton, the five-year mean of the cumulative concentrations of coniferous

trees pollen was 2024 grains / m3 (Table 4), deciduous trees pollen had the highest

cumulative concentrations of all pollen taxa in this city (5330 grains / m3, Table 3).

Season length for coniferous trees was longer (57 days for the 5-95% definition and 95

days for the 1-99% definition, Table 5) than for deciduous trees (39 days for the 5-95%

definition and 64 days for the 1-99% definition, Table 5). In each year of the period

analyzed (2008-2012), coniferous trees pollen concentrations reached peak values

between June and July (with some peaks happening as early as late May); deciduous

trees pollen concentrations reached peak values earlier in the year, between late April

and May (Figure 9, Table 3).

For grass pollen, the five-year mean of the cumulative concentrations in

Edmonton was 1523 grains / m3 (Table 4). Season length for grass pollen lasted on

average 54 days (for the 5-95% values) and 101 days (for the 1-99% values, this is the

longest season for this city, Table 5). Grass pollen concentrations reached peak values

31

later in the year (in July, almost every year) compared with the deciduous trees peaks

(Figure 9, Table 3).


grains / m3 (Table 4), the lowest values of all the pollen taxa for Edmonton. Season

length for weeds pollen lasted on average 65 days (for the 5-95% values this is the

longest season for this city) and 95 days (for the 1-99% values, Table 5). Peak values

for weeds pollen concentration were reached in July most years and August (in 2009,

Figure 9, Table 3).

Figure 9. Weekly pollen concentrations 2008-2012 in Edmonton with Mean and Standard Deviation (SD).

In Winnipeg, coniferous trees showed lower values for the five-year mean of the

cumulative concentrations than deciduous trees (3228 and 13628 grains / m3,

respectively, table 4), deciduous trees had the highest cumulative concentrations of all

the pollen taxa in this city. The season length for coniferous trees was longer (66 days

for the 5-95% definition and 90 days for the 1-99% definition, Table 5) than for

32

deciduous trees (45 days for the 5-95% definition and 55 days for the 1-99% definition,

table 5), which was the shortest pollen season for all the pollen taxa in this city.

Coniferous trees concentrations reached peak values between March and early June

(Figure 10, Table 3), with three years (2008, 2011 and 2012) displaying two peaks each

year. Deciduous trees concentrations reached peak values between late March and May



grains / m3 (Table 4), the lowest values of all the pollen taxa for Winnipeg. Season length

for grass pollen lasted on average 71 days (for the 5-95% values) and 115 days (for the

1-99% values, Table 5). Grass pollen concentrations reached peak values later in the

year (between June and July) compared with the trees pollen (Figure 10, Table 3).


grains / m3 (Table 4). Season length for weeds pollen lasted on average 72 days (for the

5-95% values) and 100 (for the 1-99% values, Table 5). Peak values for weeds pollen

concentration were reached in August and early September (Figure 10, Table 3).

33

Figure 10. Weekly pollen concentrations 2008-2012 in Winnipeg with Mean and Standard Deviation (SD).

In Toronto, coniferous trees showed much lower values for the five-year mean of

the cumulative concentrations compared with the deciduous trees (3600 and 13056

grains / m3, respectively, Table 4); however, the average season length for coniferous

trees was longer (82 days for the 5-95% definition and 130 days for the 1-99% definition,

Table 5) than for deciduous trees (56 days for the 5-95% definition and 74 days for the

1-99% definition, Table 5). Coniferous trees concentrations reached peak values

between late March and June (Figure 11, Table 3) and displayed two peaks each year.

Deciduous trees concentrations displayed peak values between late March and May and

did not have two peaks (Figure 11, Table 3).


grains / m3 (Table 4), the lowest values of all the pollen taxa for Toronto. Season length

for grass pollen lasted on average 107 days (for the 5-95% values) and 141 days (for the

1-99% values, Table 5), the longest season length for all the pollen taxa in Toronto.

Grass pollen concentrations reached peak values later in the year (between June and

34

July, sometimes as early as late May) compared with the deciduous trees pollen (Figure

11, Table 3).


grains / m3 (Table 4). Season length for weeds pollen lasted on average 90 days (for the

5-95% values) and 126 (for the 1-99% values, Table 5). Weeds pollen concentration

displayed two peak values, a small one between June and July (with values under 50

grains per m3), and a higher one (with values between 50 and 150 grains / m3) in August


Figure 11. Weekly pollen concentrations 2008-2012 in Toronto with Mean and Standard Deviation (SD).

35

4.2. Between-Station Differences for Pollen

Weekly aggregates for 2008-2012 showed that Vancouver had the highest peaks

for coniferous trees and for deciduous trees, with peak values in Vancouver (3427 grains

/ m3) being 2-4 times higher than those in the other cities (435, 997, 1470 for Edmonton,

Winnipeg and Toronto, respectively, Figure 12, Table 3). Coniferous trees showed

consistent earlier starts in Vancouver (between February 14 and March 7 for the 5-95%

definition and February 10 and March 2 for the 1-99% definition) than in Edmonton (April

18 and May 27 for the 5-95% definition, and April 2 and April 27 for the 1-99%

definition), Winnipeg (March 18, April 24 for the 5-95% definition, and March 16, April 19

for the 1-99% definition), and Toronto (March 15, April 10, for the 5-95% definition, and

March 5 and April 1 for the 1-99% definition, Figure 12, Table 5). Coniferous trees, in

particular, showed more than one peak in each year in all the cities; the separate peaks

could indicate different species reaching their peak concentration at different times.

Deciduous trees showed consistent earlier starts and peaks in Vancouver

(between February 6 and March 13 for the 5-95% definition and January 30 and March 3

for the 1-99% definition) than in Edmonton (April 9 and April 26 for the 5-95% definition,

and March 28 and April 22 for the 1-99% definition), Winnipeg (March 22, April 27 for the

5-95% definition, and March 18, April 24 for the 1-99% definition) and Toronto (March

17, April 16, for the 5-95% definition, and March 13 and April 7 for the 1-99% definition,

Figure 12, Table 5).

36

Figure 12. Weekly aggregates of coniferous and deciduous tree pollen concentrations, average of 2008-2012 in the CHILD cities.

Grass pollen peaked consistently between June and August in most of the years

assessed (with the exceptions of 2008 and 2010-2012 in Toronto and 2012 year in

Vancouver, Table 3). For grasses, longer seasons were often accompanied by higher

peaks. Edmonton had the highest peak concentrations for grass pollen (312 grains / m3)

compared to the other three cities (96 grains / m3, 249 grains / m3, 110 grains / m3, for

Vancouver, Winnipeg and Toronto, respectively, Table 3) and all four cities were above

100 grains / m3, a threshold for clinical response in adults (Lebel et al., 1988). Winnipeg

showed the highest values for weed pollen (250 grains / m3) and the second highest for

grass pollen. Toronto had the second highest values for weed pollen (Figure 13, Table

3).

Weed pollen had an earlier season start in Vancouver during the five years

studied (between May 19 and June 5 for the 5-95% definition and May 9 and May 23 for

the 1-99% definition) than in Edmonton (July 1 and July 12 for the 5-95% definition, and

June 15 and July 6 for the 1-99% definition), Winnipeg (June 26, July 9 for the 5-95%

37

definition, and June 14, June 28 for the 1-99% definition) and Toronto (June 15, June

26, for the 5-95% definition, and May 26 and June 14 for the 1-99% definition, Figure

12). Edmonton and Winnipeg had their weed pollen season during the third quarter of

the year (Figure 13). Toronto displayed two peaks, with different concentrations, both

within the second and third quarter of the year, potentially indicating two separate genus

peaking at different times (Figure 13).

Figure 13. Weekly aggregates of grass and weed pollen concentrations, average of 2008-2012 in the CHILD cities.

38

Table 4. 5-year mean and range of pollen cumulative concentrations (grains /

m3 in hundreds).

Vancouver Edmonton Winnipeg Toronto

Pollen

Cumulative count

Coniferous Mean [Min, Max]

210 [126, 364] 20 [10, 39] 32 [20, 56] 36 [19, 52]

Deciduous Mean [Min, Max]

218 [110, 308] 53 [29, 108] 136 [95, 180] 131 [90, 172]

Grasses Mean [Min, Max]

15 [11, 20] 15 [8, 25] 16 [8, 24] 10 [9 – 11]

Weeds Mean [Min, Max]

8 [7, 9] 14 [10, 17] 29 [23, 37] 31 [28, 34]

Table 5. 5-year mean and range of pollen season length between cities (number of days).


Pollen

Season length: Number of days

5-95% of cumulative pollen concentrations


98 [97, 99] 57 [37, 88] 66 [50, 83] 82 [69, 90]


58 [41, 82] 39 [32, 45] 45 [34, 56] 56 [42, 69]

Grass Mean [Min, Max]

75 [70, 81] 54 [36, 81] 71 [46, 89] 107 [90, 122]


103 [92, 111] 65 [54, 85] 72 [63, 87] 90 [80, 100]

Season length: Number of days

1-99% of cumulative pollen concentrations


151 [133, 159]

95 [83, 114] 90 [ 87, 105] 130 [86, 220]


96 [75, 115] 64 [50, 77] 55 [44, 69] 74 [61, 87]

Grass Mean [Min, Max]

124 [114, 132] 101 [93, 133] 115 [97, 129] 141 [127, 161]


130 [120, 141] 95 [80, 114] 100 [85, 100] 126 [109, 139]

4.3. Within-Station Differences for Fungal Spores

The concentrations of Ascomycetes, Basidiomycetes and Fungi Imperfecti all

showed yearly variations in the four cities (Figure 14-17, Table 6).

39

Table 6. Peak values and peak days for spores

Vancouver

Ascomycetes Basydomicetes Fungi Imperfecti

Date: 2008 July 29 May 23 August 26

grains / m3 2513 6853 3500

Date: 2009 February 22 May 29 August 12

grains / m3 4312 2897 6813

Date: 2010 September 27 October 5 August 11

grains / m3 3620 5617 4253

Date: 2011 July 17 August 25 September 24

grains / m3 5882 3397 3874

Date: 2012 July 24 July 23 April 7

grains / m3 14092 3321 8336

Edmonton


Date: 2008 June 22 July 26 May 23

grains / m3 3994 2267 13148

Date: 2009 July 09 August 17 August 7

grains / m3 3260 872 17296

Date: 2010 August 10 July 19 September 10

grains / m3 7865 7692 17536

Date: 2011 June 16 October 6 October 7

grains / m3 9598 23581 14903

Date: 2012 August 14 August 23 July 17

grains / m3 10855 9526 19372

Winnipeg


Date: 2008 July 28 July 16 August 13

grains / m3 3505 3162 15186

Date: 2009 September 8 September 8 September 8

grains / m3 9161 4649 16138

Date: 2010 June 22 August 13 August 22

grains / m3 7230 8358 9263

Date: 2011 May 20 June 27 September 4

grains / m3 10040 23741 13984

Date: 2012 August 3 September 29 August 29

grains / m3 10494 2451 15370

Toronto


Date: 2008 July 27 September 20 October 9

grains / m3 1860 2628 4826

Date: 2009 July 25 September 6 September 27

grains / m3 2629 1705 4915

Date: 2010 July 24 October 6 September 24

grains / m3 2501 3183 6436

Date: 2011 June 4 October 8 August 8

grains / m3 3574 3311 7581

Date: 2012 June 23 September 1 July 27

40

grains / m3 1782 2031 5622

In Vancouver, the five-year mean of the cumulative concentrations for

Ascomycetes spores was 142003 spores / m3 (Table 7), the lowest value for the spore

taxa in this city. Season length for Ascomycetes lasted on average 225 days (for the 5-

95% values this was the longest season) and 240 days (for the 1-99% values, Table 8).

The peaks for Ascomycetes spores showed yearly variations (Figure 14, Table 6).

For Basidiomycetes, the five-year mean of the cumulative concentrations was

142914 spores / m3 (Table 7). Season length for Basidiomycetes lasted on average 172

days (for the 5-95% values) and 237 days (for the 1-99% values, Table 8). The peaks for

Basidiomycetes spores showed yearly variations but in three years (2010 through 2012)

were reached between July and early October, 2008 and 2009 had an additional peak in

May (Figure 14, Table 6).

Fungi Imperfecti, had the highest five-year mean of the cumulative

concentrations for this city (149011 spores / m3, Table 7). Season length for Fungi

Imperfecti lasted on average 201 days (for the 5-95% values) and 245 days (for the 1-

99% values this was the longest season, Table 8). The highest values for Fungi

Imperfecti spores were reached between August and September, with an early peak in

April in 2012 (Figure 14, Table 6).

41

Figure 14. Weekly spore concentrations 2008-2012 in Vancouver with Mean and Standard Deviation (SD).

In Edmonton, the five-year mean of the cumulative concentrations for

Ascomycetes spores was 161901 spores / m3 (Table 7). Season length for Ascomycetes

lasted on average 114 days (for the 5-95% values) and 167 days (for the 1-99% values,

Table 8). The peaks for Ascomycetes spores showed yearly variations, but in the

majority of the years happened between July and August (Figure 15, Table 6).


117030 spores / m3 (Table 7), the lowest value for the spore taxa in this city. Season

length for Basidiomycetes lasted on average 95 days (for the 5-95% values) and 134 (for

the 1-99% values, Table 8). The peaks for Basidiomycetes spores were reached

between July and August, with one peak as late as October in 2011 (Figure 15, Table 6).




42

99% values, Table 8), and was the longest season for all the spore taxa in this city. The

highest values for Fungi Imperfecti spores were reached around July and October


Figure 15. Weekly spore concentrations 2008-2012 in Edmonton with Mean and Standard Deviation (SD).

In Winnipeg, the five-year mean of the cumulative concentrations for

Ascomycetes spores was 155824 spores / m3 (Table 7). Season length for Ascomycetes

lasted on average 129 days (for the 5-95% values) and 176 days (for the 1-99% values,

Table 8). The peaks for Ascomycetes spores showed yearly variations (Table 6), but in

the majority of the years happened between June and October, although an early peak

in 2011 raises the potential issue of year-long concentrations that were present in the air

but might have not been recorded (Figure 16).


122945 spores / m3 (Table 7), the lowest value for the spore taxa in this city. Season

length for Basidiomycetes lasted on average 115 days (for the 5-95% values) and 142

43

days (for the 1-99% values, Table 8). The peaks for Basidiomycetes spores were

reached between June and September (Figure 16, Table 6).





highest values for Fungi Imperfecti spores were reached around August and September,

with some high values in May during 2010, 2011 and 2012 (Figure 16, Table 6).

Figure 16. Weekly spore concentrations 2008-2012 in Winnipeg with Mean and Standard Deviation (SD).

In Toronto, the five-year mean of the cumulative concentrations for Ascomycetes

spores was 96425 spores / m3 (Table 7), the lowest value for the spore taxa in this city.

Season length for Ascomycetes lasted on average 159 days (for the 5-95% values) and

212 days (for the 1-99% values, Table 8). The peaks for Ascomycetes spores happened

between June and July; however, one early peak in 2012 raises the potential issue of

44

year-long concentrations present in the air that might have not been recorded (Figure

17, Table 6).


101270 spores / m3 (Table 7). Season length for Basidiomycetes lasted on average 129

days (for the 5-95% values) and 170 days (for the 1-99% values, Table 8). The peaks for

Basidiomycetes spores were reached between September and October (Figure 17,

Table 6).





highest values for Fungi Imperfecti spores were reached between July and October, with

these peaks being the highest of all the spore taxa for this city (Figure 17, Table 6).

Figure 17. Weekly spore concentrations 2008-2012 in Toronto with Mean and Standard Deviation (SD).

45

4.4. Between-Station Differences for Fungal Spores

In Vancouver, Ascomycetes had a baseline of values continually higher than 0

and higher peaks between April and October throughout the years. For Ascomycetes,

peaks in Edmonton, Winnipeg, and Toronto reached values higher than 1000 spores /

m3 every year (Table 6). Basidiomycetes reached the highest peaks between July and

October almost every year in the four cities, with the exception of 2008 and 2009 in

Vancouver. Fungi Imperfecti displayed unique peak values for each city, with consistent

patterns throughout the five years studied (Figures 14-17, Table 6).

For the years of 2008-2012, in Vancouver, the basidiomycetes spores had the

highest peak. Fungi imperfecti were the least prevalent in Vancouver. Edmonton,

showed the highest peaks for Ascomycetes spores (10855 spores / m3), with Winnipeg

showing similar but slightly lower values (10494 spores / m3). Edmonton had the highest

peaks of Fungi Imperfecti: 19372 spores / m3, compared with 8336 spores / m3 for

Vancouver, 17977 spores / m3 for Winnipeg and 7582 spores / m3 for Toronto (Table 6).

Toronto showed lower concentrations of ascomycetes and basidiomycetes compared

with the other three cities. In Toronto, Fungi Imperfecti and Basidiomycetes spores had

higher peaks than ascomycetes (Figure 18). Fungal spore concentrations were much

higher in Edmonton, Winnipeg, and Toronto, and showed earlier peaks than Vancouver

(Figures 14-17), where concentrations increased through the year, and reached a peak

around September and October in every year but 2012. The peaks for spore

concentration for Ascomycetes were within the range of 7500 – 10000 spores / m3,

compared with 2500-5000 spores / m3 for Vancouver. Similarly, peaks were in the range

of 10000 – 20000 spores / m3 for Fungi Imperfecti in Edmonton and Winnipeg, compared

with 2500-5000 spores / m3 in Vancouver (Table 6).

46

Figure 18. Weekly aggregates of Ascomycetes, Basydomicetes and Fungi Imperfecti spores concentrations, average of 2008-2012 in the CHILD cities.

Ascomycetes and Fungi Imperfecti spores had the highest concentrations in

Edmonton and Winnipeg. Basidiomycetes spores had the highest values in Vancouver,

with lower, but similar levels in Edmonton, Winnipeg and Toronto. The longest season

for the three groups of spores was recorded in Vancouver, and Toronto had the second

longest (Table 8).

Table 7. 5-year mean and range of spore cumulative concentrations (spores / m3 in hundreds).


Spores

Cumulative count

Ascomycetes Mean [Min, Max]

1420 [726, 2132]

1619 [543, 2362]

1558 [1274, 2171]

964 [712, 1246]

Basidiomycetes Mean [Min, Max]

1429 [887, 1754]

1170 [389, 1650]

1229 [852, 1500]

1012 [917, 1179]

Fungi Imperfecti Mean [Min, Max]

1490 [1235, 2050]

2815 [2349, 2824]

3460 [2862, 4534]

1683 [1228, 2080]

47

Table 8. 5-year mean and range of spore season length between cities (number of days).


Spores

Season length: 5-95% of cumulative spore concentrations


225 [218, 239] 114 [110, 120] 129 [109, 172] 159 [147, 174]


172 [141, 218] 95 [86, 112] 115 [94, 134] 128 [118,138]


201 [137, 225] 139 [118, 153] 131 [100, 154] 150 [133, 166]

Season length: 1-99% of cumulative spore concentrations


240 [242, 259] 167 [160, 176] 176 [156, 199] 212 [196, 221]


237 [208, 253] 134 [122, 151] 142 [125, 153] 170 [155, 182]


245 [239, 257] 187 [176, 192] 182 [163, 201] 212 [182, 237]

48

Chapter 5. Discussion

Our findings point to unique aeroallergen season lengths in each city, with

similarities in the cities located within the same ecological zone (i.e. Edmonton and

Winnipeg). There are some distinctive features that are worth highlighting such as the

fact that Vancouver had the longest season for tree and weed pollen, as well as for all

the spore taxa. Toronto had the longest season for grass pollen and the second longest

season for trees and weed pollen, as well as for the fungi spores. The cumulative

concentration of aeroallergens also displayed unique distributions, with Vancouver

recording the highest concentrations for Ascomycetes, Basidiomycetes, Fungi

Imperfecti, coniferous and deciduous trees and Toronto for weed pollen. Local abiotic

factors (i.e. temperature, topography or precipitation) that affect the temporal and spatial

variation in each region are likely responsible for the particular season lengths and

aeroallergen levels (biotic elements) in the three different ecological zones where the

four CHILD cities are located (52).

Concentration and season length are important determinants of human exposure

to aeroallergens (161), along with the species present in the environment. The

differences recorded in our study, in exposure and season length, and across

geographical regions may be significant if, along with other factors, they lead to different,

clinically important, windows of exposure for infant immune response for the CHILD

participants. Although the thresholds of aeroallergen exposure for asthma exacerbations

and for asthma development are likely to be different, it is important to consider what

levels of pollen and fungal spore exposure contribute to aeroallergen sensitization that

increases the risk of asthma and allergy in childhood (161,212). The peaks shown in our

graphs point to specific points in time when thresholds may have been crossed and

participants of the CHILD study were exposed to high concentrations during suspected

windows of immune system development. The season’s length and cumulative

concentration for each one of the aeroallergens studied have created unique patterns of

exposure for the participants from the each one of the cities in the CHILD study.

Because sensitization to aeroallergens is related to long-term exposure (213), and the

participants have been exposed to different amounts of each aeroallergen during

different periods in a sensitive developmental stage of their lives (i.e. in utero), this

environmental exposure might affect a) the incidence of atopic conditions in each city

49

and b) the specific aeroallergens that the participants are sensitized to. The exposure to

aeroallergens will interact with the genetic backgrounds of exposed individuals (94) and

with other relevant exposures such as pets (214) or air pollution (173), which is likely to

modify the risk for the development of allergic diseases.

5.1. Limitations

There are several limitations of this study. Earlier starts and longer pollen

seasons are attributed to overall higher temperatures observed with climate change

(171,175), and increased pollen counts (184). One limitation for our study is that there

were too few years in our analyses to enable exploration of the potential effects of

climate change in these Canadian cities. In some Canadian cities, data have been

collected by ARL for over 20 years. The analysis of long-term data trends using these

datasets will increase our understanding of the effects of climate change on

aeroallergens, and on the impact of these changes on the development of atopic

conditions and its exacerbations.

A second limitation was the fact that, during each year studied, the available data

came from only one station per city. The paucity of spatial information meant I could not

assess within-city exposure variation or explore the correlation of data collected at

different sites during the same period of time. Unfortunately, most cities in Canada

currently have only one active station. Increasing the number of monitoring sites that

collect data continuously has been highlighted as important for both practical and

mechanistic research in this area (161). Efforts to apply land use regression models for

aeroallergen exposure are promising (53,215) and would also require simultaneous

collection of data from multiple stations in each city, for validation. Previous studies (200)

compared daily concentrations in two sites (Toronto and Brampton) separated at a

similar distance as the stations for Winnipeg and Vancouver (approximately 15km in

each city), over a period of ten years, also by ARL. Brubacher et al (200) calculated the

Pearson’s correlation between the two datasets; their findings show correlations higher

than .70 for pollens and .60 for spores, which points to moderately correlated timing of

pollination periods between the two sites. In Vancouver and Winnipeg, two different

collection stations were used during the time period studies; based on Brubacher et al

(200) results, similar moderate correlations between the data collected in the different

stations within each city, could be expected in this study.

50

The definition of the pollen season is another limitation for our study. The criteria

to start the sampling period inevitably leads to some seasons where the collection

clearly begins after the season has started giving an arbitrary nature to the date (131)

(p.229). Data for all the aeroallergens were collected during the same period of time in

each city, no individual definition of the start and end of the season was considered;

therefore, in some cases our graphs show rising concentrations at the very beginning of

the season which creates some error due to underestimation into season length

calculations.

5.2. Strengths

To our knowledge, this is the first study that provides a description of the

aeroallergen concentrations and seasons lengths in four Canadian cities with the

differences in greenness observed through the Landsat images to this description; this is

a significant contribution to the understanding of the aeroallergens temporal and

geographical patterns. Differences in concentrations of pollen were representative of the

differences in the greenness and in the three ecological zones of the four cities, as it has

been reported to happen with pollen concentrations and phytogeographical and climatic

maps of a country (216). Even when the selection of sites does not represent all the

ecological zones within this country, our findings regarding season length and

concentration of aeroallergens can be useful to allergists and atopic individuals

(202).Ariano et al (193) and Fuertes et al. (217) reported the use of different

geographical locations for studies of pollen concentrations in Italy and Germany

respectively, and Emberlin et al (188) found significant regional contrasts with their six

bio geographical situations chosen in Europe. In Canada, Coates & Jurgens (218) used

pollen concentrations exclusively and found differences in key events of the pollen

season, such as the start and end dates (by up to a month in 30 sites), and also

significant variance on the pollen season from year to year, making the case for

continued data collection to monitor and analyze said variance.

One strength of this study is that, in line with the current standards

(193,219,220), the pollen concentrations collected were the daily average concentrations

from 0 to 24 hours. With the daily data points, I calculated the weekly aggregates and

seasons lengths for each taxon. This level of detail enables observation of the

thresholds and windows of exposure to specific concentrations of known clinical

51

relevance. Our description of aeroallergen seasons follows McInnes et al (221)

recommendation to consider the timing of pollen release when analyzing the impact of

pollen grains on human health. The detailed descriptions presented in this paper will

constitute the basis to calculate exposure of CHILD participants and further improve our

models to assess the relevance of early exposure to aeroallergens as risk factors for the

development of sensitization and atopic conditions. Studies of pollen diversity provide

useful information regarding atopic conditions (222) and in Canada, some have linked

changes in pollen and fungal concentrations with asthma morbidity (223,224),

conjunctivitis and rhinitis (137,225) and even with earlier delivery among term births

(220).

The use of remote sensing imagery is another strength of this study. Remote

sensing imagery, such as the images captured by Landsat satellites, is considered

accurate at providing estimates of the seasonal changes and location of different pollen

sources (226), vegetation coverage (227) and land-use type (228); it is also considered

the primary tool for monitoring changes in vegetation activity (i.e. Floristic pollen

production and season length) (229). Data from remote sensing imagery has been

analyzed in connection to health outcomes such as allergic outcomes in children, with

closer proximity to greenness considered as having a greater aeroallergen exposure

(217). Future projects could use images from Landsat satellites or other data to identify

vegetation types (229) or land-use (228) if such images with higher resolution become

available for the years and cities studied in this project.

5.3. Recommendations

Better understanding of both pollen and fungi concentrations, phenology,

geographic coverage, and interaction with air pollutants is needed to provide the

information that atopic individuals could use to modify their environmental exposures

(147); it is also needed, to understand the public health impacts of these exposures now

and into the future. The available methods for data collection on aeroallergens already

produce large amounts of information; however, many challenges remain and should be

addressed in order to provide a more accurate picture. One of these challenges is the

fact that fractured grains or spores are not regularly counted in the taxon concentrations;

however, when inhaled, they are still capable of triggering an immune response, due to

their allergenic proteins. While existing technology is not yet capable of addressing this

52

challenge or even of quantifying the likely magnitude of this undeterminable particles,

future developments in profiling with genetic or molecular analysis could provide the

solution. Additionally, the limitations described in the discussion also point to the need

for: (a) a long-term collection plan; (b) an increased number of monitoring stations per

city; (c) continuous aeroallergen collection throughout the year; (d) open access to

historical and current aerobiological data worldwide.

Longitudinal studies are needed to examine long-term trends beyond the yearly

variations due to variation in aeroallergen seasons; such studies would help explain

regional differences in risk and increase our understanding of the impact of climate

change on pollen and fungi and the other biotic and abiotic factors that shape the

environmental exposures in urban areas (28). Climate change has the potential to

increase the length of aeroallergen seasons as well as pollen counts, geographical

coverage, and allergenicity (29). These escalations will also increase human exposure to

the allergenic proteins found in pollen grains and fungal spores (25,189). Future

increases in the incidence and prevalence of respiratory allergies and asthma are

predicted (190), accompanied by an increase in health care expenses allotted to the

care of these conditions (32). More extreme weather events (e.g. wildfires, floods,

thunderstorms) have been predicted in light of the forecasted climate change, and these

events will also worsen our exposure to aeroallergens and other risk factors such as air

pollution. Climate change should be considered in government initiatives for

aeroallergens such as alert systems (similar to the ones in place for air quality) and for

landscaping in urban zones (7). Given the demonstrated differences on concentration

and seasons lengths between each city, any initiative should be tailor-made at the

municipal level, but also integrated with other initiatives at the provincial and national

level. It is likely that atopy-prone individuals will be sensitized to the aeroallergens of the

local plants and fungi, but all the species present in Canada have the potential to change

their geographical locations in the future due to the increasing temperatures associated

with climate change.

Given the high costs associated with the health impacts of atopic conditions and

its high prevalence in Canada, there is a pressing need for public health programs that

acknowledge that exposure to aeroallergens often aggravates these conditions. Public

health programs for atopic conditions should be designed to prevent the development of

these conditions due to sensitization to aeroallergens and also the exacerbations on

53

patients who have already developed an atopic condition. Widespread use of an

aeroallergen alert system with detailed info as the one available from the Weather

Channel, and as comprehensive as the Air Quality Health Index, could be used to

communicate with sensitized individuals and advise them to reduce their exposure when

aeroallergen concentrations start to rise. Considering that aeroallergens have different

season lengths and different start and end dates, the alert system should issue separate

alerts for each aeroallergen, so that the priming of the immune system can be curtailed

before symptoms are developed. This alert system, that could provide local

concentrations daily (however, not in real-time), would benefit from a model of

aeroallergen production and dispersion that also incorporates weather-related variations

and long-term impacts of climate change, and could be coupled with existing air quality

predictions. Given the documented clinical cross-reactivity between pollens from similar

species (80), the idea of reporting total tree, grass, and ragweed pollens is better suited

to the general public for simplicity and cost minimization, while counts of individual

species would still have value for modeling and research.

54

Chapter 6. Conclusion

Aeroallergens are an important type of particulate matter in the outdoor air (230),

and humans are often exposed to these aeroallergens due to their means of

environmental dispersion. Pollen grains and fungal spores are produced as part of the

reproductive cycle, and inhalation by humans and other animals is an unplanned event

in their pathway of dispersion (31).2

Aeroallergens play a critical role in the development of allergic conditions through

sensitization, particularly in those individuals with genetic predisposition (231). However,

spores and pollen grains do not act in isolation; there are other biotic and abiotic factors

present in the environment and distinctive of each ecological zone. The biotic and abiotic

factors also represent an environmental exposures (e.g., air pollution) and play a role in

the interaction between air and respiratory tissue (94). Environmental exposures can act

as risk or protective effect modifiers in the development of allergy to aeroallergens (232)

and have special relevance during specific periods of time such as pregnancy or the first

year after birth. After the sensitization takes place and the affected individual develops

symptoms, further exposures to risk factors and / or allergens may cause symptom

exacerbations that will start in the respiratory system and subsequently involve the

immune system too (9).

The seasonal and geographic differences in aeroallergen concentrations

highlighted in this thesis suggest specific exposure patterns for each city, which may

lead to differential risks of disease. For the CHILD participants, the concentrations and

aeroallergen season lengths create a unique pattern of a relevant environmental

exposure, during suspected windows of susceptibility, that could be linked to their

potential development of atopic conditions and asthma. The unique pattern of

environmental exposures described could be generalized to other atopy-prone

individuals living in the same cities and years. In the near future, our environmental

2 It is interesting to consider, given the negative impacts in sensitized or atopy prone

humans, that for plants pollen inhalation by humans represents a waste of their resources, since

it decreases their possibilities of successful reproduction.

55

exposures will be altered by the human activities that drive climate change; unless

effective actions are taken to slow temperature increase and further decrease air

pollution, it is likely that the environmental conditions described will worsen and cause

an increase in the negative health impacts in humans, specifically in atopic conditions.

56

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Appendix. Allergenic pollen reported by country

Country Pollen Reference

Pakistan Mixed pollen, thresher dust and raw cotton

(Ahmed, Minhas, Micheal & Ahmad, 2011)

Mexico

Guadalajara Oaks and ashes, in weeds was mugwort, in grasses was Zea mays

(Alcalá-Padilla, Bedolla-Barajas, Kestler- Gramajo, Valdez-López, 2016)

Mexico City Weeds: Amaranthus. Trees: Betulaceae, Fagaceae and Oleacea families. Grass: Pooideae (Lolium perenne), Chloroideae and Cynodon/Dactylon family.

(Gaspar-Lopez, Lopez-Rocha, Rodriguez-Mireles, Segura-Mendez, & Del Rivero-Hernandez, 2014).

Mexico City Olea europaea (Morfin-Maciel, Castillo-Morfin & Barragan, 2007).

Nuevo León Quercus, Fraxinus. (Palma et al., 2014).

Mexico City Tree: Fraxinus, Cupressaseae, Alnus, Liquidambar, Callistemon, Pinus, and Casuarina. Grass/Weeds: Compositae, Cheno-Am, Ambrosia and Gramineae

(Teran, Haselbarth-Lopez & Quiroz-Garcia, 2009).

Croatia Ambrosia elatior (Popovic-Grle, Vrbica, Jankovic & Klaric, 2009).

Saudi Arabia Prosopis juliflora (Al-Frayh, Hasnain, Gad-El-Rab, Al-Turki, Al-Mobeireek, Al-Sedairy, 1999).

Oman Maize, grasses, cotton flock, trees, Alternaria alternata, Mesquite (Prosopis glandulosa), Russian thistle (Salsola kali) (34.4%), Bermuda grass (Cynodon dactylon), wheat cultivate.

(Al-Tamemi, Al-Shidhani, Al-Abri, Jothi, Al-Rawas, Al-Riyami, 2008).

Greece Parietaria (Anastassakis, Chatzimichail, Androulakis, Charisoulis, Riga, Eleftheriadou, Danielides, 2010).

Olea europaea and Parietaria species

(Papageorgiou, 1999).

Spain

S. alba pollen (Anguita et al., 2007).

Carica papaya (Blanco, Ortega, Castillo, Alvarez, Dumpierrez & Carillo, 1998).

Gramineae, O. europaea and C. sempervirens

(Cuesta-Hernández et al., 2010).

Catalunya Parietaria (Botey, Torres, Belmonte, Eseverri, & Marin,1999).

Cordoba Olea, Platanus and Urticaceae (Cariñanos et al., 2002).

Cartagena Olea europaea

(Garcia-Marcos, Garcia-Hernández, Morales Suarez-Varela, Batlles, Castro-Rodriguez, 2007).

http://www.sciencedirect.com.proxy.lib.sfu.ca/science/article/pii/S1081120610628050












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Murcia Phoenix dactylifera (Huertas, Lopez-Saez & Carnes, 2011).

Castilla Cupressaceae, Quercus, Platanus, Olea, Populus and Poaceae

(Rojo, Rapp, Lara, Sabariego, Fernandez-Gonzalez, & Perez-Badia, 2016).

Galicia Lolium perenne, Plantago lanceolata, Betula alba, Platanus hybrida, Olea europea, and Parietaria judaica

(Varela, Mendez, Gonzalez de la Cuesta, Iglesias, Gonzalez & Menendez, 2003).

Italy Ragweed (Ambrosia) (Ariano et al., 2015).

Olive pollen (Bonofiglio, Orlandi, Ruga, Romano & Fornaciari, 2013).

Mediterranean Cypres (De Luca, Graziani, Anticoli, Simeoni, Terzano, & Mannino, 1997). (Sposato et al., 2014).

Timothy grass (Phleum pratense), olive tree, birch, pellitory, and ragweed

(Dondi et al., 2013).

Europe Cypress pollen (Arilla, Ibarrola, García, de la Hoz, Martínez, & Asturias, 2004).

Grass pollen, birch pollen and parietaria

(Arshad et al., 2001).

Olea europaea (Liccardi, D’Amato & D’Amato, 1996).

North America Ambrosia artemisifolia (Bagarozzi & Travis, 1997).

Bosnia Herzegovina

Ragweed pollen (Baalaban, Bijelic & Milicevic, 2014).

Indonesia Elaeis guineensis, Acacia auriculiformis, resam Dicranopteris

(Baratawidjaja, 1999).

Morocco Grasses, olives and Parietaria

(Bardei, Bouziane, Kadiri, Rkiek, Tebay, Saoud, 2016).

Olive, grass. (Yazidi, Nejjari & Bartal, 2001).

Kuwait Chenopodiaceae (Behbehani, Arifhodzic, Al-Mousawi, Marafie, Ashkanani, Moussa, & Al-Duwaisan, 2004).

Sweden Grass pollen (Timothy) and Birch (Bjerg et al., 2016).

France Betulaceae pollen (Bosch-Cano et al., 2011

Cupressaceae (Caimmi, Raschetti, Pons, Dhivert-Donnadieu, Bousquet, Bousquet, & Demoly, 2012).

Lolium perenne, Olea Europea, Parietaria officinalis and Cupressus sempervirens

(Panzani, Mercier, Delord, Riva, Falagiani, Reviron & Auquier, 1993).

Turkey Grass (Bozkurt, Karakaya, & Kalyoncu, 2005).

Grass (Erel, Karaayvaz, Caliskaner & Ozanguc, 1998).

Grass:Poaceae (Anthoxanthum odoratum) Weeds: Artemisia vulgaris. Trees: Oleacea family

(Harmancis & Metintas, 2000).

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Trakya Cultivated wheat (Titicum vulgare) followed by rye grass (Lolium perenne) and orchard grass (Dactylis glomerata).

(Yazicioglu, Oner, Celtik, Okutan & Pala, 2004).

Canada

Quebec Ambrosia (Breton, Garneau, Fortier, Guay & Louis, 2006).

United Kingdom

Pollen (Brown & Hawkins, 1999).

USA Mixed grass pollen, Mixed tree pollen, mugwort/sage, ragweed

(Celedón, Sredl, Weiss, Pisarski, Wakefield, & Cloutier, 2004).

California OliveMesquiteAsh, GreenPrivet,

CommonAsh, ArizonaOlive,

RussianPalo VerdeAcacia,

Golden Locust, BlackOak, Swamp

(Galant et al., 1998).

New York Mixed tree pollen (Lovasi et al., 2013).

Japan Japanese cedar (Cryptomeria japonica)

(Cheng et al., 2004).

Ragweed of Ambrosia species and grasses of the Poaceae family, such as timothy (Phleum pratense), rye (Lolium species), Kentucky blue grass (Poa pratensis), orchard grass (Dactylis glomerata), Bermuda grass (Cynodon dactylon)

(Gunawan et al., 2008).

Japanese cedar (Cryptomeria japonica)

(Kawai et al., 2009).

Australia

Ryegrass (Lolium perenne) (Davies, Li, Green, Towers, Upham, 2012).

Queensland Eucalyptus (Gibbs, 2015).

New South Wales

Ragweed (Bass, Delpech, Beard, Bass & Walls, 2000).

Sidney, New South Wales

Cupressus, Platanus, Casuarina, Gramineae, Pinus, Plantago, Acacia, Populus, Callistemon, and Eucalypt species

(Katelaris, Carrozzi, Burke, & Byth, 2000).

South Africa Corn pollen, Bermuda (Green & Luyt, 1997).

Grass pollen (Mercer & van Niekerk, 1991).

South Korea Betula, Humulus, Alnus. (Kim, Park, Jang, Kim & Lim, 2016).

Hop Japanese (Park et al., 1997).

Germany Birch, mugwort (Kramer, Schmitz, Ring & Behrendt, 2015).

Karelia (Finland)

Birch, Timothy (Laatikainen et al., 2011).

China

Beijing Artemisia, Ambrosia, Chenopodiaceae and Gramineae.

(Li, Lu, Huang, Wang, Lu, Zhang & Zhong, 2008).

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Eastern China Asteraceae (Compositae), Gramineae, Chenopodiaceae, Cannabida- ceae, Polygonaceae, Cyperaceae, Brassicaceae (Cruciferae) and Plantagonaceae


North Betulaeceae, Abietaceae and Salicaceae


Mainland Artemisia vulgaris (Li et al., 2009). (Tang, Sun, Yin & Li, 2015).

Guangzhou, Guangdong

Bermuda-sIgE, Timothy-sIgE, and Humulus scandens-sIgE

(Luo, Huang, Zheng, Wei, Luo, Sun & Zeng, 2016).

Poland Artemisia Vulgaris (May, 1990).

India Dolichandrone platycalyx, (Nile trumpet tree), Parthenium hysterophorus, Prosopis juliflora, and Artemesia vulgaris

(Shaikh & Shaikh, 2008).

Northern India Prosopis juliflora, Ricinus communis, Morus, Mallotus, Alnus, Quercus, Cedrus, Argemone, Amaranthus, Chenopodium, Holoptelea

(Singh, 2014).

Central India Argemone, Brassica, Cannabis, Asphoedelus, Parthenium, Cassia, Azadirachta, grasses, Alnus, Betula, Malotus, Trewia nudiflora.

(Singh, 2014).

Eastern India Lantana, Cucurbita maxima, Cassia fistula, Cocos nucifera and Calophyllum inophyllum

(Singh, 2014).

South India Cassia, Ageratum, Salvadora, Ricinus, Albizia lebbeck and Artemisia scoparia

(Singh, 2014).

Alnus, Amaranthus, Argemone, Brassica, Cannabis, Cassia, Cedrus, Chenopodium, Cocos, Holoptelia, Mallotus, Morus, Parthenium, Prosopis juliflora, Quercus, Ricinus communis, and grasses such as Cenchrus, Cynodon, Imperata, Pennisetum

(Singh & Shahi, 2008).

Russia Birch tree (Ogorodova, Kamaltynova, Deev, Belonogova, Solodovnikova & Gonsorunova, 2010).

Israel Pecan tree (Carya illinoensis). (Rachmiel, Verleger, Waisel, Keynan, Kivity, & Katz, 1996).

Costa Rica Poaceae (Grass) (Riggioni et al., 1994).

Malaysia Acacia, Bermuda (Sam, Kesavan-Padmaja, Liam, Soon, Lim & Ong, 1998).

Lithuania Hazelnut, birch, lamb's quarters (Staikuniene, Japertiene & Sakalauskas, 2005).

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Switzerland Ambrosia artemisiifolia (common ragweed)

(Taramarcaz, Lambelet, Clot, Keimer & Hauser, 2005).

Grass pollen, silver birch pollen, (Wuthrich, 2001).

Portugal Phoenix dactilyfera (date palm) (Tavares, Machado, Loureiro, Cemlyn-Jones & Pereira, 2008).

Iran The Salsola kali (Sal k 1) and the Phleum pratense (rPhl p 1 and/or rPhl p 5)

(Teifoori et al., 2014).

temporal and geographic variation in aeroallergen

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