Temporal clinical exacerbation of summer pasture-associated recurrent airway obstruction and relationship with climate and aeroallergens in horses

Lais R. R. Costa Equine Health Studies Program, Departments of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA 70803-8410; Pathobiological Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA 70803-8410.

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Jill R. Johnson Equine Health Studies Program, Departments of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA 70803-8410.

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Matthew E. Baur Department of Entomology, Agriculture Center, Louisiana State University, Baton Rouge, LA 70803-8410.

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Ralph E. Beadle Equine Health Studies Program, Departments of Veterinary Clinical Sciences, School of Veterinary Medicine, Louisiana State University, Baton Rouge, LA 70803-8410.

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Abstract

Objective—To describe the seasonal pattern of clinical exacerbation of summer pasture-associated recurrent airway obstruction (SPA-RAO) in relation to climate and aeroallergens in horses.

Animals—19 horses with SPA-RAO and 10 nonaffected horses.

Procedures—Daily examinations were performed on all horses while they were kept on pasture for 3 years. Onset and progression of clinical exacerbation based on a clinical score of respiratory effort were evaluated in relation to changes in maximum temperature, minimum temperature, mean temperature, maximum dew-point temperature, minimum dew-point temperature, and delta dew-point temperature. Seasonal pattern of clinical exacerbation was evaluated in relation to aeroallergen counts (20 types of fungal spores and 28 types of pollen).

Results—Seasonal pattern of clinical exacerbation of SPA-RAO was associated with increases in temperature (heat) and dew-point temperature (humidity), counts of fungal spores, and counts of grass pollen grains. Seasonal pattern of clinical exacerbation paralleled and was associated with increases in counts of specific types of fungal spores, particularly Basidiospore, Nigrospora, and Curvularia spp.

Conclusions and Clinical Relevance—Although a causal relationship could not be determined, the seasonal pattern of clinical exacerbation of SPA-RAO was associated with hot and humid conditions and high environmental counts for fungal spores and grass pollen grains. It is not known yet whether these are aeroallergens that cause clinical exacerbation of the disease.

Abstract

Objective—To describe the seasonal pattern of clinical exacerbation of summer pasture-associated recurrent airway obstruction (SPA-RAO) in relation to climate and aeroallergens in horses.

Animals—19 horses with SPA-RAO and 10 nonaffected horses.

Procedures—Daily examinations were performed on all horses while they were kept on pasture for 3 years. Onset and progression of clinical exacerbation based on a clinical score of respiratory effort were evaluated in relation to changes in maximum temperature, minimum temperature, mean temperature, maximum dew-point temperature, minimum dew-point temperature, and delta dew-point temperature. Seasonal pattern of clinical exacerbation was evaluated in relation to aeroallergen counts (20 types of fungal spores and 28 types of pollen).

Results—Seasonal pattern of clinical exacerbation of SPA-RAO was associated with increases in temperature (heat) and dew-point temperature (humidity), counts of fungal spores, and counts of grass pollen grains. Seasonal pattern of clinical exacerbation paralleled and was associated with increases in counts of specific types of fungal spores, particularly Basidiospore, Nigrospora, and Curvularia spp.

Conclusions and Clinical Relevance—Although a causal relationship could not be determined, the seasonal pattern of clinical exacerbation of SPA-RAO was associated with hot and humid conditions and high environmental counts for fungal spores and grass pollen grains. It is not known yet whether these are aeroallergens that cause clinical exacerbation of the disease.

Summer pasture-associated recurrent airway obstruction is a naturally occurring respiratory condition that affects horses residing on pasture. The disease was first reported to occur in the southeastern region of the United States.1 Clinical signs of SPA-RAO can vary from mild to life-threatening episodes of wheezing and paroxysmal coughing and chronic debilitating labored breathing that is worse during summer.2,3 The disease is considered to be an airway response to inhaled aeroallergens that differs from barn-associated RAO, primarily with respect to environmental conditions associated with the onset of clinical exacerbation.

Even though the etiology of SPA-RAO is not completely understood, it appears that seasonal changes affect the exacerbation-remission cycle of the disease. Identification of environmental factors, particularly those that precede the onset of clinical signs, would prompt the removal of horses from the environment during periods of high risk, even if the triggering agents or their mechanism were not completely understood.

In equine barn-associated RAO, clinical exacerbation can be induced in RAO-affected horses and ponies that do not have clinical signs, but not in unaffected control horses, by aerosol administration of fungal spores commonly present in hay fed to stabled horses.4,5 Moreover, fungal spores and pollen have been associated with airway hypersensitivity in humans.6

A recent study7 detected a significant positive correlation between the prevalence of airway disease in horses and rainfall, minimum temperature, total pollen counts, and total mold counts 1 to 3 months preceding the diagnosis of the disease. Moreover, environmental factors such as temperature and humidity affect the concentration of fungal spores, seasonal vegetative growth, and pollination in plants.

We hypothesized that climatic factors (especially variables of heat and humidity) and aeroallergens (especially fungal spore counts) are associated with seasonal exacerbation of SPA-RAO in southern Louisiana. The principal goals of this study were to determine the seasonal pattern of clinical exacerbation of SPA-RAO and identify the environmental factors associated with exacerbation of the disease.

Materials and Methods

Clinical data—Twenty-nine horses, including 19 affected with SPA-RAO and 10 nonaffected horses, were acquired by donation and maintained on pastures at Louisiana State University in Baton Rouge, La. Affected horses were middle-aged to old horses (median, 17 years; range, 12 to 28 years), predominantly of the Quarter Horse–type breeds (ie, 6 Quarter Horses, 4 Paints, 4 Appaloosas, and 1 Quarter Horse cross). The affected horses originated from southern and central Louisiana and developed clinical signs of airway obstruction every summer. Diagnosis of SPA-RAO was made on the basis of history, clinical signs of airway obstruction at the time of donation, marked reduction in end-expiratory abdominal lift, inspiratory nostril flare, and abnormal lung sounds after IV administration of atropine sulfate at 0.022 mg/kg or glycopyrrolate at 0.0022 mg/kg.8 Nonaffected horses were middle-aged (median, 8 years; range, 6 to 15 years), mostly of the Thoroughbred breed, with no history of respiratory disease. The study was approved by the Institutional Animal Care and Use Committee of Louisiana State University.

Evaluation of the breathing pattern was performed daily between 7 and 8 AM, by use of a standardized clinical scoring system.9,10 Daily assessment included evaluation of nostril flare and abdominal lift, which were assigned values from 0 to 4 (Appendix 1). Clinical score of respiratory effort was calculated according to the following equation:

CSRE = ([score for lateral aspect of nostrils + score for medial aspect of nostrils]/2) + score for abdominal lift

A CSRE ≥ 4.5 was considered indicative of clinical exacerbation of the disease (ie, horses had signs of airway obstruction). The horses included in the study were only those that had reversible signs of airway obstruction with baseline CSRE < 4.5 during remission. Clinically affected horses were removed from pastures for a period, and after clinical improvement, they were again kept on pastures. The clinical data evaluated in this study included only that obtained from horses while they were kept on pastures.

Climate data—Daily values of Tmax, Tmin, Tmean, DPTmax, DPTmin, and DPTdelta (DPTmax – DPTmin) were obtained from hourly recordings collected at Ryan Airport in Baton Rouge, La.a The location of the airport was approximately 9 miles from the pastures.

Aeroallergen data—Qualitative allergen counts for the year 1994 were obtained from the Acadiana(A1) Allergy and Asthma Center, Louisiana Pollen and Mold/Fungal Center, which is a counting station certified by the Aerobiology Committee of the American Academy of Allergy, Asthma, and Immunology.b The counting station was approximately 40 miles from the pastures. Daily counts were obtained for every 24-hour period (air samples were collected for 30 seconds every 10 minutes) with a samplerc situated on an unobstructed rooftop 1 story above the ground with no local pollen or fungal spore sources, according to the specifications of the National Allergy Bureau. Daily reports of environmental pollen and fungal spores included the total counts and the specific counts of 28 types of pollen and 20 types of fungal spores. Aeroallergen counts were grouped into 4 categories: tree pollen, grass pollen, herbaceous plant pollen (Appendix 2), and fungal spores. The list of specific fungal spore types includes the following: Alternaria spp, Ascospore, Basidiospore, Botrytis spp, Cercospora spp, Cladosporium spp, Curvularia spp, Drechslera/Helminthosporium, Epicoccum spp, Erysiphe/Oidium, Fusarium spp, Nigrospora spp, Periconia spp, Peronospora spp, Pithomyces, Polythrincium, rusts, smuts, Stemphylium spp, Torula spp.

Clinical and climatic evaluation of seasonality—The temporal association between clinical exacerbation and the climatic variables (ie, Tmax, Tmin, Tmean, DPTmax, DPTdelta, and DPTmin) was evaluated for 3 years. Daily frequency of CSRE ≥ 4.5 for the 3 years was graphed in conjunction with variations in the environmental factors, including Tmax, Tmin, Tmean, DPTmax, DPTmin, and DPTdelta. In addition, for each given horse, the first episode of clinical exacerbation of the disease was recorded for each of the 3 years.

Statistical analysismdash;Median and mode of CSRE of affected horses on a given date (from January 1, 1992, to December 31, 1994) were calculated and transformed to a binomial variable by setting the criterion that a median or mode score ≥ 4.5 was equivalent to clinical exacerbation of the disease. Binomial scores were then evaluated for associations with Julian date or calendar date, Tmax, Tmin, Tmean, DPTmax, DPTmin, and DPTdelta by use of logistic regression.d The log odds ratios were deemed significant if the confidence limits did not include the value 1, where a value of 1 would indicate no significant effect. A backward elimination logistic regression analysis incorporating the environmental variables (Tmax, Tmin, Tmean, DPTmax, DPTmin, and DPTdelta) was then used to determine which of the environmental variables best explained the variations in CSRE.11 A t test was used to evaluate and compare if the probability of significant CSRE was equally predicted by temperature and dew-point temperature whether median or mode scores were used. Values of P < 0.05 were considered significant.

Binomial scores were then evaluated via logistic regressiond for associations with total counts of tree pollens, herbaceous plant pollens, grass pollens, and fungal spores as well as counts of specific types of fungal spores. Log odds ratios were deemed significant if the confidence limits did not include the value 1.

The temporal pattern of each of the aeroallergen categories (tree pollen, herbaceous plant pollen, grass pollen, and fungal spores) was visually evaluated in relation to the pattern of clinical exacerbation of the disease for 1 year (1994). Also evaluated visually was the temporal pattern of each of the aeroallergen categories in relation to the climate variables (ie, Tmax, Tmin, Tmean, DPTmax, DPTdelta, and DPTmin). In addition, counts of each aeroallergen type (ie, 20 types of fungi and 28 types of pollen) were evaluated visually individually in relation to clinical exacerbation and environmental temperature variables (ie, Tmax, Tmin, Tmean, DPTmax, DPTdelta, and DPTmin) for the year 1994.

Results

Horses affected with SPA-RAO and maintained on pastures had a clear seasonal onset of clinical exacerbation starting when the climate became warm and humid. Evaluation of the dates of the first episode of clinical exacerbation for each individual horse each year revealed a consistently reproducible seasonal onset, in most instances during May to July. There was a significant positive association between the probability of clinical exacerbation of disease and the temperature variables, Tmean, Tmin, and Tmax, as well as the dew-point temperature variables, DPTmin and DPTmax. Several of these variables appeared to be redundant in the sense that Tmin, Tmax, and Tmean each provided similar information; thus, only 1 was selected from backward regression analysis. In the backward regression analysis, a measure of one of the temperature variables alone, Tmax, and a measure of one of the dew-point temperature variables, DPTmin, were included as the only variables in the explanatory model (Figure 1; Table 1). Clinical exacerbation of SPA-RAO persisted until October and November, when the climate became cooler and less humid. Nonaffected horses kept at pasture conditions had no appreciable changes in clinical score (ie, CSRE remained < 4.5) throughout the seasons of the year.

Table 1—

Results of logistic regression analyses for association of the dependent variable CSRE with independent environmental variables in horses.

Independent variableLog odds ratioConfidence limits
Tmax1.080*1.066–1.094
Tmin1.087*1.073–1.100
Tmean1.090*1.075–1.104
DPTmax1.085*1.070–1.100
DPTmin1.080*1.068–1.093
DPTdelta0.8610.834–0.889

Significant (odds ratio > 1.0) positive correlation with CSRE.

Figure 1—
Figure 1—

Temporal pattern (1992 to 1994) of clinical exacerbation of SPA-RAO in horses in relation to environmental variables. Year and month are indicated on the x-axis. Solid line indicates degrees Celsius corresponding to environmental variables (y-axis labels [left]); shaded areas indicated proportions of horses with CSRE ≥ 4.5 (y-axis [right]).

Citation: American Journal of Veterinary Research 67, 9; 10.2460/ajvr.67.9.1635

Probability of onset of clinical exacerbation was closely associated with the Julian and calendar date during all 3 years, and the point of 50% probability of clinical exacerbation was day 161 (ie, June 10) for 1992, 1993, and 1994 (Table 2). Regardless of whether the median or mode CSRE value was used in the logistic regression analysis, the statistical model predicted similar values of Julian date, temperature, and dewpoint temperature variables associated with the probability of clinical exacerbation. The logistic model fit the mode and median CSRE similarly well (P > 0.5). The probability of significant CSRE was equally predicted by temperature and dew-point temperature whether median or mode scores were used (P > 0.05). Although there was no significant difference when the analysis was performed by use of median or mode CSRE, median values were chosen for description in this report because the median value is a better descriptor when quantification of levels of effect is of interest.11 The specific changes in each of the temperature variables were closely associated with the onset of clinical exacerbation (Table 1).

Table 2—

Probability (P) of a CSRE ≥ 4.5 as evidence of clinical exacerbation of SPA-RAO in horses.

PJulian dateTmax(°C)Tmin(°C)Tmean (°C)DPTmax(°C)DPTmin(°C)DPTdelta(°C)
0.112413.95.09.78.11.610.2
0.213720.010.014.913.37.77.2
0.314623.913.918.316.611.65.5
0.415427.216.721.320.015.03.9
0.516130.018.923.522.717.32.2
0.616832.820.925.324.718.90.6
0.717534.623.126.627.020.6
0.818436.425.428.330.222.1
0.919838.428.030.134.424.2
1.0238

– = Not applicable.

The aeroallergen data, which included fungal spore and pollen counts, were only available for 1994. There was a positive association between the probability of clinical exacerbation of the disease and the increases in fungal spore counts and a positive association between the probability of clinical exacerbation of the disease and the increases in grass pollen counts (Table 3). Among the different types of fungal spores, Curvularia spp, Drechslera/Helminthosporium, Nigrospora spp and Basidiospore had the strongest positive association with onset of clinical exacerbation of the disease, and to a lesser extent, Botrytis spp and Cercospora spp had a significant positive association with clinical exacerbation of SPA-RAO.

Table 3—

Results of logistic regression analyses for association of the dependent variable CSRE with independent aeroallergen variables in horses.

Independent variableLog odds ratioConfidence limits
Tree pollen0.9270.878–0.978
Herbaceous plant pollen1.0030.996–1.009
Grass pollen1.150*1.059–1.250
Mold spores1.046*1.041–1.048
Alternaria spp0.9620.941–0.983
Ascospore1.0001.000–1.000
Basidiospore1.016*1.013–1.017
Botrytis spp1.007*1.001–1.012
Cercospora spp1.002*1.001–1.004
Cladosporium spp0.9990.999–1.000
Curvularia spp1.029*1.016–1.043
Drechslera/Helminthosporium1.019*1.001–1.037
Epicoccum spp0.9190.877–0.962
Erysiphe/Oidium1.0070.999–1.016
Fusarium spp0.9980.979–1.017
Nigrospora spp1.017*1.005–1.030
Periconia spp1.0040.998–1.010
Peronospora spp1.0010.988–1.014
Pithomyces0.9710.939–1.003
Polythrincium spp0.9920.937–1.050
Rusts0.9860.969–1.003
Smuts1.0030.997–1.008
Stemphylium spp1.0110.997–1.025
Torula spp0.9930.980–1.007

See Table 1 for key.

Visual inspection of the aeroallergen data revealed that the pattern of fungal spore counts during the calendar year paralleled the proportion of CSRE values that were ≥ 4.5 and the changes in temperature and humidity. High total fungal spore counts occurred during the same calendar periods that temperature and dew-point temperature variables were high and during clinical exacerbation (Figures 2 and 3). An increase in grass pollen counts was detected at the same time as the increase in the proportion of horses with CSRE ≥ 4.5, and this pattern continued throughout the summer and tapered off in the fall. The increase in grass pollen counts coincided with increases in the temperature and dew-point temperature (Figure 4). In contrast, the temporal pattern of tree pollen counts and herbaceous plant pollen counts did not parallel the temporal pattern of horses with CSRE ≥ 4.5 or the increases in the climatic variables.

The temporal pattern of occurrence of CSRE ≥ 4.5 was similar to the temporal pattern of counts of specific types of fungal spores for Basidiospore, Nigrospora spp, and Curvularia spp, followed by Botrytis spp, Drechslera/Helminthosporium, and Cercospora spp (Figure 5), whereas the increases in counts of other types of fungal spores (ie, Alternaria spp, Ascospore, Cladosporium spp, Epicoccum spp, Erysiphe/Oidium, Fusarium spp, Periconia spp, Peronospora spp, Pithomyces, Polythrincium spp, rusts, smuts,Stemphylium spp, and Torula spp) were not detected at the same time as the increase in the proportion of horses with CSRE ≥ 4.5.

Figure 2—
Figure 2—

Temporal pattern (1994) of clinical exacerbation of SPA-RAO in horses in relation to aeroallergen counts. Months are indicated on the x-axis. Solid line indicates aeroallergen counts (y-axis labels [left]); shaded areas indicated proportions of horses with CSRE ≥ 4.5 (y-axis [right]).

Citation: American Journal of Veterinary Research 67, 9; 10.2460/ajvr.67.9.1635

Figure 3—
Figure 3—

Temporal pattern (1994) of fungal spore counts in relation to environmental variables. Months are indicated on the x-axis. Shaded area indicates fungal spore count (y-axis [left]); solid line indicates environmental variables (y-axis labels [right]).

Citation: American Journal of Veterinary Research 67, 9; 10.2460/ajvr.67.9.1635

Figure 4—
Figure 4—

Temporal pattern (1994) of grass pollen counts in relation to environmental variables. Months are indicated on the x-axis. Shaded area indicates grass pollen count (y-axis [left]); solid line indicates environmental variables (y-axis labels [right]).

Citation: American Journal of Veterinary Research 67, 9; 10.2460/ajvr.67.9.1635

Figure 5—
Figure 5—

Temporal pattern (1994) of clinical exacerbation of SPA-RAO in horses in relation to spore counts for specific fungi. Months are indicated on the x-axis. Solid line indicates specific fungus (y-axis labels [left]); shaded areas indicated proportions of horses with CSRE ≥ 4.5(y-axis labels [right]).

Citation: American Journal of Veterinary Research 67, 9; 10.2460/ajvr.67.9.1635

Discussion

In the present study, the temporal pattern of clinical exacerbation of SPA-RAO was clearly seasonal and associated with warm and humid conditions. In southern Louisiana, warm and humid conditions extend well beyond the summer solstice and autumnal equinox. Therefore, strictly speaking, the term “summerlike” rather than “summer” pasture-associated RAO may be more suitable for this part of the country. Nevertheless, the seasonal pattern of the disease was clearly associated with the warm and humid months of the year.

Among the factors evaluated in this study, calendar date and climate variables of heat (Tmax, Tmin, and Tmean) and humidity (DPTmax, DPTdelta, and DPTmin) were temporally associated with onset and persistence of clinical exacerbations of SPA-RAO. This association could be either a direct effect or, most likely, attributable to environmental conditions that foster changes, such as increased aeroallergens. The tight clustering of Julian date of onset each year indicated that clinical exacerbation was fairly predictable with respect to calendar date for these horses in this region. During climatic aberrations, clinical exacerbation may not occur around the same calendar date. In contrast, clinical exacerbation of SPA-RAO in the United Kingdom is observed in April and May, during hot dry weather, or after exposure to dust generated during harvest or burning of nearby crops.12–14

In a recent study7 of the time-space clustering of COPD in horses admitted to 17 veterinary teaching hospitals in North America, a significant positive correlation was reported between prevalence of the disease and rainfall 3 months previously, the minimum temperature 2 months previously, total pollen counts measured 3 months previously, and total fungal spore counts measured 1 month previously and during the same month. The study population consisted of horses affected with any of the inflammatory diseases of the lower portion of the respiratory tract collectively referred to as COPD, which included indoor or barnassociated RAO, inflammatory airway disease, and SPA-RAO. The aeroallergen data were obtained from certified stations located in the proximity (median, 120 km) of each veterinary teaching hospital and included the counts of the 10 most common pollen types and the 10 most common fungal spore types. Among the pollen types, significant associations were observed between monthly prevalence of COPD and tree pollen counts, including Quercus, Fraxinus, Morus, and Acer spp and the Pinace family. Among the fungal spore types, significant associations were observed between monthly prevalence of COPD and spore counts for Alternaria spp measured during the same month, Ascospores measured 1 and 2 months previously, and Cladosporium spp measured during the same month. Horses affected with COPD were evaluated, and the aeroallergen data included the counts for all regions in North America, such that regional variations were not highlighted.7 Those findings contrast with the present study, which evaluated only horses affected with SPA-RAO in a limited area in southern Louisiana. Nonetheless, in both studies, the data indicated that climatic factors and outdoor aeroallergens appeared to contribute to the occurrence of airway disease in horses.

Considering that environmental temperature and dew-point temperature variables affect the aeroallergen counts, one could speculate that some of the aeroallergens evaluated in the present study might be potential triggering agents of SPA-RAO. The seasonal pattern of clinical exacerbations paralleled the temporal pattern of high fungal spore counts and grass pollen counts. Specifically, the pattern of fungal spore counts of

Curvularia spp, Basidiospore, Nigrospora spp, and, to a lesser extent, Botrytis sp and Drechslera/Helminthosporium best matched the seasonal pattern of clinical exacerbation of SPA-RAO. Among the grasses in the southeastern coastal plains, Bermuda grass sheds pollen principally from March to September and Johnson grass sheds pollen from June to November, both of which coincide with the time of clinical exacerbation of SPA-RAO.6,15 The horses evaluated in this study were residing in pastures containing predominantly Bermuda grass. Results of logistic regression analysis indicated that these aeroallergens were associated, although not strongly, with clinical exacerbation of the disease. However, only data from 1 year were analyzed, and the relationship may not be causal, so prospective studies are necessary to investigate the relationship further.

Airborne endotoxin concentrations are high in many agricultural environments, including barns.16 Inhalation of endotoxin induces airway inflammation and dysfunction in horses and likely contributes to the pathogenesis of barn-associated RAO.17 The role of airborne endotoxin as a contributor to airway inflammation in SPA-RAO was not addressed in the present study. It remains to be determined whether airborne endotoxin in pasture environments contributes to the clinical exacerbation of SPA-RAO.

A number of fungal spores are associated with seasonal spore-releasing patterns and have been proposed as potential triggering agents in SPA-RAO.6,18,19 In addition, pollen shedding from Bermuda grass and Johnson grass temporally coincides with the time of clinical exacerbation of SPA-RAO.15 The present study involved a small number of horses from a selected population; therefore, it is unclear how representative these findings are for other horses affected with SPA-RAO.

ABBREVIATIONS

SPA-RAO

Summer pasture-associated recurrent airway obstruction

CSRE

Clinical score of respiratory effort

Tmax

Maximum temperature

Tmin

Minimum temperature

Tmean

Mean temperature

DPTmax

Maximum dew-point temperature

DPTmin

Minimum dew-point temperature

DPTdelta

Delta dew-point temperature

COPD

Chronic obstructive pulmonary disease

a.

Data collected and provided by Kevin Robbins and Jay Grimes, Southern Regional Climate Center at Louisiana State University, Baton Rouge, La.

b.

Dr. Powlin V. Manuel and Susan Sturm, Acadiana Allergy and Asthma Center, Lafayette, La.

c.

Rotorod sampler, Sureillance Data Inc, Plymouth Meeting, Pa.

d.

Proc LOGIT, SAS Institute Inc, Cary, NC.

References

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Appendix 1

Appendix 1

Clinical score of respiratory effort in horses.

Numerical scoreNostril flareAbdominal lift
0No or very slight movement on inspirationNo or very little appreciable movement in the ventral portion of the flank
1Nostril flares only slightly during inspiration, returning to a normal position at the end of inspirationSlight abdominal flattening with heave line just beginning to form in the cranioventral portion of the flank (not easily detectable)
2Nostril flares during inspiration, returning to a near normal positionAbdominal flattening is obvious and a heave line extends to a point halfway between the tuber coxae and elbow joint (fairly easy to detect)
3Nostril is flared to a greater extent during inspiration and does not return to a normal position during exhalationAbdominal flattening and a heave line extends beyond a point halfway between the tuber coxae and elbow joint, but does not extend all the way to the elbow (easy to detect)
4Nostril is flared and remains maximally flared throughout the respiratory cycleAbdominal flattening and a heave line extends cranially all the way to the elbow joint (very easy to detect)

Appendix 2

Appendix 2

Categories of pollen grains that are potential aeroallergens in horses.

Pollen grain typeFamily or genus nameCommon name
GrassCyperaceaeSedge family
Graminaea/PoaceaGrass family
 TreeAcer
 AlnusAlder
 BetulaceaeBirch family and alikes
 CaryaHickory, pecan
 CupressaceaeJuniper family, cedar
 FagusBeech
 FraxinusAsh
 JuglansWalnut, butternut
 LiquidambarSweet gum
 MorusMulberry
 Oleaceae/OleaOlive family
 PinaceaePine family and alikes
 PlatanusSycamore
 PopulusPoplar, cottonwood
 QuercusOak
 SalixWillow
 TiliaBasswood, linden
 UlmusElm
Herbaceous plantAmbrosia/FranseriaRagweed
ArtemisiaSage, wormwood
Chenopodiaceae/Amaranthaceae
Compositae/other AsteraceaeComposites, aster family except ragweed
PlantagoPlantain
RumexSheep sorrel, dock
TyphaCattail
UrticaNettle, pellitory
  • Figure 1—

    Temporal pattern (1992 to 1994) of clinical exacerbation of SPA-RAO in horses in relation to environmental variables. Year and month are indicated on the x-axis. Solid line indicates degrees Celsius corresponding to environmental variables (y-axis labels [left]); shaded areas indicated proportions of horses with CSRE ≥ 4.5 (y-axis [right]).

  • Figure 2—

    Temporal pattern (1994) of clinical exacerbation of SPA-RAO in horses in relation to aeroallergen counts. Months are indicated on the x-axis. Solid line indicates aeroallergen counts (y-axis labels [left]); shaded areas indicated proportions of horses with CSRE ≥ 4.5 (y-axis [right]).

  • Figure 3—

    Temporal pattern (1994) of fungal spore counts in relation to environmental variables. Months are indicated on the x-axis. Shaded area indicates fungal spore count (y-axis [left]); solid line indicates environmental variables (y-axis labels [right]).

  • Figure 4—

    Temporal pattern (1994) of grass pollen counts in relation to environmental variables. Months are indicated on the x-axis. Shaded area indicates grass pollen count (y-axis [left]); solid line indicates environmental variables (y-axis labels [right]).

  • Figure 5—

    Temporal pattern (1994) of clinical exacerbation of SPA-RAO in horses in relation to spore counts for specific fungi. Months are indicated on the x-axis. Solid line indicates specific fungus (y-axis labels [left]); shaded areas indicated proportions of horses with CSRE ≥ 4.5(y-axis labels [right]).

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