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Figure 2. Crate used for exposing dogs to a heat/humidity
stress environment. The dog was free to move about.

The dogs received no drugs prior to or during testing and were given
no food or water during heat exposure. The chamber was lighted and the
dogs were observed continuously through a window in the chamber. The animals
were not disturbed during the exposure and monitoring except for occasional
adjustments of sensors or leads. In addition to recording RT, HR, R/P, and
chamber conditions, the dogs were observed for changes in behavior (barking
and excessive activity). Simple activities such as slow rising, reposi-
tioning of the body, and slow movement in the crate, were not considered
significant and were not recorded as activity. Deliberate agitated activity
such as pawing at the crate walls, continuous circling, tossing of the head
to shed the muzzle, rubbing the muzzle back and forth on the floor of the
crate, and aggressive acts on the sensor guards were recorded. Any such
activity displayed by a dog during a 5-minute period was noted. Animals
could be rated over a longer observation period by the number of 5-minute
intervals in which they displayed significant activity (see Table 1).

To permit a timely selection of conditions that produce significant
physiological endpoints, it was necessary to stress some dogs to the point
of death. To conserve animals, we used a bracket design to establish a
presumptive endpoint. Animals that died from heat stress were necropsied.
Gross and microscopic observations were recorded. Surviving animals were
observed for 7 days, with notation being made of their clinical condition
and vital signs. Pre- and post-exposure X-rays of the lungs, hemograms,
urinalyses, and blood urea nitrogen levels were compared.

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REFERENCES

Anderson, B. E.: Temperature Regulation and Environmental Physiology.
M. J. Swenson (Ed.), Duke's Physiology of Domestic Animals. 8th
edition. Ithaca, NY, and London, Comstock Publishing Associates,
Cornell University Press, pp. 1119-1134, 1970.

Animal Welfare Act ~- USDA Regulations: Revision of Standards for the
Transportation and Handling, Care, and Treatment in Connection Therewith
of Dogs, Cats, Rabbits, Hamsters, Guinea Pigs, Nonhuman Primates, and
Certain Other Warmblooded Animals. Part 3 of Subchapter A, Chapter 1,
Title 9 of the Code of Federal Regulations, Federal Register, Vol. 43,
No. 232, December 1, 1978.

Animal Welfare Act - USDA Regulations: Ventilation Requirements of the
Transportation Standards for Dogs and Cats, Part 3 of Subchapter A,
Chapter 1, Title 9 of the Code of Federal Regulations, Federal Register,
Vol. 45, No. 108, June 3, 1980.

Crawford, E. C., Jxv.: Mechanical Aspects of Panting in Dogs.
J. APPL. PHYSIOL. 17, pp. 249-51, 1962.

Detweiler, D. K.: The Heart. Haskins, H. P., J. V. Lacroix, and K.
Mayer (Eds.), Canine Medicine. 2nd edition, Santa Barbara, California,
American Veterinary Publications, Inc., pp. 275-358, 1962.

Folk, G. E.: Introduction to Environmental Physiology. Philadelphia,
Pennsylvania, Lea and Febiger, p. 181, 1966.

Frankel, H. M.: Tolerance to High Temperature in Small Animals;
Dissertation Abstracts, 29(7), p. 128, 1959.

Hanneman, G. D.: Factors Related to the Welfare of Animals During

Transport by Commercial Aircraft. FAA Office of Aviation Medicine
Report No. FAA-AM-81-11, Washington, D.C., May 1981.

31

1


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Dogs in air shipment could be en route 24 hours and, under fhe most
severe conditions, would not receive water. The condition of 95 F, 93 - 2
percent RH without water intake was chosen as a reasonable stressor protocol
for determining the desired endpoint. Any chosen endpoint was to be brack-
eted downward rapidly to minimize the number of dogs stressed to an extreme.

Panting is the primary overt expression of heat dissipation response.
Crawford (2) suggested that the most efficient panting rate for dogs is
between 300 to 360 pants or cycles per minute. A dog's main heat compen-
sating response is to evaporate moisture from the upper respiratory tract,
mouth, and tongue. Environmental moisture (humidity) interferes with
dissipation by reducing evaporative cooling from such wet body surfaces.
Thus heat and humidity are integrally related in heat stress of dogs.

Increasing the body heat load in the dog should be met by increased
panting to promote effective evaporative cooling. There were primarily two
patterns of panting. One pattern was manifested by dogs developing a fast
panting rate relatively early during the stress and effectively maintaining
a high rate throughout the test period; the other pattern was shown by ani-
mals that failed to withstand the heat and their R/P usually rose to a fast
rate early during exposure, then progressively diminished, with a further
abrupt decline when RT reached about 109 F. This latter more precipitous
decrease apparently signaled a marked failure to dissipate body heat.

The normal HR for dogs is between 70 and 120 beats per minute (3).
Heart rate generally will increase with increased activity and with increased
need to transfer heat to the periphery and lungs for heat dissipation. Heart
rate should rise as a reflection of increased core temperature and associated
increase in general metabolism. When RTI's reached about 109 °F there was a
decrease in R/P, and a significant increase in HR, indicating the animal's
failure to cope with total heat stress.

Frankel §) reported that 50 percent of dogs (LD-50) died when the RT
reached 107.1 F. His animals were of unspecified sexes, ages, sizes, and
breeds. Folk (6) stated that 42°C (107.6°F) is a fatal body temperature for
the dog. Results from the current protocol, and subsequent separate studies,
have shown that healthy young adult male dogs of the beagle type can be
stressed to 108 F and recover. Frankel's figure for the heat LD-50 for dogs
may need to be reevaluated. Clinicians and researchers should recognize
that our experiments had as their objective a specific endpoint for use in
specialized heat research studies. The beagle, a rather docile breed, is a
standard laboratory animal and is raised precisely for biomedical studies.
It is of medium size and has short hair. All these factors suggest it may
be able to tolerate heat stress better than dogs of different ages, breeds,
coats, and conformation. Results from these 10 dogs and subsequent experi-
ments on more than 100 beagles (using greater external heat loads and
shorter exposure periods), confirm that an RT of 108 F is a tolerable and
safe endpoint for studying heat stress in dogs of this type.

nana be te eo toa BS


Equipment failure, Dogs 9 and 10 removed at 20h, RT 102.5°F, and 23.2h, RT 102.7°F respectively.
+ Equip y

+ Maximum RT 103.5°.

RESULTS

The RT's, HR's, and R/P's for each dog during heat exposure are
presented in the Appendix. Results from the first six dogs were the basis
for using a rectal temperature of 108 F as the indicator of the safe physi-
ological heat stress endpoint. The last four dogs helped substantiate that
indicator.

Of the first six tests, dog 1 survived the 24-hour exposure without ill
effect, reaching a maximum RT of 103.5°F, with no precipitous changes in R/P
or HR. Dogs 3 and 4 died in the chamber with RT's of 113.1°F and 113.7°F
respectively. It was observed in both animals that at an RT of 110°F the HR
showed a notable increase and there was some decline in R/P, both suggestive
of rapid decompensation of the animals. When dogs 5 and 6 began to show
similar HR and R/P changes at RT's of about 110°F, they were removed from
the environmental chamber to room temperature. Monitoring was continued and
both animals died within 5% hours of removal. Dog 2 survived the 24-hour
chamber exposure and had an RT of 109°F when removed. Before being taken
from the chamber, this animal had also shown some indication of a noticeable
increase in HR and declining R/P. However, he survived and had no clinically
observable sequela of the stress during the 7-day postexposure observation
period.

These observations provided support for an RT of 108°F as a suitable
indicator of severe heat stress, but a level of tolerable stress for dogs.
The decision was made to test this observation by removing from the chamber
any animal whose RT reached 108 F.

Dogs 7 and 8 were removed from the chamber when their RT reached 108°F
in 9.7 and 10.9 hours, respectively, and each recovered under ambient con-
ditions without sequela. Dog 9 was removed at 20 hours because of equipment
problems. His RT never exceeded 104.5°F and he suffered no subsequent ill
effects from the testing. Dog 10 was removed from the chamber at 23.2 hours,
also, because of equipment problems. His RT never exceeded 105.3°F and he
too suffered no residual ill effects. Had there been no technical problems,
both dogs probably would have tolerated the entire 24-hour exposure with RT's
not reaching 108 F.

A number of other observations on these severely stressed animals merit
discussion. Four of ten animals died as a result of the heat. The manner
of death is of clinical interest. Of the dogs that died in the chamber, one
displayed a considerable amount of activity during the exposure and reached
an RT of 109.4°F at 2 hours. He then became quieter and was able to compen-
sate for the heat stress, as evidenced by an RI of 106.7 F at 5 hours. How-
ever, his RT again rose to 109 F at 8 hours, at which time a distinct .
increase in HR and decrease in R/P occurred. Beyond 109 F there were fur-
ther precipitous changes (Figure A-3), probably indicating decompensation
The animal appeared extremely exhausted and died quietly without tetany or
convulsions. At necropsy, 30 minutes after death, all internal organs were
still hot to the touch. The lungs were dark red and blood flowed freely

5


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first portion of the exposure period. Values illustrating physiological and
activity variability in the initial 1.5-hour period (shortest tolerance time
for any dog was 1.6 hours) are presented in Table I. Based on time to reach
an RT of 108°F the dogs fell into three general categories: least tolerant,
under 10 hours; intermediately tolerant, less than 24 hours; and most tol-
erant, not reaching an RT of 108 F in 24 hours.

Least tolerant animals had appreciably higher RT's at 1 hour and were
near the 108 F endpoint at 1.5 hours, while more tolerant animals maintained
a significantly lower body temperature. Least tolerant animals appeared to
have appreciably increased HR's for the first 1.5 hours and the HR appeared
to parallel increases in RT. Least tolerant dogs showed a decrease in R/P
at 1.5 hours as compared to the R/P at .5 hours. This decrease in R/P (also
in dogs of intermediate tolerance) probably signifies that the animals had
reached their peak R/P performance by 1.5 hours and were experiencing gener~-
alized physiological decompensation, reflected in inability to sustain a
rapid R/P rate for temperature regulation. In contrast, the most tolerant
animals were still able to increase R/P at 1.5 hours and thus continued to
dissipate heat.

The relationship of increased activity and heat intolerance, noted in
the many other dog studies, was equally dominant here. The least tolerant
animals all were noted to have significantly greater activity during the
first, second, and third half hours than their more tolerant counterparts.

Dehydration was measured as weight loss during heat exposure but the
findings were complicated by urination and occasional defecation. Consid-
ering this, weight loss ranged from 0.8 to 3.2 pounds with none of the
animals losing more than 11 percent of their initial weight during exposure.
Dehydration appeared not to be a limiting factor in these animals' abilities
to compensate for the stress.

Animals that tolerated the stress testing, although showing signs of
exhaustion, readily returned to normal within 24 hours. X-rays of the
thorax, hematologic checks, blood chemistries, and urinalyses revealed
nothing that indicated permanent or sustained stress-related change. Clini-
cally these animals appeared no different from animals that had not been
stressed.

DISCUSSION

For anticipated applied research on heat stress effects on dogs trans-—
ported in various shipping containers, we needed to establish a practical
indicator of a heat stress endpoint that was near the ultimate tolerance
level but yet safe for the animals. Invasive techniques that would cause
additional stress were not seriously considered. Physiological parameters
that could easily be monitored noninvasively in dogs were HR, R/P, and RT.
Of these, rectal temperature appeared to be a slow changing parameter, easy
to monitor, and probably best expressive of integrated responses to heat
stress,


Technical Report Documentation Page

T. Report No. 2. Government Accession No. 3. Recipient's Catalog No.
FAA-AM-84 - 5

4. Title and Subtitle 5. Report Date

Tolerance Endpoint for Evaluating the Effects of June 1984
Heat Stress in Dogs 6. Performing Organizotion Code

=|

Performing Organization Report No.

7 Avhor's) Gerald D. Hanneman and James L. Sershon

9. Performing Organization Name ond Address 10. Work Unit No. (TRAIS)
FAA Civil Aeromedical Institute
P.O. Box 25082 TT. Contract or Gront No.

Oklahoma City, Oklahoma 73125

13. Type of Report and Period Covered

12. Sponsoring Agency Nome and Address.
Office of Aviation Medicine
Federal Aviation Administration
800 Independence Avenue, S.W. 14. Sponsoring Agency Code
Washington, D.C. 20591

15. Supplementary Notes
This work was performed under Tasks AM-E-78-VM-1, AM-E-79-VM-1, and
AM-B-82-VM~ 1.

16. Abstract
Animals occasionally die from heat stress encountered during shipment in the
nation's transportation systems. To provide a basis for a series of studies

on shipping crates, environmental conditions, etc., as may be encountered in

air transport of dogs, we sought to establish a suitable tolerance endpoint

for heat/humidity stress in dogs. We monitored the heart rate, respiratory/panting
rate, and rectal temperature of 10 male beagle dogs exposed to an air temperature
of 95 -1 F (relative humidity 93 -2 percent) for less than 24 hours. Of the first
six animals, two died during exposure, two died after being removed from the test
chamber, and two survived a 24-hour exposure. Based on observations from these
six dogs, a rectal temperature of 108° F was tentatively chosen as the tolerance
endpoint for subsequent tests. Of four additional animals tested, two were removed
from the environmental chamber when their rectal temperature reached 108°F and the
two others finished the test with a rectal temperature not exceeding 102.7°F. No
ill effects were noted in any of the surviving six animals during a 7-day post-
observation period. These and subsequent findings indicate a rectal temperature
of 108°F can be safely tolerated and can serve as a tolerance limit for additional
studies of heat and humidity effects on dogs.

17. Key Words 18. Distribution Statement
Heat Stress, Environmental Document is available to the public

Stress, Animal Physiology, Heat through the National Technical

Tolerance Endpoint, Beagle Dogs, Animal Information Service, Springfield,

Shipment Virginia 22161.

19. Security Classif, (of this report) 20. Security Classif. (of this page) 21. No. of Pages | 22, Price
Unclassified Unclassified 31

Form DOT F 1700.7 (8-72) Reproduction of completed page authorized

i .


APPENDIX

RI = Rectal temperature (figure readings are actual hourly reading).

HR = Heart rate (figure readings are the average of the readings
measured at 5-minute intervals for each hour).

R/P = Respiration/panting rate (figure readings are the average of
the readings measured at 5-minute intervals for each hour).

Cycles Per Minute - Used for heart rate and respiratory/panting rate.

Graphs showing Hours of Heat Exposure/Cycles Per Minute/Rectal

Temperature
Figure A-l Dog 1
Figure A-2 Dog 2
Figure A-3 Dog 3
Figure A-4 Dog 4
Figure A-5 Dog 5
Figure A-6 Dog 6
Figure A-7 Dog 7
Figure A-8 Dog 8
Figure A-9 Dog 9

Figure A-10 Dog 10

10


2 ee

Core temperature is a function of the balance between metabolic heat
production, exogenous heat load and heat dissipation to the environment.

; Metabolic heat production is related to basic metabolic rate and work. Body
activity generates heat, as exemplified by shivering to generate body heat

to compensate for excessive heat loss on exposure to cold (1). The barking,
pawing, chewing, and other activities, as noted in some of the test animals,
would tend to increase the endogenous heat load. Animals, who remained quiet
and did not expend energy in bodily movements, tolerated the heat stress
better than those animals that displayed increased activity. The latter
usually had a rapid rise in RT which persisted until the activity slowed
markedly or ceased. During the entire observation period such animals never
tolerated the stress as well as those that remained calm. This observation
suggests that the docile animals and breeds probably can tolerate the heat
stresses of shipment better than high-strung, nervous-type animals. This
same finding also suggests that tranquilizing excited or nervous animals with
drugs may aid tolerance of heat stress during shipment. Research to identify
suitable tranquilizing agents is planned.

We are aware of a number of anecdotal reports of animals that were

t shipped and thereafter were never the same: hunting dogs that had impaired
ability to point birds; dogs shipped for stud service that were of no value
for breeding after shipment; and animals that were listless, etc., after
shipment. Conceptually, a dog could be stressed short of death and suffer a
chronic debility. We looked for, but could not find, any identifiable changes
in the animals that survived the stress. Subsequently, in handling over 100
dogs stressed to an RT of 108 F, we have not observed or identified any

sed change in any of the animals that could be related to the episode of heat
ted stress.

Generally the treatment of heat stroke is to implement forced cooling as
soon as possible. In extreme heat stroke this is probably mandatory. Two
animals that were removed from the chamber alive, with RT's of 110°F, subse-
quently died. Obviously at that temperature they were unable to dissipate
body heat and might have been saved by forced cooling. On the other hand,

or dogs whose RT reached 108 F werd able, at room temperatures of Zo -75 F, to

28, dissipate excess heat and return to a body temperature of 101.5 F without
water intake, forced cooling, or other clinical intervention. This obser-

38 vation has been confirmed in many additional beagle dogs and is worthy of

notation by pet owners and veterinarians.

Rectal temperature is not a sophisticated physiological measurement. It
is readily obtained and can be recorded continuously with a thermocouple in
the rectum and a suitable external recording device. The rectal probe is
tolerated well by dogs. Rectal temperature reflects core temperature and is
relatively slow to change, being buffered by the total mass of the animal's
body and the specific heat of tissues. It reflects the sum total of many
physiological processes, especially as related to handling body heat. It has
become a practical heat stress indicator for use in our studies. As a result
! of our observations we can recommend an RT of 108°F in young beagle type dogs
l as a physiological indicator of safe and tolerable heat stress exposure, from
: which animals can recover without residual effect.

9


from the cut surfaces. There were a few small hemorrhages around the apex
of the heart, and hemorrhagic foci were noted in the trachea, kidneys, and
small and large intestines. The brain was hyperemic. All other organs
were not remarkable.

The second dog that died in the chamber was relatively quiet throughout
exposure. His RT rose slowly and progressively and at about 109 F his HR
increased and R/P decreased markedly and decompensation was indicated. This
animal also appeared exhausted and died quietly. As with the previous dog,
the organs were hot to touch at necropsy. The lungs were congested, dark
red, and had some hemorrhage along the periphery. There were petechial
hemorrhages near the apex of the heart; the stomach contained blood and
demonstrated numerous small foci of hemorrhage in the gastric mucosa. The
spleen was pale and shrunken. There was congestion of the small intestine
and brain. Other organs were not remarkable.

Two dogs (5 and 6) were removed from the stressful environment when their
RI's reached 110°F. Dog 5 began to show a sharper increase in HR and a
declining R/P rate at an RT of 109°F, After being removed from the chamber
and placed at ambient condition, his RT declined to 103.2°F in 2.3 hours but
rose again to 108.3 F, at which time he died, 5.5 hours after being removed
from the chamber. During the postexposure period the HR ranged between 316
and 208, averaging 263 beats per minute (BPM), and R/P was less than 200 per
minute. There was no panting after 45 minutes at ambient conditions. The
RI of Dog 6 dropped to 102.5 F during postexposure monitoring; he died at
1.8 hours after removal. His HR ranged between 296 and 156, averaging 231
BPM; R/P decreased from 164 to 68 per minute. Both dogs vomited blood after
being removed from the heat chamber.

Two dogs (7 and 8) were taken from the chamber when their RT's reached
108.2°F and 108.1°F respectively. After removal, they appeared exhausted
and lay quietly. Their body temperatures returned to lower levels; HR's
increased initially but then decreased, while R/P's remained virtually
unchanged and then declined. When RT's returned to normal levels, the dogs’
activities increased; they were returned to living quarters and drank
controlled quantities of water. Twenty-four hours after removal from the
chamber the animals appeared normal.

There was considerable variation in the behavior of the dogs that
appeared to affect tolerance of the heat stress. Animals showed varying
degrees of excitement during the preconditioning but on the day of testing
were generally calm during baseline data collection. When placed in the
environmental chamber some dogs displayed more barking and excessive activity
than others. This increased activity during the first, second, and third
half hour of exposure is shown in Table 1 on a scale of 1 through 6.

From observations on these 10 dogs, as well as on many other similar
male beagles separately monitored for RT alone, it appeared that tolerance
to heat and humidity, as carried out in this paradigm (and others of shorter
duration but more stressful), was strongly related to animal behavior in the

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about 6 inches past the anal sphincter. An elastic net served to keep the
sensors and wire leads in place (Figure 1). The dogs were free to move about

Figure 1. Beagle dog prepared for monitoring of rectal temperature,
heart rate, and respiration/panting rate.

the enclosure, but were fitted with muzzles to prevent their chewing the
leads. The muzzles did not interfere with respiration, open-mouth panting,

or extension of the tongue. The dogs were tested individually in wooden-frame
erates (30 x 18 x 22 inches) covered with a number 4 mesh wire (Figure 2).
Prior to testing, the animals were accustomed to the muzzle and crate for
about 2 hours each day for 3 days. On the morning of testing, dogs were fed
one-fourth can of moist food about 8:00 a.m. (2 hours before exposure). An
hour later they were prepared for monitoring, placed in the crate, and base-
line measurements were made for 30 minutes outside the environmental chamber.
At 10:00 a.m. the crated dogs were placed inside a chamber where heat and
humidity had been adjusted to a 95 -1 °F and 93 -2 percent RH environment.
These conditions were maintained throughout the exposure period. Respiration/
panting and heart rate were recorded for 30 seconds at 5-minute intervals.
Rectal temperature was continuously displayed on a Digitec Thermistor Ther-
mometer*,

*United Systems Corporation. Dayton, Ohio, Model 5820.


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TOLERANCE ENDPOINT FOR EVALUATING
THE EFFECTS OF HEAT STRESS IN DOGS

INTRODUCTION

In hot weather, dogs and other animals occasionally die during shipment
by air; some survive the stress of shipment but apparently suffer permanent
damage. Cargo compartments of commercial aircraft were not designed to pro-
vide live animals with a desirable living environment. To the contrary, the
cargo compartments of such aircraft are designed to contain and suppress the
spread of fire should such occur (8). The Federal Aviation Administration
(FAA) has no regulations to assure a healthy environment for pets, laboratory
test species and other categories of animals carried in the cargo compart-
ments of large passenger aircraft.

| By means of the Animal Welfare Act, which is administered by the United
States Department of Agriculture (USDA), the U.S. Congress has sought to pro-
vide for safe and humane treatment of animals during transport. The act
specifies that environmental air temperature for holding animals in terminal
facilities be limited to a range of 45°F to 85 F (4). The USDA regulations
also provide for minimal ventilation of containers used for transporting dogs
by stipulating that a shipping container have at least 14 percent of its wall
surface area open for ventilation (5). Since no experiments had been con—
ducted to test the effects of these holding temperatures and ventilation
specifications, the USDA requested and provided financial assistance to the
FAA for studies relating to acceptable holding temperatures for animals and
the adequacy of the crate ventilation standard.

In the current study we looked for a useful indicator of maximum safe
heat stress in dogs, from which animals could recover uneventfully without
persistent harmful effects. Such an indicator or endpoint could be useful
in other studies to delineate heat, humidity, and ventilation parameters for
safe and humane shipment.

METHODS AND PROCEDURES

At the time of this study the USDA limiting environmental temperature
for shipping dogs was 95°F. We chose this temperature for the experimental
protocol, combined with a high relative humidity (RH) of 93 42 percent to
provide added stress. All animals were to be monitored and observed for a
period not to exceed 24 hours. Ten mature, young, male, beagle dogs were
selected for this study. They weighed between 17 and 33 pounds. Noninvasive
methods of monitoring rectal temperature (RT), heart rate (HR), and respi-
ration/panting (R/P) were used. An expandable pneumograph around the thorax
measured R/P. The HR was recorded via three electrodes, located over the
right and left thorax at the fourth intercostal spaces and over the upper
sternum. The RI was measured using a flexible thermistor probe inserted



ACKNOWLEDGMENT

We wish to thank Mrs. Reba Cotton for her secretarial assistance in
the preparation of this manuscript. We also appreciate the generous

help of Mrs. Paula Grape for her laboratory work in the collection and
analysis of specimens.

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