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infrared thermography1
A. L. Schaefer2, N. Cook2, S. V. Tessaro3, D. Deregt3, G. Desroches4, P. L. Dubeski2,
A. K. W. Tong2, and D. L. Godson5
2Lacombe
Research Centre, Agriculture and Agri-Food Canada, PO Box 6000, C and E Trail, Lacombe, Alberta,
Canada T4L 1W1; 3Lethbridge Laboratory (Animal Diseases Research Institute), Canadian Food Inspection
Agency, PO Box 640, Lethbridge, Alberta, Canada T1J 3Z4; 4Public Works and Government Services Canada.
#1000, 9700 Jasper Ave., Edmonton, Alberta, Canada T5J4E2; and 5Department of Veterinary Microbiology,
Western College of Veterinary Medicine, 52 Campus Drive, Saskatoon, Saskatchewan, Canada S7N 5B4.
Contribution no. 1018, received 14 November 2002, accepted 24 October 2003.
Schaefer, A. L., Cook, N., Tessaro, S. V., Deregt, D., Desroches, G., Dubeski, P. L., Tong, A. K. W. and Godson, D. L. 2004.
Early detection and prediction of infection using infrared thermography. Can. J. Anim. Sci. 84: 7380. Early detection and/or
prediction of disease in an animal is the first step towards its successful treatment. The objective of this study was to investigate
the capability of infrared thermography as a non-invasive, early detection method for identifying animals with a systemic infection. A viral infection model was adopted using 15 seronegative calves whose body weight averaged 172 kg. Ten of these calves
were inoculated with Type 2 bovine viral diarrhoea virus (strain 24515) and five were separately housed and served as uninfected controls. A simultaneous comparison of infrared characteristics in both infected and control animals was conducted over
approximately 15 d. In addition, measures of blood and saliva cortisol, immunoglobulin A, blood haptoglobin and clinical scores
were obtained. Infrared temperatures, especially for facial scans, increased by 1.5C to over 4C (P < 0.01) several days to 1 wk
before clinical scores or serum concentrations of acute phase protein indicated illness in the infected calves. The data suggest that
infrared thermal measurements can be used in developing an early prediction index for infection in calves.
Key words: Infection, early detection, infrared thermography, cattle
Schaefer, A. L., Cook, N., Tessaro, S. V., Deregt, D., Desroches, G., Dubeski, P. L., Tong, A. K. W. et Godson, D. L. 2004. Dpistage
et prvision prcoces des infections par thermographie infrarouge. Can. J. Anim. Sci. 84: 7380. Le dpistage ou la prvision rapide de la maladie chez un animal est la premire tape vers la gurison. La prsente tude devait vrifier lutilit de la thermographie
infrarouge comme mthode de dpistage prcoce non invasive en vue de lidentification des animaux atteints dune infection systmique.
Pour cela, les auteurs ont recouru un modle dinfection virale constitu de 15 veaux srongatifs de 172 kg en moyenne. Ils ont inocul
le virus de type 2 de la diarrhe des bovins (souche 24515) dix veaux et gard les cinq autres part comme tmoins. Ensuite, ils ont
simultanment compar les paramtres infrarouges des sujets infects et sains pendant une quinzaine de jours. Paralllement, ils ont dos
le cortisol dans le sang et la salive, limmunoglobine A, lhaptoglobine srique et not les signes cliniques. La temprature infrarouge, de
la face surtout, passe de 1,5C plus de 4C (P < 0.01) plusieurs jours une semaine avant quapparaissent les signes cliniques ou que
les concentrations sriques attribuables la phase aigu de production des protines virales nindiquent lexistence de la maladie chez les
veaux infects. Les rsultats donnent penser quon pourrait se servir des relevs thermiques infrarouges pour mettre au point un indice
de prvision rapide de linfection chez les veaux.
Mots cls: Infection, thermographie infrarouge, bovins
1Preliminary
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Score
Lethargy
0 = none
1 = mild anorexia or listlessness
2 = moderate lethargy, slow to rise, anorectic
3 = recumbent
4 = death
Haemorrhage
0 = none
1 = few petechiae on mucous membranes or sclera
2 = moderate or severe petechiation or hematomas
>1 cm
3 = large hematomas > 5 cm
4 = bloody diarrhea or epistaxis
Respiratory signs
0 = none
1 = clear nasal discharge or slight cough
2 = mucopurulent discharge or severe cough,
slight increase in lung sounds
3 = severe pneumonia
Diarrhoea
0 = none
1 = mild or slight, < 5% dehydrated
2 = moderate, 5 to 10 % dehydrated
3 = severe and profuse, > 10% dehydrated
METHODS
Animals and Management
Animals were managed in accordance with the guidelines
established by the Canadian Council on Animal Care
(1993). Fifteen Angus-Hereford cross heifers, approximately 6 mo of age, from the BVDV-free herd at the Animal
Disease Research Institute (ADRI), Lethbridge, Alberta,
were used. These calves were weaned from the main herd
and allocated to infection and control groups (10 and 5
calves, respectively); experimental groups were blocked by
weight. The calves were housed in groups of five in three
separate, environmentally controlled rooms in the biosafety
level 3 facility at ADRI. Body weights were collected on all
calves 3 wk prior to and at the end of the study.
The calves were given a balanced alfalfa cube-based diet
designed to provide 1.5 times maintenance requirements
based on National Research Council (1984) recommendations. All calves were given ad libitum access to fresh water.
A rubberised bedding mat was provided for the animals to
lie on. Any debris (straw or manure) on the animals coats
was brushed off before infrared measurements were taken.
The calves were placed in their isolation rooms for acclimatisation 3 wk prior to BVDV inoculation. The infection
challenge procedure consisted of a total intranasal dose of 2
107 TCID50 of type 2 BVDV, strain 24515 (1 mL in each
nostril). Control animals were inoculated intranasally with
cell culture medium only. Calves were monitored daily for
signs of clinical disease. Blood samples were collected and
rectal temperatures were measured on days 0, 3, 7, 10, 14,
17 and 21 d post-inoculation (dpi).
Normal biosafety level 3 procedures were maintained by all
personnel involved in the study as directed by ADRI staff. The
trials ran for 3 wk post-inoculation or, in the case of a few animals, until the severity of illness warranted euthanasia for
humane reasons. The three animal rooms used in the study
were all kept at a constant temperature (approximately 14C),
humidity (28%), and barometric pressure. The calves had been
adapted to these conditions prior to the study and were in their
thermal neutral zone. Lighting was adjusted to simulate normal
daylight and darkness (12 h light/12 h dark). Normal cleaning
and maintenance procedures for the rooms established by
ADRI were followed.
Data Collection
Infrared thermography images (IRT) on all animals were collected as follows: A hand held portable Inframetrics broadband 760 infrared scanner (FLIR Inframetrics 760, Boston,
MA, USA) was used to collect images on all animals at
approximately 1000 daily. Two separate infrared cameras
(same model and make) were needed, one for the non-infected or clean control room and one for use in the BVDV challenge rooms. Animals were not captured at this time, but
instead the infrared camera technician walked around the animals until he was able to capture the infrared thermographic
image. In addition to blood sampling days (0, 3, 7, 10, 14, 17
and 21 dpi), the hand-held camera was also used daily postinoculation to collect dorsal and selective facial, lateral, and
distal images. The objective of the current study was to exam-
75
Table 2. Clinical score data for control and BVD infected animals
Day
12
21
25
96
10
14
19
44
46
38
40
51
74
79
0
1
2
3
4
5
6
7
8
9
10
0
0
0
0
0
0
0
0
3
4
2
0
0
0
0
0
0
0
0
0
4
5
0
0
0
0
0
0
0
1
1
2
2
0
0
0
0
0
0
0
1
1
2
2
0
0
0
0
0
0
1
1
2
3
8
0
0
0
0
0
0
0
0
0
2
3
0
0
0
0
0
0
0
0
1
1
1
0
0
0
0
0
0
0
0
1
1
1
0
0
0
0
0
0
0
0
0
1
1
0
0
0
0
0
0
0
0
0
2
4
0
0
0
0
0
0
0
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
76
Table 3. Orbital infrared and rectal temperatures in BVD-infected calves. Data for the mean and max orbital temperature are the least squares
means SE of the least squares means
Day post
BVDV
induction
BVDV
mean IR
temp.
BVDV
mean SE
BVDV
max IR
temp.
BVDV
max SE
0
1
2
3
4
5
6
7
8
9
10
31.22a
32.11b
32.26bc
32.30bc
32.54bc
32.66bc
32.79bc
33.31bc
33.51bc
33.35bc
33.79bc
0.15
0.15
0.15
0.15
0.15
0.15
0.15
0.15
0.15
0.15
0.15
34.77a
35.59b
35.59bc
35.67bc
35.75bc
36.02bc
36.10bc
36.86bc
37.05bc
36.70bc
37.20bc
0.34
0.34
0.34
0.34
0.34
0.34
0.34
0.34
0.34
0.34
0.34
BVDV
rectal
temp.
BVDV
rectal
temp. SD
39.12a
0.61
39.58b
0.61
40.36b
0.61
40.37b
0.61
ac Means within columns with different letters are statistically different at P < 0.05.
and t-tests (Steel and Torrie 1960). The authors would note
that in the present study, one of the primary reasons for
using an induction model was to know precisely when disease induction occurred. Thus, for many of the comparisons
used in the present study, the animal was used as its own
control. For the infrared thermal data pertaining to the
orbital, nose, ear and dorsal surfaces, treatment means were
compared using the GLM model (SAS Institute, Inc. 1990).
RESULTS
Infrared Thermography
Thermographic scans were collected from several anatomical
sites on the calves including the side (lateral), back (dorsal) and
hooves, as well as several facial areas, such as the ears (midventral area of ear), nose (centre of hairless nose area) and eye,
which included the eye per se, plus approximately 1 cm of surrounding skin to include the lachrymal gland plus the tear duct.
The change of temperatures in these areas, or the delta T values, for the BVDV-inoculated calves over the first 10 d of the
trial were as follows: nose, 3.5C or 0.35C per day; ear, 3.9C
or 0.4C per day; side, 1.9C or 0.19C per day; dorsal, 1.8C
or 0.18C per day. For all of the above temperature sites, the
changes were significantly different (P < 0.05) from the preinoculation temperatures at approximately 45 dpi. All inoculated animals responded to the infection. Notable in the present
study was the observation that the orbital temperatures in the
BVDV-inoculated calves (Table 3) displayed the earliest, most
consistent, least variable and sensitive increases in temperature
over the first 10 d of the trial or until the clinical scores indicated a physical response to the disease. This pattern is shown
in Fig. 1. Quantitatively, this amounted to a total temperature
change of 2.6C or 0.26C per day. Of interest also was that
these changes in orbital temperature were significantly different from the pre-inoculation levels as early as day 1 (P < 0.05).
Furthermore, orbital temperatures tended to be less variable
(lower SD) than temperatures from other anatomical areas
(Tables 4 and 5). The rectal temperatures in the BVDV-inoculated calves (Table 3) also indicated fever due to infection.
Similar changes did not occur in the control animals. Orbital
mean delta T value for control animals from days 0 to 10 was
77
Table 4. Infrared radiated temperatures for the nose, ear and dorsal areas of BVD-infected calves . Data are the least squares means SE of the
least squares means
Day postBVD induction
Nose mean
IR temp
0
1
2
3
4
5
6
7
8
9
10
29.21a
29.34a
29.43a
29.96a
30.73a
30.88b
31.25b
32.69bc
32.90bc
32.83bc
32.77bc
Nose
mean SE
Ear mean
IR temp.
Ear mean SE
0.41
0.40
0.40
0.40
0.41
0.40
0.40
0.41
0.40
0.41
0.40
22.38a
22.42a
23.29a
23.19a
23.79a
24.11ab
24.60ab
24.87ab
25.37b
23.93ab
26.28b
0.96
0.96
0.96
0.96
0.96
0.96
0.96
0.96
0.96
0.96
0.96
Dorsal
mean IR temp
22.29a
22.74a
23.04ab
22.44a
23.08ab
22.70a
22.75a
22.95ab
23.54b
23.06b
24.08b
Dorsal
mean SE
0.34
0.34
0.34
0.34
0.34
0.34
0.34
0.34
0.34
0.34
0.34
ac Means within columns with different letters are statistically different at P < 0.05.
Salivary IgA
(mg mL1)
Haptoglobin
(g mL1)
Control
BVD
Control
BVD
Control
BVD
85.7a
70.3
84.7
77.7
115.2b
93.7
96.0
83.7
5.90
1.24a
3.03
3.54
6.34
4.93b
6.25
5.42
<15
<15
<15
<15a
70zx
314
218
803by
zMean for BVD haptoglobin level on day 0 is higher due to a higher level
in one animal.
a,b Means with different letters within rows are significantly different
P < 0.05.
x,y Means with different letters within columns are significantly different
P < 0.05.
display an increased incidence of disease and are subsequently often treated with higher levels of antibiotics.
However, for a host of reasons, the extensive use of antibiotics in animal agriculture is becoming increasingly unacceptable in society (Jones 1998). This use could clearly be
reduced if animals at risk, or expressing the early stages of
an infection, could be identified. This would enable an earlier, more targeted treatment strategy, likely resulting in the
use of less antibiotic product and earlier animal recovery.
Also, as mentioned previously, the early detection of a disease state could be used to remove infected animals from a
herd and/or to establish baseline criteria for when a lot of
animals merited mass treatment and when they did not.
In the current study, an induction model was used to produce disease in the calves. It is clear from the clinical scores
that BVDV inoculation was effective in producing illness
while the control calves remained healthy. Whether the discovery of infection in an animal when using an induction
model is equivalent to the discovery of disease under field
conditions is a relevant question. However, the use of the
induction model has the following advantages: 1. The infectious agent is known both in quantitative and qualitative
terms; 2. The exact time of infection is known; and 3. The
exact stage or progression of the infection is known.
Therefore, as in the present study, two comparisons are possible, namely, comparisons to the same animal pre-induction (animal as its own control) or comparisons to
contemporary, uninfected control animals.
As shown in the current study, conventional clinical scoring or even some biological measurements are often unable
to detect infection at an early stage. In this respect, it was of
interest that none of the biological measurements on their
own, cortisol, salivary IgA and haptoglobin, performed particularly well as definitive early indicators of disease onset.
Both cortisol and IgA are very sensitive indicators of stress
and disease and start to elevate very soon after BVDV inoculation. However, because of this sensitivity these indicators
also tend to be variable or noisy.
By contrast, infrared measurements and changes in these
measurements did respond early in the course of the disease.
Such sensitive changes in infrared thermal radiation would
be consistent with the knowledge that distress- and disease-
78
Day 0
Day 10
Fig. 2. Infrared facial images of a calf before and following infection with BVD virus.
induced changes in HPA activity would be one of the animals first physiological responsesthe so-called Selyenian
alarm reaction (Selye 1956). However, as such, HPA axis
activity is not particularly efficient in terms of energy use.
Therefore, considerable energy will be lost as heat with
much of that (4060%) expressed in the infrared range
(Kleiber 1975).
Data from the current study demonstrate that infrared
thermography can serve as a method for detecting infection
at an early stage. A statistical comparison of the animals
own pre-infection temperature (animal as its own control)
was effective, as was a comparison to a contemporary control (i.e., uninfected) animal or population of animals of the
same species, background and class. In addition, in the present study, we have shown that surface temperature differences of less than 1C are clinically significant. In fact, as
presented by Cook et al. (2002), IRT appear to be one of the
comparatively more sensitive, but perhaps less specific,
techniques for the early detection of disease.
Of interest in the present study also was the observation
that some anatomical scans were more sensitive than others.
For example, it was found that for some of the infrared thermographic images (orbital), significant changes in infrared
temperature were apparent as early as 1 d post-inoculation.
By contrast, significant changes in nose, ear or dorsal
infrared scans did not appear until day 5 or 6 post-induction.
Moreover, those changes in orbital infrared temperatures
appeared several days to 1 wk before many objective laboratory tests such as haptoglobin level and also before
changes in conventional clinical scores. In other words, the
infrared data displayed changes several days to 1 wk before
the current industry best practice of using clinical scores for
evaluation of disease. As discussed by Wittum et al. (1996),
the use of clinical scores alone often results in a large degree
of misclassification. The application of infrared thermography to augment clinical scores may thus be useful.
CONCLUSIONS
Data from the current study demonstrated infrared thermography to be a highly sensitive indicator of thermal changes
79
80