Multicenter study to investigate factors associated with change in rectal temperature during anesthesia in dogs

Stuart C. Clark-Price Department of Clinical Sciences, College of Veterinary Medicine, Auburn University, Auburn, AL 36849.

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Berit L. Fischer Crown Veterinary Specialists & Associates, Lebanon, NJ 08833.

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Kevin L. Kirwin Day Heights Veterinary Clinic, Milford, OH 45150.

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Stephanie C. J. Keating Department of Veterinary Clinical Medicine, College of Veterinary Medicine, University of Illinois, Urbana, IL 61821.

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Adam Auckburally Southern Counties Veterinary Specialists, Ringwood, BH24 3JW, England.

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Derek Flaherty Southern Counties Veterinary Specialists, Ringwood, BH24 3JW, England.

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OBJECTIVE

To determine factors associated with change in rectal temperature (RT) of dogs undergoing anesthesia.

ANIMALS

507 dogs.

PROCEDURES

In a prospective observational study, the RT of dogs undergoing anesthesia at 5 veterinary hospitals was recorded at the time of induction of anesthesia and at the time of recovery from anesthesia (ie, at the time of extubation). Demographic data, body condition score, American Society of Anesthesiologists (ASA) physical status classification, types of procedure performed and medications administered, duration of anesthesia, and use of heat support were also recorded. Multiple regression analysis was performed to determine factors that were significantly associated with a decrease or an increase (or no change) in RT. Odds ratios were calculated for factors significantly associated with a decrease in RT.

RESULTS

Among the 507 dogs undergoing anesthesia, RT decreased in 89% (median decrease, −1.2°C [-2.2°F]; range, −0.1°C to −5.7°C [–0.2°F to −10.3°F]), increased in 9% (median increase, 0.65°C [1.2°F]; range, 0.1°C to 2.1°C [3.8°F]), and did not change in 2%. Factors that significantly predicted and increased the odds of a decrease in RT included lower weight, ASA classification > 2, surgery for orthopedic or neurologic disease, MRI procedures, use of an α2-adrenergic or μ-opioid receptor agonist, longer duration of anesthesia, and higher heat loss rate. Lack of μ-opioid receptor agonist use, shorter duration of anesthesia, and lower heat loss rate were significantly associated with an increase in RT.

CONCLUSIONS AND CLINICAL RELEVANCE

Multiple factors that were associated with a decrease in RT in dogs undergoing anesthesia were identified. Knowledge of these factors may help identify dogs at greater risk of developing inadvertent perianesthetic hypothermia.

OBJECTIVE

To determine factors associated with change in rectal temperature (RT) of dogs undergoing anesthesia.

ANIMALS

507 dogs.

PROCEDURES

In a prospective observational study, the RT of dogs undergoing anesthesia at 5 veterinary hospitals was recorded at the time of induction of anesthesia and at the time of recovery from anesthesia (ie, at the time of extubation). Demographic data, body condition score, American Society of Anesthesiologists (ASA) physical status classification, types of procedure performed and medications administered, duration of anesthesia, and use of heat support were also recorded. Multiple regression analysis was performed to determine factors that were significantly associated with a decrease or an increase (or no change) in RT. Odds ratios were calculated for factors significantly associated with a decrease in RT.

RESULTS

Among the 507 dogs undergoing anesthesia, RT decreased in 89% (median decrease, −1.2°C [-2.2°F]; range, −0.1°C to −5.7°C [–0.2°F to −10.3°F]), increased in 9% (median increase, 0.65°C [1.2°F]; range, 0.1°C to 2.1°C [3.8°F]), and did not change in 2%. Factors that significantly predicted and increased the odds of a decrease in RT included lower weight, ASA classification > 2, surgery for orthopedic or neurologic disease, MRI procedures, use of an α2-adrenergic or μ-opioid receptor agonist, longer duration of anesthesia, and higher heat loss rate. Lack of μ-opioid receptor agonist use, shorter duration of anesthesia, and lower heat loss rate were significantly associated with an increase in RT.

CONCLUSIONS AND CLINICAL RELEVANCE

Multiple factors that were associated with a decrease in RT in dogs undergoing anesthesia were identified. Knowledge of these factors may help identify dogs at greater risk of developing inadvertent perianesthetic hypothermia.

Introduction

Unintentional loss of body heat during anesthesia or IPH is a common complication associated with general anesthesia for most species. The reported incidence of IPH in humans undergoing anesthesia for surgery ranges from 20% to 70%.1,2,3 In a study4 of 1,525 dogs, the prevalence of IPH, defined as a rectal or esophageal temperature < 38.5°C (101.3°F), at the cessation of anesthesia agent delivery was 86.5%. Hypothermia associated with anesthesia can have clinically relevant effects on an animal's health and postanesthesia outcome as a result of disrupted physiologic enzymatic function and homeostasis.5 Among humans and animals that undergo anesthesia and develop hypothermia, morbidity and mortality rates can increase because of impaired pharmacodynamics of administered drugs, surgical site infection and dehiscence, blood loss and coagulopathy, cardiac dysrhythmias and dysfunction, increased physiologic stress, delayed recovery from anesthesia, and increased duration of hospitalization.1,6,7

Minimization of IPH is beneficial and multiple techniques have been used to enhance body heat conservation in anesthetized humans and animals.2,7 In humans, techniques to counter IPH (eg, patient warming prior to anesthesia, application of external heating devices during anesthesia, and minimization of the duration of anesthesia) are based on an understanding of the factors associated with the development of hypothermia during anesthesia. Some of these factors include administration of sedatives (eg, dexmedetomidine), opioids (eg, fentanyl), and certain induction agents (eg, propofol); the person's age; the surface area of exposed skin; sweating; lack of use of active warming devices (eg, forced warm air or circulating water blankets); and use of local anesthetic techniques.8,9,10,11,12,13,14,15,16 Techniques for minimizing IPH used in humans (eg, warming prior to anesthesia and application of airway heat moisture exchangers and forced warm air units) have been investigated in dogs and have been shown to be less effective in that species.7,17,18,19,20,21,22 This may be because factors associated with the development of IPH in dogs have largely been presumed to be similar to those in humans, with little supporting evidence. A greater understanding of the factors associated with the development of IPH in dogs may allow for development of dog-specific techniques for hypothermia management. The objective of the study reported here was to determine risk factors associated with ΔRT among dogs undergoing anesthesia. The hypothesis tested was that age, weight, body condition score, and ASA physical status classification of dogs; type of procedure performed; administration of sedatives and opioids; type of induction agent used; duration of anesthesia; and use of thermal support techniques would have a significant influence on ΔRT in anesthetized dogs.

Materials and Methods

Dogs and data collection

Prior to initiation of this study, the Auburn University Institutional Animal Care and Use Committee was consulted, and it was deemed that review and approval of the study protocol was not necessary because the use of anonymized data collected in the routine treatment of an animal would not be subject to such approval or require informed client consent. Dogs undergoing inhalation anesthesia for any reason at any 1 of 5 veterinary facilities were eligible for enrollment. Of the 5 veterinary facilities, 2 were veterinary teaching hospitals, 2 were private practice specialty veterinary hospitals, and 1 was a high-volume first opinion general veterinary medical clinic. Anesthetic protocols, procedures, and care for each dog was at the discretion of the attending clinician. Dogs were anesthetized in a manner standard for that type of case for each practice. For each dog, RT (in °C) was recorded within 2 minutes of induction of anesthesia (ie, just prior to or immediately after induction of anesthesia) and again immediately after extubation during recovery from anesthesia. All facilities used a similar brand of digital thermometera that was guaranteed by the manufacturer to be accurate within ± 0.2°C (0.4°F) and did not require calibration. For each dog, age, body weight, body condition score (assessed on a 9-point scale), ASA physical status classification, induction agent used, type of procedure performed, use of an α2-adrenergic receptor agonist, administration and type of opioid drugs, use and type of heat support (ie, any supplemental patient warming device used), time of induction of anesthesia, and time of extubation were recorded in addition to RT measurements. Data for each dog were recorded on a data sheet specific for this study and sent to the lead investigator. Along with recorded data, calculations were performed to obtain duration of anesthesia (interval from induction of anesthesia to extubation), ΔRT (RT at induction of anesthesia minus RT at the time of extubation), heat loss rate (ie, heat lost per minute [ΔRT divided by time from induction of anesthesia to extubation in minutes]), and body surface area in m2 (10.1 × body weight0.67 [in g] × 10−4).23

Data handling and statistical analysis

Data sheets for all dogs were examined and those with missing data points or indecipherable entries were excluded from analysis. Data sheets were grouped into 2 categories: a –ΔRT group (evidence of a decrease in RT) or +ΔRT group (evidence of an increase or no change in RT). All data were assessed for normality with a Kolmogorov-Smirnov test. For the independent variables age, body weight, body surface area, body condition score, ASA physical status classification and duration of anesthesia, the numerical value was used for analysis. For the independent variable procedure, dogs were categorized into 1 of 6 procedure groupings as follows: open body cavity, surgery for orthopedic or neurologic disease, dental or maxillofacial procedures, MRI, all other surgical procedures, or all other diagnostic procedures. Dogs undergoing MRI and any additional procedure were placed in the MRI category. For analysis of the independent variable use of an α2-adrenergic receptor agonist (eg, dexmedetomidine), dogs were categorized as having received an α2-adrenergic receptor agonist or having not received an α2-adrenergic receptor agonist. For analysis of the independent variable administration of an opioid drug, dogs were categorized as having received a full μ-opioid receptor agonist (eg, morphine, hydromorphone, methadone, fentanyl, or remifentanil), having received a partial μ-opioid receptor agonist or agonist-antagonist (buprenorphine or butorphanol), or having not received an opioid drug. For analysis of the independent variable induction agent, dogs were categorized as having received a GABA receptor agonist agent (eg, propofol, alfaxalone, or etomidate) for induction of anesthesia or a dissociative agent (eg, ketamine or tiletamine). Dogs receiving induction agents in both categories (ketamine and propofol) were placed in the dissociative agent category. No dogs underwent induction of anesthesia by any other method. For analysis of the independent variable heat support, dogs were categorized as having received active heat support (eg, forced warm air blanket, circulating warm water pad, electric blanket, or heat disk), having received passive heat support (eg, blankets, towels, or bubble wrap), or having received no heat support.

Multiple linear regression analysis was performed on the data for dogs in the –ΔRT group and also on the data for dogs in the +ΔRT group to identify independent variables that were significantly associated with the dependent variable –ΔRT or +ΔRT. Additionally, multicollinearity between independent variables was examined by calculating the R2 value between each independent variable and each of the other independent variables. Multicollinearity was determined to be problematic between 2 independent variables when the R2 value was > 0.75. If problematic multicollinearity was determined, 1 of the 2 variables was removed from the model, and multiple linear regression analysis was performed again.

Independent variables that were found to be significantly predictive of –ΔRT were further analyzed for differences within variable categories. Variables with 2 categories were analyzed with a Mann-Whitney U test and variables with > 2 categories were analyzed with a Kruskal-Wallis test and a post hoc Dunn multiple comparisons test. For determination of categories for continuous data sets (weight and duration of anesthesia), data were graphically plotted against –ΔRT and a polynomial trend line was applied. Categories were then determined on the basis of visual inspection of the trend line changes and changes that were considered clinically relevant. Additionally, in the –ΔRT group, ORs were calculated for the variables that were significantly predictive of –ΔRT. For OR calculations, the median value for the variable of interest in the –ΔRT group was used as the cut score value. Further analysis of independent variables that were significantly predictive of +ΔRT was not performed owing to the small total number of dogs in that group. Data are reported as median (range) for all variables and ORs are reported as the ratio (95% CI). A value of P ≤ 0.05 was considered significant. A statistical software programb was used for all analyses.

Results

A total of 507 data sheets (1/dog) were considered complete and included in the analysis. Twenty-eight data sheets were considered incomplete and discarded. The facility of origin for dogs was fairly evenly distributed with 186 (36%) from the 2 veterinary teaching hospitals, 166 (33%) from the 2 private practice specialty veterinary hospitals, and 155 (31%) from the first opinion general veterinary medical clinic. Dogs had a median age of 6 years (range, 0.25 to 17 years) and a median weight of 21.8 kg (48.0 lb; range, 1.7 to 78 kg [3.7 to 171.6 lb]). On the basis of the difference between RT at induction of anesthesia and RT at the time of extubation for each dog, 450 (89%) dogs were included in the –ΔRT group and 57 (11%) dogs were included in the +ΔRT group (of those dogs, 48 [9%] had an increase in RT and 9 [2%] had no change in RT). For dogs in the –ΔRT group, the median ΔRT was −1.2°C (–2.2°F; range, −0.1°C to −5.7°C [–0.2°F to −10.3°F]). For dogs in the +ΔRT group, the median ΔRT was 0.65°C (1.2°F; range, 0.1°C to 2.1°C [3.8°F]).

In the initial multiple regression analyses, multicollinearity was found to be problematic between the variables body weight and body surface area (R2 = 0.98 for both –ΔRT and +ΔRT). Body surface area was selected for removal from the analyses because it was a calculated variable, whereas weight was an actual value from each dog and considered to be more accurate. On multiple regression analysis, individual dogs’ body weight (P < 0.001) and ASA physical status classification (P = 0.005), procedure performed (P = 0.009), administration of an α2-adrenergic receptor agonist (P = 0.006), use and type of opioid drugs (P = 0.002), duration of anesthesia (P < 0.001), and the heat loss rate (P < 0.001) were significantly associated with –ΔRT. Multiple regression identified independent variables that were significantly associated with +ΔRT, namely lack of use and type of opioid drugs (P < 0.001), duration of anesthesia (P = 0.05), and heat loss rate (P < 0.001).

Results of analyses of data within each of the variables that were significantly predictive of –ΔRT were summarized (Table 1). With regard to weight, dogs were assigned to 1 of 6 categories on the basis of visual inspection of the polynomial trend line, as follows: ≤ 6 kg, > 6 to ≤ 12 kg, > 12 to ≤ 24 kg, > 24 to ≤ 32 kg, > 32 to ≤ 45 kg, and > 45 kg (≤ 13.2 lb, > 13.2 to ≤ 26.4 lb, > 26.4 to ≤ 52.8 lb, > 52.8 to ≤ 70.4 lb, > 70.4 to ≤ 99 lb, and > 99 lb). Weight group and –ΔRT were significantly (P = 0.011) associated. There were significant differences in median –ΔRT between dogs weighing < 12 kg and those weighing 12 to 24 kg. The ASA physical status classification and –ΔRT were significantly (P = 0.006) associated. Median –ΔRT for dogs with an ASA physical status classification of 2 or 3 differed significantly from the value for dogs with an ASA physical status classification of 1. Procedure performed and –ΔRT were significantly (P < 0.001) associated. Median –ΔRT for dogs undergoing a surgical procedure for orthopedic or neurologic disease differed significantly from values for dogs undergoing dental or maxillofacial surgery or other surgery. Significant differences occurred between some procedures groups. For dogs undergoing MRI, median –ΔRT differed from that for dogs undergoing other surgery. Dogs that received an α2-adrenergic receptor agonist had a significantly (P < 0.001) greater median –ΔRT than those that did not. The median –ΔRT for dogs that received a full μ-opioid receptor agonist was significantly greater than that for dogs that received a partial μ-opioid receptor agonist or agonist-antagonist. With regard to duration of anesthesia, dogs were assigned to 1 of 9 categories on the basis of visual inspection of the polynomial trend line, as follows: < 30 minutes, 30 to < 60 minutes, 60 to < 90 minutes, 90 to < 120 minutes, 120 to < 150 minutes, 150 to < 180 minutes, 180 to < 240 minutes, 240 to < 300 minutes, and ≥ 300 minutes. Duration of anesthesia groups and –ΔRT were significantly (P < 0.001) associated. Largely, median –ΔRT for the duration of anesthesia groups of 60 minutes or longer differed significantly from value for the duration of anesthesia group < 30 minutes.

Table 1

Median (range) values of –ΔRT (°C) for dogs undergoing anesthesia at 5 veterinary medical facilities grouped by weight, ASA physical status classification, procedure performed, use of an α2-adrenergic receptor agonist drug, type of opioid drug administered, and duration of anesthesia (time from induction of anesthesia to extubation).

Variable Group No. of dogs −ΔRT
Weight (kg) ≤ 6 53 −1.4 (–0.1 to −5.6)
> 6 to ≤ 12 92 −1.4 (–0.1 to −5.7)
> 12 to ≤ 24 95 −0.9 (–0.1 to −3.3)a,b
> 24 to ≤ 32 99 −1.2 (–0.1 to −4.3)
> 32 to ≤ 45 87 −1.1 (–0.1 to −3.4)
> 45 24 −1.2 (–0.1 to −3.0)
ASA physical status 1 56 −0.6 (–0.1 to −2.8)
2 322 −1.2 (–0.1 to −5.7)c
3 65 −1.4 (–0.1 to −3.7)c
4 7 −2.0 (–0.1 to −3.2)
5 0 NA
Procedure Surgery for orthopedic or neurologic disease 111 −1.6 (–0.1 to −5.7)
MRI 49 −1.5 (–0.1 to −5.3)
Other diagnostic testing 27 −1.4 (–0.1 to −2.6)
Open body cavity procedure 71 −1.2 (–0.1 to −3.7)
Other surgery 127 −0.9 (–0.1 to −2.9)d,e
Dental or maxillofacial procedure 65 −0.9 (–0.1 to −3.3)d
Treatment with an α2-adrenergic receptor agonist drug Yes 150 −1.5 (–0.1 to −5.6)
No 300 −1.1 (–0.1 to −5.7)f
Type of opioid used Full μ-opioid receptor agonist 256 −1.4 (–0.1 to −5.7)
Partial μ-opioid receptor agonist or agonist-antagonist 188 −0.9 (–0.1 to −3.3)g
Did not receive an opioid 6 −1.2 (–0.6 to −1.9)
Duration of anesthesia (min) < 30 42 −0.6 (–0.1 to −2.0)
30 to < 60 83 −0.9 (–0.1 to −2.6)
60 to < 90 53 −1.2 (–0.1 to −3.3)h
90 to < 120 61 −1.5 (–0.1 to −3.7)h,i
120 to < 150 69 −1.5 (–0.1 to −5.6)h,i
150 to < 180 41 −1.9 (–0.3 to −4.7)h,i
180 to < 240 49 −1.5 (–0.1 to −5.7)h,i
240 to < 300 30 −1.3 (–0.1 to −3.4)h
≥ 300 22 −1.5 (–0.1 to −4.4)h

Value is significantly (P ≤ 0.05) different from that for group ≤ 6 kg.

Value is significantly (P ≤ 0.05) different from that for group > 6 to ≤ 12 kg.

Value is significantly (P ≤ 0.05) different from that for group 1.

Value is significantly (P ≤ 0.05) different from that for group surgery for orthopedic or neurologic disease.

Value is significantly (P ≤ 0.05) different from that for group MRI.

Value is significantly (P ≤ 0.05) different from that for group yes.

Value is significantly (P ≤ 0.05) different from that for group full μ-opioid receptor agonist.

Value is significantly (P ≤ 0.05) different from that for group < 30 minutes

Value is significantly (P ≤ 0.05) different from that for group 30 to < 60 minutes.

NA = Not applicable.

Odds ratio data for independent variables that were significantly predictive of –ΔRT were summarized (Table 2). Dogs that were ≤ 6 kg, assigned an ASA status of 3 or 4, undergoing a surgical procedure for orthopedic or neurologic disease or undergoing MRI, receiving an α2-adrenergic receptor or a full μ-opioid receptor agonist, or for which the duration of anesthesia was > 60 minutes had a higher likelihood of having a –ΔRT greater than the median for all dogs undergoing anesthesia (–1.2°C).

Table 2

Odds ratios (95% CI) for independent variables that were significantly predictive of –ΔRT for dogs undergoing anesthesia at 5 veterinary medical facilities.

Variable OR P value*
Weight
 Dogs ≤ 6 kg 1.4 (0.78–2.51) 0.011
ASA physical status classification
 3 or 4 1.62 (0.97–2.72) 0.042
Procedure
 Surgery for orthopedic or neurologic disease or MRI 1.68 (1.15–2.46) 0.009
Use of an α2-adrenergic receptor agonist
 Treated with drug 1.88 (1.27–2.8) 0.002
Type of opioid used
 Full μ-opioid receptor agonist 2.44 (1.66–3.57) < 0.001
Duration of anesthesia
 > 60 min 4.29 (2.72–6.77) < 0.001

A value of P ≤ 0.05 was considered significant.

There were no dogs with ASA physical status classification 5 enrolled in the study.

The median –ΔRT value for all dogs of −1.2°C was used as the cut score for calculations. For a given variable, ORs indicate the odds that a dog in that category will have a –ΔRT greater than the median value (–1.2°C), compared with the odds for dogs in all other categories.

Discussion

The present study was conducted to identify factors associated with ΔRT in 507 dogs undergoing general anesthesia for various procedures. The majority (450 [89%]) of dogs enrolled in the study had a –ΔRT at the conclusion of anesthesia. Additionally, investigated factors that were associated with –ΔRT in dogs during anesthesia included body weight, ASA physical status classification, the procedure performed, treatment with an α2-adrenergic receptor agonist, treatment with and type of opioid used, duration of anesthesia, and heat loss rate. Investigated factors that were not associated with –ΔRT were age, body condition score, induction agent used, and use and type of supplemental warming. For 57 dogs that did not have a –ΔRT, 48 (9%) had an increase and 9 (2%) had no change in RT. Factors associated with +ΔRT included the treatment with and type of opioid drug used, duration of anesthesia, and heat loss rate. However, the total number of dogs that had a +ΔRT was small (n = 48) and data analysis was therefore limited to only multiple regression analysis; thus, the results for dogs with a +ΔRT should be interpreted with caution until further studies investigating causes of increased rectal temperature during anesthesia are performed.

In humans 18 to 40 years of age, normal body temperature is tightly controlled around 36.8°C (range, 36.2°C to 37.5°C [98.2°F; range, 97.2°F to 99.5°F]) and anesthetized humans are considered to be hypothermic when their core body temperature is < 36°C (96.8°F).3,24 This temperature threshold has been defined because of an increase of adverse events associated with body temperatures < 36°C in anesthetized humans.25 Little research has been attempted to identify a similar threshold for anesthetized dogs; thus, there is no defined body temperature for classification of a dog as hypothermic during anesthesia. Arbitrary intervals have been suggested to define mild, moderate, severe, and critical hypothermia in dogs; however, those intervals have not been studied in relation to outcome and their clinical importance is unknown.26 Therefore, in the present study, we decided not to determine the prevalence of hypothermia based on an ill-defined temperature but to report the number of dogs that had a ΔRT in association with studied risk factors.

Body weight was identified as significantly associated with –ΔRT in anesthetized dogs and smaller dogs were at higher risk. This finding was supported by human medical literature that indicates lower body weight as a significant risk factor for IPH.27,28,29 Among humans and animals, smaller physical size, as indicated by low body weight, contributes to a larger surface area-to-body mass ratio, thereby allowing greater cutaneous heat loss.2,7 Additionally, a considerable proportion of body heat is generated as a byproduct of skeletal muscle metabolism, even during anesthesia; thus, animals with small muscle mass may be unable to produce as much heat to help offset heat loss as animals with more muscle mass.17,30

The ASA physical status classification was identified as significantly predictive of –ΔRT in anesthetized dogs, with a higher risk associated with status 2 and 3 versus status 1. Although it seems intuitive that status 4 and 5 dogs would be at higher risk, there were so few dogs classified as status 4 and no dogs classified as status 5 in the present study to make that determination. The ASA physical status classification was designed to assess a patient's status and has some relation to outcomes of anesthesia. It has been shown to be a valuable prognostic tool in small animal veterinary medicine, and patients with an ASA physical status classification > 2 have been shown to have an increased risk of developing hypothermia during anesthesia.31 Such a finding was not unexpected because the severity of systemic disease and metabolic instability, which limits patients’ ability to compensate for loss of body heat, increases as ASA physical status classification increases.

Procedure was identified as significantly associated with –ΔRT in anesthetized dogs. Compared with other types of procedures, dogs undergoing anesthesia for orthopedic or neurologic surgical procedures or that had an anesthetic episode that involved MRI were more likely to have a –ΔRT. The former may be due to the duration of orthopedic procedures or neurologic disease that impairs a patient's ability to initiate heat conservation methods (eg, sympathetic vasoconstriction). The latter may be due to the cold environment associated with MRI suites, long duration of MRI scans, and inability to apply active methods of heat conservation (eg, forced air warmers) because of the magnetic field of the MRI unit. Of interest is that open body cavity procedures (thoracotomy or laparotomy) were not significantly associated with –ΔRT. In 1 study,28 children undergoing a major surgical procedure (penetration or exposure of a body cavity) had lower body temperature than those undergoing a minor procedure (eg, umbilical hernia repair, circumcision, or bronchoscopy). Although data in the present study were not subcategorized by type of orthopedic procedures performed for analysis, different orthopedic procedures in humans have different rates of associated IPH. Patients undergoing total hip replacement procedures have a higher rate of IPH, compared with patients undergoing knee replacement procedures.32 This difference was postulated to be a result of longer procedure time and greater blood loss associated with total hip replacement procedures.32

In the present study, dogs that were administered an α2-adrenergic receptor agonist as part of the anesthetic protocol had a greater –ΔRT than did dogs that were not administered such a drug. α2-Adrenergic receptor agonists, such as dexmedetomidine, induce hypothermia in dogs and humans through inhibition of defenses against heat loss.8,32,33,34 In humans, peripheral vasodilation induced by this class of drugs results in more skin surface heat loss; however, in dogs, α2-adrenergic receptor agonists initially induce vasoconstriction and centralize blood flow.8,34 This may result in cooling of peripheral tissues and a reduction in mucosal RT that results in a lower reading on a thermometer. Additionally, inhibition of supraspinal sympathetic outflow secondary to α2-adrenergic receptor agonist administration may be a mechanism by which vasodilation and peripheral heat loss occurs in dogs subsequent to the initial vasoconstriction.35

In people, opioids, particularly full μ-opioid receptor agonists delivered either systemically or intrathecally, are known to be a risk factor for the development of hypothermia during anesthesia.36,37 In the present study, the type of opioid drug had a role in the development of –ΔRT. The –ΔRT in dogs that received butorphanol (a κ-opioid receptor agonist and μ-opioid receptor antagonist) or buprenorphine (a partial μ-opioid receptor agonist) was significantly less than that in dogs administered a full μ-opioid receptor agonist. Additionally, the OR for dogs administered a full μ-opioid receptor agonist having –ΔRT lower than the median –ΔRT for all dogs was 2.44. The mechanism behind the development of hypothermia after administration of opioid drugs may be a result of a decreased ability of peripheral vasoconstriction for preservation of core body heat and lowering of the thermoregulatory set point in the CNS.9,38

Among the dogs of the present study, duration of anesthesia was identified as a significant risk factor for –ΔRT. Duration of anesthesia > 60 minutes resulted in a risk of a decreased RT greater than the population median of more than 4 times that for dogs with an anesthesia time < 60 minutes. It is expected that most heat will be lost during the initial anesthetic period (approx the first 30 minutes) when vasodilation and redistribution of core heat to the periphery occurs.1 These findings were similar to those of a canine retrospective study4 and human studies1,6,28,29,39 that demonstrate anesthesia time is an important factor in IPH. Limiting anesthesia time may be one of the most important interventions that can be made to minimize IPH.

There were several factors that were found not to be significant in the regression model: age, body condition score, induction agent used, and the type of supplemental warming used. This finding was unexpected as all of these factors have been found to be predictive of IPH in anesthetized humans.1,2,3,6,12,25,28,40

In humans, neonates and those over 60 years of age are at risk for the development of IPH.6,28,40 Neonates have a reduced ability to maintain their core temperature even when environmental conditions are optimized by increasing room temperature or applying warming devices.28 Elderly patients are more likely to develop IPH than are younger adults because of an inability to deploy as vigorous a response to a cooling environment.40 Even with a large number of dogs and a wide range of ages, age was not significantly associated with the development of –ΔRT in the present study. This may have been a reflection of the fact that dogs reach physiologic maturity earlier than humans and consequently may have more mature metabolic processes in place to combat IPH.41,42

Body condition score is a scoring system used to evaluate body fat in dogs and is clinically used in a manner similar to body mass index in humans.43,44 Humans with a low body mass index lose body heat at a greater rate during the early stages of anesthesia (30 to 60 minutes), compared with persons with a high body mass index.27 However, body condition score was not significantly associated with ΔRT in the dogs of the present study.

The choice of induction agent was not identified as a risk factor for –ΔRT in the present study. This was in contrast to findings of other studies involving humans or dogs. In humans, patients that undergo induction of anesthesia with ketamine have a smaller decrease in core temperature, compared with that in patients who undergo induction of anesthesia with propofol, because of less peripheral vasodilation and less heat distribution and loss to the body's periphery.45 In dogs undergoing anesthesia for ovariohysterectomy, dogs receiving propofol for induction of anesthesia have a lower RT and require a longer time to return to normothermia after anesthesia, compared with findings for dogs receiving ketamine.46 In both those human and canine studies,45,46 uniform anesthetic management and a uniform population of patients were used. Dogs in the present study had various disease processes and were anesthetized at different facilities with differences in management that may have negated the heat-conserving effect of ketamine.

An unexpected finding of the present study was that the use of active warming techniques was not identified as a predictive factor for either +ΔRT or –ΔRT in dogs. Active warming techniques include use of devices that apply heat externally to a patient to reduce the skin-to-environment temperature gradient, thereby reducing the rate of body heat loss.7 In humans, forced-air warming blankets are considered the most effective method for active warming, compared with passive insulation or circulating warm water pads, and are most effective for anesthetic periods > 30 minutes.6,47 In dogs, the effectiveness of active warming for conservation of body heat during anesthesia is also known. The use of forced-air warming blankets is superior to passive methods or circulating water blankets but is only effective in patients undergoing anesthesia for > 20 minutes.18 Findings of 1 study22 suggest that warming dogs with resistive heating blankets is more effective than use of forced-air warming blankets; nevertheless, both appear to be helpful. Of note is that the aforementioned studies in dogs were controlled clinical trials; thus, the application of these devices was uniform and they likely were in contact with a large area of the dogs’ bodies. The reason for the difference in results between the controlled studies and the present study may be related to the manner in which the devices were applied in clinical patients. For many surgical cases, the application of heating blankets or pads may interfere with the surgical area; thus, the devices are often placed only partially on the patient, thereby minimizing contact area to a point perhaps below the contact area threshold for clinical effectiveness. Additionally, the present study categorized the use of heat conservation techniques as none, passive, or active and did not investigate whether there were differences among techniques within categories. For example, the use of heat disks and circulating warm water blankets may not be as effective as forced-air warming blankets because of their smaller area of contact area. However, forced-air warming blankets may have reduced efficacy when wet or compressed by sterile drapes or surgical implements. Further research with each technique to determine minimum body contact requirements and performance in clinical settings is warranted.

The present study identified factors associated with –ΔRT in dogs undergoing anesthesia in various clinical settings. However, the R2 in the regression model was only 45.73%, indicating that other noninvestigated factors had a role in the decrease of RT. In humans, some other risk factors for IPH include the use of inhalation anesthetic agents versus total IV anesthesia, the use of local or regional anesthesia, environmental temperature, the temperature of IV fluids or blood products administered, prewarming, and nutritional status of the patient. The design of the present study made it difficult to analyze these and other additional factors; however, such factors should be investigated in future studies as many of the risk factors for humans appear to be similar for canine patients. Nevertheless, of the factors that were investigated in the present study, those associated with –ΔRT in dogs undergoing anesthesia included lower body weight, higher ASA physical status classification, surgery for orthopedic or neurologic disease or MRI, treatment with an α2-adrenergic receptor agonist or pure μ-opioid receptor agonist, and longer duration of anesthesia. Knowledge of these factors may help to implement strategies to minimize heat loss in dogs undergoing anesthesia as well as aid the design of future studies to identify other factors and improve heat loss prevention techniques.

Abbreviations

ΔRT

Change in rectal temperature

–ΔRT

Decrease in rectal temperature

+ΔRT

Increase (or no change) in rectal temperature

ASA

American Society of Anesthesiologists

GABA

γ-Aminobutyric acid

IPH

Inadvertent perianesthetic hypothermia

RT

Rectal temperature

Footnotes

a.

Medical digital thermometer, ANKOVA, London, England.

b.

InStat, version 3.10, GraphPad Software, San Diego, Calif.

References

  • 1.

    Ruetzler K, Kurz A. Consequences of perioperative hypothermia. Handb Clin Neurol 2018;157:687697.

  • 2.

    Forstot RM. The etiology and management of inadvertent perioperative hypothermia. J Clin Anesth 1995;7:657674.

  • 3.

    Hart SR, Bordes B, Hart J, et al. Unintended perioperative hypothermia. Ochsner J 2011;11:259270.

  • 4.

    Redondo JI, Suesta P, Serra I, et al. Retrospective study of the prevalence of postanaesthetic hypothermia in dogs. Vet Rec 2012;171:374.

  • 5.

    Paal P, Brugger H, Strapazzon G. Accidental hypothermia. Handb Clin Neurol 2018;157:547563.

  • 6.

    Torossian A, Bräuer A, Höcker J, et al. Preventing inadvertent perioperative hypothermia. Dtsch Arztebl Int 2015;112:166172.

  • 7.

    Clark-Price S. Inadvertent perianesthetic hypothermia in small animal patients. Vet Clin North Am Small Anim Pract 2015;45:983994.

  • 8.

    Talke P, Tayefeh F, Sessler DI, et al. Dexmedetomidine does not alter the sweating threshold, but comparably and linearly decreases the vasoconstriction and shivering thresholds. Anesthesiology 1997;87:835841.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Kurz A, Go JC, Sessler DI, et al. Alfentanil slightly increases the sweating threshold and markedly reduces the vasoconstriction and shivering thresholds. Anesthesiology 1995;83:293299.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Matsukawa T, Kurz A, Sessler DI, et al. Propofol linearly reduces the vasoconstriction and shivering thresholds. Anesthesiology 1995;82:11691180.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Ozaki M, Sessler DI, Matsukawa T, et al. The threshold for thermoregulatory vasoconstriction during nitrous oxide/sevoflurane anesthesia is reduced in the elderly. Anesth Analg 1997;84:10291033.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Lenhardt R. Body temperature regulation and anesthesia. Handb Clin Neurol 2018;157:635644.

  • 13.

    Lopez M, Sessler DI, Walter K, et al. Rate and gender dependence of the sweating, vasoconstriction, and shivering thresholds in humans. Anesthesiology 1994;80:780788.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Yoo HS, Park SW, Yi JW, et al. The effect of forced-air warming during arthroscopic shoulder surgery with general anesthesia. Arthroscopy 2009;25:510514.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Hasegawa K, Negishi C, Nakagawa F, et al. Core temperatures during major abdominal surgery in patients warmed with new circulating-water garment, forced-air warming, or carbon-fiber resistive-heating system. J Anesth 2012;26:168173.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Joris J, Ozaki M, Sessler DI, et al. Epidural anesthesia impairs both central and peripheral thermoregulatory control during general anesthesia. Anesthesiology 1994; 80:268277.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Clark-Price SC, Phillips H, Selmic LE, et al. Effect of an intraoperative infusion of amino acids on body temperature, serum biochemistry, serum insulin and recovery variables in healthy dogs undergoing ovariohysterectomy. Vet Rec 2018;183:191.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Clark-Price SC, Dossin O, Jones KR, et al. Comparison of three different methods to prevent heat loss in healthy dogs undergoing 90 minutes of general anesthesia. Vet Anaesth Analg 2013;40:280284.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Khenissi L, Covey-Crump G, Knowles TG, et al. Do heat and moisture exchangers in the anaesthesia breathing circuit preserve body temperature in dogs undergoing anaesthesia for magnetic resonance imaging? Vet Anaesth Analg 2017;44:452460.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Rigotti CF, Jolliffe CT, Leece EA. Effect of prewarming on the body temperature of small dogs undergoing inhalation anesthesia. J Am Vet Med Assoc 2015;247:765770.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Thompson KR, MacFarlane PD. Effect of irrigation fluid temperature on body temperature during arthroscopic elbow surgery in dogs. Open Vet J 2013;3:114120.

    • Search Google Scholar
    • Export Citation
  • 22.

    Kibanda JO, Gurney M. Comparison of two methods for the management of intraoperative hypothermia in dogs. Vet Rec 2012;170:392.

  • 23.

    Gustafson DL, Page RL. Cancer chemotherapy. In: Withrow SJ, Vail DM, Page RL, eds. Withrow and MacEwen's small animal clinical oncology. 5th ed. St Louis: Elsevier Saunders, 2013;157179.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Mackowiak PA, Wasserman SS, Levine MM. A critical appraisal of 98.6°F, the upper limit of the normal body temperature, and other legacies of Carl Reinhold August Wunderlich. JAMA 1992;268:15781580.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Sessler DI. Mild perioperative hypothermia. N Engl J Med 1997;336:17301737.

  • 26.

    Brodeur A, Wright A, Cortes Y. Hypothermia and targeted temperature management in cats and dogs. J Vet Emerg Crit Care (San Antonio) 2017;27:151163.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Groene P, Zeuzem C, Baasner S, et al. The influence of body mass index on temperature management during general anaesthesia-A prospective observational study. J Eval Clin Pract 2019;25:340345.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Lai LL, See MH, Rampal S, et al. Significant factors influencing inadvertent hypothermia in pediatric anesthesia. J Clin Monit Comput 2019;33:11051112.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    National Collaborating Centre for Nursing and Supportive Care (UK). The management of inadvertent perioperative hypothermia in adults [Internet]. London: Royal College of Nursing (UK); 2008 Apr. (NICE Clinical Guidelines, No. 65.) Available at: www.ncbi.nlm.nih.gov/books/NBK53797/. Accessed May 7, 2019.

    • Search Google Scholar
    • Export Citation
  • 30.

    Hall JE. Body temperature regulation, and fever. In: Hall JE, ed. Guyton and Hall textbook of medical physiology. 12th ed. Philadelphia: Elsevier, 2011;867877.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Portier K, Ida KK. The ASA physical status classification: what is the evidence for recommending its use in veterinary anesthesia?—A systematic review. Front Vet Sci 2018;5:204.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Frisch NB, Pepper AM, Rooney E, et al. Intraoperative hypothermia in total hip and knee arthroplasty. Orthopedics 2017;40:5663.

  • 33.

    Delaunay L, Bonnet F, Liu N, et al. Clonidine comparably decreases the thermoregulatory thresholds for vasoconstriction and shivering in humans. Anesthesiology 1993;79:470474.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Granholm M, McKusick BC, Westerholm FC, et al. Evaluation of the clinical efficacy and safety of intramuscular and intravenous doses of dexmedetomidine and medetomidine in dogs and their reversal with atipamezole. Vet Rec 2007;160:891897.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Sabbe MB, Penning JP, Ozaki GT, et al. Spinal and systemic action of the alpha 2 receptor agonist dexmedetomidine in dogs. Antinociception and carbon dioxide response. Anesthesiology 1994;80:10571072.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Mendonça FT, Lucena MC, Quirino RS, et al. Risk factors for postoperative hypothermia in the post-anesthetic care unit: a prospective prognostic pilot study [in Portuguese]. Rev Bras Anestesiol 2019;69:122130.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Ryan KF, Price JW, Warriner CB, et al. Persistent hypothermia after intrathecal morphine: case report and literature review. Can J Anaesth 2012;59:384388.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Spencer RL, Hruby VJ, Burks TF. Alteration of thermoregulatory set point with opioid agonists. J Pharmacol Exp Ther 1990;252:696705.

  • 39.

    Kongsayreepong S, Chaibundit C, Chadpaibool J, et al. Predictor of core hypothermia and the surgical intensive care unit. Anesth Analg 2003;96:826833.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Kurz A, Plattner O, Sessler DI, et al. The threshold for thermoregulatory vasoconstriction during nitrous oxide/sevoflurane anesthesia is lower in elderly than in young patients. Anesthesiology 1993;79:465469.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41.

    Hawthorne AJ, Booles D, Nugent PA, et al. Body-weight changes during growth in puppies of different breeds. J Nutr 2004; 134:2027S2030S.

  • 42.

    Wood CL, Lane LC, Cheetham T. Puberty: normal physiology (brief overview). Best Pract Res Clin Endocrinol Metab 2019;33:101265.

  • 43.

    Mawby DI, Bartges JW, d'Avignon A, et al. Comparison of various methods for estimating body fat in dogs. J Am Anim Hosp Assoc 2004;40:109114.

  • 44.

    Okorodudu DO, Jumean MF, Montori VM, et al. Diagnostic performance of body mass index to identify obesity as defined by body adiposity: a systematic review and meta-analysis. Int J Obes (Lond) 2010;34:791799.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Ikeda T, Kazama T, Sessler DI, et al. Induction of anesthesia with ketamine reduces the magnitude of redistribution hypothermia. Anesth Analg 2001;93:934938.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46.

    Bornkamp JL, Roberston S, Isaza NM, et al. Effects of anesthetic induction with a benzodiazepine plus ketamine hydrochloride or propofol on hypothermia in dogs undergoing ovariohysterectomy. Am J Vet Res 2016;77:351357.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47.

    Nieh HC, Su SF. Meta-analysis: effectiveness of forced-air warming for prevention of perioperative hypothermia in surgical patients. J Adv Nurs 2016;72:22942314.

    • Crossref
    • Search Google Scholar
    • Export Citation

Contributor Notes

Address correspondence to Dr. Clark-Price (scc0066@auburn.edu).
  • 1.

    Ruetzler K, Kurz A. Consequences of perioperative hypothermia. Handb Clin Neurol 2018;157:687697.

  • 2.

    Forstot RM. The etiology and management of inadvertent perioperative hypothermia. J Clin Anesth 1995;7:657674.

  • 3.

    Hart SR, Bordes B, Hart J, et al. Unintended perioperative hypothermia. Ochsner J 2011;11:259270.

  • 4.

    Redondo JI, Suesta P, Serra I, et al. Retrospective study of the prevalence of postanaesthetic hypothermia in dogs. Vet Rec 2012;171:374.

  • 5.

    Paal P, Brugger H, Strapazzon G. Accidental hypothermia. Handb Clin Neurol 2018;157:547563.

  • 6.

    Torossian A, Bräuer A, Höcker J, et al. Preventing inadvertent perioperative hypothermia. Dtsch Arztebl Int 2015;112:166172.

  • 7.

    Clark-Price S. Inadvertent perianesthetic hypothermia in small animal patients. Vet Clin North Am Small Anim Pract 2015;45:983994.

  • 8.

    Talke P, Tayefeh F, Sessler DI, et al. Dexmedetomidine does not alter the sweating threshold, but comparably and linearly decreases the vasoconstriction and shivering thresholds. Anesthesiology 1997;87:835841.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 9.

    Kurz A, Go JC, Sessler DI, et al. Alfentanil slightly increases the sweating threshold and markedly reduces the vasoconstriction and shivering thresholds. Anesthesiology 1995;83:293299.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 10.

    Matsukawa T, Kurz A, Sessler DI, et al. Propofol linearly reduces the vasoconstriction and shivering thresholds. Anesthesiology 1995;82:11691180.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 11.

    Ozaki M, Sessler DI, Matsukawa T, et al. The threshold for thermoregulatory vasoconstriction during nitrous oxide/sevoflurane anesthesia is reduced in the elderly. Anesth Analg 1997;84:10291033.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 12.

    Lenhardt R. Body temperature regulation and anesthesia. Handb Clin Neurol 2018;157:635644.

  • 13.

    Lopez M, Sessler DI, Walter K, et al. Rate and gender dependence of the sweating, vasoconstriction, and shivering thresholds in humans. Anesthesiology 1994;80:780788.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 14.

    Yoo HS, Park SW, Yi JW, et al. The effect of forced-air warming during arthroscopic shoulder surgery with general anesthesia. Arthroscopy 2009;25:510514.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 15.

    Hasegawa K, Negishi C, Nakagawa F, et al. Core temperatures during major abdominal surgery in patients warmed with new circulating-water garment, forced-air warming, or carbon-fiber resistive-heating system. J Anesth 2012;26:168173.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 16.

    Joris J, Ozaki M, Sessler DI, et al. Epidural anesthesia impairs both central and peripheral thermoregulatory control during general anesthesia. Anesthesiology 1994; 80:268277.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 17.

    Clark-Price SC, Phillips H, Selmic LE, et al. Effect of an intraoperative infusion of amino acids on body temperature, serum biochemistry, serum insulin and recovery variables in healthy dogs undergoing ovariohysterectomy. Vet Rec 2018;183:191.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 18.

    Clark-Price SC, Dossin O, Jones KR, et al. Comparison of three different methods to prevent heat loss in healthy dogs undergoing 90 minutes of general anesthesia. Vet Anaesth Analg 2013;40:280284.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 19.

    Khenissi L, Covey-Crump G, Knowles TG, et al. Do heat and moisture exchangers in the anaesthesia breathing circuit preserve body temperature in dogs undergoing anaesthesia for magnetic resonance imaging? Vet Anaesth Analg 2017;44:452460.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 20.

    Rigotti CF, Jolliffe CT, Leece EA. Effect of prewarming on the body temperature of small dogs undergoing inhalation anesthesia. J Am Vet Med Assoc 2015;247:765770.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 21.

    Thompson KR, MacFarlane PD. Effect of irrigation fluid temperature on body temperature during arthroscopic elbow surgery in dogs. Open Vet J 2013;3:114120.

    • Search Google Scholar
    • Export Citation
  • 22.

    Kibanda JO, Gurney M. Comparison of two methods for the management of intraoperative hypothermia in dogs. Vet Rec 2012;170:392.

  • 23.

    Gustafson DL, Page RL. Cancer chemotherapy. In: Withrow SJ, Vail DM, Page RL, eds. Withrow and MacEwen's small animal clinical oncology. 5th ed. St Louis: Elsevier Saunders, 2013;157179.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 24.

    Mackowiak PA, Wasserman SS, Levine MM. A critical appraisal of 98.6°F, the upper limit of the normal body temperature, and other legacies of Carl Reinhold August Wunderlich. JAMA 1992;268:15781580.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 25.

    Sessler DI. Mild perioperative hypothermia. N Engl J Med 1997;336:17301737.

  • 26.

    Brodeur A, Wright A, Cortes Y. Hypothermia and targeted temperature management in cats and dogs. J Vet Emerg Crit Care (San Antonio) 2017;27:151163.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 27.

    Groene P, Zeuzem C, Baasner S, et al. The influence of body mass index on temperature management during general anaesthesia-A prospective observational study. J Eval Clin Pract 2019;25:340345.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 28.

    Lai LL, See MH, Rampal S, et al. Significant factors influencing inadvertent hypothermia in pediatric anesthesia. J Clin Monit Comput 2019;33:11051112.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 29.

    National Collaborating Centre for Nursing and Supportive Care (UK). The management of inadvertent perioperative hypothermia in adults [Internet]. London: Royal College of Nursing (UK); 2008 Apr. (NICE Clinical Guidelines, No. 65.) Available at: www.ncbi.nlm.nih.gov/books/NBK53797/. Accessed May 7, 2019.

    • Search Google Scholar
    • Export Citation
  • 30.

    Hall JE. Body temperature regulation, and fever. In: Hall JE, ed. Guyton and Hall textbook of medical physiology. 12th ed. Philadelphia: Elsevier, 2011;867877.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 31.

    Portier K, Ida KK. The ASA physical status classification: what is the evidence for recommending its use in veterinary anesthesia?—A systematic review. Front Vet Sci 2018;5:204.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 32.

    Frisch NB, Pepper AM, Rooney E, et al. Intraoperative hypothermia in total hip and knee arthroplasty. Orthopedics 2017;40:5663.

  • 33.

    Delaunay L, Bonnet F, Liu N, et al. Clonidine comparably decreases the thermoregulatory thresholds for vasoconstriction and shivering in humans. Anesthesiology 1993;79:470474.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 34.

    Granholm M, McKusick BC, Westerholm FC, et al. Evaluation of the clinical efficacy and safety of intramuscular and intravenous doses of dexmedetomidine and medetomidine in dogs and their reversal with atipamezole. Vet Rec 2007;160:891897.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 35.

    Sabbe MB, Penning JP, Ozaki GT, et al. Spinal and systemic action of the alpha 2 receptor agonist dexmedetomidine in dogs. Antinociception and carbon dioxide response. Anesthesiology 1994;80:10571072.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 36.

    Mendonça FT, Lucena MC, Quirino RS, et al. Risk factors for postoperative hypothermia in the post-anesthetic care unit: a prospective prognostic pilot study [in Portuguese]. Rev Bras Anestesiol 2019;69:122130.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 37.

    Ryan KF, Price JW, Warriner CB, et al. Persistent hypothermia after intrathecal morphine: case report and literature review. Can J Anaesth 2012;59:384388.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 38.

    Spencer RL, Hruby VJ, Burks TF. Alteration of thermoregulatory set point with opioid agonists. J Pharmacol Exp Ther 1990;252:696705.

  • 39.

    Kongsayreepong S, Chaibundit C, Chadpaibool J, et al. Predictor of core hypothermia and the surgical intensive care unit. Anesth Analg 2003;96:826833.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 40.

    Kurz A, Plattner O, Sessler DI, et al. The threshold for thermoregulatory vasoconstriction during nitrous oxide/sevoflurane anesthesia is lower in elderly than in young patients. Anesthesiology 1993;79:465469.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 41.

    Hawthorne AJ, Booles D, Nugent PA, et al. Body-weight changes during growth in puppies of different breeds. J Nutr 2004; 134:2027S2030S.

  • 42.

    Wood CL, Lane LC, Cheetham T. Puberty: normal physiology (brief overview). Best Pract Res Clin Endocrinol Metab 2019;33:101265.

  • 43.

    Mawby DI, Bartges JW, d'Avignon A, et al. Comparison of various methods for estimating body fat in dogs. J Am Anim Hosp Assoc 2004;40:109114.

  • 44.

    Okorodudu DO, Jumean MF, Montori VM, et al. Diagnostic performance of body mass index to identify obesity as defined by body adiposity: a systematic review and meta-analysis. Int J Obes (Lond) 2010;34:791799.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 45.

    Ikeda T, Kazama T, Sessler DI, et al. Induction of anesthesia with ketamine reduces the magnitude of redistribution hypothermia. Anesth Analg 2001;93:934938.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 46.

    Bornkamp JL, Roberston S, Isaza NM, et al. Effects of anesthetic induction with a benzodiazepine plus ketamine hydrochloride or propofol on hypothermia in dogs undergoing ovariohysterectomy. Am J Vet Res 2016;77:351357.

    • Crossref
    • Search Google Scholar
    • Export Citation
  • 47.

    Nieh HC, Su SF. Meta-analysis: effectiveness of forced-air warming for prevention of perioperative hypothermia in surgical patients. J Adv Nurs 2016;72:22942314.

    • Crossref
    • Search Google Scholar
    • Export Citation

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