Slov Vet Res | Vol 60 No 1 | 9 Suitability of Alternatives to Rectal Temperature Measurements in Pet Rodents, Rabbits and Ferrets: A Literature Review Key words rectal temperature, rodents, rabbits, ferrets, alternatives Jelle Stans Institute for Globally Distributed Open Research and Education, Beringen, Belgium *Corresponding author: jelle.stans@igdore.org Abstract: Body temperature is a vital parameter to assess the health of exotic animals. Rectal thermometry is a common way to measure body temperature in rodents, rabbits and ferrets and often considered the gold standard. However, taking a rectal tempera- ture often involves restraint and can lead to stress in these animals. To avoid the stress of rectal temperature measurements, alternative (often less invasive) techniques have been utilized in several species. These methods include tympanic thermometry, axillary thermometry and infrared thermography. It is however important to establish whether these strategies yield comparable readings to the gold standard. Therefore, a literature review was performed using the MedLine and Google Scholar databases. Base terms referring to rectal temperature and thermometry were combined with species-specific search terms. Relatively few studies were identified about alternatives to rectal tempera- ture measurements in rodents, rabbits and ferrets. In general, it can be noted that only transponder measurements have repeatedly been described to be a valid alternative to rectal temperature measurement. Further research should be conducted. Received: 14 November 2022 Accepted: 8 March 2023 DOI 10.26873/SVR-1640-2023 UDC 612.56:536.5:636.045:636.932 Pages: 9–14 Review Article Introduction Body temperature is a vital parameter to assess the health of exotic animals (1). An elevated body temperature can signal an infection or systemic inflammation (2) while hy- pothermia may, for example, arise as a complication as a complication of general anaesthesia and surgery (3). In ro- dents and rabbits, body temperature was shown to be of prognostic value in a clinical setting (4, 5). Rectal thermometry is a common way to measure body temperature in rodents (6), rabbits (7) and ferrets (8) and of- ten considered the gold standard. However, taking a rectal temperature often involves restraint and can lead to stress in these animals (9, 10). This can, amongst others, impact the readings (11). To avoid the stress of rectal temperature measurements, alternative (often less invasive) techniques have been uti- lized in several species. These methods include tympanic thermometry (12), axillary thermometry (13) and infrared thermography (14). It is however important to establish whether these strategies yield comparable readings to the gold standard. In cats and dogs, such studies have been conducted suggesting that alternative methods are not always a good replacement for rectal thermometry (14, 15). In rodents, rabbits and ferrets, the body of literature comparing temperature measurement seems to be limited while this is a particularly important topic because of the stress-inducing consequences of rectal thermometry. Therefore, the aim of the current review article is to sum- marize the non-invasive temperate measure methods in- vestigated in pet rodents, rabbits and ferrets and assess whether they are a suitable alternative to rectal tempera- ture measurement. Additionally, suggestions for further re- search are formulated. SloVetRes_NOTRANJOST ver2.indd 9 09/05/2023 10:14 10 | Slov Vet Res | Vol 60 No 1 Search strategy and inclusion Between the 3rd and 5th of September 2022, the MedLine database was searched through Pubmed. The base term “(“rect*”) AND ((“temp*”) OR (“therm*”))” was combined with species-specific terms: “AND ((“guinea pig*”) OR (“cavy”) OR (“cavies”))”, “AND ((“mouse*”) OR (“mice”))”, “AND ((“rat”) OR (“rats”))”, “AND (“hamster*”)”, “AND (“ger- bil*”)”, “AND (“degu*”)”, “AND (“chinchilla*”)”, “AND (“rab- bit*”)” and “AND (“ferret*”)”. Google Scholar was searched during the same period with the base term “rectal tempera- ture” combined with the following species-specific terms: “guinea pig*”, “mice”, “rat*”, “hamster*”, “gerbil*”, “degu*”, “chinchilla*”, “rabbit*” and “ferret*”. The titles of the publications in the search results were screened for papers that could be eligible for inclusion. The abstracts of potentially eligible publications were read and included if (1) they described a comparison between rectal temperature measurement and at least one non-invasive method, (2) described agreement between rectal measure- ment and a non-invasive method and (3) the study was conducted in at least one eligible species (rodent, ferret or rabbit). Characteristics of included studies The searches yielded eligible studies for guinea pigs (3 studies, 16-18), mice (5 studies; 16, 19-22), rats (4 studies; 9, 19, 23-24), chinchillas (1 study, 25), rabbits (3 studies; 7, 16, 26) and ferrets (3 studies; 8, 27, 28). No eligible studies were identified for hamsters, gerbils and degus. The included studies and important characteristics are shown in table 1. All publications described prospective studies of multiple animals with sample sizes ranging from 6 to 48. Studies were conducted in both healthy animals and patients. In selected studies, there was a focus on laboratory animals. Publication dates ranged from 1997 and 2021, but it is clear that a significant number was published over 15 years ago. Suitability of alternative methods per species In Guinea pigs, two studies (16,17) investigated the use of transponders to measure body temperature, with mixed re- sults. Both studies were conducted in an experimental set- ting using animals raised as laboratory animals. One study mentioned it to be a valid alternative to rectal temperature (17) while the other mentioned it was not (16). Other meth- ods compared to rectal temperatures were tympanic, laser, axillary and inguinal thermometry (4, 17, 18). None of these methods were mentioned to be a valid alternative for rec- tal temperature measurement. The authors of the second study (17) mentioned that the transponder system they used made sounds that may be disturbing to the guinea pigs. Additionally, they stated that due to the hand-held na- ture of non-contact thermometers, it is difficult to obtain measurements from a comparable distance. In mice, microchip transponders were also investigated, both subcutaneously and intraperitoneally (16, 19). One of these studies reported subcutaneously and intraperitoneal transponders to be a valid alternative to rectal temperature measurement (19). One study also mentioned infrared ther- mometry of the ear and back skin to be a valid alternative (20). They also stated that this technique allows skin tem- perature to be measured easily at these sites. Other strate- gies were not deemed a suitable alternative in all cases (20, 21, 22). All of these studies were performed in laboratory animals. In rats, microchip transponders (intraperitoneally and sub- cutaneously) and (temperature-sensitive) telemetry were deemed to be usable alternatives to rectal thermometry (9,19, 23, 24). However, as stated above, it is important to assess whether the specific detection method does not disturb the animals. Additionally, the telemetry was only in- vestigated in a research setting (9, 23). This means it should be assessed whether these results can be translat- ed to the clinic. Finally, all of these studies were performed in laboratory rats. Human and veterinary thermometers were investigated as an alternative to rectal temperature measurement in chin- chillas (25). Unfortunately, both methods were deemed un- satisfactory. In this case, the studies were also conducted in an experimental setting. The animals were sourced from breeding facilities. Thermography was assessed in the eye, inner ear, external ear and nose of rabbits (26). The publica- tion mentioned that this was an effective tool to measure the temperature of several regions. However, this is not the same as being a reliable alternative for body temperature measurement in a clinical setting. Implantable microchip transponders were mentioned as a suitable alternative (7). Noncontact infrared thermometer (ear and thigh) and tympanic thermometer (human and veterinary) were not a replacement for rectal temperature measurement (7). All of these studies were performed in a research setting with laboratory animals. In ferrets, microchip transponder thermometry was men- tioned as an alternative to rectal temperature measurement (8). Paediatric and veterinary auricular, axillary, dorsal skin, inguinal, noncontact infrared and tympanic thermometry were not deemed to be alternatives (27, 28). One study (27) was conducted in animals presented within a clinical set- ting. The other studies were conducted in an experimental setting in laboratory animals. Discussion Relatively few studies have been published about alterna- tives to rectal temperature measurements in rodents, rab- bits and ferrets. The internal and external validity of the pub- lished studies also leaves room for improvement. In general, it can be noted that only transponder measurements have SloVetRes_NOTRANJOST ver2.indd 10 09/05/2023 10:14 Slov Vet Res | Vol 60 No 1 | 11 repeatedly been described to be a valid alternative to rectal temperature measurement. It is clear that there is a difference in number of studies per species. One potential reason for the higher number of stud- ies in mice and rats is that they are often used as laboratory animals. Temperature measurements are often performed in animal experiments (6) and need to be reliable and not be impacted by stress-induced responses. This may stimulate research into this area, which can be translated into clinical practice. Further research is needed to address the lack of studies in hamsters, gerbils and degus. Table 1: Study design of includes studies Reference Title Study design Sample size Database Guinea pigs Hartinger et al., 2003 Suitability of temperature-sensitive transponders to measure body temperature during animal experiments required for regulatory tests Prospective 10 PubMed Devalle, 2005 Comparison of tympanic, transponder, and noncontact infrared laser thermometry with rectal thermometry with rectal thermometry in strain 13 Guinea pigs (Cavia porcellus) Prospective 28 PubMed Google Scholar Levy et al., 2020 Comparison of axillary and inguinal body temperature to rectal temperature in healthy guinea pigs (Cavia porcellus) Prospective 40 Google Scholar Mice Kort et al., 1997 A microchip implant system as a method to determine body temperature of terminally ill rats and mice Prospective 10 PubMed Google Scholar Hartinger et al., 2003 Suitability of temperature-sensitive transponders to measure body temperature during animal experiments required for regulatory tests Prospective 12 PubMed Saegusa and Tabata, 2003 Usefulness of infrared thermometry in determining body temperature in mice Prospective 6 PubMed Newsom et al., 2004 Comparison of body surface temperature measurement and conventional methods for measuring temperature in the mouse Prospective 12 PubMed Google Scholar Fiebig et al., 2018 Evaluation of Infrared thermography for temperature measurement for temperature measurement in adult male NMRI nude mice Prospective 10 PubMed Rats Dilsaver et al., 1992 Measurement of temperature in the rat by rectal probe and telemetry yields compatible results Prospective 12 PubMed Google Scholar Kort et al., 1997 A microchip implant system as a method to determine body temperature of terminally ill rats and mice Prospective 30 PubMed Google Scholar Eshraghi et al., 2005 Cochlear temperature correlates with both temporalis muscle and rectal temperatures. Application for testing the otoprotective effect of hypothermia Prospective 6 PubMed Google Scholar Dangarembizi et al., 2017 Measurement of body temperature in normothermic and febrile rats: Limitations of using rectal thermometry Prospective 31 PubMed Google Scholar Hamsters Gerbils Degus Chinchillas Ozawa et al., 2017 Comparison of rectal and tympanic thermometry in chinchillas (Chinchilla lanigera) Prospective 47 PubMed Google Scholar Rabbits Hartinger et al., 2003 Suitability of temperature-sensitive transponders to measure body temperature during animal experiments required for regulatory tests Prospective 10 PubMed Chen and White, 2006 Comparison of rectal, microchip transponder, and infrared thermometry techniques for obtaining body temperature in the laboratory rabbit (Oryctolagus cuniculus) Prospective 46 PubMed Google Scholar Jaén-Téllez et al., 2021 Relationship between rectal temperature measured with a conventional thermometer and the temperature of several body regions measured by infrared thermography in fat- tening rabbits. Influence of different environmental factors Prospective 48 Google Scholar Ferrets Maxwell et al., 2016 Comparison of digital rectal and microchip transponder thermometry in ferrets (Mustela putorius furo) Prospective 16 PubMed Google Scholar Aguilar et al., 2018 Comparison of body temperature acquired via auricular and rectal methods in ferrets Prospective 27 Google Scholar Keeney et al., 2020 Comparison of body temperature using digital, infrared, and tympanic thermometry in healthy ferrets (Mustela putorius furo) Prospective 20 Google Scholar SloVetRes_NOTRANJOST ver2.indd 11 09/05/2023 10:14 12 | Slov Vet Res | Vol 60 No 1 Table 2: Data extracted from included studies Reference Alternative temperature measurement method Agreement metric with rectal measurement Valid alternative for rectal measurement according to publication? Guinea pigs Hartinger et al., 2003 Implanted temperature-sensitive transponders Only graphically No Devalle, 2005 Tympanic thermometer 0.3956 intraclass correlation coefficient No Devalle, 2005 Laser 0.1229 intraclass correlation coefficient No Devalle, 2005 Transponder 0.5880 intraclass correlation coefficient Yes Levy et al., 2020 Axillary difference of mean -0.39 (95% CI -0.54 - -0.23) No Levy et al., 2021 Inguinal difference of mean was -0.73 (95% CI -0.94 - -0.52) No Mice Kort et al., 1997 Microship transponder (subcutaneous) differences within ± 0.5°C Yes Kort et al., 1997 Microship transponder (intraperitoneally) differences within ± 0.5°C Yes Hartinger et al., 2003 Implanted temperature-sensitive transponders Only graphically No Saegusa and Tabata, 2003 Infrared thermometry (ear) correlation r = 0.95 Yes Saegusa and Tabata, 2003 Infrared thermometry (back skin) correlation r = 0.96 Yes Saegusa and Tabata, 2003 Infrared thermometry (tail skin) correlation r = 0.59 No Saegusa and Tabata, 2003 Infrared thermometry (sole skin) correlation r = 0.59 No Newsom et al., 2004 Surface temperature measurements correlation r = 0.9773 No Newsom et al., 2004 Telemetry correlation r = 0.9699 No Fiebig et al., 2018 Infrared Thermography/Camera mean difference of 0.56 °C Yes* (in nude mice) Rats Dangarembizi et al., 2017 Temperature-sensitive radiotelemeters (intraperitoneally) rectal 0.5°C lower or 0.7°C greater than radiotelemeter Yes* (but investigated for research setting) Eshraghi et al., 2005 Cochlear temperature Correlation r = 0.959 No Kort et al., 1997 Microship transponder (subcutaneous) differences within ± 0.5°C Yes Kort et al., 1997 Microship transponder (intraperitoneally) differences within ± 0.5°C Yes Dilsaver et al., 1992 Telemetry after salicylate r = +0.83, after oxotremorine r = +0.93 Yes* (but investigated for research setting) Hamsters Gerbils Degus Chinchillas Ozawa et al., 2017 Human tympanic thermometer margin of error (combined human/veterinary) 1.7°C No Ozawa et al., 2017 Veterinary tympanic thermometer margin of error (combined human/veterinary) 1.7°C No Rabbits Hartinger et al., 2003 Implanted temperature-sensitive transponders Only graphically No Chen and White, 2006 Implantable microchip transponder 95% agreement limit: ±1.48 Yes Chen and White, 2006 Noncontact infrared thermometer (ear) Not calculated due to systematic deviations from avg temp No Chen and White, 2006 Noncontact infrared thermometer (thigh) Not calculated due to systematic deviations from avg temp No Chen and White, 2006 Human tympanic thermometer Not calculated due to systematic deviations from avg temp No Chen and White, 2006 Animal tympanic thermometer Not calculated due to systematic deviations from avg temp No Jaén-Téllez et al., 2021 Thermography (eye) Coefficient of determination: 0.15 Unclear Jaén-Téllez et al., 2021 Thermography (inner ear) Coefficient of determination: 0.22 “Best” Jaén-Téllez et al., 2021 Thermography (external ear) Coefficient of determination: 0.24 “Inefficient” Jaén-Téllez et al., 2021 Thermography (nose) Coefficient of determination: 0.20 Unclear Ferrets Maxwell et al., 2016 Microchip transponder thermometry 95% Agreement limits (°F): −1.82 to +1.96 (comp. to calibrated rectal) −2.19 to +0.84 (comp. to common rectal) Yes Aguilar et al., 2018 Pediatric auricular thermometers correlation thermometer 1: 0.4726 correlation thermometer 2: 0.5388 No Aguilar et al., 2018 Veterinary auricular thermometers correlation 0.6311 No Keeney et al., 2020 Axillary 95% CI of Mean Difference -1.32, -0.67 No Keeney et al., 2020 Dorsal Skin 95% CI of Mean Difference -0.14, 0.24 No* (possibly after further studies) Keeney et al., 2020 Inguinal 95% CI of Mean Difference -1.15, -0.63 No Keeney et al., 2020 Noncontact Infrared 95% CI of Mean Difference -8.37, -6.43 No Keeney et al., 2020 Tympanic 95% CI of Mean Difference -0.78, -0.38 No SloVetRes_NOTRANJOST ver2.indd 12 09/05/2023 10:14 Slov Vet Res | Vol 60 No 1 | 13 A further limitation is that most of the studies were con- ducted in an experimental setting and may therefore not fully resemble the clinical setting. 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SloVetRes_NOTRANJOST ver2.indd 13 09/05/2023 10:14 14 | Slov Vet Res | Vol 60 No 1 Ustreznost alternativnih tehnik rektalnemu merjenju temperature pri hišnih glodavcih, kuncih in belih dihurjih - pregled literature J. Stans Izvleček: Telesna temperatura je pomemben parameter za oceno zdravja eksotičnih živali. Rektalno merjenje tempera- ture je običajen način merjenja telesne temperature pri glodavcih, kuncih in belih dihurjih in pogosto velja za zlati stan- dard. Vendar je merjenje rektalne temperature pri teh živalih pogosto povezano z omejevanjem gibanja in povzročanjem stresa. Da bi se izognili stresu pri merjenju rektalne temperature, so bile pri več vrstah živali uporabljene alternativne (pogosto manj invazivne) tehnike. Te metode vključujejo infrardečo termografijo ter merjenje temperature timpanično in aksilarno. Vendar pa je pomembno ugotoviti, ali te strategije dajejo primerljive rezultate z zlatim standardom. Zato smo opravili pregled literature z uporabo podatkovnih zbirk MedLine in Google Scholar. Osnovni izrazi, ki se nanašajo na rektalno temperaturo in merjenje temperature, so bili združeni z iskalnimi izrazi, značilnimi za posamezne vrste. Pri glodavcih, kuncih in belih dihurjih je bilo najdenih razmeroma malo študij o alternativah rektalnim meritvam temperature. Na splošno lahko ugotovimo, da so bile le meritve s transponderjem večkrat opisane kot veljavna alternativa rektalnemu merjenju temperature. Potrebne so nadaljnje raziskave. Ključne besede: rektalna temperatura; glodavci; kunci; beli dihurji; alternative SloVetRes_NOTRANJOST ver2.indd 14 09/05/2023 10:14