Archivos Latinoamericanos de Producción Animal. 2023. 31 (2)
Vaginally use of iButton® loggers to measure body temperature
in grazing red deer (Cervus elaphus)
Received: 20221125. Accepted: 20230501
1Corresponding author: Lorenzo Álvarez, alorenzo@unam.mx Av. Universidad 3000 SN, Colonia UNAM CU, Delegación Coyoacán, 04510,
México D.F. Tel. 52 414 291 81 00, Fax 52 414 291 81 05
187
Lorenzo Álvarez Ramírez1
Abstract. When collecting accurate physiological data, it is important to eliminate human interference in situations
when it is necessary to record continuously over several days. Noninvasive methods for measuring body
temperature can be useful for monitoring health status and assessing environmental and climatic effects. The aim of
this study was to describe a) two methods for automatically recording of body temperature, by means of a vaginal
device in grazing red deer (Cervus elaphus) and b) the daily body temperature pattern. All animals were sedated
with xylazine, and had automatic thermal recording devices (iButton®, ThermochronTM, Maxim Integrated, San
Jose, CA, USA) inserted into a vaginal sponge (10 animals, 10 days) or CIDRG (13 animals, 10 days). Devices were
programmed to record temperature every 10 minutes. All devices except one corresponding to a sponge were
successfully recovered. The devices recorded a rhythmic pattern of body temperature, with the highest value
registered during the afternoon and the lowest during the morning. No major inconveniences were observed,
suggesting that the iButton® device can be successfully used in cases where records of continuous body temperature
recording are required for up to 10 days while avoiding any notable interference.
Keywords: physiological traits; heat stress; circadian rhythm; daily pattern.
https://doi.org/10.53588/alpa.310205
Facultad de Medicina Veterinaria y Zootecnia, Universidad Nacional Autónoma de México, México.
Gabriela Arteaga Salazar2
Uso intravaginal de registradores iButton para medir la temperatura corporal en
ciervos rojos (Cervus elaphus) a pastoreo
Resumen. Para recopilar datos fisiológicos precisos, es importante eliminar la interferencia humana y tener un
registro continuo durante varios días de ser necesario. Los métodos no invasivos para medir la temperatura
corporal pueden ser útiles para monitorear el estado de salud e investigar los efectos ambientales y climáticos. El
objetivo de este estudio fue describir a) dos métodos para el registro automático de la temperatura corporal
mediante un dispositivo vaginal en ciervo rojo en pastoreo (Cervus elaphus) y b) el patrón diario de temperatura
corporal. Todos los animales fueron sedados con xilazina y se colocaron dispositivos automáticos de registro
térmico (iButton®, ThermochronTM, Maxim Integrated, San Jose, CA, USA) adheridos a una esponja vaginal (10
animales, 10 días) o CIDRG (13 animales, 10 días). Los dispositivos se programaron para registrar cada 10 minutos.
Todos los dispositivos se recuperaron con éxito con excepción de uno de los animales con esponja. Los dispositivos
registraron un patrón rítmico de la temperatura corporal, con el valor más alto durante la tarde y el más bajo
durante la mañana. No se observaron mayores inconvenientes, lo que sugiere que el dispositivo iButton® puede ser
utilizado con éxito en los casos en que se requiera un registro continuo de la temperatura corporal hasta por 10 días
sin mayores interferencias.
Palabras clave: datos fisiológicos; estrés térmico, ritmo circadiano; patrón diario.
Alejandra Sánchez Cervantes3
Uso intravaginal de registradores iButton para medir a temperatura corporal em
veadovermelho (Cervus elaphus) em pastejo
Resumo. Para coletar dados fisiológicos precisos, é importante eliminar a interferência humana para obter registros
contínuos por vários dias. Métodos não invasivos para medir a temperatura corporal podem ser úteis para
monitorar o estado de saúde e investigar os efeitos ambientais e climáticos. O objetivo deste estudo foi descrever a)
dois métodos de registro automático da temperatura corporal usando um dispositivo vaginal em veadovermelho
(Cervus elaphus); e b) o padrão diário de temperatura corporal por 10 dias. Os dispositivos foram programados para
gravar a cada 10 minutos. Todos os dispositivos foram recuperados com sucesso, com exceção de um dos animais
com esponja. Os aparelhos registraram um padrão rítmico de temperatura corporal, com maior valor à tarde e
188
Introduction
ÁlvarezRamírez et al
Materials and Methods
The study was undertaken with the approval from
the Animal Care and Use Committee of the Faculty of
Veterinary Medicine, National Autonomous University
of Mexico (protocol #028).
Location and animals
The study was carried out at a research station located
north of Mexico City (Alvarez Ramírez et al., 2021) among
a captive population of noncyclic and nonpregnant
adult red deer (1.2 2.3 years of age). According to the
menor pela manhã. Não foram observadas grandes desvantagens, sugerindo que o dispositivo iButton pode ser
usado com sucesso e sem grandes interferências nos casos em que é necessário o registro contínuo da temperatura
corporal por até 10 dias.
Palavraschave: dados fisiológicos; estresse calórico, ritmo circadiano; padrão diário.
Body temperature is one of the most relevant
physiological traits of animals (Godyń et al., 2019).
Temperature values may indicate an animal's
metabolic state (Burfeind et al., 2014), presence of
infections (Lee et al., 2015; Godyń et al., 2019), or the
exposure to a challenging thermal environment
(Kinahan et al., 2007; De et al., 2017). Rectal temperature
is the most reliable indicator of core body temperature.
However, the handling practices required to
repetitively record rectal temperature may cause
serious problems, such as stressinduced hyperthermia
and possible animal welfare affectations (Hilmer et al.,
2010; Chapon et al., 2012).
Rectal and vaginal temperature have shown to be
nearly identical, and their agreement indicates that
they are interchangeable (Suthar et al., 2013; Lees et al.,
2018); differences between them are insignificant and
both values are considered reliable indicators of
physiological information (Vickers et al., 2010; Burdick
et al., 2012; Maeder et al., 2012; Suthar et al., 2013).
Recording body temperature over a prolonged period
requires the use of an automated device that once
implanted, continues to record without interrupted. A
variety of devices fulfill these requirements (Hilmer et
al., 2010; Vickers et al., 2010; Burdick et al., 2012; Maeder
et al., 2012). Automatic devices for body temperature
assessment now provide a valuable tool for researching
almost any kind of animal and its habitat (Hartman
and Oring, 2006; Hilmer et al., 2010; Signer et al., 2010;
Chapon et al., 2012; Roznik and Alford, 2012); however
specific techniques for their use must be evaluated.
The iButton® device (Thermochron™, Maxim
Integrated, San Jose, CA, USA) is one of the most
popular temperature dataloggers, it records and stores
data points into an internal memory (Davidson et al.,
2003). For continuous body temperature recording,
iButton® devices can either be ingested (Kinahan et al.,
2007), surgically implanted (Taylor et al., 2004; Hilmer et
al., 2010; Lee et al., 2015) or attached to the animal's
body surface (Grayson and Dorcas, 2004; Munn et al.,
2009; Abecia et al., 2019). In cows, it has been used
subcutaneously (Lee et al., 2015) or attached to an
intravaginalintrarectal implant (Lea et al., 2008; Polsky
et al., 2017; Lees et al., 2018).
The pattern of daily body temperature is usually
defined as a circadian rhythm that extends over an
approximate 24 h period. Mean value of body
temperature (mesor), together with amplitude of the
oscillation and shape (waveform) of the rhythm are
also important factors; these parameters may have a
strong physiological significance. The rhythm reflects a
constant conflict between homeostasis and circadian
rhythmicity for control of the animal’s core
temperature, it is the result of an interplay of
mechanisms of heat production and heat loss,
controlled by the circadian system (Refinetti, 1992,
2010).
Red deer (Cervus elaphus) is a wild ruminant that has
been introduced into different regions of the globe. In
many of these regions, the species is exposed to
thermal conditions that impose a challenge and require
monitoring (Mattiello, 2009; Alvarez Ramírez et al.,
2021). In these cases, it is necessary to study body
temperature without disturbing the animal. In species
of this kind, it is not possible to record body
temperature using traditional methods, nor has an
easy, automatic method that avoids disturbing the red
deer been described. The objective of this document
was to describe a) the use of the iButton® device to
record vaginal temperature in red deer, coupled either
to a CIDR or to a polyurethane sponge, and b) assess
daily vaginal temperature pattern and its relationship
with particular environmental factors.
ISSNL 10221301. Archivos Latinoamericanos de Producción Animal. 2023. 31 (2): 187194
Figure 1. Preparation of polyurethane sponges for insertion of the iButton® device.
189
Recording body temperature in red deer
Part B) iButton® devices in a CIDRG
During the month of February, a total of 13 red deer
females received hormonefree recycled sterilized
CIDRG devices with an attached iButton® data logger.
The middle of the CIDR (figure 2A) was slit open 16
mm. A datalogger was inserted into the slit (figure 2B)
and then this portion of the CIDR and the iButton®
were covered using Thermofilm tape (Steren® Mexico;
figure 2C). Hot air from a hair dryer was applied to
cause shrinkage to the Thermofilm, thus firmly
attaching the iButton® to the CIDR (figure 2D).
farm's management program, animals were maintained
in rotational grazing conditions, in 5000 m2 alfalfa
paddocks (Medicago sativa), where no artificial or
natural shade was available. Water was permanently
provided using plastic 200 L basins.
Part A) iButton® devices in polyurethane sponges
During the month of December, a total of 10 red deer
females were vaginally implanted with a polyurethane
sponge containing a data logger (iButton®, models DS
1921G and DS1921H; ThermochronTM, Maxim
Integrated, San Jose, CA, USA). Sponges were
elaborated using hormonefree commercial sterilized
polyurethane. A horizontal line was cut in the middle
of the sponge (figure 1A) to enable total introduction of
the iButton® (figure 1B), and subsequently this slit was
closed with simple stitches, using sterile non
absorbable thread (figure 1C).
Figure 2. Procedure to adhere an iButton® device into a CIDRG.
All dataloggers were factorycalibrated and previous
ly programed to record temperature every 10 minutes.
iButtons were not waxed. Sponges and CIDRs were
sterilized by autoclaving, prior to their preparation.
Once prepared, sponges and CIDRs were smeared with
disinfectantlubricant cream and introduced into the
vagina using straight forceps (figures 1D, 2E). The
devices were withdrawn after 10 days of effective
recording. For the insertion and removal of the devices,
all animals were previously sedated with an i.m.
injection of xylazine (0.7 mg/kg) (Walsh and Wilson,
2002) within the research station's management pen.
Environmental factors
Solar radiation (SR), environmental temperature (ET),
sunrise and sunset time were recorded from an online
meteorological station, located at 3 km from the
experimental site (www.wunderground.com). During
December, average ET was 10.9 0.12 °C with a mini
mum of 1.3 °C and a maximum of 21.3 °C; during
February, average ET was 18.2 0.14 °C ( SE) with a
minimum of 6.6 °C and a maximum of 27.4 °C. Recorded
SR was 329 9.4 w/m2 and 492 8.6 w/m2 during De
cember and February respectively (mean SE). Average
sunrise and sunset time during December were 07:18 h
(07:1707:20 h) and 18:14 h (18:1118:17 h) respectively.
ISSNL 10221301. Archivos Latinoamericanos de Producción Animal. 2023. 31 (2): 187194
Little or no reaction to the introduction of the vagi
nal devices were observed. Following recovery from
sedation, some animals were seen to urinate, but then
returned to grazing without any other perceived
discomfort.
All vaginal devices except one, inserted into a spon
ge were recovered. On removal, mucous and purulent
secretion was observed around the sponges, a common
finding when using these devices (Fleisch et al., 2012),
but no other complications emerged. No blood was
detected on any of the devices. No or little vaginal
discharge was observed on CIDRs at withdrawal.
Removal of CIDRs appeared to be slightly easier,
probably due to the material from which they are
made and to their diminished adhesion to vaginal
mucosa, compared to sponges (Fleisch et al., 2012).
One iButton® from the sponge group ceased re
cording on the last day of the study. Mean body
temperature obtained during the 10 days of recording,
relating to each vaginal device is presented in figure 3.
In both cases, body temperature showed a rhythmic
pattern over a period of 24 h (p < 0.05), with a mesor of
38.5 and 38.7 °C, an amplitude of 0.22 and 0.38 °C;
acrophase occurred at 20 and 19 h, and bathyphase at 8.5
and 7 h of the day for sponge and CIDR devices,
respectively (figure 4). Recorded means for vaginal
temperatures in both cases (mesor) resemble rumen
temperature among red deer living in seminatural
conditions (Turbill et al., 2011) and also body
temperature of other domestic ruminants (Jessen and
Kuhnen, 1996; Piccione et al., 2003). During both
recording periods, the correlation between mean body
temperature and ET was positive. A high correlation
was found in February (r = 0.72, p < 0.00001), when ET
was also higher, while the correlation during December
was weak and nonsignificant (r = 0.14, p = 08).
Daily rhythmicity of body temperature has been
documented among a wide variety of species; its
specific pattern can be affected by environmental cycles
by means of synchronizing the endogenous clock and
thus changing its period. Other environmental
variations may also modify the circadian rhythm by
disturbing its wave form and altering its mesor and
amplitude. The lightdark cycle, ET and food
availability have been shown to represent some of the
Results and Discussion
190
During February, sunrise occurred at 07:05 h (07:0907
02 h) and sunset at 18:44 h (18:4218:46 h).
Data analysis
Data was analyzed using descriptive statistics, co
sinor analysis (Molc
an, 2019; https://cosinor.online/
app/cosinor.php) to explore rhythmicity; Pearson,
linear regression, and the BlandAltman plot (Bland
and Altman, 1986; Doğan, 2018) were also used to
evaluate correlations and agreement between methods
of recording.
Figure 3. Mean daily pattern of body temperature during ten consecutive days of recording, using the iButton® device embedded
in vaginal polyurethane sponges (A) and CIDRG vaginal inserts (B). The black and white horizontal bars represent the dark and
light phases of the prevailing sunrisesunset cycle.
ÁlvarezRamírez et al
ISSNL 10221301. Archivos Latinoamericanos de Producción Animal. 2023. 31 (2): 187194
191
most important factors entraining and affecting daily
rhythm of body temperature and its wave form
(Rensing and Ruoff, 2002; Mendoza, 2007; Refinetti,
2010). For example, in goats exposed to different ET,
circadian rhythm of body temperature is preserved but
its amplitude and mean value are significantly affected
(Piccione et al., 2005). Furthermore, the diurnal phase is
clearly associated with an increment of body
temperature, whereas during the night a clear drop has
been documented in goats (Ayo et al., 1999; Piccione et
al., 2005) and donkeys (Zakari et al., 2018), as in our
case. Other factors as locomotor activity, body size and
reproductive state can also affect the appearance of the
pattern; however, although changes in these
environmental and biological factors can affect body
temperature, its circadian rhythm is not a consequence
of them (Refinetti and Menaker, 1992). Although our
study was not designed to determine the specific
influence of those factors on deer body temperature, it
shows a clear rhythmic pattern with the lowest and
highest values at the beginning and the end of the light
phase of the day, respectively (figures 3 and 4). To our
knowledge, this is the first report to characterize a
circadian rhythmic pattern of body temperature in red
deer.
Figure 4. Mean pattern of daily oscillation (real data, •), cosinor curve () and mesor () of red deer vaginal temperature
recorded with iButtons attached to a sponge (A) or to a CIDRG (B). The black and white horizontal bars represent the dark and
light phases of the prevailing sunrisesunset cycle.
Pearson correlation showed a strong association
between the values recorded, using both methods
(r = 0.83, p < 0.05). The regression line indicated a good
agreement between both methods (r2 = 0.68; y = 1.3665x
13.921), although the data did not show a perfect
dispersion from the line; instead revealing considerable
discrepancy, as the use of sponges seemed to show
lower estimates than those obtained with CIDR.
However, caution should be exercised when making
this interpretation, as information was obtained during
different periods and in different animals, possibly
influencing the values.
The BlandAltman plot showed the mean bias ±SD
between sponge and CIDR measurements as 0.21 ± 0.17
°C, and the limits of agreement were 0.56 and 0.13.
This means that when the sponge was used, iButton®
recordings were 0.21 °C lower on average than those
for CIDR (figure 5). As this study did not intend to
validate the methods used, no objective
recommendation can be given regarding which
method is better for reflecting physiological data.
Human presence and direct management can affect
an animal's behavioural and physiological traits
(Burdick et al., 2012); which might be more significant
in less domesticated animals, such as red deer. Thus,
using devices to automatically record animal
responses, with minimal human interference, may
represent an advantage (Reuter et al., 2010; Angle and
Gillette, 2011; Maeder et al., 2012). Using iButtons in
vaginal sponges or CIDRs in other animal species like
cows, sheep or goats seems totally possible. In cows,
successful experiences using the CIDR implant have
already been reported (Suthar et al., 2013; Polsky et al.,
2017).
Although both vaginal devices performed
satisfactorily, the CIDR always proved easier to
withdraw. In some cases, the sponges seemed to
adhere to the vaginal walls, and in one case a speculum
had to be used to remove it completely, a difficulty
which was not observed with the CIDRs. This
represents a limitation to the use of the iButton® in
sponges and CIDRs over longer periods; for
reproductive purposes, these vaginal implants have
been used for up to 14 days; although in isolated cases,
the CIDR was used over a longer period (20 and 45
days), with no reports of negative consequences
(Wheaton et al., 1993). However, we do not recommend
Recording body temperature in red deer
ISSNL 10221301. Archivos Latinoamericanos de Producción Animal. 2023. 31 (2): 187194
192
the use of either vaginal device for more than 14
consecutive days, as the risk of vaginitis and adhesions
increases significantly (MartinezRos et al., 2018). When
longer logging periods are required, dataloggers
should be implanted using a different technique.
Figure 5. BlandAltman plot for the agreement of temperature recorded using sponges or CIDRG vaginal implants.
The iButton® is a datalogger that records date, time
and temperature and stores the information in a single
chip. This information can be recovered using
OneWireViewer® software (Maxim Integrated™, San
Jose, CA, USA) and a USBport adapter. This device
can be used in field studies and represents one of
several methods for continually recording animal traits
(Davidson et al., 2003). These loggers have been used to
record body temperature in a variety of ways and
among a number of animal species (intraperitoneal,
shrew: Mzilikazi et al., 2002; carapace, turtle: Grayson
and Dorcas, 2004; rectal, cattle: Lea et al., 2008;
intraperitoneal, feral cat: Hilmer et al., 2010;
subcutaneous, calves: Lee et al., 2015; external, sheep:
Abecia et al., 2019). To our knowledge, this is the first
demonstration that the iButton® can be used vaginally
in red deer to successfully measure body temperature
for up to 10 continuous days.
Conclusion
In red deer, the iButton® device was successfully
used in vaginal implants to continuously record body
temperature for a period of up to 10 days. If validated,
this procedure may become a valuable research and
clinical followup tool in various areas of study
focusing on animal populations, where interference
should be avoided. Red deer’s body temperature
showed a rhythmic pattern during the day, with the
highest values during the afternoon and the lowest
during the morning.
Conflict of interests: None
Ethics statement: The Internal Animal Care and Use Ethics Committee of the Faculty of Veterinary Medicine of the
National Autonomous University of Mexico approved the experimental protocol (CICUA #028).
Author contributions: All authors contributed equally.
Funding: We would like to thank the PAPIITUNAM program (grant number IN205810) for the grant given to
carry out this study.
Edited by Aline Freitas de Melo.
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