Intraperitoneal versus subcutaneous telemetry devices in young by fgl12588

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									Intraperitoneal versus subcutaneous telemetry
devices in young Mongolian gerbils (Meriones
unguiculatus)
Christel P H Moons1, Katleen Hermans2, Rene Remie3, Luc Duchateau4
                                          ´
and Frank O Odberg1
              ¨
1
  Department of Animal Nutrition, Genetics, Breeding and Ethology, Faculty of Veterinary Medicine,
Ghent University, Merelbeke; 2Division of Poultry, Exotic and Laboratory Animals, Faculty of Veterinary
Medicine, Ghent University, Merelbeke, Belgium; 3International Microsurgical Training Centre, Lelystad,
The Netherlands; 4Department of Physiology and Biometry, Faculty of Veterinary Medicine, Ghent
University, Merelbeke, Belgium



Summary
Radiotelemetry has become a very popular biotelemetric tool for measuring physiological
parameters such as heart rate, blood pressure, body temperature and muscle activity, as well
as general behavioural activity in undisturbed, freely moving animals. In most studies using
this technique, adult subjects are used. However, sometimes an ontogenetic approach is
required to clarify whether changes in one parameter are preceeded or followed by changes in
another parameter. Tracking physiological changes in young, developing individuals could
explain given states of these animals as adults. Implanting telemetry devices can be done
subcutaneously and intraperitoneally, the former method posing less of a challenge on the
animal and its recovery from surgery. Because telemetry will be used in weanling gerbils
during subsequent studies, we needed to investigate whether subcutaneous implantation of
telemetric devices is preferable to intraperitoneal surgery with respect to animal welfare.
This is a technical paper describing anaesthetic and surgical techniques in detail during a
pre-trial involving subcutaneous (n ¼ 10, aged 21–29 days) and intraperitoneal (n ¼ 10, aged
19–34 days) implantation of dummy telemetry transmitters (1.9 cm3, 3.6 g after shortening of
leads) in weanling gerbils, Meriones unguiculatus. Body weight was measured and analysed
over four-day intervals. Optimizing anaesthetic dosages was a first step in this pilot trial.
This occurred during the first few subcutaneous implantations. Three animals died while
anaesthetized during the subcutaneous procedure but none post-surgery. All animals
survived anaesthesia during the intraperitoneal implantation, but two died in the first three
days post-surgery. In the former method, the tension on the dermal sutures caused by the
presence of the transmitters was too great, resulting in the animals opening the sutures by
chewing them. The animals died during the latter procedure probably due to strangulation of
the intestine by the excess lead that was coiled in the abdomen. Furthermore, placement of
the exposed negative lead of the transmitter on the underlying muscle had to be done on the
m. pectoralis transversus in order for it to stay in place as the animal developed. This paper
showed that the implantation of a telemetric device in weanling gerbils is feasible and is best
executed through the intraperitoneal technique.

Keywords Implantable telemetry; weanling gerbils; heart rate; body temperature;
surgical techniques



Correspondence: Christel P H Moons, Animal Nutrition, Breeding, Genetics and Ethology, Faculty of Veterinary Medicine,
Ghent University, Heidestraat 19, 9820 Merelbeke, Belgium. Email: christel.moons@ugent.be

Accepted 19 June 2006                                  r Laboratory Animals Ltd. Laboratory Animals (2007) 41, 262–269
Telemetry in young gerbils                                                                         263


Biotelemetry, the ‘measurement of life from         welfare (Mason 1991). A stereotypy consists
a distance’, is nowadays frequently                 of repeated morphologically relatively
implemented to monitor physiological                identical movements, and the behaviour as a
parameters in animals. It can be used in            whole has no obvious goal or function. In the
almost all species and exists in many               Mongolian gerbil, there are two forms:
different forms with varying degrees of             digging and bar chewing, onset of both is
invasiveness (Morton et al. 2003).                                                          ¨
                                                    seen between 24 and 35 days of age (Odberg
Applications include video monitoring               1978, Wiedenmayer 1997a,b, Waiblinger &
(Moons et al. 2005), radio collars to track free-   Konig 2004). One could compare
ranging animals (Haines et al. 2004),               physiological parameters between
electrode belts adapted from devices for            stereotypers and non-stereotypers. But
human heart-rate monitoring (Marchant-              if a difference is found, it cannot be
Forde & Marchant-Forde 2004), probes to             demonstrated whether the behaviour is the
measure rectal and tympanic temperature                                                   ¨
                                                    cause or the consequence thereof (Odberg
(Prendiville et al. 2002), and implantable          1993). Developmental studies are therefore
devices to monitor blood pressure, heart rate,      very important, but no transmitters are
muscle activity, core body temperature and          commercially available for implantation in
general activity (Johansson & Thoren 1997,          animals weighing a few grams, as is the case
Kettlewell et al. 1997, van den Buuse &             with small rodents.
Malpas 1997; Gacsalyi et al. 2000; Matthew             Implanting biotelemetry devices used
et al. 2004). In this paper, we focus on the use    for adults in young animals thus entails
of implantable radiotelemetry devices. The          taking additional issues into account. First
main benefit of using such biotelemetry is           of all, a study by Schneider et al. (1995)
that it is an accurate way of collecting data       showed that nine-day-old gerbils are quite
frequently without disturbing or restraining        sensitive to the implantation procedure as
the animal (Kramer et al. 1993). Because            30% died during anaesthesia, surgery or
the information obtained per animal is              anaesthetic recovery. The weight and
maximized and the stress of physiological           volume of the implanted device may cause
data collection minimized at the same time,         more discomfort than in adult individuals
telemetry contributes to reduction and              and chronic pain may impair recovery.
refinement as described in the 3R principle          Furthermore, young animals are growing,
proposed by Russel and Burch (1959). The            their organs are still developing and
principal drawback is that, even though data        implanting a mechanical obstruction can
collection is non-invasive, implantable             compromise organ function and growth.
biotelemetry requires surgery and a period          Additionally, increase in body size of the
during which the animal recovers before valid       animal itself needs to be taken into account
data can be collected (Baumans et al. 2001).        when positioning the transmitter to prevent
   The majority of publications report that         signal detection problems (Morton et al.
transmitters are implanted in adult animals         2003). Finally, when implanting telemetry
or subadults, but not in neonates or juveniles      devices in pre-weanling animals, there is a
(Weinandy & Gattermann 1997, Meerlo                 considerable risk that the parents may reject
et al. 1999, Baumans et al. 2001, Jelen &           their young upon return to the nest, as
Zagrodzka 2001, Davies et al. 2004).                was shown in nine-day-old gerbils where
However, it can be important to know how            acceptance rate was only 54% (Schneider
physiological parameters change in young            et al. 1995).
animals during the development of the                  This paper describes a pre-trial and
central nervous system, as adult phy-               presents detailed information about the
siological and behavioural function is a            technique and comparison of subcutaneous
result thereof. For instance, in the field           (n ¼ 10, aged 21–29 days) and intraperitoneal
of ethology, stereotypic behaviour is an            (n ¼ 10, aged 19–34 days) implantation of
important indicator of suboptimal hus-              transmitters in Mongolian gerbils. Although
bandry conditions and, possibly, reduced            the successful implantation of similar
                                                                           Laboratory Animals (2007) 41
264                                                                              C P H Moons et al.


transmitters in rats and mice has been             Torkt paper tissue (Tork, Guildford,
documented (Baumans et al. 2001, Matthew           Australia) and chew blocks for cage
et al. 2002), it is important to verify prior to   enrichment. The chew blocks were home-
conducting an experiment that the same             made by cutting and dividing branches
is true for gerbils (Morton et al. 2003).          from apple and cherry trees. Pellets from
Furthermore, it is with the animals’ welfare       2018 Teklad Global 18% protein rodent diet
in mind that we evaluate the use of a              (Harlan, Horst, The Netherlands) and tap
subcutaneous implantation procedure in             water were available ad libitum. All animals
comparison with an intraperitoneal surgery         were kept under a 14:10 L:D cycle with
(Butz & Davisson 2001). The use of tele-           lights off between 09:00 and 19:00 h.
metry in the author’s case is intended for         Temperatures ranged mostly between 201C
the investigation of functional aspects of         and 251C, whereas relative humidity values
stereotypies in weanling gerbils, but data         were measured between 24% and 55%.
collection in these young animals can serve        However, when outside temperatures were
other purposes like pharmacological,               high, the room temperature sometimes
neurological and cardiovascular studies as         rose to 271C. Similarly, relative humidity
well. The authors hope that this detailed          increased to 68% on extremely humid days.
technical paper will also serve veterinary         Continuous ventilation was provided.
scientists or researchers and their assisting
veterinarians interested in telemetry but
who are not familiar with the techniques.          Anaesthesia and patient preparation
                                                   At least 24 h prior to surgery, each gerbil
                                                   received 5 mg/kg carprofen s.c. (Rimadyls,
Methods                                            Pfizer Animal Health, USA) and an oral dose
Prior to the experiment, approval for the          of 10 mg/kg enrofloxacin (Baytrils, Bayer,
procedures from the Ethical Committee of           Brussels, Belgium) every 12 h. Surgery was
the Faculty of Veterinary Medicine at Ghent        carried out at the Clinic for Avian and Exotic
University was obtained. The Laboratory            Animal Medicine. Anaesthesia was induced
for Ethology is licensed for breeding and          in an induction chamber using 4% iso-
housing gerbils (LA2400377; LA1400096).            flurane (Isoflos, EcuPhar Animal Health,
                                                   Oostkamp, Belgium) for induction and 2–3%
                                                   for maintenance in an oxygen flow of
Animals and housing                                500 mL. Once anaesthetized, the animal was
Twenty animals were used. Ten of which             removed from the chamber and held in
were implanted subcutaneously during four          dorsal recumbency throughout the surgery
surgery sessions and 10, intraperitoneally,        on a heating pad (ColdHott, 3M Health
during three sessions. The ages ranged from        Care, Neuss, Germany), which was covered
21–29 days (20–30.5 g body weight) for the         with a non-sterile drape. The heating pad
former and 19–34 days (20.5–28.4 g body            was microwavable and was heated twice at
weight) for the latter. Our subjects were          750 W for 1 min prior to surgery. The limbs
bred from five pairs of Mongolian gerbils           of the animal were extended and fixed using
purchased from the outbred SPF RjTub:              adhesive tape. The anaesthetic mixture was
MON stock from Elevage Janvier                     continuously administered using a non-
(Le Genest-St-Isle, France). Prior to surgery,     rebreathing system with a mask fitting the
all animals were housed with their parents         gerbil’s snout.
and siblings in Makrolon type IV cages                The abdomen and part of the thorax of
(55 Â 33 Â 20 cm, Bio-Services, Schaijk, The       the animal were close-clipped using small
Netherlands) in the colony room at the             clippers (Wella, Bio-Services, Schaijk, The
Department of Animal Nutrition, Genetics,          Netherlands). Next, the incision area was
Breeding and Ethology. The cages were              disinfected with 7% povidone iodine
bedded with Gold Mix wood shavings                 (Braunols, B Braun Melsungen, 34209,
(Carfil, Turnhout, Belgium) and had Mini-           Melsungen, Germany). Finally, an operating
Laboratory Animals (2007) 41
Telemetry in young gerbils                                                                      265


field was created using Busters Sterile           sutures to prevent gerbils from damaging the
Op-Cover (Kruuse, Marslev, Denmark) and          stitches and 0.2 mL warm sterile 0.9%
Steridrapet (3M Health Care, Neuss,              NaCl (B Braun Melsungen, 34209,
Germany).                                        Melsungen, Germany) was administered
  For both subcutaneous and intraperitoneal      intraperitoneally to compensate for
implantation procedures, we used dummy           dehydration. The entire subcutaneous
ETA-F20 (1.9 cm3, 3.6 g after shortening of      procedure lasted between 30 and 40 min.
leads, Data Sciences International, Arden
Hills, MN, USA) devices with leads cut to
the appropriate length prior to making the       Intraperitoneal implantation
first incision.                                   Using a method similar to the subcuta-
                                                 neous implantation, a ventral midline skin
                                                 incision (A) of approximately 1.5 cm was
Subcutaneous implantation                        made. Through blunt dissection, we created
First, a ventral skin incision (A) of approxi-   a pouch around the posterior part of the
mately 1.5 cm was made.                          incision to fit the leads subcutaneously later
   Skin incision (B) was made just caudal to     on. A ventral incision was made through the
the gerbil’s right upper limb and measured       abdominal wall (along the linea alba) of the
0.5 cm maximum. From the latter incision, a      same size as incision A. We then inserted a
pair of thumb forceps was tunnelled under        dummy transmitter longitudinally on top of
the skin to reach the site of ventral midline    the intestines with the leads directed
incision A. Using the forceps, the tip of the    caudally.
negative lead of the transmitter was pulled        A 14-gauge needle was used to guide
cranially where it protruded from the            the leads through the abdominal muscles
incision. The exposed part of the lead was       approximately 0.5 cm lateral to the incision,
fixed to the underlying muscle tissue with        the negative lead to the right and the
6.0 Perma-Hands silk sutures (Ethicon,           positive lead to the left, respectively. After
Johnson & Johnson Medical, Dilbeek,              puncturing the abdominal wall and fitting
Belgium) using a Lembert stitch. This type of    the lead tip in the needle cavity, retracting
stitch ensures optimal contact between the       the needle left the lead pointing outwards
electrode and the muscle. Next, the tip of       through the abdominal muscles with
the lead was tucked underneath the skin          minimal tissue trauma. Positioning and
cranial to incision B.                           fixing the lead tips was analogous to the
   A third skin incision (C) of 0.5 cm           procedure during the subcutaneous
maximum was made cranial to the left             implantation.
hindlimb. From this incision, a pair of            The excess positive lead (about 2 cm) was
forceps was tunnelled underneath the skin        coiled (coil of 0.64 cm diameter, approxi-
to incision A. Analogous to the negative         mately) and placed in the abdominal cavity,
lead, the positive lead was positioned and       whereas the excess negative lead was coiled
fixed.                                            and placed subcutaneously to allow cranial
   Through blunt dissection, a pouch was         movement of the lead tip during animal
created near incision A to fit the transmitter    growth. We closed the abdominal muscles
lengthwise, leads directed caudally. The         and peritoneum using the same 4.0 Vicryl
excess leads were coiled and put underneath      Rapids sutures in a continuous pattern,
the transmitter. A 4.0 Vicryl Rapids             making sure to use the three suturing holes
(Ethicon, Johnson & Johnson Medical,             on the transmitter to fix it to the abdominal
Dilbeek, Belgium) suture was used to close       wall. When necessary, warm 0.9% NaCl
incisions A, B and C using a continuous          drops were applied during the procedure
pattern. Next, interrupted sutures were          to protect the abdominal wall from
used as an additional safety. A piece of         dehydration. The closure of incisions
Tegaderms (3M Health Care, D-46325               A, B and C was analogous to that of the
Borken, Germany) was applied on the              subcutaneous implantation procedure. The
                                                                        Laboratory Animals (2007) 41
266                                                                               C P H Moons et al.


entire procedure lasted between 50 and              and control animals were compared at each
75 min.                                             time interval using Bonferroni’s multiple
                                                    comparisons adjustment to guarantee a global
                                                    significance level of 5%.
Anaesthetic recovery and postoperative care
After the last sutures had been made, the
adhesive tape on the limbs was removed.             Results
The animal was placed in ventral
recumbency and the isoflurane, but not the           Subcutaneous implantation
oxygen, administration was stopped. When            Out of 10 animals, we lost three animals
the animal was awake, we housed it together         during the first two implantation sessions
with a non-operated littermate in a                 because of the anaesthesia. A regular
Makrolon type IV cage bedded with Gold              breathing pattern was needed for the animals
Mix and one sheet of Mini-Torkt paper               to survive the surgery. Changes in res-
tissue. The cage was placed in an incubator         piration pattern in response to surgical
set at 281C and remained there until the            manipulations indicated that the percentage
implanted animal was sufficiently conscious          of isoflurane needed to be adjusted.
and mobile (usually less than 1 h). Next, we        Sometimes, this required leaving the dose at
returned the cages to the colony room and           close to 3%, even though this would seem
placed them under a 220 V infrared light for        a lot for gerbils. We also checked pain
6 h. A few dry and moistened feed pellets           perception in the animal by pinching the
were placed on the cage bottom to stimulate         skin prior to making the first incision and
feeding. The implantations always occurred          adjusted the isoflurane concentration
before noon. Three times throughout the             accordingly.
afternoon we fed the operated animals                  One animal did not eat or drink after the
0.4 mL of a room-temperature mixture of             surgery, and it died despite extending the
water, soaked pellets, sugar and Critical Care      postoperative care measures beyond the first
for Herbivoress (Oxbow Pet Products,                day post-surgery. This animal was the first to
Murdock, NE 68407, USA) to prevent                  be implanted and the surgery lasted the
hypoglycaemia. We continued to administer           longest of all procedures executed. In
Baytrils and Rimadyls every 12 h for                addition, it required much more mani-
another three days following the day of             pulation of the transmitter and leads.
surgery. Because we expected the non-operated          The remaining issue was the dermal
gerbils to be more active at first and because       tension caused by the subcutaneous
the risk existed that they would inspect and        transmitter. Two animals did not chew their
gnaw the sutures of their cage mate, we             sutures, but three animals chewed either
provided distraction in the form of chew            sutures from incisions B or C. One animal
blocks, paper tissue and a handful of hay.          chewed sutures from incisions B and C as
Morton et al. (2003) recommend tracking the         well as A. At first we re-anaesthetized the
restoration of circadian rhythmicity in heart       animals to close the wounds, and this
rate, body temperature and activity in the          lengthened the time needed for the gerbils to
animal as an indication of recovery from            wake up and increased the time until data
surgery. However, given the fact that this was      collection (an extra 3 days according to the
not possible in our pilot study, we monitored       postoperative protocol). Therefore, small
body weight instead (Baumans et al. 2001).          openings in the sutured incision were often
The weight gain in four-day intervals was           repaired with tissue glue. However, this
determined for each animal and compared             appeared to dehydrate the skin, which
between implanted and control animals, based        caused wound dehiscence. Between six and
on a mixed model, with animal as random             16 days after the last suture manipulation
effect and gender, time interval, treatment and     (mean: 10.471.5), incision A had opened in
their interaction as categorical fixed effects. In   all but one individual (where it concerned
the case of a significant interaction, implanted     incision C), exposing the transmitter
Laboratory Animals (2007) 41
Telemetry in young gerbils                                                                        267


to such an extent that it would require            the positive lead tip was the same as in the
re-sterilization to be able to implant it again.   young animal. We attributed this to the fact
The transmitters were removed and the              that we had missed the appropriate fixation
animals were allowed to live if they did not       site and that this consisted of merely a few
show signs of pain or discomfort that would        millimetres. Most likely, we failed to attach
warrant euthanizing them. We suspect the           it to the m. pectoralis transversus and
animals did not chew the sutures at that           instead sutured it onto the m. obliquus
point like they did in case of initial post-       externus abdominis. Young gerbils are quite
surgery irritation. Instead, it is more            small. Therefore, one must pay attention to
likely that the absorbable material had            discriminate between muscles during
disintegrated without wound closure. We            surgery.
decided that the subcutaneous implantation
of ETA-F20 transmitters in young gerbils
was not sustainable. Therefore, we followed        Body weight
the recommendation by Morton et al. (2003)         There was a significant overall treatment
that when an implant is too large it is more       effect (P ¼ 0.002) and time interval effect
appropriate to fit it into the peritoneal           (Po0.0001), but no gender effect (P ¼ 0.98).
cavity.                                            There was a significant interaction between
                                                   time interval and treatment (P ¼ 0.0022).
                                                   During the first time interval, the implanted
Intraperitoneal implantation                       animals were losing weight and differed
Two animals died the day after surgery             significantly from the control animals
during the time they were still receiving          (Po0.0001). During the following time
analgesic and antibiotic treatment. During         intervals, however, the implanted animals
the surgery of both these animals, the             gained weight similar to the weight gain of
transmitter slipped under the intestine            the control animals without any significant
while wedging the leads in the abdominal           differences between the two groups.
cavity. We repositioned the transmitter
while it was still in the abdominal cavity,
making sure that the intestine was not             Conclusion
coiled on top of the device. During necropsy,      This procedure describes anaesthesia and the
however, in both animals we found a                surgical technique for subcutaneous and
strangulation of the intestine, leading to the     intraperitoneal transmitter implantation in
onset of peritonitis. Besides the presence of      weanling gerbils of 21–29 days old. After
the transmitter in the abdomen, the fact that      initial losses, no gerbil died during the
we left some of the positive lead in the           implantation procedure. Postoperative care
abdomen is probably a more important               in the form of analgesics and antibiotics
contributing factor. The excess lead               were given during three days after
accounted for the growth of the animal as          implantation. Animals from both procedures
well as allowing re-use of transmitters            were originally intended to be monitored for
without refurbishing the leads. The                21 days until they were euthanized, and a
necropsies did not show any other anomaly.         necropsy was performed to evaluate the
  The remaining issue concerned the growth         position of the transmitter as well as the
of the gerbils and the point of fixation of the     condition of the internal organs in the case
negative lead tip. The suture on the negative      of the intraperitoneal implantation
lead sometimes became undone, and the              procedure.
negative lead did not always move cranially          Three animals out of 10 died during
as the animal grew, resulting in the fact that     anaesthesia of the subcutaneous procedure
the lead tip was found on the abdomen              as we were optimizing the isoflurane dose.
during the necropsy. But even after securing       None of the subcutaneous implantations
the suture with a few extra knots, the             succeeded because the ventral incision (and
absolute distance between the negative and         in one case a non-ventral incision) had
                                                                          Laboratory Animals (2007) 41
268                                                                                  C P H Moons et al.


opened. The transmitters were removed            Acknowledgements The training model
without euthanizing the animals. The             transmitters were provided by E Rieux from Data
                                                 Sciences International, a division of Transoma
tension on sutures and skin caused by the        Medical. Gratitude is also extended to D Depoortere
presence of the telemetry device appeared        and I Vermeulen for excellent technical support.
to be too high in these young animals.
Oftentimes a scab had formed over the skin,
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