The BTPD (Cynomys ludovicianus) is a member of the order Rodentia and the family Sciuridae.1 Although these animals are native to the grasslands of North America, BTPDs have also become an increasingly popular species in zoological collections and private homes.1,2 Given the often fractious nature of prairie dogs, chemical restraint is usually necessary to perform diagnostic or experimental procedures and administer treatments.3,4
Injectable and inhalation anesthetic agents are known to have variable effects on ocular characteristics, such as tear production and IOP, in a range of species.5–11 Anesthetic agents can decrease tear production, and although this decrease is only transient, it necessitates tear replacement to ensure adequate corneal protection during perianesthetic periods. Anesthetic agents can also alter IOP by changing the rate of aqueous humor production or outflow or by increasing extraocular muscle tone.5 Because changes in IOP during anesthesia can substantially influence outcomes for patients undergoing ocular surgery, the effect of anesthetic agents on IOP must be taken into consideration when selecting the appropriate anesthetic protocol. In 1 study12 of a group of 17 zoo-kept BTPDs evaluated during inhalation anesthesia, measurements of tear production and IOP ranged widely. The objective of the prospective study reported here was to compare the effects of injectable DKM and ISO anesthetic protocols on ocular variables in BTPDs. The hypotheses were that both anesthesia protocols would impact measured ocular variables and that those measurements would differ significantly between protocols.
Materials and Methods
Nine zoo-kept BTPDs were admitted for annual health evaluations prior to incorporation into an established BTPD colony.a For the purpose of this study, the animals were group housed in a climate-controlled room with a 12-hour light-dark cycle (lights on from 7 am to 7 pm), room temperature of approximately 23°C, and relative humidity of 40% to 55%. The enclosure contained plastic hiding boxes and tubing for environmental enrichment. The BTPDs were fed commercial rodent pellets; the pellet diet was supplemented with a variety of grasses and vegetables. Fresh water was available ad libitum. This study was reviewed and approved by the Institutional Animal Care and Use Committee at Kansas State University and the ethics committee of the participating zoo.
Each BTPD underwent a periocular and anterior segment examination with slit-lamp biomicroscopyb performed by a board-certified veterinary ophthalmologist (JMM) as part of a full physical examination prior to inclusion in the study. By use of an online randomizer tool,c the BTPDs were each assigned to receive either the DKM or the ISO anesthetic protocol on the first study day. The BTPDs underwent the other anesthetic protocol after a 2-day interval. For the DKM protocol, a BTPD was collected from its enclosure and manually restrained. Dexmedetomidine hydrochlorided (0.25 mg/kg, IM), ketamine hydrochloridee (40 mg/kg, IM), and midazolam hydrochloridef (1.5 mg/kg, IM) were combined in 1 syringe and administered in the epaxial muscles. The BTPD was then placed in a clear plastic chamber for monitoring. Loss of the righting reflex was evaluated by rolling the BTPD into dorsal recumbency and monitoring whether the animal attempted to move itself back into sternal recumbency. Following completion of data collection, anesthesia was reversed with atipamezoleg (0.25 mg/kg, IM) and flumazenilh (0.1 mg/kg, IM), combined in 1 syringe and administered in the epaxial muscles. A second dose of flumazenil was administered if necessary. For the ISO protocol, a BTPD was collected from its enclosure and placed in a clear plastic induction chamber. The isoflurane vaporizer was set at 5% in oxygen at a flow rate of 5 L/min, and the inhalation anesthetic agent was introduced into the induction chamber until loss of the righting reflex was observed. The BTPD was then removed from the chamber, and delivery of the anesthetic gas was achieved through a close-fitting mask placed over the nose and mouth. The isoflurane vaporizer setting was decreased to 2% in oxygen at a flow rate of 2 L/min for maintenance of anesthesia. After completion of data collection, the isoflurane vaporizer was turned off, and the BTPD was provided with supplemental oxygen (100%) through the mask until spontaneous movement was observed. The BTPD was then moved to a recovery incubator, where it was observed during continued recovery from anesthesia. For each BTPD during both anesthetic periods, respiratory rate, heart rate, rectal temperature, oxygen saturation (as measured by pulse oximetry), arterial blood pressure (indirect measurement), and reflexes were continuously monitored and recorded every 5 minutes (from loss of righting reflex to recovery from anesthesia).
For all BTPDs undergoing each anesthetic protocol, the time at which loss of the righting reflex occurred was considered time of induction of anesthesia (0 minutes). All ocular variables were assessed by a single investigator (JKR) at 5, 30, and 45 minutes after induction of anesthesia. Horizontal pupil diameter (pupil size), globe position, and IOP were measured in both eyes of each BTPD. Pupil size was measured in millimeters with Castroviejo calipers (Figure 1). Pupils with a horizontal diameter < 1 mm were estimated at 0.5 mm. Globe position was recorded as central, ventrolateral, or ventromedial.
Photograph of 1 of 9 BTPDs during anesthesia with the DKM protocol (a combination of dexmedetomidine [0.25 mg/kg, IM], ketamine [40 mg/kg, IM], and midazolam [1.5 mg/kg, IM]). The pupil size (horizontal diameter) was measured in millimeters with Castroviejo calipers. This measurement was performed at 5, 30, and 45 minutes after induction of anesthesia (time of loss of righting reflex [0 minutes]). Similar measurements were obtained at these time points when the BTPDs underwent the ISO protocol (inhalation of isoflurane and oxygen).
Citation: American Journal of Veterinary Research 80, 9; 10.2460/ajvr.80.9.878
During both anesthetic episodes, tear production by each BTPD was evaluated by 2 methods: a PRTTi and an mSTTI.j Prior to examination and testing of each BTPD, an online randomizer toolc was used to determine the tear test method to be applied to each eye. To accommodate for the small palpebral fissure size and reportedly low volume of the aqueous portion of the tear film in BTPDs, the Schirmer tear test strips were modified as previously described by cutting each strip in half along its longitudinal axis through the plastic protective covering.12–14 The tear test thread or strip was inserted into the ventrolateral conjunctival fornix of the assigned eye with the aid of a small ophthalmic forceps (Figure 2). Between tear production measurements, the eyelids were taped closed to prevent corneal desiccation (Figure 3). Following the conclusion of data collection and cessation of anesthesia, the eyes were lubricated with a commercially available hyaluronic acid–based ocular gel.k
Photographs of a BTPD that was anesthetized with the DKM protocol illustrating the 2 methods used to quantitatively evaluate tear production. A—For this BTPD, the right eye was randomly selected to undergo a PRTT. A 3-mm folded portion of the thread is inserted into the ventral conjunctival fornix of the right eye with the aid of a small ophthalmic forceps. After 15 seconds, the thread is removed and the entire wet (red) portion is measured in millimeters with the ruler provided on the test strip packaging. This measurement was performed at 5, 30, and 45 minutes after induction of anesthesia. Similar measurements were obtained at these time points when the study BTPDs underwent the ISO protocol. B—The left eye underwent an mSTTI. To accommodate for the small size of the palpebral fissure and the reportedly low liquid tear volume in BTPDs, the Schirmer tear test strip is modified prior to use by cutting the strip in half along its longitudinal axis through the plastic protective covering. The notched end of the modified filter paper strip is inserted into the ventral conjunctival fornix of the left eye with the aid of a small ophthalmic forceps. After 1 minute, the filter paper strip is removed, and the amount of wetting is measured in millimeters. This measurement was performed at 5, 30, and 45 minutes after induction of anesthesia. Similar measurements were obtained at these time points when the study BTPDs underwent the ISO protocol.
Citation: American Journal of Veterinary Research 80, 9; 10.2460/ajvr.80.9.878
Photograph of a BTPD that was anesthetized with the DKM protocol. The eyelids of both eyes are taped closed between tear measurements to prevent corneal desiccation.
Citation: American Journal of Veterinary Research 80, 9; 10.2460/ajvr.80.9.878
Intraocular pressure was measured with a rebound tonometerl (D setting [internally calibrated for use in dogs]; Figure 4). For each eye at a given time point, a set of 6 IOP measurements was obtained; the highest and lowest measurements were automatically discarded, and the mean of the remaining 4 measurements was displayed as a single readout (ie, an individual IOP reading) on the tonometer display. An error bar (corresponding to the SD for the mean of the set of measurements) appeared with the IOP readout on the digital display. The low-error bar was associated with SD between IOP measurements of 1.8 to 2.5 mm Hg, and absence of an error bar was associated with SD ≤ 1 mm Hg. Only readings with a low-error or absence of an error notification on the tonometer display were accepted. Five consecutive individual IOP readings were obtained for each eye of each BTPD, and the mean IOP value for each eye at each time point was calculated.
Photograph of a BTPD that was anesthetized with the ISO protocol illustrating the method used to measure IOP. The BTPD was first placed in a clear plastic induction chamber into which isoflurane and oxygen were delivered; subsequently, isoflurane was delivered through a close-fitting mask over the nose and mouth. Intraocular pressure measurement of the eye was performed with a rebound tonometer (D setting [internal calibration used for dogs]). For each eye, IOP data were obtained at 5, 30, and 45 minutes after induction of anesthesia (0 minutes). Similar measurements were obtained at these time points when the BTPDs underwent the DKM protocol.
Citation: American Journal of Veterinary Research 80, 9; 10.2460/ajvr.80.9.878
Statistical analysis was performed with commercially available computer software.m Longitudinal data analysis was performed with linear mixed modeling of the various outcome variables with time, protocols (DKM and ISO), other variables (side [ie, right eye vs left eye]), and interaction effect as fixed effects and BTPD as the random effect. Residual plots were used to assess linearity, homogeneity of variances, normality, and outliers. Quantile plots were also performed on the residuals by protocol for normality assessment. Autocorrelation of the residuals over time was assessed with the autocorrelation function method. An ANOVA was performed on the fixed effects, and post-hoc comparisons were performed with a Tukey adjustment. Binary variables were analyzed with a logistic mixed model with the aforementioned explanatory variables. Residuals were evaluated graphically. With regard to globe position, logistic regression analysis could not be used because the DKM protocol did not result in any position other than central; thus, a McNemar test for dependent proportions was used instead. Results were considered significant at a value of P ≤ 0.05.
Results
The 9 BTPDs included in the study were sexually intact males; their ages ranged from 6 to 12 months and weights ranged from 600 to 894 g. There were no significant differences between right and left eyes for values of pupil size, globe position, PRTT, mSTTI, or IOP at any time point. Mean values for pupil size, PRTT, STT, and IOP were each calculated by combining data (both right and left eyes) at each time point (5, 30, and 45 minutes) for each anesthetic protocol. Because of self-trauma during the induction period of the DKM protocol, data from 1 BTPD were excluded from analyses.
Ocular variables were measured during each protocol and summarized (Table 1). When the BTPDs underwent the ISO protocol, mean pupil size at all 3 time points was significantly (P < 0.001) smaller than that determined when the BTPDs underwent the DKM protocol. The overall mean ± SD pupil size across all time points when the BTPDs underwent the ISO protocol was 0.67 ± 0.2 mm. The overall mean ± SD pupil size across all time points when the BTPDs underwent the DKM protocol was 2.80 ± 0.52 mm. Pupil size decreased significantly (P < 0.001) over time with both protocols.
Ocular variables measured in 9 BTPDs that were anesthetized with a DKM or ISO protocol in a randomized complete crossover study (2-day interval between anesthetic episodes).
| Time after induction of anesthesia (min) | ||||
|---|---|---|---|---|
| Variable | Protocol | 5 | 30 | 45 |
| Pupil size (mm)* | DKM | 3.09 ± 0.64 | 2.63 ± 0.53 | 2.69 ± 0.40 |
| ISO | 1.03 ± 0.61† | 0.50 ± 0† | 0.50 ± 0† | |
| Globe position | DKM | Central (16) | Central (16) | Central (16) |
| (No. of eyes) | Other (0) | Other (0) | Other (0) | |
| ISO | Central (12) | Central (12) | Central (11) | |
| Other (6)‡ | Other (6)‡ | Other (7)‡ | ||
| PRTT (mm/15 s)§ | DKM | 11.00 ± 2.27‖ | 5.25 ± 1.98‖ | 6.38 ± 3.07‖ |
| ISO | 15.00 ± 5.34 | 7.22 ± 3.27 | 6.56 ± 1.88 | |
| mSTTI (mm/min)¶ | DKM | 3.88 ± 0.35 | 2.75 ± 0.71 | 2.69 ± 0.80 |
| ISO | 3.56 ± 0.73 | 3.44 ± 0.73 | 3.11 ± 0.78 | |
| IOP (mm Hg)# | DKM | 8.45 ± 2.82 | 5.68 ± 1.93 | 4.90 ± 1.25 |
| ISO | 7.93 ± 2.61 | 5.88 ± 2.20 | 5.51 ± 2.56 | |
Except for globe position, data are reported as mean ± SD. Because of self-trauma during the induction period of the DKM protocol, data from 1 BTPD were excluded from analyses for this protocol.
Pupil size decreased significantly (P < 0.001) over time with both protocols.
Mean pupil size was significantly (P < 0.001) smaller when the BTPDs underwent the ISO protocol, compared with findings for the DKM protocol.
Significantly (P < 0.001) more eyes had globe positions other than central during the ISO protocol, compared with findings for the DKM protocol.
The PRTT value decreased significantly (P < 0.001) over time with both protocols.
Mean PRTT values were significantly (P = 0.04) lower when the BTPDs underwent the DKM protocol, compared with findings for the ISO protocol.
The mSTT1 value decreased significantly (P = 0.002) over time with both protocols.
The IOP decreased significantly (P < 0.001) over time (mean rate of change, 1.1 mm Hg/15 min) with both protocols.
For the DKM protocol, each BTPD was administered a combination of dexmedetomidine (0.25 mg/kg, IM), ketamine (40 mg/kg, IM), and midazolam (1.5 mg/kg, IM). For the ISO protocol, each BTPD underwent inhalation of isoflurane and oxygen. Variables were assessed for both eyes at 5, 30, and 45 minutes after induction of anesthesia. Horizontal pupil diameter (pupil size) was measured in millimeters with Castroviejo calipers; pupils with a horizontal diameter < 1 mm were estimated at 0.5 mm. Globe position was recorded as central, ventrolateral, or ventromedial. For each BTPD, a PRTT was performed in one randomly selected eye and an mSTTI was performed in the other eye. Intraocular pressure was measured by rebound tonometry.
There was no significant effect of time on globe position, but significantly (P < 0.001) more BTPD eyes had globe positions other than central during the ISO protocol, compared with findings during the DKM protocol. With the ISO protocol, eyes were recorded as having globe positions other than central at 5 minutes in 6 eyes (n = 4 BTPDS), at 30 minutes in 6 eyes (5 BTPDs), and at 45 minutes in 7 eyes (7 BTPDs).
Tear production was measured by PRTT and mSTTI in all 9 BTPDs during the ISO protocol (n = 18 eyes) and in 8 of the 9 BTPDs during the DKM protocol (16 eyes). At all time points, the mean PRTT values were significantly (P = 0.04) lower when the BTPDs underwent the DKM protocol, compared with those obtained when the BTPDs underwent the ISO protocol. The mSTTI values did not differ significantly (P > 0.11) between the DKM and ISO protocols at any time point. The PRTT values and the mSTTI values decreased significantly (P < 0.001 and P = 0.002, respectively) over time when BTPDs underwent either the DKM protocol or the ISO protocol.
Intraocular pressure was measured in all 9 BTPDs during the ISO protocol (n = 18 eyes) and in 8 of the 9 BTPDs during the DKM protocol (16 eyes). Comparison of data collected during the 2 anesthetic episodes revealed no significant (P = 0.2) difference in IOP between protocols at any time point. Intraocular pressure decreased significantly (P < 0.001) over time (mean rate of change, 1.1 mm Hg/15 min) when BTPDs underwent either the DKM protocol or the ISO protocol.
Discussion
In the study of the present report, the effects of injectable and inhalation anesthetic protocols on pupil size, globe position, tear production, and IOP in captive BTPDs were evaluated and compared. Ocular examination of BTPDs is challenging because of their fractious nature, and an anesthetic protocol that is both safe and reliable is necessary to facilitate proper handling and examination. A study by Meekins et al12 reported in 2015 provided values for tear production and IOP in isoflurane-anesthetized BTPDs, and data obtained when BTPDs underwent the ISO protocol in the present study were similar.
In the present study, the BTPDs had significantly smaller pupil size during the ISO protocol, compared with data obtained during the DKM protocol, at all time points. Pupil size was significantly decreased at 45 minutes after induction of anesthesia, compared with the findings at 5 minutes after induction of anesthesia with either protocol. For BTPDs, the small size of the eyes and chemically induced pupil constriction make examination of the lens and posterior segment challenging. Although pharmacological pupil dilation was not attempted as part of this investigation, a previous study12 revealed poor response to pharmacological pupil dilation in a group of BTPDs during inhalation anesthesia. The miosis induced in the BTPDs during the ISO protocol in the present study occurred more rapidly and was more profound, compared with that observed during the DKM protocol. Additional research is needed to determine the influence of anesthesia or inherent factors within the species that may contribute to a small pupil size and failure to respond to pharmacological pupil dilation among BTPDs. It would also be interesting to determine whether the effects of tropicamide or another mydriatic agent could override the miosis induced by anesthetic agents. This may be important when considering posterior segment examination of anesthetized BTPDs.
Although there was no significant effect of time on globe position in the present study, significantly more BTPD eyes had globe positions other than central during the ISO protocol, compared with findings during the DKM protocol. Such alterations from a central globe position make performing a complete ophthalmic examination on BTPDs more difficult.
An important feature of the rodent eye is the small tear volume, which hinders quantitative tear measurement by standard methods.15 Tear production has been measured in other rodent species including chinchillas,16 guinea pigs,17,18 hamsters,19,20 capybaras,21 and lowland pacas.22 In veterinary medicine, the most commonly used quantitative tear film assessment method is the Schirmer tear test. An alternative test is the PRTT, which requires only a small volume of tears and a short testing time, making it ideal for use in very small animals such as rodents and other exotic species.
The mean values for both tear tests in the present study significantly decreased over time when BTPDs underwent the DKM or ISO protocol. At 5 minutes after induction of anesthesia, PRTT and mSTTI values in the BTPDs were comparable to values obtained in similar studies of chinchillas and guinea pigs.16–18 Tear test values in BTPDs and other small rodents are disproportionately low, compared with values in larger domestic mammals, such as dogs and cats. One theory to explain this discrepancy is that small rodents, such as chinchillas, guinea pigs, and BTPDs, inhabit desert or dry grassland environments; hence, low aqueous tear production may be a fluid conservation mechanism. Another explanation for the low tear test values may be that the aqueous component measured by the mSTTI and PRTT represents a smaller percentage of the overall trilaminar tear film composition, the greater proportion of which may be of mucus or lipid origin. This hypothetically more viscous tear film may serve as a protective barrier against organic debris encountered when rodents are burrowing in their environments.
Injectable and inhalation anesthetic agents are known to transiently decrease tear production in dogs,6–8 and this was also observed in the BTPDs of the present study. Although tear production measured by mSTTI and PRTT decreased significantly over time when BTPDs underwent the DKM or ISO protocol, there were no significant differences between the time-matched mean mSTTI or PRTT values for the DKM and ISO protocols. It has been documented that the anesthesia-induced decrease in tear production is transient in dogs, with tear production returning to normal 10 hours following cessation of general anesthesia in 1 study.6 The long-term effects of injectable and inhalation anesthesia protocols on tear production in BTPDs remain unknown, as it is generally impractical and unsafe to handle this species without chemical restraint.
Injectable and inhalation anesthetics also have known effects on IOP.5,9 −-11 With the exception of ketamine, all of the agents commonly used to induce general anesthesia reduce IOP through various mechanisms including relaxation of extraocular muscles, depression of the cerebral IOP control centers, facilitation of increased aqueous humor outflow, and reduction of arterial and venous blood pressures.9 Ketamine is a particularly useful anesthetic agent for immobilization of nondomestic animals because of the drug's capability of inducing a cataleptic state. However, because of its effect on IOP, ketamine is often a less desirable induction agent for animals undergoing ophthalmic surgery. The proposed mechanism for an increase in IOP associated with the use of ketamine is contraction of the extraocular muscles.10 α2-Adrenoceptor agonists such as dexmedetomidine have been extensively studied in veterinary species. The α2-adrenergic modulation of IOP is thought to involve inhibition of norepinephrine release and reduction of the stimulus for production of aqueous humor as well as ciliary vasoconstriction with subsequent decreased ciliary blood flow.11 In the present study, IOP significantly decreased over time when BTPDs underwent the DKM or ISO protocol, which supported the theory that the decrease in IOP may be time dependent. At each time point during the 2 anesthetic episodes, the IOP did not differ significantly between protocols. On the basis of these data, it appears that the DKM and ISO protocols are equally appropriate choices for anesthesia of animals in which maintenance of a low-normal IOP is necessary. The IOP values obtained from the BTPDs during the ISO protocol were also consistent with those reported previously for another group of isoflurane-anesthetized BTPDs.12
Limitations of the present study included the lack of oxygen supplementation in the DKM protocol and the relative subjectivity in horizontal pupil diameter measurements obtained by use of calipers during the anesthetic episodes. The BTPDs did not receive supplemental oxygen when undergoing the DKM protocol because the study was part of a larger investigation evaluating the feasibility of an injectable anesthetic protocol for field use in this species. Conditions were designed to mimic circumstances that may be encountered in the field, where certain supplies and equipment (eg, supplemental oxygen and a means of delivery) may not be available. Hypoxemia may influence some of the measured ocular variables during the DKM protocol, and lack of oxygen supplementation was considered an inherent difference between the 2 protocols. However, the data obtained reflected a clinical situation in which injectable anesthetic agents may have to be administered because of a lack of equipment required to deliver anesthetic gas and oxygen.
Use of direct caliper measurement is a common technique for evaluation of the effect of variables such as anesthetic agents on pupil size. Evaluation of horizontal pupil diameter by photodocumentation at the conclusion of the present study would have provided the most precise pupil size assessment. However, the accuracy of the caliper method was enhanced by having a single investigator conduct the measurements, thereby eliminating interobserver variability.
With the exception of a report12 published in 2015, there is a noticeable lack of information about ocular physiologic variables in BTPDs. To date, diagnosis and treatment of ophthalmic conditions in this species have been based on normative data established for other rodent species, even though extrapolation among species is not always appropriate. The data obtained from the present study suggested that different anesthetic protocols can lead to significant changes in certain ocular variables, which should be considered when performing ophthalmic examination in anesthetized BTPDs.
Acknowledgments
Funded by the Department of Clinical Sciences, College of Veterinary Medicine, Kansas State University and the Association of Exotic Mammal Veterinarians Research Grant.
The authors thank Kirk Nemechek and Jessie Roberts at the Sunset Zoo and Christine Hackworth, Dr. Elizabeth Hyde, Dr. Beverly Finneburgh, Sarah Ostrom, and Brian Becker for technical assistance.
ABBREVIATIONS
| BTPD | Black-tailed prairie dog |
| DKM | Dexmedetomidine-ketamine-midazolam |
| IOP | Intraocular pressure |
| ISO | Isoflurane inhalation |
| mSTTI | Modified Schirmer tear test I |
| PRTT | Phenol red thread test |
Footnotes
Sunset Zoo, Manhattan, Kan.
SL-15 slit lamp, Kowa Co, Tokyo, Japan.
Online randomizer tool. Available at: randomization.com. Accessed Sep 8, 2017.
Dexdomitor, Zoetis, New York, NY.
Ketaset, Zoetis, Madrid, Spain.
Versed, West-Ward Pharmaceutical Corp, Eatontown, NJ.
Antisedan, Zoetis, Madrid, Spain.
Flumazenil, Hikma Farmaceutica, Terrugem, Portugal.
Zone-Quick, Showa Yakuhin Kako Co, Tokyo, Japan.
Schirmer tear test, Intervet, Summit, NJ.
Optixcare ocular lubricant, Aventix, Burlington, ON, Canada.
Tonovet, Tiolat Oy Lumic International, Baltimore, Md.
R package, version 3.1-121, R Foundation for Statistical Computing, Vienna, Austria. Available at: www.r-project.org. Accessed Nov 6, 2017.
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