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Intraocular Pressure Measurement by Rebound Tonometry (TonoVet) in Normal Pigeons (Columba livia).

Abstract: We evaluated the applicability of a rebound tonometer (TonoVet) in pigeon eyes and established normal reference intraocular pressure (IOP) values in healthy pigeons; 20 eyes of euthanized pigeons were used for calibration of the TonoVet and 48 eyes of 24 adult pigeons were used for measurement of reference IOP. First, IOP of pigeon eyes ex vivo were measured using the 'd' and the 'p' modes of the TonoVet and compared to manometric IOP values from 5 to 80 mm Hg. Then, to establish normal reference values, IOP was measured from clinically normal pigeons in vivo. The 'd' and the 'p' modes of the TonoVet showed a strong linear correlation with the manometric IOP ([R.sup.2] = .996 and .991, respectively). The obtained regression formulas were: [y.sub.1] = 0.439x + 2.059 and [y.sub.2] = 0.330x - 0.673, respectively ([y.sub.1], 'd' mode of TonoVet; [y.sub.2], 'p' mode of TonoVet; x, manometric IOP). The 'd' and the 'p' modes consistently measured one-half and one-third of the actual IOP, respectively. Therefore, the formula obtained through the 'd' mode was applied to obtain reference values. The calibrated IOP of normal pigeon eyes was 19.5 [+ or -] 4.4 mm Hg. The actual IOP could be calculated using the presented formula. Considering the limitations of the 'p' mode, use of the 'd' mode is more appropriate. Therefore, the TonoVet rebound tonometry under the 'd' mode is a reliable method for measuring IOP in pigeons.

Key words: intraocular pressure, rebound tonometry, TonoVet, reference values, avian, pigeons, Columba livia


Pigeons (Columba Livia) have a long history interacting with humans, and there are several domestic breeds. (1) Pigeons have been used as a model for several studies, such as atherosclerosis, (2) pulmonary extrinsic allergic alveolitis, (3) movement disorders, (4) ablating primary feather follicles, (5) effects of hormones and growth factors on cell growth and differentiation, (6) ischemic hypertension of the eye, (7) and so forth. Although pigeons have been used in various fields, such as an avian model for research, studies on pigeons are scarce, especially regarding their intraocular pressure (IOP). Measurement of IOP is an important part of ophthalmic examinations and an essential process for diagnosing glaucoma or uveitis. (8) To the best of our knowledge, there is no documented report of glaucoma in pigeons. However, glaucoma in other birds, especially secondary glaucoma due to causes, such as trauma, uveitis, and lens luxation, has been documented. (9) Because glaucoma is possible in pigeons, a reliable and precise method of IOP measurement for pigeons is needed.

Applanation and rebound tonometers are used widely in veterinary fields. The most commonly used tonometers are the TonoPen XL (Reichart; Depew, NY, USA; applanation tonometer) and the TonoVet (Icare; Tiolat, Helsinki, Finland; rebound tonometer). (10) Recent studies have widely used the TonoPen XL and TonoVet in other animals. (10-13) In a previous study, the TonoVet was tolerated well in pigeons. (14) The TonoVet is designed for animals, but an internal calibration curve has been developed only for the measurement of IOP in dogs and cats (the 'd' mode) and horses (the 'h' mode). (15) The tonometer should be calibrated because corneal characteristics vary among different species. (8) Therefore, it has been necessary to calibrate the IOP of pigeons and obtain a regression formula for measuring the actual IOP of live pigeons.

We calibrated the IOP values of the tonometer by manometry and established a reference IOP in normal pigeons.

Materials and Methods


Twelve pigeons (20 eyes) that were euthanatized for other research purposes were used immediately after euthanasia for manometric calibration, and 24 clinically normal pigeons (48 eyes) were surveyed to establish normal reference values of IOP. Healthy adult pigeons of undetermined sex were used in this study. Before the experiments, full ophthalmic examinations of all pigeons, including slit-lamp biomicroscopy (Keeler PSL One Portable Slit Lamp; Keeler Ltd, Windsor, UK) and direct ophthalmoscopy (WA 11720; Welch Allyn, Skaneateles Falls, NY, USA), were performed to confirm the absence of ocular diseases. All ophthalmic examinations and IOP measurements were performed by the same experienced examiner (JL) to reduce examiner bias. Three successive measurements per eye were obtained, and only values within the range of allowable standard deviation per the manufacturer ([less than or equal to] 2.5 mm Hg) were recorded. This was indicated by "no bar" or "bar down" on the display.

Manometric calibration of the TonoVet

Pigeons were fixated in a standing posture using a stereotaxic instrument (Model 900; Kopf Instruments, Tujunga, CA, USA). Lateral canthotomy was performed and the anterior chamber was cannulated medially at the limbus with a 30-gauge needle (Fig 1) connected to a system consisting of a pressure monitoring kit (Transpac IV Monitoring Kit; ICU Medical Inc, San Clemente, CA, USA) with a transducer, polyethylene tubes, monitoring cable (Transpac Reusable Cable; Hospira Inc, Lake Forest, IL, USA), and a monitor (CARESCAPE Monitor B650; GE Healthcare Finland Oy, Finland). The digital manometer was used to detect instantaneous IOP changes and to ensure that there was no leakage from the anterior chamber. A 3-way stopcock was used to connect the anterior chamber to the manometer and a NaCl solution. Artificial tears (Refresh Plus; Allergan, Irvine, CA, USA) frequently were applied topically to prevent the cornea from desiccation. Accuracy and reliability of the device were checked against a mercury manometer before conducting the experiments. For measurements, the 'd' and the 'p' modes (for dogs and unspecified, respectively) of the TonoVet were used. The IOP values measured by the TonoVet were compared with manometric IOP values from 5 to 80 mm Hg using a height-adjustable stand with the NaCl solution reservoir. The IOP measurements were performed when IOP was considered constant without fluctuation on the digital manometer. Measurements were performed in 5 mm Hg steps from 5 to 40 mm Hg, which was considered clinically significant, and in 10 mm Hg increments from 40 to 80 mm Hg. Animal care and procedures were approved by the Institutional Animal Care and Use Committees of the Seoul National University (SNU-160812-5).

Determination of normal pigeon IOP

Each pigeon was held in a relaxed posture and the wings were gently pressed against the body (Fig 2). The pigeons were measured after waiting approximately 3 minutes for stabilization. All measurements were obtained between 6:00 and 10:00 pm. The IOP was measured three times using the 'd' mode. Values were averaged and the obtained mean value was applied to the regression formula to calculate the actual IOP.

Statistical analyses

A paired Student's f-test was used to compare the IOP measurements per eye between left and right eyes. Data are presented as mean [+ or -] standard deviation (SD). The regression formula of the tonometry versus manometry was obtained via linear regression analysis. Tonometric and manometric values were compared using Bland-Altman plots. Statistical analyses were conducted with SPSS 23 software (IBM SPSS Statistics; Armonk, NY, USA).


Manometric calibration of the TonoVet

The postmortem IOP of 12 pigeons (20 eyes) was measured. Four eyes with abnormal findings were excluded. Comparison of manometric and tonometric IOP measurements showed significant differences between the methods (P < .001) over the entire pressure range. At 5 mm Hg, the values measured using the 'd' mode were comparable to the manometrically obtained values despite the fact that the difference was statistically significant. The 'd' mode consistently underestimated the actual IOP by approximately one-half from 10 to 80 mm Hg, whereas the 'p' mode consistently recorded approximately one-third of the actual IOP. Although the 'd' and 'p' modes of the TonoVet tended to underestimate the actual manometric values, both modes showed a strong linear correlation between tonometric and manometric values (Fig 3). The regression formulas for the 'd' and the 'p' modes were: [IOP.sub.d] - 0.439 x [IOP.sub.mano] + 2.059 (F = 2740.453, [R.sup.2] = .996, P < .001) and [IOP.sub.p] = 0.330 x [IOP.sub.mano] -0.673 1124.182, [R.sup.2] = .991, P < .001), respectively. Bland-Altman plots were used to show the difference between tonometry and manometry. The values gradually differed in the high IOP range in the 'd' and 'p' modes (Figs 4, 5). Manometric IOP was greater than tonometric IOP within the whole pressure range. Nevertheless, most plots were distributed within 95% limits, confirming that the measurement methods were well correlated.

Determination of normal pigeon IOP

Pigeons tolerated the procedure well because of the fast and reduced stress-inducing approach of rebound tonometry during the IOP measurement (24 pigeons, 48 eyes). Ophthalmic examinations revealed no evidence of ophthalmic diseases in all pigeons. There was no difference in IOP between left and right eyes (P = .381 and P = .556 in the 'd' and 'p' modes, respectively). Therefore, both eyes were analyzed without distinction.

The 'd' and 'p' modes were used for the measurements. However, only the values measured using the 'd' mode were analyzed for calibration, because the 'p' mode severely underestimated the actual IOP. The mean, median, and range of IOP values measured using the 'd' mode were 10.6 [+ or -] 1.9, 11, and 7-13 mm Hg, respectively. The calculated mean, median, and range of IOP values were 19.5 [+ or -] 4.4, 20.4, and 11.3-24.9 mm Hg, respectively (Table 1).


Normal IOP references have been established in domestic animals, such as dogs,' (16-20) cats, (21-22) horses, (17) calves, (23) and sheep, (24) and in laboratory animals, such as rats, (25,26) rabbits, (27,28) and mouse lemurs. (10) The IOP references for several avian species also have been reported. (8,15,29-39) In this study, the normal IOP reference data of the pigeon were evaluated.

The most commonly used tonometers in the veterinary field are the rebound tonometer, (TonoVet) and the applanation tonometer (TonoPen XL). (10) Previous studies have suggested differences in IOPs measured in birds between the 2 tonometers. (15,29) In addition, the basic settings of the TonoVet are applicable only to specific species, such as dogs, cats, and horses. (10) Therefore, to obtain the actual IOP from new species, tonometry should be calibrated using manometry. (10)

For various reasons, the TonoPen XL was not used for the measurements in this study. As mentioned in the previous study, the TonoPen XL causes stress, high systemic blood pressure, and additional compression to the eyeball, which could result in a high IOP value. (10) Also, the corneal diameter of the pigeon is <9 mm, which is unsuitable for application of the TonoPen XL. (9)

Manometric IOP (mmHg)

The transducer tip of the TonoPen XL (1.0 mm) is too large for small eyes and could cause reflex blinking. In addition, topical anesthesia is necessary and requires an extended measurement time up to 10 minutes. Furthermore, excessive focus on pressure, contact area, and body position can result in a high failure rate. (10)

A TonoLab (Icare) has been developed for small corneas, but the device was not considered in this study for two main reasons. First, the TonoLab was considered inappropriate for pigeons because it is rodent-specific for animals, such as mice and rats. Secondly, the TonoVet and the TonoPen XL have been used in various avian studies and are more commonly used in clinical practice than the TonoLab.

In this study, the TonoVet was selected for the measurements, because it is known to cause minimal response and reflex blinking when the probe contacts the cornea, and no additional force is needed to fixate the eye. In addition, the measuring time is short--approximately 30 seconds; the TonoVet is appropriate for the small cornea of the pigeon and topical anesthesia is unnecessary. Moreover, the measurements can be standardized and routinized quickly. (10)

In the previous study, the TonoVet was able to be used even in very small globes and was well tolerated, but as IOP increased, the accuracy of the TonoVet decreased. (14) However, using the obtained regression formula in this study to compensate for the difference, it is possible to obtain an accurate IOP in pigeons.

The TonoVet is a rebound tonometer that has 3 modes: 'd', 'h', and 'p' modes. The 'd' mode is applied to dogs and cats, 'h' mode to horses, and 'p' mode to unspecified animals. In our study, the 'd' and 'p' modes showed a strong linear correlation and had a tendency to underestimate the actual IOP. However, the 'd' mode was used to obtain the reference IOP because of some limitations in measuring with the 'p' mode. The 'p' mode values showed a larger difference from actual IOP values than the 'd' mode values. The 'd' mode measured approximately 50% of the actual IOP, whereas the 'p' mode was only able to measure approximately a third of the actual IOP. Moreover, in some eyes at the 5 mm Hg step, the IOP, as measured by the 'p" mode, was 0 mm Hg.

A previous study found that the average IOP values of pigeons in the 'd' mode was 11.7 [+ or -] 1.6 mm Hg (10 pigeons, 20 eyes). (40) Calculating this through the 'd' mode formula, the mean IOP was 22.0 mm Hg. In another study using the 'p' mode, mean IOP was 6.1 [+ or -] 0.9 mm Hg (100 pigeons, 200 eyes). (41) Applying this to the 'p' mode formula, the mean IOP was 20.5 mm Hg. In this study, the mean value of the pigeon IOP measured in the *d' mode was 10.6 [+ or -] 1.9 mm Hg (24 pigeons, 48 eyes). Converting this into the regression formula, the reference IOP of pigeons was actually 19.5 [+ or -] 4.4 mm Hg.

Direct measurements of IOP through an invasive method can be used only for calibration of noninvasive methods. (8) Considering the welfare of animals, postmortem measurement was conducted. Measurements after enucleation can result in lack of the orbital boundaries, which can affect the IOP measurement by changing the surrounding orbital structures. (8) Thus, only a lateral canthotomy was performed without enucleation, such that unnecessary procedures would not affect the IOP. Using the stereotaxic instrument, it was possible to avoid any other interference to the measurement of IOP.

In determining the reference IOP, there was a lack of information, such as sex and age. There also were insufficient pigeon populations. In addition, diurnal variation was not investigated. In this study, IOP was measured only in clinically normal pigeons. Further studies on pigeons with ophthalmic diseases, such as glaucoma or uveitis, are needed.

Our results suggested that the TonoVet is a well-tolerated and accurate instrument for measuring the IOP of pigeons. The 'd' mode of the TonoVet rebound tonometry is proper in measuring the IOP in normal pigeons. The 'd' mode consistently underestimated the actual IOP by approximately 50%. The actual IOP can be achieved by converting tonometric values using the regression formula.

Acknowledgments: Supported by a grant to Control of Animal Brain using MEMS Chip (CABMC) project funded by the Defense Acquisition Program Administration (UD140069ID).

Jaegook Lim, DVM, MS, Seonmi Kang, DVM, MS, PhD, Sangwan Park, DVM, Eunjin Park, DVM, Taekjin Nam, DVM, MS, Seowoo Jeong, DVM, MS, and Kangmoon Seo, DVM, MS, PhD, Dipl AiCVO

From the Department of Veterinary Clinical Sciences, College of Veterinary Medicine. Research Institute for Veterinary Science and BK 21 Creative Veterinary Research Center, Seoul National University, 1 Gwanak-ro, Gwanak-gu. Seoul. 08826. Korea.


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Caption: Figure 1. Experimental setting for the manometric calibration of the TonoVet used in measurement of intraocular pressure (IOP) in normal pigeon eyes in this study.

Caption: Figure 2. Rebound tonometry using the TonoVet in a pigeon that is being held in a relaxed posture.

Caption: Figure 3. All intraocular pressure (IOP) readings measured using the 'd' (open square) and 'p' (open circle) modes of the TonoVet in the study of IOP in normal pigeon eyes. Some points are superimposed.

Caption: Figure 4. Bland-Altman plot for comparison of intraocular pressure (IOP) measured using'd' mode of the TonoVet and the manometer in normal pigeon eyes. Dashed lines indicate 95% confidence intervals. Some points are superimposed.

Caption: Figure 5. Bland-Altman plot for comparison of intraocular pressure (IOP) measured using 'p' mode of the TonoVet and the manometer in normal pigeon eyes. Dashed lines indicate 95% confidence intervals. Some points are superimposed.
Table 1. The IOP values measured by rebound
tonometry of 48 eyes in 24 clinically normal pigeons.

Method             Median     Range     Mean [+ or -] SD

TonoVet'd' IOP,
mm Hg               11.0    7.0-13.0    10.6 [+ or -] 1.9

Calculated IOP,
mm Hg               20.4    11.3-24.9   19.5 [+ or -] 4.4
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Author:Lim, Jaegook; Kang, Seonmi; Park, Sangwan; Park, Eunjin; Nam, Taekjin; Jeong, Seowoo; Seo, Kangmoon
Publication:Journal of Avian Medicine and Surgery
Article Type:Report
Date:Mar 1, 2019
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