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Correlation of Serial Scleral and Corneal Pneumatonometry

      Purpose

      To evaluate the usefulness of scleral pneumatonometry as an alternative for corneal measurements of intraocular pressure (IOP) over a broad range of IOPs.

      Design

      Prospective, observational cohort study.

      Participants

      The study was conducted in the University of California, San Francisco, Retina Clinic between August and November 2013 in 33 adult patients (age range, 34–94 years; mean ± standard deviation, 74.1±13.4 years) receiving anti–vascular endothelial growth factor intravitreal injections, which transiently increase IOP.

      Methods

      Corneal pachymetry and serial corneal and temporal scleral pneumatonometry (baseline, immediately after, and 10, 20, and 30 minutes after injection) were collected. One-time baseline corneal and scleral pneumatonometry readings were obtained in the noninjected eye.

      Main Outcome Measures

      Correlation analysis and a Bland-Altman plot were used to evaluate reliability and agreement between scleral and corneal measurements of IOP. A linear mixed model was used to determine the relationship between measurements and to perform covariate analyses.

      Results

      Scleral and corneal pneumatonometry showed nearly 1:1 linear correlation, although scleral pneumatonometry was biased toward higher values (r = 0.94; P < 0.001). Scleral pneumatonometry averaged 9.0 mmHg higher than corneal pneumatonometry (95% limits of agreement, −1.5 to 19.5 mmHg). A linear mixed model resulted in the following equation: corneal IOP = 1.04 × scleral IOP − 10.37. Age, central corneal thickness, laterality, and glaucoma and lens status did not impact this relationship. The difference between corneal and scleral pneumotonometry was correlated between the two eyes of individual patients (r = 0.75; P < 0.001).

      Conclusions

      Differences between serial scleral measurements reflect differences between serial corneal measurements. Scleral pneumatonometry should be considered as an alternative to corneal pneumatonometry for following patients in whom corneal measurements are unreliable or unobtainable.

      Abbreviations and Acronyms:

      Corneal IOP (corneal pneumatonometry), IOP (intraocular pressure), Scleral IOP (scleral pneumatonometry)
      Intraocular pressure (IOP) normally is measured over the cornea. However, for patients with significant corneal pathology, such as scarring, thinning, and edema, or for those who have keratoprosthesis implants, corneal tonometry can be inaccurate or impossible to obtain. However, these corneal diseases are associated commonly with either primary or secondary glaucoma. For example, in the case of keratoprosthesis, difficulty with IOP measurement is a significant problem. Glaucoma has been reported to be a preoperative comorbidity in more than two-thirds of patients and to be newly diagnosed in an additional 13% to 25% of patients after keratoprosthesis implantation.
      • Talajic J.C.
      • Agoumi Y.
      • Gagné S.
      • et al.
      Prevalence, progression, and impact of glaucoma on vision after Boston type 1 keratoprosthesis surgery.
      • Kamyar R.
      • Weizer J.S.
      • de Paula F.H.
      • et al.
      Glaucoma associated with Boston type I keratoprosthesis.
      • Crnej A.
      • Paschalis E.I.
      • Salvador-Culla B.
      • et al.
      Glaucoma progression and role of glaucoma surgery in patients with Boston keratoprosthesis.
      Furthermore, keratoprostheses are associated with postoperative elevation in IOP and progression of glaucoma, which can become vision limiting.
      • Talajic J.C.
      • Agoumi Y.
      • Gagné S.
      • et al.
      Prevalence, progression, and impact of glaucoma on vision after Boston type 1 keratoprosthesis surgery.
      • Kamyar R.
      • Weizer J.S.
      • de Paula F.H.
      • et al.
      Glaucoma associated with Boston type I keratoprosthesis.
      • Crnej A.
      • Paschalis E.I.
      • Salvador-Culla B.
      • et al.
      Glaucoma progression and role of glaucoma surgery in patients with Boston keratoprosthesis.
      Scleral pneumatonometry has been proposed as an alternative method for IOP measurement in patients for whom corneal measurements are not possible. In a study performed in cadaveric eyes, we previously showed that serial measurements of scleral pneumotonometry correlate strongly and linearly to IOP when IOP was set from 20 to 50 mmHg by infusion cannula.
      • Lin C.C.
      • Chen A.
      • Jeng B.H.
      • et al.
      Scleral intraocular pressure measurement in cadaver eyes pre- and postkeratoprosthesis implantation.
      Importantly, this relationship was unchanged after the eyes underwent keratoprosthesis implantation. In patients, a cross-sectional study by Kapamajian et al
      • Kapamajian M.A.
      • de la Cruz J.
      • Hallak J.A.
      • Vajaranant T.S.
      Correlation between corneal and scleral pneumotonometry: an alternative method for intraocular pressure measurement.
      found a positive correlation between one-time corneal and scleral pneumatonometry in healthy adult patients. However, the IOP range was limited by the physiologic pressures of this population (10.5–27 mmHg), and the relationship between changes in corneal and scleral pneumatonometry in patients was not studied. Furthermore, scleral pneumatonometry generally resulted in higher measurements than corneal pneumatonometry, but this difference was highly variable across individuals (mean ± standard deviation, 8.4±5.7 mmHg).
      • Kapamajian M.A.
      • de la Cruz J.
      • Hallak J.A.
      • Vajaranant T.S.
      Correlation between corneal and scleral pneumotonometry: an alternative method for intraocular pressure measurement.
      For scleral pneumotonometry to be a useful clinical tool, scleral measurements should correlate to corneal measurements over a wide range of both physiologic and pathological pressures and have a predictable relationship over multiple measurements when used to follow patients clinically. Therefore, in the current study, we measured serial scleral and corneal pneumatonometry in patients receiving intravitreal injections, which transiently increase IOP, to evaluate the relationship between these 2 measurements over a broad range of IOPs. Since the baseline difference between scleral and corneal pneumatonometry in an eye with corneal disease may be unknown, in the case of unilateral or asymmetric disease, we hypothesized that one could use the contralateral eye as a surrogate for the baseline difference in the eye of interest. Thus, we also evaluated whether the difference between corneal and scleral measurements was correlated between the 2 eyes of individual patients.

      Methods

       Study Design

      The Institutional Review Board/Ethics Committee at University of California, San Francisco, approved this prospective observational study. This study complied with Health Insurance Portability and Accountability Act regulations and adhered to the tenets of the Declaration of Helsinki.
      Adult patients receiving anti–vascular endothelial growth factor intravitreal injections in the Retina Clinic of the University of California, San Francisco, were recruited between August and November 2013. We had a minimum target enrollment of 28 patients, which was predicted to have a 90% power to detect a correlation coefficient of 0.57 (based on the results from Kapamajian et al
      • Kapamajian M.A.
      • de la Cruz J.
      • Hallak J.A.
      • Vajaranant T.S.
      Correlation between corneal and scleral pneumotonometry: an alternative method for intraocular pressure measurement.
      ) with an α of 0.05 in an a priori sample size calculation. Patients with previous incisional glaucoma surgery, scleral buckle, strabismus surgery, refractive cornea surgery, scleral pathology such as thinning or scarring, or significant corneal pathology such as scarring or edema that would prevent accurate measurement of IOP over the cornea were excluded. The risks and benefits of participation were discussed with each participant and informed consent was obtained. We collected patient information on demographics, diagnosis of glaucoma, and lens status (phakia or pseudophakia) by chart review.

       Measurements

      A single observer (D.S.K.) obtained all measurements. Eyes were anesthetized with 1% proparacaine. At each time point, IOP measurements were obtained from the central cornea and temporal sclera with the edge of the pneumatonometer probe (Model 30 Classic; Reichert Ophthalmic Instruments, Depew, NY) placed directly temporal 1 mm from the limbus with the patient in primary gaze, which centered the probe approximately 3.5 mm posterior to the limbus. Corneal and temporal scleral pneumotonometry measurements (abbreviated as corneal IOP and scleral IOP, respectively) were obtained at baseline in both eyes before injection, and then serial measurement were obtained in the treated eye immediately after injection and 10, 20, and 30 minutes after injection. All measurements were obtained with patients sitting up. For each pair of measurements, we checked the corneal IOP before the scleral IOP. All corneal measurements had a standard deviation of less than 0.5 mmHg and all scleral measurements had a standard deviation of less than 1 mmHg for IOPs between 0 and 40 mmHg and a standard deviation of less than 1.5 mmHg for IOPs of more than 40 mmHg. The waveform was examined for good quality in all measurements with IOPs of less than 40 mmHg, where it was within the limits of the paper printout. We measured central corneal thickness by pachymetry (DGH-550 Pachette 2; DGH Technology, Inc, Exton, PA), averaging 5 measurements, at the time of the baseline measurements.

       Statistical Analysis

      The Pearson correlation coefficient is reported herein. For paired data with more than 1 time point for each study subject, an ordinary correlation coefficient is not appropriate because it does not take into account the lack of independence between repeated measurements for the same subject.
      • Bland J.M.
      • Altman D.G.
      Calculating correlation coefficients with repeated observations: part 1—correlation within subjects.
      Instead, we calculated a within-subjects correlation coefficient, which removes the variation between subjects to examine whether an increase in a variable within the same subject is associated with an increase in another variable.
      • Bland J.M.
      • Altman D.G.
      Calculating correlation coefficients with repeated observations: part 1—correlation within subjects.
      Similarly, agreement between scleral and corneal IOP was analyzed using a Bland-Altman plot with correction for multiple measurements per subject using MedCalc Statistical Software (MedCalc Software, Ostend, Belgium).
      • Bland J.M.
      • Altman D.G.
      Agreement between methods of measurement with multiple observations per individual.
      The data were fit with a linear mixed model with random slope and intercept using R (R Foundation for Statistical Computing, Vienna, Austria). Confidence intervals were derived from bootstrap analysis, an iterative resampling of the data. Covariate analysis was performed using the linear mixed model and likelihood ratio test with P < 0.05 considered statistically significant.

      Results

      Thirty-three patients ranging in age from 34 to 94 years were included in the study. Baseline characteristics are shown in Table 1. Pseudophakia was present in 52% of patients and glaucoma was present in 15% of patients. A total of 164 serial paired measurements of corneal and scleral IOP were obtained in the treated eye (1 subject missed 1 time point). Corneal IOPs ranged from 9 to 61.5 mmHg and scleral IOPs ranged from 13.5 to 74 mmHg. Thirty-two patients had baseline measurements of scleral and corneal pneumatonometry in the contralateral untreated eye. At baseline, the difference between scleral and corneal pneumatonometry measurements in the 2 eyes of individual patients was correlated significantly (r = 0.75; P < 0.001; Fig 1).
      Table 1Baseline Characteristics
      No. of patients enrolled33
      Mean age ± SD (yrs)74.1±13.4
      Eye (no.)
       Right20
       Left13
      Mean CCT ± SD (μm)552.4±37.0
      Lens status (no.)
       Phakic16
       Pseudophakic17
      Glaucoma (no.)5 (2 POAG, 1 steroid-induced, 2 NOS)
      CCT = central corneal thickness; NOS = not otherwise specified; POAG = primary open angle glaucoma; SD = standard deviation.
      Figure thumbnail gr1
      Figure 1Scatterplot showing baseline differences in scleral and corneal pneumatonometry in the 2 eyes of each patient. The value for the eye scheduled to undergo treatment with an anti–vascular endothelial growth factor agent is plotted on the x-axis and for the contralateral eye on the y-axis. Pearson correlation coefficient is shown. Reference values x = y are shown as a dotted line. IOP = intraocular pressure.
      We used correlation to analyze the linear association between serial scleral and corneal IOP by pneumatonometry and found that they were significantly correlated (r = 0.94; P < 0.001) for the injected eyes (Fig 2). The data were fit using a linear mixed model, which takes into account longitudinal measurements over time. This analysis resulted in the following equation: scleral IOP = 0.97 × corneal IOP + 10.0. The standard deviation of the residuals, an error measurement for the entire model, was 2.78 mmHg. The slope (mean ± standard deviation, 0.97±0.21 mmHg) was statistically significant (P < 0.001) and showed a nearly 1:1 relationship between changes in scleral and corneal IOP on average with some variability between individual patients (Fig 3A). Similarly, the intercept (mean ± standard deviation, 10.0±5.83 mmHg) was statistically significant (P < 0.001), but demonstrated greater variability among patients (Fig 3B).
      Figure thumbnail gr2
      Figure 2Scatterplot showing scleral versus corneal pneumatonometry. Data points from all measurements were plotted. The within-subjects Pearson correlation coefficient, evaluating the relationship between scleral and corneal intraocular pressure (IOP) in the same subject over multiple measurements, is shown. The solid line represents line of best fit from a linear mixed model with random slope and intercept (scleral IOP = 0.97 × corneal IOP + 10.0).
      Figure thumbnail gr3
      Figure 3Estimated (A) slope and (B) intercept for individual patients from a linear mixed model with random slope and random intercept. Slope represents the change in scleral intraocular pressure (IOP) per unit of change in corneal IOP. Intercept represents a systematic difference in baseline values between scleral and corneal IOP. The solid lines represent the means (slope, 0.97; intercept, 10.0) and the dotted lines show the 95% confidence intervals (slope, 0.87–1.06; intercept, 7.55–12.50) derived from bootstrap analysis, using repetitive data resampling to obtain a normal distribution of values for a collection of samples. The random effect standard deviation (SD) represents an additional variable accounting for stochastic differences between subjects. A histogram with the distribution of values is shown on the right of each graph.
      A Bland-Altman plot was created to examine the agreement of scleral IOP and corneal IOP over a range of IOP using data from serial IOP measurements (Fig 4). Scleral IOP averaged 9.0 mmHg higher than corneal IOP (95% limits of agreement, −1.5 to 19.5 mmHg). Importantly, there was not a trend toward larger differences at higher IOPs, but there were fewer data points and more outliers at higher values. For measurements with a mean of scleral and corneal IOP less than 40 mmHg, which are potentially more clinically relevant, 81.7% of the measurements were within 5 mmHg of the mean difference between scleral and corneal IOP.
      Figure thumbnail gr4
      Figure 4Difference plot of scleral and corneal pneumatonometry versus the mean of scleral and corneal pneumatonometry. Agreement between scleral and corneal intraocular pressure (IOP) was analyzed using a Bland-Altman plot with correction for multiple measurements per subject. Data from each subject are plotted with a different symbol. Perfect agreement would show a value of 0 for the difference between scleral IOP and corneal IOP across the range of IOPs. Mean IOP of 40 mmHg is marked as a clinically relevant reference point. Scleral IOP showed a bias toward higher values compared with corneal IOP, averaging 9.0 mmHg (95% limits of agreement, −1.5 to 19.5 mmHg). SD = standard deviation.
      To test the impact of age, eye laterality, central corneal thickness, lens status (phakia versus pseudophakia), and glaucoma on the relationship between scleral and corneal pneumotonometry, we added these covariates to the linear mixed model and evaluated them with a likelihood ratio test. None of these factors was statistically significant (Table 2).
      Table 2Covariates Do Not Impact Relationship between Scleral and Corneal Pneumotonometry
      FactorP Value
      Age0.36
      Eye0.41
      Central corneal thickness0.48
      Lens status0.60
      Glaucoma0.92

      Discussion

      This study was designed to evaluate the relationship between serial corneal and scleral pneumatonometry over a wide range of physiologic and pathologic levels of IOP. We found that scleral pneumatonometry was significantly correlated to corneal pneumatonometry, but was biased toward higher values. Although we did not compare scleral pneumatonometry directly with Goldmann applanation, the relationship between Goldmann applanation and corneal pneumatonometry has been well described (Tapplanation = Tpneumatonometry − 1.2), and corneal pneumatonometry has been reported to be age-independent and to correlate best with manometric IOP measurements compared with applanation and Tono-Pen (Reichert Ophthalmic Instruments, Depew, NY) IOP measurements in patients.
      • Eisenberg D.L.
      • Sherman B.G.
      • McKeown C.A.
      • Schuman J.S.
      Tonometry in adults and children. A manometric evaluation of pneumotonometry, applanation and Tono-Pen in vitro and in vivo.
      Scleral pneumatonometry previously was found to be increased compared with both corneal measurements and assigned IOP, and our results are consistent with prior reports (Table 3).
      • Lin C.C.
      • Chen A.
      • Jeng B.H.
      • et al.
      Scleral intraocular pressure measurement in cadaver eyes pre- and postkeratoprosthesis implantation.
      • Kapamajian M.A.
      • de la Cruz J.
      • Hallak J.A.
      • Vajaranant T.S.
      Correlation between corneal and scleral pneumotonometry: an alternative method for intraocular pressure measurement.
      The difference measured between scleral and corneal IOP likely reflects differences in the biomechanical properties between cornea and sclera, which can vary by quadrant and anterior–posterior location within an individual.
      • Friberg T.R.
      • Lace J.W.
      A comparison of the elastic properties of human choroid and sclera.
      • Patel H.
      • Gilmartin B.
      • Cubbidge R.P.
      • Logan N.S.
      In vivo measurement of regional variation in anterior scleral resistance to Schiotz indentation.
      We chose to obtain measurements over the sclera temporally in primary gaze because eccentric eye position can change IOP measurement and the temporal region is the most accessible and would be preserved even after glaucoma surgery.
      • Moses R.A.
      • Lurie P.
      • Wette R.
      Horizontal gaze position effect on intraocular pressure.
      • Nardi M.
      • Bartolomei M.P.
      • Romani A.
      • Barca L.
      Intraocular pressure changes in secondary positions of gaze in normal subjects and in restrictive ocular motility disorders.
      However, more studies are required to determine the optimal location for scleral pneumatonometry in patients.
      Table 3Studies of Scleral Pneumatonometry
      StudyCorrelation (r)Mean DifferenceEquation
      Kuo et al0.949.0 mmHg compared with corneal IOPcorneal IOP = 1.04 × scleral IOP − 10.37
      Lin et al
      • Lin C.C.
      • Chen A.
      • Jeng B.H.
      • et al.
      Scleral intraocular pressure measurement in cadaver eyes pre- and postkeratoprosthesis implantation.
      13.2 mmHg compared with assigned IOP
      Assigned IOP > corneal IOP by 3.78.
      assigned IOP = 1.01 × scleral IOP − 14.14
      Kapamajian et al
      • Kapamajian M.A.
      • de la Cruz J.
      • Hallak J.A.
      • Vajaranant T.S.
      Correlation between corneal and scleral pneumotonometry: an alternative method for intraocular pressure measurement.
      0.578.08 mmHg compared with corneal IOPcorneal IOP = 0.32 × scleral IOP − 0.05 × age + 11.90
      IOP = intraocular pressure; — = no data.
      Assigned IOP > corneal IOP by 3.78.
      Our results showed a significant correlation (r = 0.94) between scleral and corneal pneumatonometry in patients using a different approach from Kapamajian et al
      • Kapamajian M.A.
      • de la Cruz J.
      • Hallak J.A.
      • Vajaranant T.S.
      Correlation between corneal and scleral pneumotonometry: an alternative method for intraocular pressure measurement.
      (r = 0.57). Kapamajian et al obtained one-time measurements of scleral and corneal pneumatonometry in patients, which can give variable results for the relationship between corneal and scleral measurements because of the individual differences in scleral rigidity. In our study using patients from the retina clinic receiving intraocular injections, we were able to obtain multiple measurements per patient over a short period, spanning a large range of IOPs in each subject. This strategy allowed us to remove the variation among subjects and evaluate whether an increase in scleral pneumatonometry was associated with an increase in corneal pneumatonometry within an individual using a within-subjects Pearson correlation coefficient.
      In serial IOP measurements, we found close to a 1:1 linear relationship between changes in scleral and corneal pneumatonometry. This finding supports that following scleral pneumatonometry measurements would be useful clinically, because differences in scleral tonometry measurements reflect differences in corneal tonometry even at pathologically elevated levels of IOP. To calculate the predicted corneal IOP from a scleral IOP measurement, our data yielded the following equation: corneal IOP = 1.04 × scleral IOP − 10.37. This formula is remarkably similar to the one we found in our study of cadaveric eyes (Table 3).
      • Lin C.C.
      • Chen A.
      • Jeng B.H.
      • et al.
      Scleral intraocular pressure measurement in cadaver eyes pre- and postkeratoprosthesis implantation.
      The standard deviation of the residuals, which is a measure of the accuracy of predictions made with our model, is 2.8 mmHg. Therefore, measured differences greater than this value are likely to represent true changes in scleral pneumatonometry. This value is similar to the 95% measurement accuracy published for corneal pneumatonometry (1.5 mmHg between 0 and 40 mmHg and 3.5 mmHg between 40 and 80 mmHg).
      Model 30 Pneumatonometer User's Guide.
      On average, we found that scleral pneumatonometry was approximately 10 mmHg higher than corneal pneumatonometry in our model. This value was close to that obtained by analyzing the raw data using a Bland-Altman plot. The Bland-Altman plot also showed that the average difference between scleral and corneal pneumatonometry measurements appeared consistent over the range of IOPs that we tested. Furthermore, at more clinically relevant levels of IOP, such as mean scleral and corneal IOPs of less than 40 mmHg, more than 80% of measurements were within 5 mmHg of the average difference between scleral and corneal IOP (Fig 4).
      Ideally, to estimate best the corneal IOP from a scleral IOP measurement, a baseline measurement of corneal and scleral pneumatonometry should be obtained in the eye of interest before the development of significant corneal pathology to know the exact relationship between these measurements. In practice, this may not be feasible, and our data support the use of the contralateral eye to estimate the baseline difference between scleral and corneal IOP in the eye of interest, because the 2 eyes are significantly correlated within an individual (Fig 1). Using this calculated relationship between scleral and corneal pressure in the contralateral eye of an individual would be more accurate than using an estimate from a population-based equation. Because the relationship between Goldmann applanation tonometry and pneumotonometry is linear, one could use the baseline difference between Goldmann applanation of the cornea and scleral pneumatonometry in the contralateral eye to estimate the predicted Goldmann applanation value for the eye of interest using scleral pneumatonometry.
      • Eisenberg D.L.
      • Sherman B.G.
      • McKeown C.A.
      • Schuman J.S.
      Tonometry in adults and children. A manometric evaluation of pneumotonometry, applanation and Tono-Pen in vitro and in vivo.
      In our patient population, the relationship between scleral and corneal pneumatonometry was not impacted by age, eye laterality, central corneal thickness, glaucoma, or lens status. Age has been shown to affect scleral rigidity and was reported to affect the relationship between scleral and corneal pneumatonometry significantly in the study of Kapamajian et al.
      • Kapamajian M.A.
      • de la Cruz J.
      • Hallak J.A.
      • Vajaranant T.S.
      Correlation between corneal and scleral pneumotonometry: an alternative method for intraocular pressure measurement.
      • Pallikaris I.G.
      • Kymionis G.D.
      • Ginis H.S.
      • et al.
      Ocular rigidity in living human eyes.
      One possibility for age not affecting our model significantly is that we had an older population of patients. The mean age of our population was 74.1±13.4 years compared with 54.4±17.7 years in the study by Kapamajian et al. Although the range of ages in our patient population did span 34 to 94 years, we may not have been powered adequately to detect a difference in age on scleral IOP. Furthermore, there may be changes to the sclera related to intravitreal injections or underlying disease that were not assessed. Additionally, we evaluated only adult patients in our study, which limits the generalizability of our results. Additional studies are needed to understand the relationship of scleral IOP to corneal IOP for children because there are significant differences in scleral rigidity between adult and pediatric populations.
      Accurate and reliable IOP measurements are important for both diagnosing and treating glaucoma. In patients for whom corneal measurements are not possible or are unreliable, scleral pneumatonometry should be considered as a potential alternative. Our results support consistency of the relationship between scleral and corneal pneumatonometry across the range of physiologic and pathologic IOPs for individual patients and show that changes in scleral pneumatonometry reflect changes in corneal pneumatonometry.

      Acknowledgments

      The authors thank Seth Blumberg, MD, PhD, and Travis Porco, MPH, PhD, for their guidance with statistical analysis.

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