The treatment of choice for recurrent laryngeal neuropathy in horses is prosthetic laryngoplasty1–3 with uni-/bilateral ventriculocordectomy. However, coughing resulting from dysphagia is the most reported complication, ranging from 5 to 57% of horses affected.1,2,4–8 One of the proposed mechanisms for postoperative dysphagia is glottal closure insufficiency leading to glottic incontinence during swallowing.1,8–11 A deficit at the level of the vocal fold remnant, as a result of scarring from vocalcordectomy, can cause glottic incontinence such that adduction of the normal arytenoid results in a persistent opening to the rima glottidis.10,12 Augmentation (ie, bulking) of the vocal fold to restore normal geometry of the rima glottidis has been employed by the authors for the treatment of glottal insufficiency in horses.10
Vocal fold augmentation (VFA), also known as injection medialization laryngoplasty, has been performed in human medicine as a barrier enhancement for the treatment of glottal closure insufficiency and for restoration of voice after vocal fold paralysis.13 Teflon was originally introduced as a bulking agent, which remained the standard for 30 years.14,15 However, long-term studies revealed granulomatous reactions in some patients.13 A number of long-lasting products have been evaluated in humans including autologous fat, calcium hydroxyapatite (Radisse), and polydimethylsiloxane.16–19 The problem with these materials used in humans is that they are designed to last 6 months to 2 years after which time laryngeal reinnervation is expected to have occurred.19 In horses, laryngeal reinnervation is described as a treatment for laryngeal hemiplegia; however, this procedure targets the cricoarytenoid dorsalis muscle alone. The need in horses requiring VFA is permanent, and a long-term substance is desirable.10,20
Polymethyl methacrylate was initially selected as a material because it is a durable, inert substance that rarely results in inflammatory tissue reaction, and, in human research, survival probabilities of implanted PMMA have been upward of 50 years.21–23 However, the chemical reaction occurring from mixing the PMMA polymer with the liquid monomer is exothermic, yielding temperatures greater than 124 °C.21,24 Polymethyl methacrylate is a polyphasic substance; it initially has the properties of a liquid but becomes more elastic as it approaches the doughing phase.25 More recently, PMMA has been used during its liquid phase for injection vertebroplasty in vertebral body compression fractures.25–27 Its use in the equine larynx requires a moderately viscous state to facilitate injection through an 18-gauge 3.5-inch spinal needle, and a luer-lock syringe.10 The addition of hyaluronic acid to PMMA to alter peak temperatures and working times has been investigated, in which higher aqueous fractions of hyaluronic acid resulted in lower peak temperatures but did not change the substrate injectability.27 PMMA has also been used for facial augmentation, facial reconstruction, and medialization laryngoplasty in humans as preformed PMMA microspheres suspended in bovine collagen, thereby eliminating the exothermic reaction to occur in the patient.22,23,28,29 The influence of decreasing the concentration of PMMA powder has not previously been investigated. The aims of this study were to determine the working time, setting time, peak temperature, and time to peak temperature of varying concentrations of PMMA in vitro.
The hypothesis was that using lower volumes of powder with the same volume of liquid would yield PMMA substrates with lower peak temperatures and longer working times, setting times, and times to peak temperature using an in vitro injection device.
Methods
Experimental model
Polymethyl methacrylate radiopaque bone cement (Surgical Simplex P Bone Cement; Stryker) was used for this study. It is packaged into 2 components: a 20-mL liquid ampule (97.4% vol/vol methyl methacrylate monomer, 2.6% vol/vol N,N-dimethyl-p-toluidine, and 75 ± 15 ppm hydroquinone) and a 40-gram packet of fine white powder (15% wt/wt polymethyl methacrylate, 75% wt/wt methyl methacrylate-styrene-copolymer, and 10% wt/wt barium sulfate UPS) hereto referred to as PMMAp. Manufacturer-recommended concentration results in a ratio of 6:1 PMMAp:solvent (Table 1). Clinical experience guided the volumes chosen in this study, where historically the concentration of PMMA used for VFA in horses was between half strength (3:1 dilution) and quarter strength (1.5:1 dilution). In this study, 4 ratios were investigated: 1.5:1, 2:1, 2.5:1, and 3:1, which are equivalent to volumes of 15, 20, 25, and 30 mL, weighing 5, 6.66, 8.32, and 10 grams of the powder. Powder volumes are referenced throughout the remainder of the text as they pertain to PMMA measurement clinically. For all experiments, the designated volume of PMMAp was weighed and hand mixed with 10 mL liquid solvent for 1 minute at a rate of ∼100 movements per minute using a bowl and spatula exposed to ambient atmosphere.
Dilutions of polymethyl methacrylate (PMMA).
| PMMA dilution (powder:liquid) | Volume PMMAp (mL) | Weight PMMAp (g) | Volume liquid solvent (mL) |
|---|---|---|---|
| 1.5:1 | 15 | 5 | 10 |
| 2:1 | 20 | 6.66 | 10 |
| 2.5:1 | 25 | 8.32 | 10 |
| 3:1 | 30 | 10 | 10 |
| 6:1 (standard package) | 120 | 40 | 20 |
The equivalent volume or weight of polymethyl methacrylate powder (PMMAp) mixed with 10 mL liquid solvent is indicated.
Temperature data were acquired using a handheld digital 4-channel data logger thermometer (model HH374; Omega Engineering Inc) with PC interface for data storage (sample rate, 0.2 Hz) using 20-gauge TT insulated type K-wire thermocouples. Following mixing, the formulation was transferred into 6-mL syringes with a total volume of 4 mL in each syringe; each test was run in triplicate. The K-wire thermocouples were inserted into the injection port of the syringes for temperature recording from the center of the volume of PMMA. Data acquisition was started following complete mixing and transferring of PMMA to syringes; 1 minute was allotted for mixing and 1 minute for transfer of PMMA. Temperature readings were recorded until the PMMA equilibrated back to room temperature after reaching peak. A fourth probe was used to measure ambient temperature. In accordance with ISO 5833, testing conditions were carried out at an ambient temperature 23 ± 1 °C and a humidity of not less than 40%. Temperature was plotted against time to extract peak temperature (Tmax), set time (tset), and time to peak temp (tmax). Peak temperature was recorded for each probe and rounded to the nearest degree Celsius. The setting time (tset) was calculated as the time at which set temperature (Tset) was reached and rounded to the nearest 15 seconds;
The force data were collected using the same mixing methods and conditions. After complete mixing of the PMMA, it was transferred to the injection device consisting of a 6 mL luer-lock syringe attached to an 18-gauge 3.5-inch spinal needle. Two minutes were allotted for complete mixing and transfer of PMMA to the injection device. A digital force meter (Torbal FB200; Cole-Parmer) was used to measure the force required to manually push 0.2 mL through the injection device into air. Force measurements were collected in Newtons (N) at a sample rate of 0.017 Hz (1-minute intervals) until 0.2 mL PMMA could no longer be expressed. Force was plotted against time to represent injectability; a linear regression was used for each sample to calculate the working time or the time at which 150 N of force was required to extrude PMMA. A force of 150 N has been used previously as a reflection of working time for injection vertebroplasty.26,27 Each experiment was run concurrently with a temperature data collection experiment providing the ambient temperature for both data sets. Tests were run in duplicate based on the volume of PMMA available per package, and each experiment was run twice to simulate ISO 5833 temperature testing requirements resulting in 4 experiments per volume of PMMAp. A power calculation was not performed given this technique is novel, and outcomes were unknown before carrying out the experiments. Statistical analysis was performed following the 4 experiments to determine if statistical significance was achieved or if further experiments were required. Additionally, data were analyzed with a post hoc power calculation.
Statistical analysis
Data were tested for normality using a Shapiro-Wilks test. One-way ANOVA Kruskal-Wallis test was used with post hoc Tukey application to compare differences between PMMAp volumes for peak temperature, set time, and time to peak temperature. Linear regression was used to report force versus time for each concentration; regression coefficients and coefficients of determination (R2) were reported. The impact of different concentrations of PMMAp on the force required to inject while controlling for time was analyzed using a mixed model with fixed effects time and concentration and random effects test number (n = 4, repeated measures). A pairwise comparison post hoc Tukey of least squares means was used to compare the different volumes of PMMA. One-way ANOVA Kruskal-Wallis test with post hoc Wilcoxon application was used for pairwise comparison of working times. All statistical analyses were performed in commercially available software (JMP Pro 16), and significance was set at α = 0.05 or P ≤ .05.
Results
Peak temperatures increased with increasing volume PMMAp while setting times, times to peak temperature, and working times decreased. The mean ± SD is reported for peak temperature, setting times, times to peak temperature, and the median (IQR) reported for working time; each is reported sequentially per volume of PMMAp: 15, 20, 25, and 30 mL with the mean/median rounded to the nearest whole number or minute and 15 seconds (converted to a decimal). Complete experimental data are reported elsewhere (Supplementary Tables S1 and S2).
Peak temperatures and setting times
The peak temperatures ranged from 53 °C to 106 °C with peak temperatures that increased with increasing volumes of PMMAp (Figure 1). Mean peak temperatures for each concentration were as follows: 56 ± 2, 86 ± 4, 99 ± 7, and 101 ± 4 °C with all temperatures being significantly different from each other except for temperatures reported for 25 and 30 mL PMMAp. Setting times ranged from 24.25 to 13.50 minutes and decreased with increasing concentration of PMMAp. Pairwise comparisons of the means were all significantly different: 23 ± 0.56, 21 ± 1.06, 17 ± 0.83, and 14 ± 0.38 minutes, respectively, for 15, 20, 25, and 30 mL PMMAp (Figure 2). The time to peak temperature mirrored setting time trends, ranging from 28.75 to 15 minutes with pairwise comparisons of the means also being significantly different: 28 ± 0.74, 24 ± 0.95, 19 ± 0.68, and 16 ± 0.37 minutes for 15, 20, 25, and 30 mL PMMAp (Figure 3).
Box and whiskers plot for peak temperatures documented for each volume of polymethyl methacrylate powder (PMMAp). All pairwise comparisons are significantly different (P < .001) unless denoted not significant (ns).
Citation: American Journal of Veterinary Research 84, 12; 10.2460/ajvr.23.05.0110
Box and whiskers plot for the setting times calculated for each volume of PMMAp. All pairwise comparisons are significantly different (P < .0001).
Citation: American Journal of Veterinary Research 84, 12; 10.2460/ajvr.23.05.0110
Box and whiskers plot for the time to reach peak temperature for each volume of PMMAp. All pairwise comparisons are significantly different (P < .0001).
Citation: American Journal of Veterinary Research 84, 12; 10.2460/ajvr.23.05.0110
Injectability and working times
The force (N) required to inject 0.2 mL PMMA through the injection device was correlated with time via linear regression to represent the injectability (Figure 4). Regression coefficients, or the rate of polymerization, increased with increasing volumes of PMMAp and are reported as the regression coefficient ± SE followed by the coefficient of determination (R2). The 15-mL volume of PMMAp resulted in the lowest regression coefficient 7.67 ± 0.45 (R2 = 0.96). Sequentially, the 20-mL volume had a regression coefficient of 12.93 ± 0.41 (R2 = 0.99), 25 mL had a regression coefficient of 16.24 ± 2.04 (R2 = 0.9), and 30 mL had the highest regression coefficient of 21.56 ± 6.18 (R2 = 0.86). From the mixed model, fixed effects time and concentration were significant (P < .0001 for each) with all pairwise comparisons of each concentration being significantly different. From the linear regressions, the working times (time at force = 150 N) were calculated and were inversely proportional to the volume of PMMAp: 22.75 (19.75 to 24.55), 12.25 (8.93 to 12.79), 7 (6.25 to 9.46), and 4 (3.33 to 4.72) minutes, respectively, for 15, 20, 25, and 30 mL powder (Figure 5). Pairwise comparisons of each working time were significantly different, except for the volumes of 20 and 25, which approached significance (P = .06). Post hoc power calculation yielded a power of 96%.
Linear regression of the injectability (force required to push 0.2 mL PMMA bone cement through the injection device) for different volumes of PMMAp. Each plotted point represents the mean force at each time point.
Citation: American Journal of Veterinary Research 84, 12; 10.2460/ajvr.23.05.0110
Box and whiskers plot for working time or the time until greater than 150 N of force is required to inject PMMA bone cement through the injection device for different volumes of PMMAp. All pairwise comparisons are significantly different except the 20- and 25-mL volume of PMMAp (P = .06).
Citation: American Journal of Veterinary Research 84, 12; 10.2460/ajvr.23.05.0110
Discussion
This study determined the peak temperatures, the working times, setting times, and the times to peak temperature of varying concentrations of PMMA in vitro. The hypothesis that lower concentrations of PMMA would result in longer working times, setting times, and times to peak temperature was accepted. However, the hypothesis that lower peak temperatures would be associated with lower concentrations of powder was partially rejected.
Peak temperatures increased with increasing concentrations of PMMA powder; however, there was no significant difference between 25 and 30 mL of powder, with mean values being nearly equal at 99 °C and 101 °C (Figure 1). The SDs for 25 and 30 mL of powder were larger, most notably for 25 mL of powder, which suggests there was more variability in the data. While the same mixing protocols were adhered to for all samples, it is possible the amount of PMMA powder in each syringe was variable, resulting in differences in peak temperature. It is also possible peak temperatures are not linearly related to the concentration of PMMA. Ambient temperature has also been proven to alter the handling, thermal, and physical properties of PMMA.25 As ambient temperature rises, the exothermic reaction is accelerated resulting in an elevation of peak temperature and more rapid setting times.25 In 1 study,25 the time to reach a given viscosity decreased by half when ambient temperatures increased from 19 to 25 °C. ISO 5833 requires tests be carried out at 23 ± 1 °C; upon reflection of ambient temperatures recorded, 1 sample of the 25-mL volume was carried out at 24 °C, which could explain the higher peak temperatures recorded, and emphasizes the influence of ambient temperature on the exothermic reaction of PMMA. Injection in vivo requires injection into body temperature, which is approximately 15 °C higher than the ambient temperatures reported. Funk et al30 in 2021 reported that simulated in vivo conditions for total knee arthroplasty using dental impression material PMMA resulted in a decrease of peak temperature from 34.33 °C to 9.74 °C with a decrease in setting time by approximately 5.5 minutes. While the aforementioned study was not carried out in true in vivo conditions and they used dental impression material, the principles of decreasing peak temperatures and decreasing set time may be inferred from the use of PMMA in the vocal fold of horses. Peak temperatures for full-strength PMMA have been reported in the literature as high as 124 °C in vitro.24,31 Temperature and duration of exposure both affect the degree of thermal necrosis.32 Thermal necrosis of bone tissue exposed to PMMA has been documented to occur at temperatures of 50 °C for a 1-minute duration and has resulted in hip arthroplasty implant failure in humans with temperatures exceeding 100 °C.31,33 Similarly, another study32 reported epidermal hyperthermic edema from 44 °C to 55 °C with irreversible damage occurring between 50 °C and 55 °C in the skin of guinea pigs. In the current study, peak temperatures ranged from 56 °C to 106 °C; therefore, regardless of the volume of PMMAp, some degree of thermal necrosis could be expected. It is surprising the exothermic reaction does not preclude the use clinically in humans; however, it is postulated the body is efficient at conducting heat away from the PMMA like a heat sink.34 This is supported by Funk et al30 as well as another study34 that found temperatures in in vivo PMMA bone cement arthroplasty peaked at 49 °C, where the remaining PMMA in the mixing bowl peaked at 110 °C. Other research35 has investigated the use of PMMA for craniofacial surgery, in which in vitro PMMA implants were irrigated with cooled saline (4 °C) resulting in a reduction of peak temperature from 81.4 °C to 41.8 °C. Therefore, our intention to cool the injection area in clinical cases with refrigerated saline as temperatures peak is warranted,10 ergo, the impetus of reporting times to peak temperature in this study. Clinically, the authors have experienced few complications with VFA in horses with 1 horse, of the previously 35 reported, having extrusion of the column of PMMA into the larynx 3 months postoperation.10 It is unknown if this could have been the result of thermal necrosis or possibly implant infection. The procedure requires injection submucosally; therefore, it is reasonable to consider the mucosa overlying the PMMA is at risk of thermal necrosis. Given the low incidence of complications, it is suspected the peak temperatures in vivo do not reach the same in vitro peak temperatures. Since the previous publication, the authors have performed the procedure on over 30 additional of horses with no other horses having suspected complications from thermal necrosis.
As volumes of PMMA powder increased, the working times, setting times, and times to peak temperature decreased. The working time reflects the time the PMMA can be injected, and it is important to consider in the clinical setting as horses are sedated and may unpredictably move during the procedure. Therefore, a concentration that allows sufficient time to inject, but does not prolong the procedure, is ideal. In this study, the working times calculated from the linear regression model were 22.75, 12.25, 7, and 4 minutes, respectively, for 15, 20, 25, and 30 mL powder. It is important to note the coefficients of determination (R2 values) decreased with increasing concentrations, which implies there was more variability in the data for the higher concentrations of PMMA. With higher concentrations of PMMA, the PMMA polymerized faster, which resulted in only a few minutes of injection time and therefore limited data points. More samples or testing injectability more frequently (ie, every 15 seconds vs every 60 seconds) may have decreased the variance by producing more data points, thereby creating a fit line with a higher coefficient of determination. Alternatively, the rate at which PMMA polymerizes may not be linear, especially at higher concentrations. The working times decreased with increasing PMMAp, with all concentrations being significantly different, apart from 20 and 25 mL PMMAp. The P value approached significance at P = .06; with a larger sample size, significance may have been achieved. Previous research by our group, reporting VFA in horses, used a volume of 25 to 28 mL PMMAp (2.5:1 to 2.8:1 ratio). With experience performing the procedure, the time required to successfully bulk the vocal fold decreased; therefore, the volume of PMMAp used has erred toward 28 mL in more recent procedures to decrease the setting time.10 During the injection period, if the PMMA is injected immediately, it will be too liquid and not sufficiently bulk the vocal fold, or a larger volume will be required to bulk the vocal fold. One limitation of this study is not documenting the time at which the viscosity of the PMMA becomes such that it would result in bulking of the tissue and not diffuse or settle in the ventral larynx. Nevertheless, anecdotally, the PMMA has been deemed ready to inject when 0.1 to 0.2 mL extruded from the needle onto the operating table remained in a droplet form versus settling out. In the aforementioned study,10 on average horses were injected with a total volume of 7.7 mL of PMMA in the vocal fold; however, with experience, the total volume decreased to 3 to 4 mL. Smaller volumes are likely to dissipate heat more readily due to increased surface area-to-volume ratio. As described previously, peak temperature and setting times seem to be largely influenced by in vitro versus in vivo conditions. However, working time is likely less affected by in vivo conditions given the PMMA to be injected is primarily exposed to ambient temperatures alone. It is unknown if the presence of the needle in equine soft tissues at body temperature could influence PMMA properties such that the working time is significantly different.
The primary limitation of this study is the inability to replicate the conditions in vivo, and therefore, conclusions can be inferred but are not absolute. Further research is warranted to assess PMMA properties in settings more representative of in vivo procedures, which could elucidate the risk of thermal necrosis in vivo as well as setting and working times. Additionally, a larger sample size could have minimized the variability in the force data. Preliminary injectability experiments were performed on the lowest concentration of PMMA, which had considerably less variability. A power calculation was not performed for the force data; however, post hoc power calculation yielded a power of 96% and the mixed model resulted in significant differences between all volumes of PMMA. A small sample size may have led to insignificant differences in peak temperatures between 25 and 30 mL PMMAp, a type II statistical error. With larger sample sizes, it is possible there is a difference between both concentrations. Alternatively, peak temperatures may increase nonlinearly, and there may be a threshold for peak temperatures in relation to PMMAp volume in which, at a certain volume of PMMAp, peak temperatures do not differ. Finally, a control sample at full strength was not included in the temperature data; however, there are robust data from the manufacturer and in the literature representing peak temperatures and setting times carried out at the conditions required by ISO 5833. A preliminary full-strength control sample was performed for the force data collection; however, no volume of PMMA could be extruded through the injection device even immediately after preparation and therefore was not included in the analysis.
The overarching conclusions are that working times, setting times, and times to peak temperature decrease with increasing concentrations of PMMA, and peak temperatures may reach as high as 101 °C in vitro. More research is required to determine ideal PMMA concentrations for use in vivo; however, this research may be translatable to use in vivo. The volume of PMMAp used should be chosen based on the desired working time as in vitro conditions are likely similar to operating room conditions.
Supplementary Materials
Supplementary materials are posted online at the journal website: avmajournals.avma.org.
Acknowledgments
None reported.
Disclosures
The authors have nothing to disclose. No AI-assisted technologies were used in the generation of this manuscript.
Funding
Funding was provided by Harry M. Zweig Fund for Equine Research Account 4808582.
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