Evaluation of Pulse Oximetry in Healthy Brachycephalic Dogs
ABSTRACT
Brachycephalic airway syndrome (BAS) is characterized by increased upper airway resistance due to conformational abnormalities occurring in brachycephalic dogs (BD). In this prospective study, we evaluated pulse oximetry (SpO2) and arterial blood gas values in 18 healthy BD and compared these values with those of 18 healthy mesocephalic and dolichocephalic dogs (MDD). All dogs were assigned a BAS score based on an owner questionnaire. Inclusion criteria included presentation to the hospital for a problem unrelated to the respiratory system and unremarkable blood analyses and physical examination. In awake dogs, SpO2 values were obtained from a minimum of two sites. Dogs were then sedated, and SpO2 values were obtained again concurrently with an arterial blood gas sample. The SpO2 values were significantly lower in BD compared with MDD, but there were no statistically significant differences between BD and MDD for any arterial blood gas parameters. Based on the BAS score, BD who were moderately BAS-affected (n = 5), had significantly lower arterial saturation of hemoglobin with oxygen values on arterial blood gas when compared with MDD (n = 18). Although BD had statistically lower SpO2 values than MDD, the mean SpO2 values for both groups were within the normal range.
Introduction
Brachycephalic dogs (BD) are commonly treated in veterinary hospitals for conditions related to respiratory tract disease. When BD are not presented primarily for respiratory tract disease, they may still show clinical signs associated with brachycephalic airway syndrome (BAS) including snoring, coughing, and respiratory stertor or stridor, as well as gastrointestinal tract signs such as vomiting, regurgitation, and laryngeal and pharyngeal dysfunction.1–3 These clinical signs result from the primary components of BAS, which include stenotic nares, elongated soft palate, redundant pharyngeal folds, hypoplastic trachea, recently identified nasopharyngeal turbinates, and secondary changes such as everted laryngeal saccules and laryngeal collapse.4–6
The gold standard for evaluating hypoxemia in patients presenting with respiratory disease is arterial blood gas analysis, which directly measures the partial pressure of oxygen (PaO2) and saturation of hemoglobin with oxygen (SaO2).7,8 However, obtaining arterial blood samples can be technically challenging and may not be possible in patients who are in respiratory distress or are easily distressed. Additionally, this diagnostic test may not be readily available in all veterinary hospitals. In human patients, concerns associated with cost, arterial hematoma, thrombosis, and pain from arterial blood collection have contributed to judicious use of arterial blood gas analysis.9–11
Pulse oximetry (SpO2) is a less invasive and readily available method of estimating SaO2. SpO2 measures the saturation of hemoglobin with oxygen in arterial blood on the basis of pulsatile changes in relative absorption of red and infrared light by oxyhemoglobin and reduced hemoglobin.8,12,13 SpO2 has been found to be an accurate method of estimating SaO2.14–16 Therefore, the use of SpO2 has become ubiquitous in human medicine, and recent studies have shown that the ratio of SpO2 to the fraction of inspired oxygen (FiO2) is a viable, noninvasive surrogate for the PaO2/FiO2 ratio (PF) in critically ill adult and pediatric human patients.17,18 Recent veterinary studies have demonstrated that SaO2/FiO2 and SpO2/FiO2 ratios (SF) have good correlation with PF ratios in dogs recovering postoperatively and critically ill dogs, respectively.19,20
Generally, SpO2 readings of <95% are indicative of hypoxemia, and therefore, the normal SpO2 range for dogs breathing room air is 95–100%.21 To the authors’ knowledge, there are no studies evaluating SpO2 ranges in healthy BD. A previous study found that BD have a significantly lower PaO2 when compared with mesocephalic and dolichocephalic dogs (MDD).22 Given the correlation between SF and PF ratios and the previous finding that BD are prone to a lower PaO2 compared with MDD, it is important to determine whether BD are also prone to lower SpO2 values.22 SpO2 values are more readily obtainable than arterial blood gas samples, and knowledge of SpO2 values in healthy BD may be more practical information for the majority of veterinarians.
The purpose of this study was to compare SpO2, SF, PaO2, PF, and SaO2 values between healthy BD and MDD. We hypothesized that healthy BD would have lower SpO2, SF, PaO2, PF, and SaO2 values when compared with MDD.
Materials and Methods
This study was performed at the University of Tennessee College of Veterinary Medicine from August 2014 to August 2015. All dogs were enrolled after owner consent was obtained. The study protocol was reviewed and approved by the University of Tennessee College of Veterinary Medicine Institutional Animal Care and Use Committee. Enrollment of all dogs was based on the results of physical examination, complete blood count (CBC), biochemistry profile, and an owner questionnaire.
Owner Questionnaire
The owners of all dogs were asked to complete a questionnaire, which was designed by the authors and modified from a previously published study by Poncet et al. (Supplementary File I) regarding the frequency of snoring, exercise intolerance, sleeping problems (sleep apnea, needing to sleep with head elevated), vomiting, regurgitation, cyanosis, and collapse.1 Owners were asked to note all medications given to their pets in the last 24 hr and if their pet had undergone previous airway surgery, and if so, the date of the airway surgery.
Brachycephalic Airway Syndrome Severity Scoring
Based on the results of the owner questionnaire, all dogs received one of the following BAS grades (modified from a previously published study): clinically unaffected, mildly BAS-affected, moderately BAS-affected, or severely BAS-affected (Supplementary File II).1 Clinically unaffected dogs had no history of exercise intolerance, sleeping problems, stertorous breathing, or frequent snoring. Mildly affected dogs had any of the clinical signs of snoring most or all the time, stertorous breathing, mild exercise intolerance, inspiratory effort during exercise, and heat intolerance. Moderately affected dogs had any of the clinical signs of the mildly affected group plus at least two of the following: moderate exercise intolerance, sleeping problems, and inspiratory effort at rest. Severely affected dogs had any of the signs of the mildly or moderately affected group plus syncope, collapse, and/or cyanosis.
Inclusion Criteria
Dogs considered for inclusion could be presented to the hospital for a wellness examination, routine vaccinations, orthopedic evaluation, or for the study. To be considered systemically healthy, all dogs were required to have an unremarkable CBC, biochemistry profile, and physical examination. Although BD were allowed conformational changes associated with BAS, to be considered healthy and eligible for the study, their quality of life had to be unaffected or minimally affected by BAS. As a result, BD were excluded if they had ever suffered an episode of cyanosis, syncope, or collapse at any point in their life (severely BAS-affected) or if they had airway surgery performed in the past 3 mo. BD were required to be a purebreed English bulldog, French bulldog, pug, or Boston terrier. Dogs in the MDD population were enrolled as controls. For inclusion, MDD had to be classified into the clinically unaffected group and have no history of previous respiratory disease or airway surgery. BD and MDD were excluded if they had received any steroids or opioids in the previous 24 hr.
Procedures
All measurements were obtained on room air with a FiO2 of 21%. Pulse oximeter readings were obtained using a transmission probea. Three readings each were attempted at three different anatomical sites (tongue, lip, prepuce/vulva) that have previously been found to be acceptable in dogs.8,14,23 In each location, the probe was left in place at least 30 s or until a stable signal was obtained for at least 10 s. SpO2 readings were considered acceptable only if a normal plethysmographic waveform with a dicrotic notch was observed and the heart rate on the pulse oximeter matched the dog’s heart rate measured by palpating the femoral pulse.14,15 The highest of all acceptable SpO2 readings acquired were recorded and used for data analysis.15
All dogs were then sedated with 0.3 mg/kg butorphanol given IV, ∼10 min prior to arterial blood gas collection. Dogs were restrained in either full lateral recumbency or partial lateral recumbency with the front half of the body sternal and the back half lateral for the arterial blood gas collection. With the back half of the dog in lateral recumbency, the arterial blood gas was taken from the femoral artery of the leg that was down on the table. Approximately 0.5 mL blood was obtained for an arterial blood gas sample from the femoral artery using commercially available arterial blood gas syringesb. Each sample was obtained in <1 min and analyzed on a blood gas analyzer within 3 min of collectionc. The syringes were immediately capped after collection and handled according to standard guidelines to minimize air exposure. After arterial blood gas collection, postsedation SpO2 readings were performed in the same manner as reported above, and again, the highest of all acceptable SpO2 readings acquired were recorded and used for data analysis. Three oscillometric systolic blood pressure readings were obtained from a hind limb and the mean value recordedd. The cuff size used for each dog was ∼40% of the circumference of the leg above the tibiotarsal joint.
Statistical Analysis
All data was analyzed using commercially available statistical softwaree with the help of a statistician. Descriptive statistics for normally distributed data were reported as mean values with standard deviations (SD) for patient age, weight, body condition score (BCS), pulse oximeter readings, blood gas analytes, systolic blood pressure, and SF and PF ratios. Data was analyzed using a one-way multivariate analysis of variance with the groups of dogs (MDD, BD, unaffected or mildly BAS-affected BD, moderately BAS-affected BD, BD with previous airway surgery, and BD without previous airway surgery) with the independent factors age, weight, BCS, temperature, heart rate, respiratory rate, highest presedation SpO2 reading, highest postsedation SpO2 reading, presedation SF, postsedation SF, mean systolic oscillometric blood pressure, pH, arterial PaO2, arterial partial pressure of carbon dioxide, bicarbonate, hematocrit, hemoglobin, and SaO2 as the response variables. Correlation between the highest pre- and postsedation SpO2 readings and each dog’s corresponding SaO2 values was evaluated using Pearson’s linear correlation coefficient (r) and the mean difference between the SpO2 and SaO2 values. To evaluate the correlation between the highest pre- and postsedation SpO2 readings and each dog’s corresponding PaO2 values, a two-way scatterplot was generated for SF versus PF ratio, and Spearman’s correlation coefficient was calculated. Statistical significance was set at P < .05.
Results
A total of 18 BD met the inclusion criteria: 4 pugs, 6 French bulldogs, 4 English bulldogs, and 4 Boston terriers. Eighteen MDD dogs consisted of 13 mixed-breed dogs, 2 Chihuahuas, 2 Staffordshire terriers, and 1 rottweiler. All MDD dogs presented to the hospital solely for the study. Of the 18 BD, 14 presented solely for the study, and 4 presented for orthopedic disease. No dog had any complications or side effects, respectively, from the arterial blood gas collection or sedation. No dogs had any significant abnormalities on either the CBC or biochemistry profiles. Five of the 18 BD had previous airway surgery a median of 21 mo prior to participation in the study (range 9–72 mo). Of the 18 BD, 3 were classified as clinically unaffected using the BAS severity grading system, 10 were mildly affected, and 5 were moderately affected. Two dogs were moderately BAS-affected and had also undergone previous airway surgery. Of the remaining three dogs who had undergone previous airway surgery, two dogs were mildly BAS-affected, and one was clinically unaffected.
Age, weight, BCS, physical exam parameters (temperature, pulse, respiratory rate), and indirect systolic blood pressure for BD and MDD are summarized in Table 1. There were no significant differences in age, weight, BCS, physical exam parameters, or systolic blood pressure readings between BD and MDD.
The pre- and postsedation SpO2 readings for all study and control dogs are summarized in Tables 2 and 3. Although readings were attempted at all three sites (tongue, lip, prepuce/vulva), no dog allowed a reliable reading to be taken on the tongue, neither while awake nor with sedation. BD, when compared with MDD, had significantly lower presedation (mean BD SpO2 = 98.22%, mean MDD SpO2 = 99.33%; P = .0004) and postsedation (mean BD SpO2 = 97.78%, mean MDD SpO2 = 98.72%; P = .0053) SpO2 readings. Moderately BAS-affected BD had significantly lower presedation SpO2 readings than unaffected or mildly BAS-affected BD (mean SpO2 = 97.80 and 98.38%, respectively; P = .0354). No significant difference was found between these two groups for postsedation SpO2. BD with previous airway surgery had significantly lower presedation SpO2 readings than BD without previous airway surgery (mean SpO2 = 97.00 and 98.69%, respectively, P = .0162). No significant difference was found between BD airway surgery groups for postsedation SpO2.
Complete results of blood gas analyses and SF and PF ratios among the groups are presented in Table 4. No significant difference was found between BD, MDD, and BD with previous airway surgery for any specific blood gas values. However, moderately BAS-affected BD had significantly lower SaO2 values when compared with MDD (mean SaO2 = 94.58% and 96.10%, respectively; P = .0447). The BD group compared with the MDD group had significantly lower presedation SF (mean BD SF = 467.72, mean MDD presedation SF = 473.02; P = .0004) and postsedation SF ratios (mean BD SF = 465.61, mean MDD SF = 470.11; P = .0053). Only the presedation SF ratio for the moderately affected BD (mean SF = 465.71) and BD with previous airway surgery (mean SF = 461.90) were significantly lower than the MDD (mean SF = 473.02) presedation SF ratio (P = .0084 and P = .0016, respectively). No significant difference was found among MDD, BD, moderately BAS-affected BD, and BD with previous airway surgery for PF. Although not statistically significant, the PF ratio for the BD group was lower than for the MDD group (mean BD PF = 376.38, mean MDD PF = 398.81; P = .0656).
Presedation SpO2 readings for all BD and MDD were significantly higher than postsedation SpO2 readings (mean ± SD presedation SpO2 of BD and MDD = 98.78 ± 1.48%, mean ± SD postsedation SpO2 of BD and MDD = 98.25 ± 1.57%; P = .0327), and there was a significant correlation between the pre- and postsedation SpO2 readings for each dog (P = .0003). There was no significant correlation between either pre- or postsedation SF ratios of the BD and MDD groups and their respective PF ratio (r = 0.18, P = .29; r = 0.02, P = .93, respectively). There was significant correlation between the presedation SpO2 readings of the BD and MDD groups and their respective SaO2 values on arterial blood gas analysis (mean ± SD presedation SpO2 of BD and MDD = 98.78% ± 1.48%, mean ± SD SaO2 of BD and MDD = 95.53% ± 1.32%; P = .038). However, there was no significant correlation between postsedation SpO2 readings and respective SaO2 values (P = .3699).
The mean difference (± SD) between presedation SpO2 values and SaO2 for all dogs was 3.24 ± 1.60%. The mean difference between postsedation SpO2 values and SaO2 for all dogs was 2.71 ± 1.89%.
Discussion
In this study comparing the oxygenation of healthy BD and MDD, BD had significantly lower SpO2 and SF (both pre- and postsedation) when compared with MDD. There were no significant differences in PF, PaO2, SaO2, or any of the other arterial blood gas analytes between this population of healthy BD and MDD. Only BD dogs who were moderately BAS-affected had SaO2 values that were significantly lower than in MDD. This result contrasts with the findings of a recent study that evaluated arterial blood gases in BD compared with MDD.22 Hoareau et al. reported that BD had significantly lower PaO2, higher packed cell volume, and higher PaCO2 when compared with MDD, but found no difference between groups for SaO2.22 In that study, only French and English bulldogs were included, and there was no mention of exclusion of dogs with previous episodes of cyanosis or collapse. The goal of our study was to evaluate only healthy dogs whose quality of life was minimally affected by BAS. Any dog with a previous history of cyanosis or collapse was excluded because of the concern that these dogs may not truly be systemically healthy, as well as for the concerns of patient safety when restraining for arterial blood gas sampling. Our exclusion criteria may have selected for a different and potentially less BAS-affected BD population.
For the BD group, we chose to include French bulldogs, English bulldogs, Boston terriers, and pugs because these breeds are most commonly affected with BAS.1,4,6 In two studies, French bulldogs, English bulldogs, and pugs represented 92% of dogs who presented for upper respiratory tract disease.1,24 In another study, French bulldogs, English bulldogs, and Boston terriers represented 77% of dogs who presented for surgical correction of their BAS.4 English bulldogs, pugs, and Boston terriers represented 91% of dogs diagnosed with BAS via laryngoscopic examination in another study.6 The inclusion of pugs and Boston terriers could have caused our arterial blood gas results to differ from the previous study evaluating PaO2.22 The five dogs in our BD group who were the most severely BAS-affected were all either French bulldogs or English bulldogs. These findings suggest that although these breeds are all considered brachycephalic, the severity of the clinical disease of BAS may not be uniform among all brachycephalic breeds, and English and French bulldogs may suffer from a more severe form of BAS.
There was no significant correlation between SF and PF ratios. These findings contrast with results of a previous study in which SF and PF ratios had good correlation in critically ill dogs spontaneously breathing room air.19 Thus far, SF and PF ratio correlations have been performed only on critically ill patients requiring oxygenation assessment.17–19 The BD and MDD dogs in the current study were healthy, and oxygenation assessment was performed as part of the study. These healthy dogs had SF and PF ratios in a much narrower and normal range compared with the SF and PF ratios reported in critically ill dogs. The SF ratio range in the current study was 452.38–476.19, and the PF ratio range was 323.81–447.62 for all BD and MDD. In the study by Calabro et al., the SF range was 381.0–461 and the PF range was 211.9–494.3.19 The narrower range of SF and PF ratios in our healthy population could have contributed to the lack of correlation, because those ratios fall within the flat portion of the oxygen dissociation curve. If SF and PF ratios were included from patients with a wide range of oxygenation levels, we might have seen a significant correlation. In addition to our narrow range of SF and PF ratios, we evaluated a relatively small sample size, which may have contributed to the lack of correlation between SF and PF ratios in this population of dogs.
Inaccuracy of the pulse oximeter machine is another potential cause of the lack of correlation between SF and PF. The authors attempted to obtain the most accurate SpO2 values possible by recording readings only when the pulse oximeter heart rate matched the dog’s pulse rate on palpation and when the waveform on the plethysmogram was a sharp waveform with a clear dicrotic notch, suggesting a reliable reading.25 Also, the anatomical sites chosen to obtain the SpO2 readings have been previously documented to be sites providing accuracy in awake dogs.8,14,23 Although every attempt was made to obtain the most accurate pulse oximeter readings, variable readings can occur and have been documented in previous studies.14–16,26
Another less likely cause of the lack of correlation between SF and PF ratios in our study could be errors in arterial blood sampling from the femoral artery. However, after arteriopuncture of each dog, the syringes immediately filled with bright red blood without the need for syringe aspiration, which is consistent with sampling an artery.27 Although arteriopuncture was considered to be uncomplicated and successful in each dog, admixture of venous blood with the arterial sample cannot be completely ruled out.
There was a significant correlation between pre- and postsedation SpO2 values for each dog. This likely reflects a consistency in the protocol for obtaining the pulse oximeter readings in each dog. Despite the correlation, presedation SpO2 readings were significantly higher than postsedation SpO2 readings of all dogs, suggesting that the butorphanol sedation likely had a significant effect on SpO2 readings. Although the presedation pulse oximeter readings were significantly higher than postsedation readings, they were, on average, ≤1% higher, and this difference is not likely to be clinically relevant. The authors of this study chose butorphanol to provide sedation to successfully obtain the arterial blood gas samples while minimizing stress and discomfort to the dogs. Butorphanol was selected because it produces minimal cardiovascular effects.28 However, butorphanol still caused a small but statistically significant decrease in arterial blood pressure, heart rate, and PaO2 in dogs in one study.28 Although our study evaluated neither arterial blood pressure nor the change in PaO2, the findings of the Trim study could explain the significant difference seen between pre- and postsedation SpO2 readings seen in our population of dogs.28 A significant correlation was found between presedation but not postsedation SpO2 readings and SaO2. Given that SaO2 is a directly measured variable, and SpO2 is a reading obtained based on arterial pulsatile blood flow, it is possible that butorphanol administration contributed to the lack of significant correlation between postsedation SpO2 values and SaO2. Decreases in blood pressure, heart rate, and PaO2 secondary to butorphanol administration could all cause decreased perfusion and subsequently affect only postsedation SpO2 readings.
The mean difference (± SD) between presedation SpO2 values and SaO2 for all dogs was 3.24 ± 1.60%, indicating that for an SaO2 value of 90%, 95% of SpO2 values were between 90.04 and 96.44% ([90 + 3.24] ± 3.2%). The mean difference between postsedation SpO2 values and SaO2 for all dogs was 2.71 ± 1.89%, meaning that for an SaO2 value of 90%, 95% of SpO2 values were between 88.93 and 96.49% ([90 + 2.71] ± 3.78%). Other human and veterinary studies have reported the SD of the mean difference to be between 2 and 6.5%, and our SDs were within this range. Previous veterinary studies have found the mean difference between SaO2 and SpO2 values to range from –0.06 to –3.4% with SpO2 tending to underestimate high SaO2 values (>70%).15,16,26 The mean difference between SpO2 and SaO2 in this study population was a positive number (3.24 and 2.71), indicating that SpO2 tended to overestimate high SaO2 values. It is not clear why our SpO2 readings tended to overestimate SaO2. Interestingly, a recent study documented that SpO2 readings in children, on average, overestimate SaO2 values for SpO2 values in the range of 76–90%.29
Limitations to this study include having a small sample size and the inclusion of BD who have had previous airway surgery. Including BD who have had previous airway surgery could have skewed the results in favor of improved oxygenation in this group of dogs and could have contributed to the lack of significant differences between BD and MDD on arterial blood gas analysis.30 Future studies evaluating SpO2 readings in BD before and after surgery would be useful. Additionally, this study specifically excluded BD who had previous episodes of cyanosis and collapse, removing the most severely BAS-affected BD from evaluation. Future studies collecting SpO2 readings and/or arterial blood gas samples on any BD presenting for general anesthesia would also provide useful information.
Within this study, healthy BD had significantly lower SpO2 readings than healthy MDD, although these values were still within the normal SpO2 reference range. These findings highlight the importance of noting a dog’s SpO2 prior to sedation, anesthesia, or surgery to be used as a baseline for that dog. The results of this study also found no significant differences between BD and MDD for any of the arterial blood gas analytes. When the BD group was subdivided according to BAS severity, it was found that moderately BAS-affected BD had significantly lower SaO2 values than MDD. Additionally, French and English bulldogs may suffer from a more severe clinical disease of BAS, as these were the only brachycephalic breeds in the moderately BAS-affected BD group.
Conclusion
In this study of healthy dogs, although BD had significantly lower SpO2 readings than MDD, all dogs had SpO2 readings within the reference range of 95–100%. Although these findings were statistically significant, the clinical relevance may lie in noting a change in SpO2 value for an individual, even if the value is still within the normal reference range. BD may be prone to decreased oxygenation, but they should be evaluated and treated in a similar fashion to MDD regarding oxygenation. Therefore, hypoxemia, as measured by pulse oximeter or arterial blood gas, should never be considered normal and acceptable for any breed, and treatment should be initiated if hypoxemia is diagnosed.
Contributor Notes
S. Arulpagasam’s present affiliation is Advanced Veterinary Care Center, Davie, Florida.
