- Email: [email protected]
The normal electrocardiogram of four species of conscious raptors
Available online at www.sciencedirect.com
Research in Veterinary Science 84 (2008) 119–125 www.elsevier.com/locate/rvsc
The normal electrocardiogram of four species of conscious raptors J. Talavera *, M.J. Guzma´n, M.J. Ferna´ndez del Palacio, A.P. Albert, A. Bayo´n Department of Animal Medicine and Surgery, University of Murcia, Campus de Espinardo, 30100 Murcia, Spain Accepted 6 March 2007
Abstract The aim of this study was to describe normal ECG patterns and values in four species of conscious raptors (Eurasian kestrel, Griffon vulture, Little owl, and Eurasian Eagle owl). Electrocardiograms were carried out in 75 conscious birds belonging to four species of raptors. Lead II waveforms were analysed to determine amplitudes and durations of waves and intervals. Morphologic patterns of P-QRS-T deflections were analysed in the six limb leads. Rhythm, heart rate, mean electrical axis, presence of Ta wave, ST slurring, and P-on-T phenomenon were also studied. The influence of species, body weight and heart rate in electrocardiographic variables were statistically analysed (P < 0.05). Sinus rhythm was present in all tracings, showing sinus arrhythmia in four cases. Ta wave was present in six tracings and P-on-T phenomenon in four. ST segment could be identified in all tracings, being mainly high above baseline. Significant differences between species were found for all the electrocardiographic parameters. The heart rate and body weight were also found to be a significant influence in most parameters. This study provides electrocardiographic data for four species of raptors that can be used to establish comparisons for clinical purposes. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Normal electrocardiogram; Unanaesthetised raptor; Bird
1. Introduction The electrocardiogram (ECG) is a well established important tool in the evaluation of small and large animal patients with cardiac diseases and it is essential in the diagnosis and monitoring of arrhythmias and conduction disturbances (Tilley, 1992). In addition, ECG is also useful in the evaluation of diseases that secondarily affect the heart such as metabolic and electrolyte abnormalities (Tilley, 1992). However, in birds ECG is not widely used in a clinical setting probably because of the lack of information about normal ECG values and electrocardiographic patterns in healthy animals. The study of the ECG in raptors, besides being of pure scientific interest it pursues a clinical application. Clinical situations in which an ECG can be advised are frequent, since raptors are often admitted for veterinary evaluation subsequent to severe trauma, electrocution, intoxications, *
Corresponding author. Tel.: +34 968367156; fax: +34 968364737. E-mail address: [email protected] (J. Talavera).
0034-5288/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.rvsc.2007.03.001
etc. and may show non-specific signs that can be related with cardiac, metabolic and/or electrolyte abnormalities. Until now however, little information about ECG in raptors has been available (Edjtehadi et al., 1977; Burtnick and Degernes, 1993; Espino et al., 2001; Rodrı´guez et al., 2004). In some cases ECGs have been obtained in raptors under sedation and/or anaesthesia (Burtnick and Degernes, 1993; Espino et al., 2001). Although chemical restraint may be far less stressful that when conscious, nevertheless during initial evaluation of the sick and weak birds anaesthesia or sedation can be not ideal and could be clinically compromising. Moreover, data obtained from sedated or anaesthetised animals could not be extrapolated to conscious animals (Miller, 1986; Lumeij and Ritchie, 1999; Tilley, 1992). Therefore, it would be ideal to have reference to ECG values and patterns obtained from conscious birds as well. The purpose of this study is to analyse the feasibility of obtaining ECG tracings in conscious raptors and to describe normal ECG patterns and values in four species of raptors. To the authors’ knowledge, the ECG of the species included in the present study has never been studied.
120
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
Ta wave, P-on-T phenomenon and ST slurring was also taken into consideration.
2. Materials and methods 2.1. Animals
2.4. Statistical analysis A total of 75 healthy adult raptors of both sexes weighing between 50 and 7000 g were selected. Table 1 provides the list of species examined with their respective abbreviations used in the study. The source of the animals was the Centro de Recuperacio´n de Fauna Silvestre ‘‘El Valle’’ (Wildlife Centre ‘‘El Valle’’) in Murcia (Spain). The ECG was recorded just before the liberation of the bird to his natural habitat. 2.2. ECG recording A six-channel electrocardiograph (Siemens Megacart R, Electromedical Systems Division (ECS), Sweden) was used. Neither sedation nor anaesthesia were used for the ECG recording. The birds were placed in a dorsal recumbent position on a wooden table covered with a plastic material. In easily stressed birds the head was covered with a surgical cloth in order to relieve stress during handling. Four alligator clip electrodes were attached to the cranial area of the skin-fold in the angle between the arm and forearm of the left and right wings (propatagium) and to the skin on the left and right knees. Alcohol was used to obtain good clip-to-skin contact. When optimal immobilisation and good contact were obtained, standard bipolar (I–III) and augmented bipolar limb (aVR, aVL and aVF) leads were simultaneously recorded. According to heart rate (HR) and amplitude of the waves, the electrocardiographs were calibrated at 50–100 mm/s and 10–20 mm/mV. All procedures took place in an isolated room in order to minimise the stress for birds. 2.3. ECG trace analysis Nomenclature and ECG interpretation were performed according to standard methods (Tilley, 1992). A general analysis of all the electrocardiographic recordings was first performed by a veterinary cardiologist (MJFP) to ensure the quality of the recording. In each tracing five beats (lead II) were selected for quality and mean values of waves and intervals of P-QRS-T deflections were determined. The mean electric axis (MEA) of ventricular depolarisation in the frontal plane was calculated by the vector method with the leads II and III. The morphologic patterns of P-QRS-T deflections were evaluated for every lead. The presence of
A commercial software package (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. All measurements are expressed as mean ± standard deviation (SD). Non-parametric data were analysed by means of descriptive statistics. Parametric data (measurements of waves and intervals, body weight, HR and MEA) were analysed by means of one-way analysis of variance or by means of Kurskall–Wallis test. The influence of body weight and HR in electrocardiographic variables were analysed by means of Pearson (variables normally distributed) or Spearman (variables not-normally distributed) correlation tests. In all the analyses differences were considered to be significant when P < 0.05. 3. Results The protocol used in the study allowed recording of ECG tracings in conscious raptors of sufficient quality to evaluate the cardiac rhythm and HR and for reliable measurements of waves and intervals for at least five beats (Fig. 1). In general, the procedure was well tolerated by the raptors. Some struggling movements took place frequently during bird positioning and electrode placement. Otherwise the animals remained motionless in most cases. 3.1. Heart rate The HR range for the raptors studied was from 81 (GF) to 542 (FT) beats per minute (bpm). The mean HR was significantly different between species (P < 0.001) (Table 3) and inversely to the body weight (P = 0.003). The HR showed a significant negative relationship to the length of all waves and intervals (P duration, PR duration, QRS duration, R duration, S duration, ST duration, T duration, and QT duration, P < 0.001) (Table 2). 3.2. Rhythm Most of the tracings evaluated showed a regular sinus rhythm (93.3%). Sinus arrhythmia was evident in 5.3% of the tracings, corresponding to one GF and three ATN. One isolated supraventricular extrasystole was observed in one BB.
Table 1 Description of the species of raptors included in the study Family
Vulgar name
Scientific name
Abbreviation
Number of animals
Body weight (g) (mean ± SD)
Falconidae Accipitridae Strigidae
Eurasian kestrel Griffon vulture Little owl Eurasian Eagle owl
Falco tinnunculus Gyps fulvus Athene noctua Bubo bubo
FT GF ATN BB
35 10 20 10
185 ± 30 6370 ± 567 106 ± 39 1980 ± 383
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
121
Fig. 1. Electrocardiographic (standard bipolar limb leads) tracing of a Griffon vulture (Gyps fulvus): 50 mm/s and 20 mm/mV.
Table 2 Mean, standard deviation (SD) and range for lead II durations of component deflections in the studied raptors PR+#* (ms)
QRS+* (ms)
R+* (ms)
S+# (ms)
ST+#* (ms)
T+* (ms)
QT+#* (ms)
Eurasian kestrel (Falco tinnunculus) Mean ± SD 21.63 ± 2.51 40.38 ± 6.18 Range 17–27 27–54
18.84 ± 3.01 12–24
9.04 ± 1.53 5–11
16.49 ± 3.33 11–24
14.93 ± 6.66 2–31
45.50 ± 6.40 33–60
79.58 ± 8.83 61–97
Griffon vulture (Gyps fulvus) Mean ± SD 38.53 ± 4.43 Range 32–46
76.0 ± 12.45 63–101
40.10 ± 19.66 19–92
17.38 ± 5.16 11–25
29.21 ± 5.12 19–37
35.64 ± 14.60 12–59
70.63 ± 11.06 53–88
144.81 ± 8.91 133–159
Little owl (Athene noctua) Mean ± SD 29.36 ± 7.15 Range 21–42
59.43 ± 9.93 51–81
27.71 ± 12.08 18–47
13.65 ± 6.59 7–24
16.93 ± 4.82 13–27
28.36 ± 4.76 24–38
54.29 ± 6.98 47–65
110.3 ± 22.24 90–151
Eurasian Eagle owl (Bubo bubo) Mean ± SD 30.28 ± 5.91 Range 18–39
60.44 ± 9.76 41–74
31.61 ± 7.65 23–45
14.34 ± 4.84 8–20
25.17 ± 3.48 20–31
60.33 ± 9.02 49–72
50.78 ± 5.34 45–62
141.39 ± 10.10 121–154
Species
P+#* (ms)
+
Significant differences in function of the species of raptors (P < 0.001). #Significant body weight effect (P < 0.05). *Significant heart rate effect (P < 0.05).
3.3. P wave The P wave (atrial depolarisation) duration range on lead II was from 17 ms (FT) to 46 ms (GF). This parameter was significantly different between species (P < 0.001) and showed a positive relationship to the size (i.e. body weight) of the raptor (P = 0.047): the larger the bird the longer the P wave duration (Table 2). The lead II P wave amplitude range was from 0.06 mV (BB) to 0.28 mV (FT), having a mean value significantly different between species (P < 0.001). No significant relationship between this parameter and body weight was found (P = 0.118) (Table 3). The P wave was always positive on lead I, II and aVF (Table 4). In lead III the predominant morphology was positive (72.5%), followed by negative (15.7%) and biphasic (11.8%) morphology. In lead aVR, P wave was mainly negative (98.3%) being positive in only one GF (1.7%). Three morphologies were represented in lead aVL: positive (81.4%), negative (7%), and biphasic (11.6%). 3.4. PR interval The PR interval range on lead II was from 27 ms (FT) to 101 ms (GF) (Table 2). Significant differences between species were found in this parameter (P < 0.001). One positive
significant body weight effect was found (P = 0.007): the larger the bird of prey the longer the PR interval. Ta wave (atrial repolarisation), identified as a negative wave or depression in PR interval, was present in 6 FT. 3.5. QRS complex The QRS complex length range was from 12 ms (FT) to 92 ms (GF) having a mean value significantly different between species (P < 0.001) and showing a positive but not significant relationship to body weight (P = 0.116) (Table 2). Table 4 shows the relative percentages of morphology patterns of QRS deflections in the four species of raptors covered by the study. Of the total percentages lead I showed wider ranges of QRS morphologies, QS being the most frequent. In leads II, III and aVF the most frequent morphologies were QS and rS. Leads aVR and aVL showed the narrowest range of morphologies, R clearly being the most frequent. Q wave was only present in aVR and aVL leads showing a qR morphology. In lead II, R wave (when present) range was from 5 ms (FT) to 25 ms (GF) duration and 0.01 mV (FT and ATN) to 0.28 mV (GF) of amplitude (Tables 2 and 3). No significant influence of body weight in R wave duration and amplitude was found. Significant differences between spe-
122
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
Table 3 Mean, standard deviation (SD) and range for lead II amplitudes of component deflections, mean electrical axis (MEA) and heart rate (HR) in the studied raptors P+ (mV)
R+ (mV)
S+ (mV)
ST+# (mV)
T+# (mV)
HR+# (bpm)
Eurasian kestrel (Falco tinnunculus) Mean ± SD 0.2 ± 0.05 Range 0.08–0.28
0.06 ± 0.02 0.01–0.12
0.62 ± 0.21 0.31–1.27
0.26 ± 0.12 0.02–0.55
0.52 ± 0.17 0.24–0.98
425 ± 67 275–542
98 ± 4 107 to
Griffon vulture (Gyps fulvus) Mean ± SD 0.17 ± 0.04 Range 0.13–0.24
0.08 ± 0.08 0.03–0.28
0.49 ± 0.19 0.28–0.73
0.06 ± 0.03 0.02–0.1
0.21 ± 0.09 0.11–0.42
160 ± 45 81–228
78 ± 24 113 to 20
Little owl (Athene noctua) Mean ± SD 0.11 ± 0.02 Range 0.09–0.15
0.04 ± 0.01 0.01–0.05
0.19 ± 0.09 0.07–0.33
0.06 ± 0.05 0.01–0.13
0.21 ± 0.06 0.12–0.33
256 ± 58 110–336
88 ± 26 121 to 88
Eurasian Eagle owl (Bubo bubo) Mean ± SD 0.08 ± 0.02 Range 0.06–0.11
0.04 ± 0.01 0.02–0.06
0.32 ± 0.12 0.16–0.52
0.05 ± 0.03 0–0.11
0.18 ± 0.05 0.1–0.24
222 ± 47 160–295
95 ± 6 103 to
Species
MEA+ (°)
91
85
+
Significant differences in function of the species of raptors (P < 0.001). #Significant body weight effect (P < 0.05).
Table 4 Morphologies of P-QRS-T deflexions in the six bipolar standard leads in the studied raptors Eurasian kestrel (Falco tinnunculus) (%)
Griffon vulture (Gyps fulvus) (%)
Little owl (Athene noctua) (%)
Eurasian Eagle owl (Bubo bubo) (%)
Totals (%)
P QRS
Ps = 100 QS = 96.4, Rs = 3.6 Ps = 21.05, B = 78.95
Ps = 100 QS = 33.3, Rs = 33.3, RS = 33.3 Ps = 100
Ps = 100 rS = 14.3, QS = 85.7
T
Ps = 100 QS = 10, Rs = 20, RS = 50, R = 20 B = 87.5, N = 12.5
Ps = 100 rS = 2, Rs = 9.8, QS = 70.6, R = 3.9, RS = 13.7 Ps = 18.8, B = 78.1, N = 3.1
Ps QRS
Ps = 100 rS = 51.5, QS = 48.5 Ps = 100
Ps = 100 rS = 41.7, RS = 16.7, QS = 33.3, Rs = 8.3 Ps = 100
Ps = 100 rS = 11.1, QS = 88.9
T
Ps = 100 rS = 30, RS = 10, QS = 60 Ps = 100
Ps = 100
Ps = 100 rS = 40.6, RS = 4.7, QS = 53.1, Rs = 1.6 Ps = 100
Ps = 33.33, B = 33.33, N = 33.33 rS = 30, QS = 70 Ps = 100
Ps = 87.5, B = 12.5
Ps = 16.67, N = 83.33
Ps = 72.5, B = 11.8, N = 15.7
rS = 60, QS = 40 Ps = 100
QS = 100 Ps = 100
rS = 38.7, QS = 61.3 Ps = 100
Ps = 10, N = 90 QS = 10, qR = 40, R = 50 N = 100
N = 100 R = 55.6, qR = 44.4
N = 100 R = 100
Ps = 1.7, N = 98.3 QS = 1.6, qR = 17.7, R = 80.6
N = 100
N = 100
N = 100
I
Ps = 25, B = 75
II
III Ps QRS T aVR Ps QRS T aVL Ps QRS T aVF Ps QRS T
Ps = 92.86, B = 7.14 rS = 45.5, QS = 54.5 Ps = 100 N = 100 R = 91.2, qR = 8.8 N = 100 Ps = 73.91, B = 21.74, N = 4.35 R = 97.1, qR = 2.9 N = 100
Ps = 88.89, N = 11.11
Ps = 75, N = 25
Ps = 100
Ps = 81.4, B = 11.6, N = 7
R = 100 Ps = 10, N = 90
R = 100 N = 100
R = 100 N = 100
R = 98.3, qR = 1.7 Ps = 1.8, N = 98.2
Ps = 100 rS = 48.5, QS = 51.5
Ps = 100 rS = 40, QS = 60
Ps = 100 rS = 11.1, QS = 88.9
Ps = 100 rS = 42.9, R = 1.6, QS = 55.6
Ps = 100
Ps = 100
Ps = 100 rS = 54.5, R = 9.1, QS = 36.4 Ps = 100
Ps = 100
Ps = 100
I–III, standard bipolar limb leads; aVR, aVL and aVF, augmented bipolar limb leads; Ps, positive; N, negative; B, biphasic; Iso, isoelectric. Nomenclature of QRS complex follows standard methodology (Tilley, 1992).
cies of raptors were found in both parameters (P = 0.001 and 0.017, duration and amplitude of R wave, respectively). In the S wave lead II duration range was from 10 ms (FT) to 37 ms (GF) and its amplitude range covered
0.07 mV (ATN) to 1.27 mV (FT) (Tables 2 and 3). A positive correlation between the body weight and the S wave duration (but not in the amplitude) was found (P = 0.001). Mean values for S amplitude (but not in the
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
duration) were significantly different between raptor species (P < 0.001). 3.6. ST segment The ST segment in lead II was isoelectric in one case (BB), and elevated (>0.01 mV) in the rest. The degree of elevation was statistically different according to the species of bird (P < 0.001). 3.7. T wave The range of T wave duration was from 33 ms (FT) to 88 ms (GF) and 0.10 mV (BB) to 0.98 mV (FT) in amplitude (Tables 2 and 3). Means in both parameters of T wave were significantly different between species (P < 0.001). One negative significant body weight effect in T wave amplitude was found (P = 0.014): the larger the bird of prey the smaller the T wave. No significant body weight effect in T wave duration was identified (P = 0.051). In lead I morphology of T wave was mainly biphasic (78.1%) or positive (18.8%) and rarely negative (3.1%) (Table 4). In lead II, III and aVF, T wave was positive in all cases. By contrast, in aVR and aVL leads T wave was mainly negative (100% and 98.2%, respectively). P-on-T phenomenon was confirmed in four tracings (3 FT and 1 ATN). 3.8. QT interval The duration range of the QT interval in lead II was from 61 ms (FT) to 159 ms (GF) (Table 2), having a positive relation to the body weight (P = 0.006). Mean values of QT interval were significantly different between species of raptor (P < 0.001). 3.9. Mean electrical axis The MEA in the frontal plane presented a cranial direction in all cases within a range from 20° (GF) to 121° (ATN) (Table 3). The widest range corresponded to GF ( 20° to 113°) and the narrowest to FT ( 91° to 107°). Mean values for MEA were significantly different between species (P = 0.005). No significant relationship to body weight was found. 4. Discussion An abnormal ECG correlated with compatible historical information, physical examination findings and radiographic changes could be useful in the diagnosis of cardiac diseases in vivo (Miller, 1986). Information about the incidence of cardiac diseases in birds is scarce. Electrocardiographic changes have been described as being associated with infectious and non-infectious diseases (Gross, 1966; Mckenzie and Will, 1972; Andersen, 1975; Olkowski et al., 1997; Olkowski and Classen, 1998). Nevertheless,
123
some studies of necropsy have shown that heart disease in birds may occur more frequently than previously assumed (Cooper and Pomerance, 1982; Oglesbee and Oglesbee, 1998), suggesting that it could be clinically underdiagnosed in avian species. The main purpose of this study was to contribute to the use of ECG in the cardiac evaluation of raptors in a clinical setting. Many studies on avian electrocardiography have been performed using anaesthesia in order to restrain the animals (Szabuniewicz and Mcgrady, 1974; Nap et al., 1992; Burtnick and Degernes, 1993; Olkowski et al., 1997; Olkowski and Classen, 1998; Casares et al., 2000; Espino et al., 2001). Sedation and anaesthesia may influence several ECG values of waves and intervals as well as cardiac rhythm and HR (Nap et al., 1992; Tilley, 1992; Burtnick and Degernes, 1993), therefore ECG recordings should be obtained, if possible, from conscious animals (Miller, 1986; Tilley, 1992). Dorsal recumbence is recommended as the standard position to obtain ECG recordings (Miller, 1986; Burtnick and Degernes, 1993). In the present study, careful positioning of the conscious raptors in this way in an isolated quiet room (covering the head with a surgical cloth when necessary) allowed optimal immobilisation with mild restraining. Valuable information on cardiac rhythm, HR and morphology patterns was always possible with the recordings obtained. Measurements of at least five good quality P-QRS-T complexes in lead II were also possible. In addition, serious arrhythmia was not found in our study in contrast with other studies on anaesthetised birds (Nap et al., 1992; Burtnick and Degernes, 1993; Casares et al., 2000). As in the case of mammals (Tilley, 1992), significant differences between species of birds have been described in most of ECG parameters (Miller, 1986; Nap et al., 1992; Burtnick and Degernes, 1993; Cinar et al., 1996; Casares et al., 2000; Machida and Aohagi, 2001). In our study all measurements of waves and intervals were significantly different between species and differences in morphology patterns of the waves could also be identified. These findings support the need to know the specific electrocardiographic patterns and to have reference values for each species of bird of prey as well. A wide variability in morphology patterns of P-QRS-T deflections in each lead could be established by the present study, with each particular morphology differently represented between species but also within particular species of raptors. Given that all the birds used in the present study were healthy, this variability should be considered physiologic since it has already been considered in previous studies on domestic (Sturkie, 1949; Lumeij and Stokhof, 1985; Cinar et al., 1996) and non-domestic birds (Burtnick and Degernes, 1993; Machida and Aohagi, 2001; Espino et al., 2001). In the present study, the P wave was predominantly positive in leads I–III, aVL and aVF, and mainly negative in lead aVR. Leads III and aVL showed the wider range of morphologies (positive, negative, biphasic). On the whole, these findings agree with previous studies on
124
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
raptors (Burtnick and Degernes, 1993; Casares et al., 2000; Espino et al., 2001; Rodrı´guez et al., 2004) and non-raptor species (Mckenzie et al., 1971; Cinar et al., 1996). The low curve in the initial part of the PR-segment (called atrial T wave or Ta wave) depicts the repolarisation of the atria. In the case of dogs its presence is attributed to large atrial repolarisation forces caused by atrial hypertrophy (Tilley, 1992) and can also be seen with a rapid HR (Machida and Aohagi, 2001). In avian species, the Ta wave has been frequently described in healthy specimens without general abnormalities in the atrial size (Lumeij and Stokhof, 1985; Machida and Aohagi, 2001; Lopez Murcia et al., 2005). Although the reason is unknown, it is considered physiologic in birds (Machida and Aohagi, 2001). Within this study the phenomenon was present in 6 FT. To the best of the authors’ knowledge no previous reference to its presence in raptors exists. In the present study, the QRS polarity was mainly negative in I–III and aVF leads, being mainly positive in aVR and aVL leads. That way, if there was a positive and negative deflection during the QRS complex in I–III and aVF leads, the positive deflection was always seen first. These general findings agree with the described patterns for many avian species (Sturkie, 1949; Szabuniewicz and Mcgrady, 1974; Edjtehadi et al., 1977; Nap et al., 1992; Burtnick and Degernes, 1993; Casares et al., 2000; Espino et al., 2001; Rodrı´guez et al., 2004). However, just as in the case of P wave, we found a physiologic variability of QRS patterns between species and within a particular species. Duration and amplitudes of QRS complex showed similar variability with significant influences according to the species and body weight in many cases. This makes difficult and imprecise the evaluation of chamber enlargement based on morphology patterns and QRS complex measurements. In any event comparisons should always be done with reference data for each particular species. With a rapid HR, P wave and preceding T wave as well as T wave and preceding QRS complex may intermix (Miller, 1986; Tilley, 1992; Machida and Aohagi, 2001). In the first instance, when P wave and preceding T wave fuse (P-on-T phenomenon), the true morphology of each sample P and T waves may change (Miller, 1986). Previous studies have suggested that when P-on-T phenomenon is not associated with high HR, it may indicate alterations in ventricular repolarisation (Olkowski et al., 1997). In the present study P-on-T phenomenon was observed only in four tracings, always associated with high HR (458 ± 82 bpm). Secondly, ST segment is very short or absent and the S wave rises directly into the T wave (ST slurring) (Lumeij and Ritchie, 1999). In mammals this change can be attributed to myocardial ischemia (Tilley, 1992). In healthy birds, however, ST slurring is frequently described with an undetermined cause (Lumeij and Ritchie, 1999; Lopez Murcia et al., 2005). In our study ST segment was identifiable in all tracings, and hence ST slurring was not found in any of them. In agreement with previous works on birds (Lumeij and Stokhof, 1985; Nap et al.,
1992; Lumeij and Ritchie, 1999; Rodrı´guez et al., 2004), the ST segment appeared mainly elevated over baseline. T wave represents the ventricular repolarisation, being its polarity usually opposed to the main vector of QRS complex and always positive in lead II (Mckenzie et al., 1971; Cinar et al., 1996; Lumeij and Ritchie, 1999; Espino et al., 2001; Machida and Aohagi, 2001; Rodrı´guez et al., 2004). In the present study, T wave was always discordant with QRS complex and positive in lead II. Changes in QT interval may be seen in electrolyte disturbances, drug toxicity, anaesthesia, hypothermia, and central venous system disease in dogs and cats, although the QT interval alone is usually not enough to make a diagnosis (Tilley, 1992). In the present study, significant influence of species, body weight and HR in mean values of QT intervals were found. In accordance with previous studies on raptors (Burtnick and Degernes, 1993) this reveals a big variety within this parameter. Consequently, the interpretation of differences in QT interval in sequential tracings for diagnosis purposes should be carried out with caution. Again, comparisons should always be done with reference to data for particular species. A net MEA of around 90° (cranial) is characteristic of the avian ECG and implies the negative polarity of QRS complex in II, III, and aVF leads (Burtnick and Degernes, 1993; Lumeij and Ritchie, 1999). This constitutes the major difference in the normal ECG of the bird versus the dog, cat, or man (Tilley, 1992; Lumeij and Ritchie, 1999). This difference can be explained by the fact that in birds, the depolarisation wave of the ventricles begins subepicardially and spreads through the myocardium to the endocardium while in the dog depolarisation of the ventricles starts subendocardially (Lumeij and Ritchie, 1999). The mean MEA in the present study was 92 ± 2°, in accordance with described values for birds (Lumeij and Ritchie, 1999; Burtnick and Degernes, 1993). A wide range of values (always negative) was nevertheless found in selected species and significant inter-specific variability was seen. Major deviations from a normal MEA is useful in identifying different cardiac diseases in turkeys and chickens (Burtnick and Degernes, 1993; Olkowski et al., 1997). In order to ensure that any deviations from the norm are truly associated with pathology, comparisons should always be done with reference to data for a particular species. More precise comparisons of our data are difficult to make since no previous published data for the species included in our study have been found. Electrocardiographic data for 14 species of raptors have been published (Edjtehadi et al., 1977; Burtnick and Degernes, 1993; Espino et al., 2001; Rodrı´guez et al., 2004). Most of them are species phylogenetically and/or morphologically different from ours. Nevertheless, our Eurasian Eagle owls (Bubo bubo) and the Great horned owls (Bubo virginianus) of the study of Burtnick and Degernes (1993) as well as our Eurasian kestrels (Falco tinnunculus) and their American kestrels (Falco sparverious) are probably phylogenetically and morphologically close enough to make the comparison
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
interesting. In both cases, raptors in Burtnick’s study present very similar values for amplitudes of waves and MEA than our respective owls and kestrels. The most important difference is that our owls present higher HR and smaller durations of waves and intervals. The slower HR of the owls and kestrel in Burtnick’s study (more than half) can be definitively attributable to the effect of sedation used to register the ECG. Considering the significant negative relationship between HR and durations of component deflections found in our study, the longer duration of waves and intervals of Burtnick’s raptors could be also a consequence of the sedation, since it induces slower HR. In conclusion, the protocol described here allowed us to obtain interpretative ECG tracings in conscious raptors where valuable information about rhythm, HR, morphologic patterns and magnitude of component deflections could be obtained. Important electrocardiographic differences among species of raptors were found. This study provides electrocardiographic data for four species of raptors that can be used to establish comparisons for clinical purposes. In this way, the study contributes to the routine use of the ECG in the evaluation of cardiac status and the in vivo identification of cardiac diseases in raptors. References Andersen, H.T., 1975. Hyperpotasemia and electrocardiographic changes in the duck during prolonged living. Acta Physiologica Scandinavica 63, 292–295. Burtnick, N.L., Degernes, L.A., 1993. Electrocardiography on fifty-nine anesthetized convalescing raptors. In: Redig, P.T., Cooper, J.E., Remple, J.D., Hunter, D.B. (Eds.), Raptor Biomedicine. Chiron Publications Ltd., Keighley, pp. 111–121. Casares, M., Enders, F., Montoya, A., 2000. Comparative electrocardiography in four species of macaws (Genera Anadorhynchus and Ara). Journal of Veterinary Medicine A 47, 277–281. Cinar, A., Bagci, C., Belge, F., Uzun, M., 1996. The electrocardiogram of the Pekin Duck. Avian Diseases 40, 919–923. Cooper, J.E., Pomerance, A., 1982. Cardiac lesions in birds of prey. Journal of Comparative Pathology 92, 161–168. Edjtehadi, M., Rezakhani, D.A., Szabuniewicz, M., 1977. The electrocardiogram of the buzzard (Buteo buteo). Zentralblatt fur Veterinarmedizin Reihe A 24, 597–600.
125
Espino, L., Sua´rez, M.L., Lo´pez-beceiro, A., Santamarina, G., 2001. Electrocardiogram reference values for the buzzard in Spain. Journal of Wildlife Diseases 37, 680–685. Gross, W.B., 1966. Electrocardiographic changes of Escherichia coli infected birds. American Journal of Veterinary Research 27, 1427– 1436. Lopez Murcia, M.M., Bernal, L.J., Montes, A.M., Garcia Martinez, J.D., Ayala, I., 2005. The normal electrocardiogram of the unanaesthetized competition ‘‘Spanish Pouler’’ pigeon (Columba livia gutturosa). Journal of Veterinary Medicine A 52, 347–349. Lumeij, J.T., Ritchie, B.W., 1999. Cardiology. In: Ritchie, B.W., Harrison, G.J., Harrison, L.R. (Eds.), Avian Medicine: Principles and Application. HBB International, Delray Beach, pp. 695–722. Lumeij, J.T., Stokhof, A.A., 1985. Electrocardiogram of the racing pigeon (Columba livia domestica). Research in Veterinary Science 38, 275–278. Machida, N., Aohagi, Y., 2001. Electrocardiography, heart rates and heart weights of free-livings birds. Journal of Zoo and Wildlife Medicine 32, 47–54. Mckenzie, B.E., Will, J.A., 1972. Electrocardiographic changes following influenza infection in turkeys. Avian Diseases 16, 308–318. Mckenzie, B.E., Will, J.A., Hardie, A., 1971. The electrocardiogram of the turkey. Avian Diseases 15, 737–744. Miller, M.S., 1986. Electrocardiography. In: Harrison, G.J., Harrison, L.R. (Eds.), Clinical Avian Medicine and Surgery. W.B. Saunders, Philadelphia, pp. 286–292. Nap, A., Lumeij, J.T., Stokhof, A.A., 1992. Electrocardiogram of the African Gray (Psittacus erithacus) and Amazon (Amazona spp.) parrot. Avian Pathology 21, 45–53. Oglesbee, B.L., Oglesbee, M.J., 1998. Results of postmortem examination of psittacine birds with cardiac disease: 26 cases (1991–1995). Journal of American Veterinary Medical Association 212, 1737–1742. Olkowski, A.A., Classen, H.L., 1998. High incidence of cardiac arrhythmias in broiler chickens. Journal of Veterinary Medicine A 43, 83–91. Olkowski, A.A., Classen, H.L., Riddell, C., Bennett, C.D., 1997. A study of electrocardiographic patterns in a population of commercial broiler chickens. Veterinary Research Communications 21, 51–62. Rodrı´guez, R., Prieto-montan˜a, F., Montes, A.M., Bernal, L.J., Gutie´rrez panizo, C., Ayala, I., 2004. The normal electrocardiogram of the unasesthetized peregrine falcon (Falco peregrinus brookei). Avian Diseases 48, 405–409. Sturkie, P.D., 1949. The electrocardiogram of the chicken. American Journal of Veterinary Research 10, 168–175. Szabuniewicz, M., Mcgrady, J.D., 1974. The electrocardiogram of the Japanese (Coturnix coturnix japonica) and Bobwhite (Colinus virginianus) Quail. Zentralblatt fur Veterinarmedizin Reihe A 21, 198–207. Tilley, L.P., 1992. Essentials of Canine and Feline Electrocardiography. Interpretation and Treatment, third ed. Lea & Febiger, Philadelphia.
Research in Veterinary Science 84 (2008) 119–125 www.elsevier.com/locate/rvsc
The normal electrocardiogram of four species of conscious raptors J. Talavera *, M.J. Guzma´n, M.J. Ferna´ndez del Palacio, A.P. Albert, A. Bayo´n Department of Animal Medicine and Surgery, University of Murcia, Campus de Espinardo, 30100 Murcia, Spain Accepted 6 March 2007
Abstract The aim of this study was to describe normal ECG patterns and values in four species of conscious raptors (Eurasian kestrel, Griffon vulture, Little owl, and Eurasian Eagle owl). Electrocardiograms were carried out in 75 conscious birds belonging to four species of raptors. Lead II waveforms were analysed to determine amplitudes and durations of waves and intervals. Morphologic patterns of P-QRS-T deflections were analysed in the six limb leads. Rhythm, heart rate, mean electrical axis, presence of Ta wave, ST slurring, and P-on-T phenomenon were also studied. The influence of species, body weight and heart rate in electrocardiographic variables were statistically analysed (P < 0.05). Sinus rhythm was present in all tracings, showing sinus arrhythmia in four cases. Ta wave was present in six tracings and P-on-T phenomenon in four. ST segment could be identified in all tracings, being mainly high above baseline. Significant differences between species were found for all the electrocardiographic parameters. The heart rate and body weight were also found to be a significant influence in most parameters. This study provides electrocardiographic data for four species of raptors that can be used to establish comparisons for clinical purposes. Ó 2007 Elsevier Ltd. All rights reserved. Keywords: Normal electrocardiogram; Unanaesthetised raptor; Bird
1. Introduction The electrocardiogram (ECG) is a well established important tool in the evaluation of small and large animal patients with cardiac diseases and it is essential in the diagnosis and monitoring of arrhythmias and conduction disturbances (Tilley, 1992). In addition, ECG is also useful in the evaluation of diseases that secondarily affect the heart such as metabolic and electrolyte abnormalities (Tilley, 1992). However, in birds ECG is not widely used in a clinical setting probably because of the lack of information about normal ECG values and electrocardiographic patterns in healthy animals. The study of the ECG in raptors, besides being of pure scientific interest it pursues a clinical application. Clinical situations in which an ECG can be advised are frequent, since raptors are often admitted for veterinary evaluation subsequent to severe trauma, electrocution, intoxications, *
Corresponding author. Tel.: +34 968367156; fax: +34 968364737. E-mail address: [email protected] (J. Talavera).
0034-5288/$ - see front matter Ó 2007 Elsevier Ltd. All rights reserved. doi:10.1016/j.rvsc.2007.03.001
etc. and may show non-specific signs that can be related with cardiac, metabolic and/or electrolyte abnormalities. Until now however, little information about ECG in raptors has been available (Edjtehadi et al., 1977; Burtnick and Degernes, 1993; Espino et al., 2001; Rodrı´guez et al., 2004). In some cases ECGs have been obtained in raptors under sedation and/or anaesthesia (Burtnick and Degernes, 1993; Espino et al., 2001). Although chemical restraint may be far less stressful that when conscious, nevertheless during initial evaluation of the sick and weak birds anaesthesia or sedation can be not ideal and could be clinically compromising. Moreover, data obtained from sedated or anaesthetised animals could not be extrapolated to conscious animals (Miller, 1986; Lumeij and Ritchie, 1999; Tilley, 1992). Therefore, it would be ideal to have reference to ECG values and patterns obtained from conscious birds as well. The purpose of this study is to analyse the feasibility of obtaining ECG tracings in conscious raptors and to describe normal ECG patterns and values in four species of raptors. To the authors’ knowledge, the ECG of the species included in the present study has never been studied.
120
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
Ta wave, P-on-T phenomenon and ST slurring was also taken into consideration.
2. Materials and methods 2.1. Animals
2.4. Statistical analysis A total of 75 healthy adult raptors of both sexes weighing between 50 and 7000 g were selected. Table 1 provides the list of species examined with their respective abbreviations used in the study. The source of the animals was the Centro de Recuperacio´n de Fauna Silvestre ‘‘El Valle’’ (Wildlife Centre ‘‘El Valle’’) in Murcia (Spain). The ECG was recorded just before the liberation of the bird to his natural habitat. 2.2. ECG recording A six-channel electrocardiograph (Siemens Megacart R, Electromedical Systems Division (ECS), Sweden) was used. Neither sedation nor anaesthesia were used for the ECG recording. The birds were placed in a dorsal recumbent position on a wooden table covered with a plastic material. In easily stressed birds the head was covered with a surgical cloth in order to relieve stress during handling. Four alligator clip electrodes were attached to the cranial area of the skin-fold in the angle between the arm and forearm of the left and right wings (propatagium) and to the skin on the left and right knees. Alcohol was used to obtain good clip-to-skin contact. When optimal immobilisation and good contact were obtained, standard bipolar (I–III) and augmented bipolar limb (aVR, aVL and aVF) leads were simultaneously recorded. According to heart rate (HR) and amplitude of the waves, the electrocardiographs were calibrated at 50–100 mm/s and 10–20 mm/mV. All procedures took place in an isolated room in order to minimise the stress for birds. 2.3. ECG trace analysis Nomenclature and ECG interpretation were performed according to standard methods (Tilley, 1992). A general analysis of all the electrocardiographic recordings was first performed by a veterinary cardiologist (MJFP) to ensure the quality of the recording. In each tracing five beats (lead II) were selected for quality and mean values of waves and intervals of P-QRS-T deflections were determined. The mean electric axis (MEA) of ventricular depolarisation in the frontal plane was calculated by the vector method with the leads II and III. The morphologic patterns of P-QRS-T deflections were evaluated for every lead. The presence of
A commercial software package (SPSS Inc., Chicago, IL, USA) was used for statistical analysis. All measurements are expressed as mean ± standard deviation (SD). Non-parametric data were analysed by means of descriptive statistics. Parametric data (measurements of waves and intervals, body weight, HR and MEA) were analysed by means of one-way analysis of variance or by means of Kurskall–Wallis test. The influence of body weight and HR in electrocardiographic variables were analysed by means of Pearson (variables normally distributed) or Spearman (variables not-normally distributed) correlation tests. In all the analyses differences were considered to be significant when P < 0.05. 3. Results The protocol used in the study allowed recording of ECG tracings in conscious raptors of sufficient quality to evaluate the cardiac rhythm and HR and for reliable measurements of waves and intervals for at least five beats (Fig. 1). In general, the procedure was well tolerated by the raptors. Some struggling movements took place frequently during bird positioning and electrode placement. Otherwise the animals remained motionless in most cases. 3.1. Heart rate The HR range for the raptors studied was from 81 (GF) to 542 (FT) beats per minute (bpm). The mean HR was significantly different between species (P < 0.001) (Table 3) and inversely to the body weight (P = 0.003). The HR showed a significant negative relationship to the length of all waves and intervals (P duration, PR duration, QRS duration, R duration, S duration, ST duration, T duration, and QT duration, P < 0.001) (Table 2). 3.2. Rhythm Most of the tracings evaluated showed a regular sinus rhythm (93.3%). Sinus arrhythmia was evident in 5.3% of the tracings, corresponding to one GF and three ATN. One isolated supraventricular extrasystole was observed in one BB.
Table 1 Description of the species of raptors included in the study Family
Vulgar name
Scientific name
Abbreviation
Number of animals
Body weight (g) (mean ± SD)
Falconidae Accipitridae Strigidae
Eurasian kestrel Griffon vulture Little owl Eurasian Eagle owl
Falco tinnunculus Gyps fulvus Athene noctua Bubo bubo
FT GF ATN BB
35 10 20 10
185 ± 30 6370 ± 567 106 ± 39 1980 ± 383
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
121
Fig. 1. Electrocardiographic (standard bipolar limb leads) tracing of a Griffon vulture (Gyps fulvus): 50 mm/s and 20 mm/mV.
Table 2 Mean, standard deviation (SD) and range for lead II durations of component deflections in the studied raptors PR+#* (ms)
QRS+* (ms)
R+* (ms)
S+# (ms)
ST+#* (ms)
T+* (ms)
QT+#* (ms)
Eurasian kestrel (Falco tinnunculus) Mean ± SD 21.63 ± 2.51 40.38 ± 6.18 Range 17–27 27–54
18.84 ± 3.01 12–24
9.04 ± 1.53 5–11
16.49 ± 3.33 11–24
14.93 ± 6.66 2–31
45.50 ± 6.40 33–60
79.58 ± 8.83 61–97
Griffon vulture (Gyps fulvus) Mean ± SD 38.53 ± 4.43 Range 32–46
76.0 ± 12.45 63–101
40.10 ± 19.66 19–92
17.38 ± 5.16 11–25
29.21 ± 5.12 19–37
35.64 ± 14.60 12–59
70.63 ± 11.06 53–88
144.81 ± 8.91 133–159
Little owl (Athene noctua) Mean ± SD 29.36 ± 7.15 Range 21–42
59.43 ± 9.93 51–81
27.71 ± 12.08 18–47
13.65 ± 6.59 7–24
16.93 ± 4.82 13–27
28.36 ± 4.76 24–38
54.29 ± 6.98 47–65
110.3 ± 22.24 90–151
Eurasian Eagle owl (Bubo bubo) Mean ± SD 30.28 ± 5.91 Range 18–39
60.44 ± 9.76 41–74
31.61 ± 7.65 23–45
14.34 ± 4.84 8–20
25.17 ± 3.48 20–31
60.33 ± 9.02 49–72
50.78 ± 5.34 45–62
141.39 ± 10.10 121–154
Species
P+#* (ms)
+
Significant differences in function of the species of raptors (P < 0.001). #Significant body weight effect (P < 0.05). *Significant heart rate effect (P < 0.05).
3.3. P wave The P wave (atrial depolarisation) duration range on lead II was from 17 ms (FT) to 46 ms (GF). This parameter was significantly different between species (P < 0.001) and showed a positive relationship to the size (i.e. body weight) of the raptor (P = 0.047): the larger the bird the longer the P wave duration (Table 2). The lead II P wave amplitude range was from 0.06 mV (BB) to 0.28 mV (FT), having a mean value significantly different between species (P < 0.001). No significant relationship between this parameter and body weight was found (P = 0.118) (Table 3). The P wave was always positive on lead I, II and aVF (Table 4). In lead III the predominant morphology was positive (72.5%), followed by negative (15.7%) and biphasic (11.8%) morphology. In lead aVR, P wave was mainly negative (98.3%) being positive in only one GF (1.7%). Three morphologies were represented in lead aVL: positive (81.4%), negative (7%), and biphasic (11.6%). 3.4. PR interval The PR interval range on lead II was from 27 ms (FT) to 101 ms (GF) (Table 2). Significant differences between species were found in this parameter (P < 0.001). One positive
significant body weight effect was found (P = 0.007): the larger the bird of prey the longer the PR interval. Ta wave (atrial repolarisation), identified as a negative wave or depression in PR interval, was present in 6 FT. 3.5. QRS complex The QRS complex length range was from 12 ms (FT) to 92 ms (GF) having a mean value significantly different between species (P < 0.001) and showing a positive but not significant relationship to body weight (P = 0.116) (Table 2). Table 4 shows the relative percentages of morphology patterns of QRS deflections in the four species of raptors covered by the study. Of the total percentages lead I showed wider ranges of QRS morphologies, QS being the most frequent. In leads II, III and aVF the most frequent morphologies were QS and rS. Leads aVR and aVL showed the narrowest range of morphologies, R clearly being the most frequent. Q wave was only present in aVR and aVL leads showing a qR morphology. In lead II, R wave (when present) range was from 5 ms (FT) to 25 ms (GF) duration and 0.01 mV (FT and ATN) to 0.28 mV (GF) of amplitude (Tables 2 and 3). No significant influence of body weight in R wave duration and amplitude was found. Significant differences between spe-
122
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
Table 3 Mean, standard deviation (SD) and range for lead II amplitudes of component deflections, mean electrical axis (MEA) and heart rate (HR) in the studied raptors P+ (mV)
R+ (mV)
S+ (mV)
ST+# (mV)
T+# (mV)
HR+# (bpm)
Eurasian kestrel (Falco tinnunculus) Mean ± SD 0.2 ± 0.05 Range 0.08–0.28
0.06 ± 0.02 0.01–0.12
0.62 ± 0.21 0.31–1.27
0.26 ± 0.12 0.02–0.55
0.52 ± 0.17 0.24–0.98
425 ± 67 275–542
98 ± 4 107 to
Griffon vulture (Gyps fulvus) Mean ± SD 0.17 ± 0.04 Range 0.13–0.24
0.08 ± 0.08 0.03–0.28
0.49 ± 0.19 0.28–0.73
0.06 ± 0.03 0.02–0.1
0.21 ± 0.09 0.11–0.42
160 ± 45 81–228
78 ± 24 113 to 20
Little owl (Athene noctua) Mean ± SD 0.11 ± 0.02 Range 0.09–0.15
0.04 ± 0.01 0.01–0.05
0.19 ± 0.09 0.07–0.33
0.06 ± 0.05 0.01–0.13
0.21 ± 0.06 0.12–0.33
256 ± 58 110–336
88 ± 26 121 to 88
Eurasian Eagle owl (Bubo bubo) Mean ± SD 0.08 ± 0.02 Range 0.06–0.11
0.04 ± 0.01 0.02–0.06
0.32 ± 0.12 0.16–0.52
0.05 ± 0.03 0–0.11
0.18 ± 0.05 0.1–0.24
222 ± 47 160–295
95 ± 6 103 to
Species
MEA+ (°)
91
85
+
Significant differences in function of the species of raptors (P < 0.001). #Significant body weight effect (P < 0.05).
Table 4 Morphologies of P-QRS-T deflexions in the six bipolar standard leads in the studied raptors Eurasian kestrel (Falco tinnunculus) (%)
Griffon vulture (Gyps fulvus) (%)
Little owl (Athene noctua) (%)
Eurasian Eagle owl (Bubo bubo) (%)
Totals (%)
P QRS
Ps = 100 QS = 96.4, Rs = 3.6 Ps = 21.05, B = 78.95
Ps = 100 QS = 33.3, Rs = 33.3, RS = 33.3 Ps = 100
Ps = 100 rS = 14.3, QS = 85.7
T
Ps = 100 QS = 10, Rs = 20, RS = 50, R = 20 B = 87.5, N = 12.5
Ps = 100 rS = 2, Rs = 9.8, QS = 70.6, R = 3.9, RS = 13.7 Ps = 18.8, B = 78.1, N = 3.1
Ps QRS
Ps = 100 rS = 51.5, QS = 48.5 Ps = 100
Ps = 100 rS = 41.7, RS = 16.7, QS = 33.3, Rs = 8.3 Ps = 100
Ps = 100 rS = 11.1, QS = 88.9
T
Ps = 100 rS = 30, RS = 10, QS = 60 Ps = 100
Ps = 100
Ps = 100 rS = 40.6, RS = 4.7, QS = 53.1, Rs = 1.6 Ps = 100
Ps = 33.33, B = 33.33, N = 33.33 rS = 30, QS = 70 Ps = 100
Ps = 87.5, B = 12.5
Ps = 16.67, N = 83.33
Ps = 72.5, B = 11.8, N = 15.7
rS = 60, QS = 40 Ps = 100
QS = 100 Ps = 100
rS = 38.7, QS = 61.3 Ps = 100
Ps = 10, N = 90 QS = 10, qR = 40, R = 50 N = 100
N = 100 R = 55.6, qR = 44.4
N = 100 R = 100
Ps = 1.7, N = 98.3 QS = 1.6, qR = 17.7, R = 80.6
N = 100
N = 100
N = 100
I
Ps = 25, B = 75
II
III Ps QRS T aVR Ps QRS T aVL Ps QRS T aVF Ps QRS T
Ps = 92.86, B = 7.14 rS = 45.5, QS = 54.5 Ps = 100 N = 100 R = 91.2, qR = 8.8 N = 100 Ps = 73.91, B = 21.74, N = 4.35 R = 97.1, qR = 2.9 N = 100
Ps = 88.89, N = 11.11
Ps = 75, N = 25
Ps = 100
Ps = 81.4, B = 11.6, N = 7
R = 100 Ps = 10, N = 90
R = 100 N = 100
R = 100 N = 100
R = 98.3, qR = 1.7 Ps = 1.8, N = 98.2
Ps = 100 rS = 48.5, QS = 51.5
Ps = 100 rS = 40, QS = 60
Ps = 100 rS = 11.1, QS = 88.9
Ps = 100 rS = 42.9, R = 1.6, QS = 55.6
Ps = 100
Ps = 100
Ps = 100 rS = 54.5, R = 9.1, QS = 36.4 Ps = 100
Ps = 100
Ps = 100
I–III, standard bipolar limb leads; aVR, aVL and aVF, augmented bipolar limb leads; Ps, positive; N, negative; B, biphasic; Iso, isoelectric. Nomenclature of QRS complex follows standard methodology (Tilley, 1992).
cies of raptors were found in both parameters (P = 0.001 and 0.017, duration and amplitude of R wave, respectively). In the S wave lead II duration range was from 10 ms (FT) to 37 ms (GF) and its amplitude range covered
0.07 mV (ATN) to 1.27 mV (FT) (Tables 2 and 3). A positive correlation between the body weight and the S wave duration (but not in the amplitude) was found (P = 0.001). Mean values for S amplitude (but not in the
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
duration) were significantly different between raptor species (P < 0.001). 3.6. ST segment The ST segment in lead II was isoelectric in one case (BB), and elevated (>0.01 mV) in the rest. The degree of elevation was statistically different according to the species of bird (P < 0.001). 3.7. T wave The range of T wave duration was from 33 ms (FT) to 88 ms (GF) and 0.10 mV (BB) to 0.98 mV (FT) in amplitude (Tables 2 and 3). Means in both parameters of T wave were significantly different between species (P < 0.001). One negative significant body weight effect in T wave amplitude was found (P = 0.014): the larger the bird of prey the smaller the T wave. No significant body weight effect in T wave duration was identified (P = 0.051). In lead I morphology of T wave was mainly biphasic (78.1%) or positive (18.8%) and rarely negative (3.1%) (Table 4). In lead II, III and aVF, T wave was positive in all cases. By contrast, in aVR and aVL leads T wave was mainly negative (100% and 98.2%, respectively). P-on-T phenomenon was confirmed in four tracings (3 FT and 1 ATN). 3.8. QT interval The duration range of the QT interval in lead II was from 61 ms (FT) to 159 ms (GF) (Table 2), having a positive relation to the body weight (P = 0.006). Mean values of QT interval were significantly different between species of raptor (P < 0.001). 3.9. Mean electrical axis The MEA in the frontal plane presented a cranial direction in all cases within a range from 20° (GF) to 121° (ATN) (Table 3). The widest range corresponded to GF ( 20° to 113°) and the narrowest to FT ( 91° to 107°). Mean values for MEA were significantly different between species (P = 0.005). No significant relationship to body weight was found. 4. Discussion An abnormal ECG correlated with compatible historical information, physical examination findings and radiographic changes could be useful in the diagnosis of cardiac diseases in vivo (Miller, 1986). Information about the incidence of cardiac diseases in birds is scarce. Electrocardiographic changes have been described as being associated with infectious and non-infectious diseases (Gross, 1966; Mckenzie and Will, 1972; Andersen, 1975; Olkowski et al., 1997; Olkowski and Classen, 1998). Nevertheless,
123
some studies of necropsy have shown that heart disease in birds may occur more frequently than previously assumed (Cooper and Pomerance, 1982; Oglesbee and Oglesbee, 1998), suggesting that it could be clinically underdiagnosed in avian species. The main purpose of this study was to contribute to the use of ECG in the cardiac evaluation of raptors in a clinical setting. Many studies on avian electrocardiography have been performed using anaesthesia in order to restrain the animals (Szabuniewicz and Mcgrady, 1974; Nap et al., 1992; Burtnick and Degernes, 1993; Olkowski et al., 1997; Olkowski and Classen, 1998; Casares et al., 2000; Espino et al., 2001). Sedation and anaesthesia may influence several ECG values of waves and intervals as well as cardiac rhythm and HR (Nap et al., 1992; Tilley, 1992; Burtnick and Degernes, 1993), therefore ECG recordings should be obtained, if possible, from conscious animals (Miller, 1986; Tilley, 1992). Dorsal recumbence is recommended as the standard position to obtain ECG recordings (Miller, 1986; Burtnick and Degernes, 1993). In the present study, careful positioning of the conscious raptors in this way in an isolated quiet room (covering the head with a surgical cloth when necessary) allowed optimal immobilisation with mild restraining. Valuable information on cardiac rhythm, HR and morphology patterns was always possible with the recordings obtained. Measurements of at least five good quality P-QRS-T complexes in lead II were also possible. In addition, serious arrhythmia was not found in our study in contrast with other studies on anaesthetised birds (Nap et al., 1992; Burtnick and Degernes, 1993; Casares et al., 2000). As in the case of mammals (Tilley, 1992), significant differences between species of birds have been described in most of ECG parameters (Miller, 1986; Nap et al., 1992; Burtnick and Degernes, 1993; Cinar et al., 1996; Casares et al., 2000; Machida and Aohagi, 2001). In our study all measurements of waves and intervals were significantly different between species and differences in morphology patterns of the waves could also be identified. These findings support the need to know the specific electrocardiographic patterns and to have reference values for each species of bird of prey as well. A wide variability in morphology patterns of P-QRS-T deflections in each lead could be established by the present study, with each particular morphology differently represented between species but also within particular species of raptors. Given that all the birds used in the present study were healthy, this variability should be considered physiologic since it has already been considered in previous studies on domestic (Sturkie, 1949; Lumeij and Stokhof, 1985; Cinar et al., 1996) and non-domestic birds (Burtnick and Degernes, 1993; Machida and Aohagi, 2001; Espino et al., 2001). In the present study, the P wave was predominantly positive in leads I–III, aVL and aVF, and mainly negative in lead aVR. Leads III and aVL showed the wider range of morphologies (positive, negative, biphasic). On the whole, these findings agree with previous studies on
124
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
raptors (Burtnick and Degernes, 1993; Casares et al., 2000; Espino et al., 2001; Rodrı´guez et al., 2004) and non-raptor species (Mckenzie et al., 1971; Cinar et al., 1996). The low curve in the initial part of the PR-segment (called atrial T wave or Ta wave) depicts the repolarisation of the atria. In the case of dogs its presence is attributed to large atrial repolarisation forces caused by atrial hypertrophy (Tilley, 1992) and can also be seen with a rapid HR (Machida and Aohagi, 2001). In avian species, the Ta wave has been frequently described in healthy specimens without general abnormalities in the atrial size (Lumeij and Stokhof, 1985; Machida and Aohagi, 2001; Lopez Murcia et al., 2005). Although the reason is unknown, it is considered physiologic in birds (Machida and Aohagi, 2001). Within this study the phenomenon was present in 6 FT. To the best of the authors’ knowledge no previous reference to its presence in raptors exists. In the present study, the QRS polarity was mainly negative in I–III and aVF leads, being mainly positive in aVR and aVL leads. That way, if there was a positive and negative deflection during the QRS complex in I–III and aVF leads, the positive deflection was always seen first. These general findings agree with the described patterns for many avian species (Sturkie, 1949; Szabuniewicz and Mcgrady, 1974; Edjtehadi et al., 1977; Nap et al., 1992; Burtnick and Degernes, 1993; Casares et al., 2000; Espino et al., 2001; Rodrı´guez et al., 2004). However, just as in the case of P wave, we found a physiologic variability of QRS patterns between species and within a particular species. Duration and amplitudes of QRS complex showed similar variability with significant influences according to the species and body weight in many cases. This makes difficult and imprecise the evaluation of chamber enlargement based on morphology patterns and QRS complex measurements. In any event comparisons should always be done with reference data for each particular species. With a rapid HR, P wave and preceding T wave as well as T wave and preceding QRS complex may intermix (Miller, 1986; Tilley, 1992; Machida and Aohagi, 2001). In the first instance, when P wave and preceding T wave fuse (P-on-T phenomenon), the true morphology of each sample P and T waves may change (Miller, 1986). Previous studies have suggested that when P-on-T phenomenon is not associated with high HR, it may indicate alterations in ventricular repolarisation (Olkowski et al., 1997). In the present study P-on-T phenomenon was observed only in four tracings, always associated with high HR (458 ± 82 bpm). Secondly, ST segment is very short or absent and the S wave rises directly into the T wave (ST slurring) (Lumeij and Ritchie, 1999). In mammals this change can be attributed to myocardial ischemia (Tilley, 1992). In healthy birds, however, ST slurring is frequently described with an undetermined cause (Lumeij and Ritchie, 1999; Lopez Murcia et al., 2005). In our study ST segment was identifiable in all tracings, and hence ST slurring was not found in any of them. In agreement with previous works on birds (Lumeij and Stokhof, 1985; Nap et al.,
1992; Lumeij and Ritchie, 1999; Rodrı´guez et al., 2004), the ST segment appeared mainly elevated over baseline. T wave represents the ventricular repolarisation, being its polarity usually opposed to the main vector of QRS complex and always positive in lead II (Mckenzie et al., 1971; Cinar et al., 1996; Lumeij and Ritchie, 1999; Espino et al., 2001; Machida and Aohagi, 2001; Rodrı´guez et al., 2004). In the present study, T wave was always discordant with QRS complex and positive in lead II. Changes in QT interval may be seen in electrolyte disturbances, drug toxicity, anaesthesia, hypothermia, and central venous system disease in dogs and cats, although the QT interval alone is usually not enough to make a diagnosis (Tilley, 1992). In the present study, significant influence of species, body weight and HR in mean values of QT intervals were found. In accordance with previous studies on raptors (Burtnick and Degernes, 1993) this reveals a big variety within this parameter. Consequently, the interpretation of differences in QT interval in sequential tracings for diagnosis purposes should be carried out with caution. Again, comparisons should always be done with reference to data for particular species. A net MEA of around 90° (cranial) is characteristic of the avian ECG and implies the negative polarity of QRS complex in II, III, and aVF leads (Burtnick and Degernes, 1993; Lumeij and Ritchie, 1999). This constitutes the major difference in the normal ECG of the bird versus the dog, cat, or man (Tilley, 1992; Lumeij and Ritchie, 1999). This difference can be explained by the fact that in birds, the depolarisation wave of the ventricles begins subepicardially and spreads through the myocardium to the endocardium while in the dog depolarisation of the ventricles starts subendocardially (Lumeij and Ritchie, 1999). The mean MEA in the present study was 92 ± 2°, in accordance with described values for birds (Lumeij and Ritchie, 1999; Burtnick and Degernes, 1993). A wide range of values (always negative) was nevertheless found in selected species and significant inter-specific variability was seen. Major deviations from a normal MEA is useful in identifying different cardiac diseases in turkeys and chickens (Burtnick and Degernes, 1993; Olkowski et al., 1997). In order to ensure that any deviations from the norm are truly associated with pathology, comparisons should always be done with reference to data for a particular species. More precise comparisons of our data are difficult to make since no previous published data for the species included in our study have been found. Electrocardiographic data for 14 species of raptors have been published (Edjtehadi et al., 1977; Burtnick and Degernes, 1993; Espino et al., 2001; Rodrı´guez et al., 2004). Most of them are species phylogenetically and/or morphologically different from ours. Nevertheless, our Eurasian Eagle owls (Bubo bubo) and the Great horned owls (Bubo virginianus) of the study of Burtnick and Degernes (1993) as well as our Eurasian kestrels (Falco tinnunculus) and their American kestrels (Falco sparverious) are probably phylogenetically and morphologically close enough to make the comparison
J. Talavera et al. / Research in Veterinary Science 84 (2008) 119–125
interesting. In both cases, raptors in Burtnick’s study present very similar values for amplitudes of waves and MEA than our respective owls and kestrels. The most important difference is that our owls present higher HR and smaller durations of waves and intervals. The slower HR of the owls and kestrel in Burtnick’s study (more than half) can be definitively attributable to the effect of sedation used to register the ECG. Considering the significant negative relationship between HR and durations of component deflections found in our study, the longer duration of waves and intervals of Burtnick’s raptors could be also a consequence of the sedation, since it induces slower HR. In conclusion, the protocol described here allowed us to obtain interpretative ECG tracings in conscious raptors where valuable information about rhythm, HR, morphologic patterns and magnitude of component deflections could be obtained. Important electrocardiographic differences among species of raptors were found. This study provides electrocardiographic data for four species of raptors that can be used to establish comparisons for clinical purposes. In this way, the study contributes to the routine use of the ECG in the evaluation of cardiac status and the in vivo identification of cardiac diseases in raptors. References Andersen, H.T., 1975. Hyperpotasemia and electrocardiographic changes in the duck during prolonged living. Acta Physiologica Scandinavica 63, 292–295. Burtnick, N.L., Degernes, L.A., 1993. Electrocardiography on fifty-nine anesthetized convalescing raptors. In: Redig, P.T., Cooper, J.E., Remple, J.D., Hunter, D.B. (Eds.), Raptor Biomedicine. Chiron Publications Ltd., Keighley, pp. 111–121. Casares, M., Enders, F., Montoya, A., 2000. Comparative electrocardiography in four species of macaws (Genera Anadorhynchus and Ara). Journal of Veterinary Medicine A 47, 277–281. Cinar, A., Bagci, C., Belge, F., Uzun, M., 1996. The electrocardiogram of the Pekin Duck. Avian Diseases 40, 919–923. Cooper, J.E., Pomerance, A., 1982. Cardiac lesions in birds of prey. Journal of Comparative Pathology 92, 161–168. Edjtehadi, M., Rezakhani, D.A., Szabuniewicz, M., 1977. The electrocardiogram of the buzzard (Buteo buteo). Zentralblatt fur Veterinarmedizin Reihe A 24, 597–600.
125
Espino, L., Sua´rez, M.L., Lo´pez-beceiro, A., Santamarina, G., 2001. Electrocardiogram reference values for the buzzard in Spain. Journal of Wildlife Diseases 37, 680–685. Gross, W.B., 1966. Electrocardiographic changes of Escherichia coli infected birds. American Journal of Veterinary Research 27, 1427– 1436. Lopez Murcia, M.M., Bernal, L.J., Montes, A.M., Garcia Martinez, J.D., Ayala, I., 2005. The normal electrocardiogram of the unanaesthetized competition ‘‘Spanish Pouler’’ pigeon (Columba livia gutturosa). Journal of Veterinary Medicine A 52, 347–349. Lumeij, J.T., Ritchie, B.W., 1999. Cardiology. In: Ritchie, B.W., Harrison, G.J., Harrison, L.R. (Eds.), Avian Medicine: Principles and Application. HBB International, Delray Beach, pp. 695–722. Lumeij, J.T., Stokhof, A.A., 1985. Electrocardiogram of the racing pigeon (Columba livia domestica). Research in Veterinary Science 38, 275–278. Machida, N., Aohagi, Y., 2001. Electrocardiography, heart rates and heart weights of free-livings birds. Journal of Zoo and Wildlife Medicine 32, 47–54. Mckenzie, B.E., Will, J.A., 1972. Electrocardiographic changes following influenza infection in turkeys. Avian Diseases 16, 308–318. Mckenzie, B.E., Will, J.A., Hardie, A., 1971. The electrocardiogram of the turkey. Avian Diseases 15, 737–744. Miller, M.S., 1986. Electrocardiography. In: Harrison, G.J., Harrison, L.R. (Eds.), Clinical Avian Medicine and Surgery. W.B. Saunders, Philadelphia, pp. 286–292. Nap, A., Lumeij, J.T., Stokhof, A.A., 1992. Electrocardiogram of the African Gray (Psittacus erithacus) and Amazon (Amazona spp.) parrot. Avian Pathology 21, 45–53. Oglesbee, B.L., Oglesbee, M.J., 1998. Results of postmortem examination of psittacine birds with cardiac disease: 26 cases (1991–1995). Journal of American Veterinary Medical Association 212, 1737–1742. Olkowski, A.A., Classen, H.L., 1998. High incidence of cardiac arrhythmias in broiler chickens. Journal of Veterinary Medicine A 43, 83–91. Olkowski, A.A., Classen, H.L., Riddell, C., Bennett, C.D., 1997. A study of electrocardiographic patterns in a population of commercial broiler chickens. Veterinary Research Communications 21, 51–62. Rodrı´guez, R., Prieto-montan˜a, F., Montes, A.M., Bernal, L.J., Gutie´rrez panizo, C., Ayala, I., 2004. The normal electrocardiogram of the unasesthetized peregrine falcon (Falco peregrinus brookei). Avian Diseases 48, 405–409. Sturkie, P.D., 1949. The electrocardiogram of the chicken. American Journal of Veterinary Research 10, 168–175. Szabuniewicz, M., Mcgrady, J.D., 1974. The electrocardiogram of the Japanese (Coturnix coturnix japonica) and Bobwhite (Colinus virginianus) Quail. Zentralblatt fur Veterinarmedizin Reihe A 21, 198–207. Tilley, L.P., 1992. Essentials of Canine and Feline Electrocardiography. Interpretation and Treatment, third ed. Lea & Febiger, Philadelphia.