Morphometry of the heart of budgerigars (Melopsittacus undulatus), Alisterus parrots (Alisterus s scapularis) and common buzzards (Buteo buteo)

Research in Veterinary Science 2002, 72, 147±151 doi:10.1053/rvsc.2001.0540, available online at http://www.idealibrary.com on

Morphometry of the heart of budgerigars (Melopsittacus undulatus), Alisterus parrots (Alisterus s scapularis) and common buzzards (Buteo buteo) J. STRAUB*y, K.-P. VALERIUSz, M. PEESy, M.-E. KRAUTWALD-JUNGHANNSy y

Institute for Avian Diseases, Department of Small Animal Medicine, University of Leipzig, An den Tierkliniken 17, D-04103 Leipzig, Germany, zInstitute for Anatomy and Cell Biology, Faculty of Medicine, University of Giessen, Aulweg 123, D-35392 Giessen, Germany SUMMARY In order to establish data and reference values for the thickness of the myocardium and the length of the left and the right ventricle of the avian heart, the hearts of 14 budgerigars (Melopsittacus undulatus), five Alisterus parrots (Alisterus s scapularis) (also known as Australian king parrot) and 10 common buzzards (Buteo buteo) of both sexes were examined according to a standard protocol. In order to compare the results of birds of different sizes all data were related to the size of the bird's body (length of the sternum) and the results of the measurements of the myocardial thickness in relation to the length of the heart. Results of different zones were compared by means of statistical methods within one species. Besides that a comparison between the different species was performed. Only minor significant differences were noted. # 2002 Elsevier Science Ltd. All rights reserved.

MORPHOLOGICAL alterations of the heart are well known and often described in poultry (e.g. hypertrophy due to `round heart disease') (Eber and Pallaske-Eber 1934, SchroÈter 1952, Franze 1981, Bergmann 1992). By way of contrast little is known about similar aberrations in cage and aviary birds (Oglesbee and Oglesbee 1998, Straub et al 2000). Due to lack of reference values for the size of the avian heart and especially the thickness of the myocardium judgement of these parameters, for example during necropsy, often causes difficulties. Independent of species the right ventricle is described as `relatively thin' and the free wall of the left ventricle being 2 to 3 (or even up to 4) times as thick as the free wall of the right ventricle. The interventricular septum is as thick as the myocardium of the left ventricle (Salomon 1993, Lumeij and Ritchie 1994, Evans 1996, Smith et al 2000, Waibl and Sinowatz 1992). With regard to the length of the ventricles, the right ventricle is described as being 2/ 3 of the length of the left ventricle (Waibl and Sinowatz 1992). Specific data are only present for the budgerigar (Melopsittacus undulatus). The length of the heart is 14
1 mm and the width is 7
5 mm (SchoÈne and Arnold 1980). Bodyweight or other parameters of the birds examined are not reported. Due to the lack of detail in previous reports measurements of the length of defined distances and the thickness of specific locations of the myocardium have been performed in 29 euthanised birds to record normal *Corresponding author: Institute for Avian Diseases, Department of Small Animal Medicine, University of Leipzig, An den Tierkliniken 17, D-04103 Leipzig, Germany; E-mail: [email protected]

0034-5288/02/020147 ‡ 05 $35.00/0

reference values for the first time. The results obtained from different zones were compared by statistical analysis of the data obtained from one species. To get an idea about the differences or similarities with regard to common characteristics between the species examined, the results obtained for each species were compared with each other. MATERIAL AND METHODS For this study the hearts of 14 budgerigars (Melopsittacus undulatus) (8 male, 6 female, 9±24 months old), 5 Alisterus parrots (Alisterus s scapularis) (3 male, 2 female, 2 to 4 years old) and 10 common buzzards (Buteo buteo) (6 male, 4 female, adult) have been examined. All the parakeets were anaesthetised with diazepam (1 mg kgÿ1BM, I.M.) and ketamine hydrochloride (25 mg kgÿ1BM, I.M.) and then euthanised with an aqueous solution (1 mg kgÿ1BM, via intrapulmonary inj.) of embutramide (200 mg mlÿ1), mebezonium iodide (50 mg mlÿ1), and tetracaine hydrochloride (5 mg mlÿ1). Euthanasia was carried out because of severe non-infectious feather dysplasia. Six of the common buzzards were euthanised under the same regime due to irreparable fractures. Four common buzzards died soon after they were brought to the clinic subsequent to trauma. Mean values of the body mass, the heart mass and the relationship of body mass to heart mass as well as the length of the sternum are listed in Table 1. The body cavity of all birds was opened by a longitudinal incision through the abdominal wall. The sternum was removed after severing the breast muscles # 2002 Elsevier Science Ltd. All rights reserved.

148

J. Straub, K.-P. Valerius, M. Pees, M.-E. Krautwald-Junghanns

and the bones of the pectoral girdle. After removing the hearts all birds were examined by standard techniques. None of the birds showed any sign for internal disease which may have affected the cardiovascular system. TABLE 1: Mean values of bodymass, heartmass, relation of bodymass to heartmass, and length of the sternum of the three examined species

M. u. (n ˆ14) Mean SD

Max Min A. s. (n ˆ 5) Mean SD

Max Min B. b. (n ˆ10) Mean SD

Max Min

BM (g)

HM (g)

HM /BM (%)

Sternum (mm)

44
86 6
63 53
00 32
00

0
65 0
10 0
83 0
38

1
45 0
15 1
76 1
19

33
11 1
20 36
20 31
30

119
00 10
05 130
00 103
00

1
62 0
26 1
94 1
24

1
36 0
18 1
62 1
18

44
74 1
99 47
00 41
80

886
60 257
08 1,286
00 485
00

6
23 1
39 9
62 4
85

0
73 0
17 1
00 0
49

64
63 3
13 69
10 59
00

M. u. ˆ Melopsittacus undulates, A. s. ˆ Alisterus s. scapularis, B. b. ˆ Buteo buteo, SD ˆ standard deviation, Max ˆ maximum, Min ˆ minimum, BM ˆ bodymass, HM ˆheartmass.

The pericardium of each heart was completely removed. Afterwards the hearts were separated into two almost symmetrical parts. The hearts were placed on their left sides on a cutting board and a longitudinal cut running through the apex of the heart, the uppermost region of the right ventricular wall and the centre of the interventricular septum was performed. All blood clots were removed and the total mass of the heart was determined. Measurements of the thickness of the myocardium of three regions of the left and the right ventricular free wall as well as the interventricular septum were made by using precision callipers. Additionally measurements for the length of the left and the right ventricles were ascertained (Fig 1). In order to compare the results of the measurements in birds of different sizes all values were related to the length of the sternum of each bird. Furthermore the results of the measurements of the myocardial thickness were related to the length of the left ventricle. Statistical evaluation was performed with the SPSS 10
0 program. The Wilcoxon test was performed for the comparison of measurements of different regions within one bird. In order to compare the different species the Mann-Whitney test was used. The margins of significance were determined as followed: significant P  0
05, highly significant P  0
001. RESULTS

FIG 1: Schematical illustration of the measured sites and distances Vl ˆleft ventricle, Vr ˆ right ventricle; a toi ˆ thicknessofthe myocardium: a to c ˆ left ventricular free wall, a ˆ basal, b ˆ middle, c ˆ apical; d to f ˆ interventricular septum, d ˆ basal, e ˆ middle, f ˆ apical; gto i ˆright ventricular free wall, g ˆ basal, h ˆ middle, i ˆ apical; distances: d to c ˆ length of the left ventricle close to the interventricular septum; d to f ˆ length of the right ventricle close to the interventricular septum.

The mean thickness of the apical myocardium of the left ventricle (point c in Fig 1) in all examined birds was between 2
30 and 2
85 per cent of the sternal length respectively 6
82 to 8
14 per cent of the length of the left ventricle of the bird (Table 2). Thus in all examined species the apex of the heart was significantly thinner (Alisterus parrot and common buzzard P  0
05, budgerigar P  0
001) than the other regions of the left free wall (middle region ˆ point b in Fig 1 ˆ 8
26 to 8
65 per cent of the sternal length respectively 23
49 to 24
54 per cent of the length of the left ventricle, basal region ˆ point a in Fig 1 ˆ 7
94 to 9
01 per cent of the sternal length, respectively 21
71 to 26
63 per cent of the length of the left ventricle). No statistically significant differences could be demonstrated between the middle and the basal parts. By comparing the results of the measurements of the three regions (apical, middle, basal) of the three species no statistical significant differences were found between the species. In all species examined the mean thickness of the apical part of the interventricular septum (point f in

TABLE 2: Mean thickness of the left ventricular free wall in relation to the length of the sternum and the length of the left ventricle Basal (point a) … x  s†

B. b. M. u. A. s.

Middle (point b) … x  s†

Apical (point c) … x  s†

(% S)

(% Vl)

(% S)

(% Vl)

(% S)

(% Vl)

7
94 (1
20) 8
11 (1
24) 9
01 (1
42)

22
42 (3
31) 21
71 (3
70) 26
63 (4
01)

8
28 (1
82) 8
65 (1
40) 8
26 (1
55)

23
49 (5
65) 23
86 (4
34) 24
54 (5
30)

2
85 (1
01) 2
74 (0
48) 2
30 (0
57)

8
14 (3
18) 7
01 (1
73) 6
82 (1
73)

B. b. ˆ Buteo buteo, M. u. ˆ Melopsittacus undulates, A. s. ˆ Alisterus s scapularis, S ˆ length of the sternum, Vl ˆlength of the left ventricle.

149

Morphometry of the heart of budgerigars, parrots and buzzards TABLE 3: Mean thickness of the interventricular septum in relation to the length of the sternum and the length of the left ventricle Basal (point d) … x  s†

B. b. M. u. A. s.

Middle (point e) … x  s†

Apical (point f) … x  s†

(% S)

(% Vl)

(% S)

(% Vl)

(% S)

5
94 (1
59) 6
44 (1
22) 6
82 (2
01)

16
78 (4
75) 16
68 (3
26) 20
59 (7
83)

7
69 (1
22) 7
32 (1
05) 7
81 (1
42)

21
79 (3
99) 18
82 (2
95) 23
51 (6
74)

6
07 (0
78) 5
82 (1
32) 6
63 (0
54)

(% Vl) 17
21 (2
92) 15
83 (3
23) 19
71 (2
94)

B. b. ˆ Buteo buteo, M. u. ˆ Melopsittacus undulates, A. s. ˆ Alisterus s scapularis, S ˆ length of the sternum, Vl ˆlength of the left ventricle.

TABLE 4: Mean thickness of the right ventricular free wall in relation to the length of the sternum and the length of the left ventricle Basal (point g) … x  s†

B. b. M. u. A. s.

Middle (point h) … x  s†

Apical (point i) … x  s†

(% S)

(% Vl)

(% S)

(% Vl)

(% S)

(% Vl)

2
17 (0
45) 2
66 (0
46) 1
58 (0
47)

6
15 (1
58) 7
41 (1
63) 4
80 (1
86)

2
42 (0
63) 2
39 (0
57) 2
18 (0
51)

6
81 (1
70) 6
72 (1
65) 6
49 (1
93)

2
02 (0
49) 1
75 (0
38) 1
42 (0
34)

5
66 (1
20) 4
97 (1
09) 4
19 (0
99)

B. b. ˆ Buteo buteo, M. u. ˆ Melopsittacus undulates, A. s. ˆ Alisterus s scapularis, S ˆ length of the sternum, Vl ˆlength of the left ventricle.

Fig 1) was also significantly smaller (P  0
05) than in the middle region (point e in Fig 1) (Table 3). In contrast to the left free wall a difference of the mean thickness of the middle and the basal region of the interventricular septum was also evident. In all species the uppermost region of the interventricular septum (point d in Fig 1) was thinner than the middle part. A statistical significance (P  0
05) for this difference was proven in common buzzards and budgerigars. In the Alisterus parrot the difference was also evident but was not significant. Between the basal and the apical region of the interventricular septum no significant difference concerning the myocardial thickness could be demonstrated. As a conclusion it can be stated that the thickness of the interventricular septum increases from basal to the middle region and then decreases on its way to the apex. No significant differences between the species could be shown. Concerning the thickness of the myocardium of the right ventricular free wall uniform results were obtained for the middle region (point h in Fig 1) (Table 4). Comparable to the left free wall and the interventricular septum the apical part of the right ventricular free wall (point i in Fig 1) was thinner than the middle part (P  0
05). No statistical difference for the thickness of the apical and the middle region of the right ventricular free wall between the species was shown. Statistically significant differences between the species were only evident for the comparison of the thickness of the basal part of the right ventricular free wall (point g in Fig 1). The relative thickness of the myocardium in this point was significantly higher in budgerigars than in Alisterus parrots and in common buzzards. With regard to the relative thickness of the myocardium only minor differences between the species were evident, greater differences were found when comparing the length of the ventricles (Table 5). The relative length of the left and the right ventricle (measured close to the interventricular septum, distance d±c and d±f in Fig 1, in relation to the length of the sternum)

TABLE 5: Mean length of the right and the left ventricle measured close to the interventricular septum in relation to the length of the sternum and relationship of left and right ventricular length

B. b. M. u. A. s.

x  s† Vl … (% S)

Vr … x  s† (% S)

Vl/Vr …x  s† (%)

35
58 (2
87) 38
26 (4
27) 33
97 (3
28)

25
62 (2
12) 29
91 (3
08) 26
06 (3
08)

72
13 (4
23) 76
07 (5
23) 78
16 (5
48)

B. b. ˆ Buteo buteo, M. u. ˆ Melopsittacus undulatus, A. s. ˆ Alisterus s scapularis, S ˆ length of the sternum, Vl ˆlength of the left ventricle, Vr ˆ length of the right ventricle.

in Alisterus parrots was significantly smaller than in the other species. Furthermore the length of the right ventricle of the common buzzard was significantly smaller than of the budgerigars. By comparing the relative length of the ventricles (in relation to each other) a significant difference between Alisterus parrots and common buzzards was evident. DISCUSSION Due to current clinical work at this centre the importance of heart disease in cage and aviary birds has been found to be much higher (Straub et al 2000) than might have been suspected by reading the limited literature available on the subject (Oglesbee and Oglesbee 1998, Braun et al 2000). For the assessment of the results of pathological examination reference values are absolutely necessary. To our knowledge, so far no data have been published about the size of the heart and the thickness of the myocardium of psittacines or raptors, except for one study (Valerius et al 2000). For this reason the thickness of the left and the right ventricular free wall as well as the thickness of the interventricular septum and the length of the left and the right ventricles were determined in birds of three species which are commonly presented to the veterinarian.

150

J. Straub, K.-P. Valerius, M. Pees, M.-E. Krautwald-Junghanns

Firstly examination of budgerigars was carried out because this species is very popular, being often kept as a companion species, and therefore probably the bird that is most often presented to the veterinarian. In the next stage the results obtained from the budgerigars were compared with the results of the other psittacines. Because of the problem of comparing birds of different sizes, all measurements were related to the length of the sternum of each bird. By using the length of the sternum the problem of the variation in bodymass was overcome. Additionally the thickness of the myocardium was related to the length of left ventricle and the length of the two ventricles was related to each other. By comparing the results for the two species of psittacines mentioned above it became obvious that the hearts of budgerigars and Alisterus parrots showed a lot of similarities. To obtain more information about the proportions of the avian heart common buzzards were examined. This had two advantages, on the one hand birds of another order (Accipitriformes) became part of the study and on the other hand free living birds were examined. Once again by comparing the results it could be shown that only minor differences were evident between the parameters of the hearts of all three species. Accordingly, and with some reservations, a tentative proposal can be made that the hearts of all avian species follow a set morphological pattern. The myocardium of the ventricles as well as the interventricular septum in all three examined species showed more or less the same changes of the thickness from the basis to the apex of the heart. Whilst the thickness of the left ventricular free wall decreases in the direction to the apex the interventricular septum and the right

ventricular free wall becomes thicker from the basis to the middle region and than decreases in thickness towards the apex (Fig 2). Further investigation of the birds of other species and other orders will have to be made to confirm to what extend this basic layout is applicable to all or most avian species of birds. Regardless of whether a further generalization is possible or not, with this study, reference values for the species examined have been determined and reliable judgement of ventricular hypertrophy and dilatation is now possible. Furthermore it is shown by this work that for these evaluations the comparative relationship of heart parameters can be related to the length of the sternum as well as into relation to the length of the left ventricle. Whilst the length of the sternum was used for the creation of relative values before (Hanley et al 1997, Boskovic et al 1999) the relationship of the thickness of the myocardium versus the length of the left ventricle has now been used for the first time. Additionally with this study a first overview about the structure of the ventricular myocardium is established. It could be clearly demonstrated that in contrast to older illustrations (Hummel 2000) regions of different thicknesses are a physiological normal of the avian heart. An answer as to why these differences in thickness exist cannot at this stage be given. With regard to the length of the ventricles and regardless of the differences between the species investigated it was shown that the length of the right ventricle is between 70 and 80 per cent of the length of the left ventricle which is longer than previously described (Waibl and Sinowatz 1992). ACKNOWLEDGEMENT This study was funded by the `Deutsche Forschungsgemeinschaft' (DFG). The authors would like to thank Mr. B. Coles for linguistic support. REFERENCES

FIG 2: Heart of a common buzzard (Buteo buteo) LVFW ˆleft ventricular free wall, IVS ˆ interventricular septum, RVFW ˆright ventricular free wall.

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Accepted December 19, 2001