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Ocular Histomorphometry of Free-Living Common Kestrels (Falco tinnunculus).

Abstract: We evaluated the histomorphometry of the eye structures (cornea, retina, choroid, and sclera) of 13 adult free-living common kestrels (Falco tinnunculus). Birds included in the study were euthanatized because of severe trauma from a motor vehicle injury. The eyes were enucleated immediately after euthanasia, fixed in 10% buffered formalin, and decalcified. The right eyes were cut vertically (dorsoventrally) and the left eyes cut horizontally (temporonasally). Tissues were processed, stained with hematoxylin and eosin, and evaluated by an image analysis software. The thicknesses of the diverse corneal layers were measured at 3 points; 2 at the peripheral region (A and C) and one at the central region (B). The thicknesses of the retina, choroid, and sclera were evaluated at 6 different positions. Measurements of the left and right eyes of the male and female birds were compared. The median thicknesses of the cornea at the peripheral points were 210.78 (A) and 197.79 (C) [micro]m, and 129 pm at the central point (B). The thickness of the cornea did not differ significantly between males and females or between right or left eyes. The mean thicknesses of the retina, choroid, and sclera were 91.13, 20.74, and 92.8 [micro]m, respectively. The thickness of the choroid and sclera did not differ significantly between the sexes or between the right and left eyeballs. The retinas of the females were significantly thicker than those of males at the points in the fundus of the eyeball, near the insertion of the pecten (optical nerves).

Key words: eye, cornea, thickness, retina, choroid, sclera, histomorphometry, avian, kestrel, Falco tinnunculus

Introduction

Vision is the most important sensory modality for many birds. (1-4) To diagnose ocular alterations correctly, knowledge of the diverse structures, anatomy, and histology of avian eyes is fundamental. Avian eye anatomy is very different than that of the mammalian eye. Some structures observed only in birds are the pectin, a vascular structure protruding into the vitreous chamber that is responsible for avascular retina nourishment; the scleral ossicles ring; and the presence of a striated sphincter muscle of the iris, which controls voluntary contraction of the pupil. (5-7) Additionally, some avian species have a fovea, which is a specialized region of the retina responsible for increased visual acuity. (6,8)

The avian eyeball is formed by the anterior segment (cornea, anterior chamber, iris, and lens) and the posterior segment (vitreous chamber, retina, pectin, choroid, and sclera). The avian cornea tends to be relatively thin, with the exception of waterfowl and some diurnal birds of prey. The 5 layers (from the outermost to the innermost) of the cornea are: (1) the epithelium (epithelium corneae externum), (2) Bowman's membrane (lamina limitans superficialis), (3) stroma (substantia propria corneae), (4) Descemet's membrane (lamina limitans posterior), and (5) endothelium (epithelium corneae internum). (5,8) Bowman's membrane in birds is acellular and extremely thick compared to the membrane in humans and primates. This membrane is responsible for corneal stability. (8,9) Descemet's membrane, the layer below the stroma, is relatively thin and is not present in all avian species. The lack of blood vessels at the cornea requires nutrition and protection by the diffusion of fluid from the anterior chamber and precorneal tear film. (8) A lack of adequate cell nutrition can cause swelling, which in turn then can alter the spacing between collagen fibrils and cause opacity of the stroma. (10) Among the ocular structures, the cornea is the most strongly affected by a variety of disorders. (11) Knowledge of the normal corneal physiologic conditions is necessary to recognize alterations.

The retina is a tissue that internally covers the posterior chamber of the eye and is responsible for the formation of images. (12) The avian retina is not vascularized. (6,7,13,14) It has all of the same types of cells and layers present in vertebrates, (8) but it has a larger concentration of photoreceptors in the fovea. The retinal pigment epithelium is firmly adherent to the choroid and, in diurnal birds, it is rich in melanin granules, (5) hindering the ophthalmoscopic examination. However, in nocturnal birds, the pigmentation is much more discreet. These layers are located inside the stratum nervosum retinae and the adherence between them is very fragile, which physiologically becomes stabilized by the vitreous body. The retina of birds is thicker than other animals because of the large amount of nerve cell associations. Thus, the dove's retina is twice as thick as that of humans because of the more developed granular and plexiform layer. (5)

The choroid is located between the retina and sclera and originates caudally from the ciliary body to the ora serrata. (5) In birds, the choroid has a strong link with the retinal pigment epithelium layer and less adherence with the sclera. (5,15) It is a relatively highly vascularized structure, and its main function is the nutrition and oxygenation by retinal diffusion, (5,7,8,15,16) as well as serving as a "cooling system" involved in the dissipation of heat (generated from light absorption by retinal photoreceptors). (8,15) Choroidal thickness varies according to the birds' age and sex, and also according to the location, being thicker under the fovea in some species and thinner around the optic disc. (7)

The sclera is the outermost layer of the posterior part of the eye. It is a very sturdy structure, preventing modification of its shape by internal and external pressure. (17,18) The avian sclera is composed of hyaline cartilage lined by dense connective tissue (18-20) and at the intersection of the conjunctiva-sclera is the ossicles scleral ring. (21)

Knowledge of normal morphologic aspects in different avian species is important for histopathologic evaluation of the eye bulb. There is a lack of published studies describing the anatomy and histomorphology of the eyes of healthy wild birds. The aim of this research was to describe morphometric aspects of healthy right and left eyeballs from wild, adult, male and female common kestrels (Falco tinnunculus) and to measure the thickness of their cornea, retina, choroid, and sclera.

Materials and Methods

A total of 13 free-living common kestrels that were admitted to the Clinics for Birds. Reptiles, Amphibians and Pet Fish at LMU University in Munich, Germany because of motor vehicle trauma were used in this study. The birds underwent clinical, radiographic, and ophthalmologic ultrasound examinations. Birds with severe injuries, such as fractures of the wings, legs, or sternum, which are incompatible with survival or animal welfare, were euthanatized. The ocular globes, without ultrasound alterations, were enucleated immediately after euthanasia and fixed for 24 to 48 hours in 10% buffered formalin (pH 7.3). The ocular globes were decalcified in a ready-to-use kit (Decalcifier MERCK; Merck Millipore, Billerica, MA, USA) for 6 to 12 hours. Using the optic nerve and insertion of the third eyelid tendon as references, (22) the right eyes were cut vertically (dorsoventrally) into 2 halves, so that the pecten and optic nerve could be cut longitudinally. The left eye was cut horizontally (temporonasally), perpendicular to the cut line of the right eye, to produce 2 halves, without cutting the pecten or optic nerve.

The ocular globe halves were embedded in paraffin, sectioned at 5-[micro]m thickness, and then stained with hematoxylin and eosin. Each eye produced 2 paraffin blocks, and at least 6 semiserial sections were prepared from each block.

The histologic sections were observed initially with the aid of a stereomicroscope (Nikon YS2-T; Nikon, Tokyo, Japan) so that 3 distinct points of the cornea (A, B, and C), and 6 points of the posterior eye wall could be defined (points 1-6; Figs 1 and 2). From the original group of 13 birds that were admitted during a 1-year period (July 2008-June 2009), eyeballs of 13 birds were used (5 males and 8 females) for the ocular fundus analysis, whereas for the measurement of the cornea, 10 birds were used (3 males and 7 females). The sections were analyzed using light microscopy (Nikon Eclipse E200) and image analysis software (ImageTool for Windows, version 3.0, available in the public domain at http://compdent.uthscsa.edu/ dig/itdesc.html). The thicknesses of the cornea at the respective points and the thicknesses of the 3 distinct layers, the epithelium (outermost layer), middle layer (Bowman's membrane, stroma, and Descemet's membrane), and endothelium (inner most layer) were measured in micrometers (pm). The thickness of the retina, choroid, and sclera were measured at the six points (1-6).

Results from measurements of the cornea and retina of the female and male birds and right and left eyeballs were evaluated by a repeated measure analysis of variance (ANOVA) and the Tukey test using commercial statistical software (SAS Institute, Inc, Cary, NC, USA). (23)

Results

Corneal thickness measures

Corneal thickness were measured through histologic slides from 10 specimens of wild kestrels (3 males and 7 females), including the 3 layers: epithelial, middle, and endothelial (Fig 3). The measured values from the 3 layers at the 3 points described above from males and females, and from both eyeballs, are listed in Table 1.

The corneas were thicker at their peripheral points (mean thickness, A = 210.8 and C = 197.8 [micro]m) when compared to the central point (B = 129.0 [micro]m; Fig 4). Although the corneal thicknesses observed on the 3 points of the left eyes were thicker than those of the right eyes and the corneas in females were thicker than in males (Fig 5), these differences were not statistically significant.

Retinal, choroid, and scleral thickness measures

All measures of the retinal, choroid, and scleral thickness were compiled (Table 2). These data showed the mean values, standard deviations, and minimum and maximum values at the six different points (1-6) in the right and left eyeballs of wild kestrels (male and female).

The results of measurements of the retinal thickness at various points and correlation with sex and right and left eyes are shown in Figure 6. Retinal thickness gradually increased at points 1 to 3 and then gradually decreased at the points 4 to 6. The retina was statistically thinner at points 1 and 6 and the largest region of the retina was at point 3. The difference in comparative retinal thickness in the right and left eyes was not statistically significant. Females tended to have a thicker retina than males at points 2 to 6, and this difference was statistically significant at points 3 to 5.

Mean choroid thickness at the 6 points, in males and females, and in the right and left eyes, are shown in Figure 7. Although there were numerical differences regarding choroid thickness between the right and left eyes, and also between males and females at various points, these differences were not statistically significant.

The results of the scleral thickness at different measuring points, in both sexes and in both eyes, are shown in Figure 8. Although numerical differences were present in the scleral thickness of the right and left eyes and between males and females, these differences were not statistically significant. Only point 4 was significantly different in scleral thickness (P < .05) when compared to other points.

The mean percentages of the retinal, choroid, and scleral thickness of the 6 points measured (correlated with the birds' sex) are shown in Figure 9. Of the three structures studied (retina, choroid, and sclera) in males and females, the pattern was similar between them; the retina increased its thickness from points 1 to 3 and decreased from points 4 to 6. The sclera inversely followed the retinal pattern; that is, where the retina was the thickest, the sclera was the thinnest, and vice versa. The choroid thickness remained essentially unchanged on all 6 points. Thickness of the retina differed significantly between sexes, with the female structure thicker than that of males at points 3 to 5.

Discussion

Results of this study of the corneal, retinal, choroid, and scleral membranes of right and left eyeballs from male and female free-living kestrels revealed a significant difference only in the thickness of the retina, which is thicker in females than in males. All other parameters measured showed no significant differences between eyes or sexes. Whether this difference in the female retinal thickness suggests a better visual acuity or if the females need more accurate vision during their reproduction period is unknown and requires further study.

Research about the anatomy and histology of the tissues and organs of various animal species is important to define reference values and when performing comparative studies across species, age groups, and pathologic alterations. To our knowledge, no previous studies have evaluated the three corneal layers (epithelial, middle, and endothelial) in birds.

The results of histologic analysis of F tinnunculus corneas showed that the right and left eyes exhibited increased thicknesses in the periphery (points A and C) and decreased thicknesses in the center (point B). These findings were consistent with results of other studies using different measurement techniques on diverse animal species, including dogs, (24-28) pigs, (28-30) horses, (31-33) and people. (34) Other studies have reported opposite results in dogs, (27) cats, (35) and rabbits. (36) The increased thickness of the avian cornea at the periphery may arise because the cornea and sclera are responsible for maintaining the ocular globe shape and protecting the internal structures that support various internal and external pressures. (37)

In our study, the mean corneal thickness of kestrels was 129 pm, which was determined on histologic examination. Measurements done by ultrasound techniques with the same species revealed a mean corneal thickness of 305.3 [micro]m. (38) These differences show that the histologic technique caused corneal thinning. The thickness of the cornea also can vary depending on the breed, age, weight, and sex of the animals, and on the time at which the examinations are performed. (28,30) A directly proportional correlation between age and corneal thickness in mammals has been reported. (24,25,32,35,39) In a study in domestic chickens, the central corneal thickness decreased during the first 12 days of age and then increased gradually until 70 days of age, after which the thickness did not change significantly throughout the remainder of the study period (450 days). (40) The results of the current study demonstrated that the total thickness of the cornea was greater in females than in males at each of the 3 points studied (A-C) in both eyes. However, these differences were not statistically significant. Results also demonstrated that the absolute thickness values of the right (121.6 [micro]m) and left (136.4 [micro]m) eyes are different. By using the ultrasound techniques with the same individual birds, the thickness of the right and left corneas was 299.5 and 311 [micro]m, respectively. (38) Despite the numerical differences observed on the histologic measures, the differences were not statistically significant.

The thickness of the retina from kestrels studied in this work was measured from the internal limiting membrane to the retinal pigment epithelium. A gradual increase in points 1 to 3 and a gradual decrease in points 4 to 6 has been observed, and the thicker points (points 3 and 4) corresponded to the insertion place of the optic nerve. Similar histologic measures were observed in the human retina. (41) Smaller thicknesses correspond to points 1 and 6, called the ora serrata, increasing gradually in points 2 and 5 (equator) to reach the thickest portion in the macular edge, corresponding to points 3 and 4. The average thickness analyzed in kestrel eyeballs ranged from 19.56 to 394.84 [micro]m, depending on the inspected point. To our knowledge, no references to these measurements in animal species have been published. Also, no data were found comparing the retinal thickness in the right and left eyes. Regarding the comparison of the average thickness in males and females, a significant difference was observed at three points (points 3-5). Females showed a thicker retina than males. In humans, using a retinal thickness analyzer, it also was found that the retina is thicker in women than in men. (42) Nevertheless, using another measurement technique (optical coherence tomography), no significant differences were found between the retinas of men and women. (43)

Although the choroid was numerically thicker in the left eyes and thinner in the right eyes, these differences were not significant. There also was no significant difference between the measurements in males and females. In people, a gradual thinning is described associated with age. (44,45) In this study, the age of the birds was unknown. The scleral thickness showed numerical differences from the right and left eyes and also between males and females, but these differences were not statistically significant.

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Karin Werther, Prof, Dr med Vet, Cinthia Graziela Candioto, DVM, Msc, Rudiger Korbel, Prof, Dr med Vet

From the Veterinary Pathology Department (Werther, Candioto). Faculdade de Ciencias Agrarias e Veterinarias, Univ. Estadual Paulista (UNESP). Via de Acesso Prof. Paulo Donato Castellane, s/n Bairro rural, 14884-900, Jaboticabal, SP. Brazil; and the Clinic for Birds, Reptiles, Amphibians and Pet Fishes (Korbel). Ludwig-Maximilians-Universitat (LMU), Sonnenstrasse 18, D-85764 Oberschleissheim, Munchen, Germany.

Caption: Figure 1. Macroscopic aspects of the right eyeball of a kestrel cut vertically (dorsoventrally) showing the cornea with the 3 points for thickness measure (A-C) and the 6 points at the fundus (1-6) to evaluate the thickness of the retina, choroid, and sclera. Note also the lens (L), pecten (arrow), and insertion of the optic nerve (ON).

Caption: Figure 2. Histologic aspect of the right avian eyeball of a kestrel cute vertically (dorsoventrally) showing the cornea with the 3 points for thickness measure (A-C) and the 6 points at the fundus (1-6) to evaluate the thickness of the retina, choroid, and sclera. Note also the lens (L) and the pecten (arrow).

Caption: Figure 3. Photomicrograph of the cornea (middle point) of a kestrel showing the epithelial, middle, and endothelial layers. (X20 magnification; Hematoxylin and eosin stain. Bar = 50 [micro]m).

Caption: Figure 4. Mean thickness of the cornea at points A to C of right and left eye from male and female kestrels.

Caption: Figure 5. Mean thickness of the cornea at points A to C of the right (RE) and left (LE) eyes in male (M) and female (F) free-living kestrels.

Caption: Figure 6. Mean thickness ([micro]m) of the retina at the 6 points (1-6) of the right (RE) and left (LE) eyes from male (M) and female (F) free-living kestrels.

Caption: Figure 7. Mean choroidal thickness ([micro]m) at the 6 points (1-6) of the right (RE) and left (LE) eyes from male (M) and female (F) free-living kestrels.

Caption: Figure 8. Mean thickness ([micro]m) of sclera at the 6 points (1-6) of the right (RE) and left (LE) eyes for male (M) and female (F) free-living kestrels.

Caption: Figure 9. Average percentage of the thickness of the retina, choroid, and sclera at the 6 points (1-6) of male and female free-living kestrels.
Table 1. Mean values and standard deviation of corneal thickness
([micro]m) at points (A-C) in the epithelial, middle, and endothelial
layers of the right (RE) and left (LE) eyes of male (M) and female
(F) free-living kestrels.

                                             Point A
Layers        Sex
                               Right eye             Left eye

Epithelial    Male         7.7 [+ or -] 2.4      9.0 [+ or -] 3.4
              Female       9.3 [+ or -] 5.6      8.0 [+ or -] 4.1
              Both         8.3 [+ or -] 4.4      8.3 [+ or -] 3.8
              Min-Max          2.3-23.9              2.3-17.3
Middle        Male        164.1 [+ or -] 83.6   172.3 [+ or -] 76.8
              Female      187.6 [+ or -] 79.0   209.9 [+ or -] 77.1
              Both        176.2 [+ or -] 81.5   198.2 [+ or -] 78.5
              Min-Max         54.0-346.5            56.3-350.6
Endothelial   Male         2.6 [+ or -] 2.0      2.9 [+ or -] 1.9
              Female       2.3 [+ or -] 1.9      3.2 [+ or -] 1.9
              Both         2.5 [+ or -] 1.7      3.1 [+ or -] 1.9
              Min-Max           0.5-6.6               0.6-8.4
Total         Male        174.1 [+ or -] 84.0   183.7 [+ or -] 79.2
              Female      199.0 [+ or -] 83.5   220.4 [+ or -] 78.0
              Both        186.9 [+ or -] 84.0   208.5 [+ or -] 79.8
              Min-Max         62.4-373.4            69.4-370.2

                                             Point B
Layers        Sex
                               Right eye             Left eye

Epithelial    Male         9.9 [+ or -] 4.2      9.6 [+ or -] 3.4
              Female       9.3 [+ or -] 3.1      9.0 [+ or -] 3.8
              Both         8.5 [+ or -] 3.8      9.2 [+ or -] 4.2
              Min-Max          1.8-17.2              1.8-28.0
Middle        Male        79.8 [+ or -] 30.5    83.8 [+ or -] 51.0
              Female      108.5 [+ or -] 38.9   126.6 [+ or -] 53.4
              Both        96.0 [+ or -] 38.0    112.2 [+ or -] 56.2
              Min-Max         40.1-188.8            38.3-252.9
Endothelial   Male         2.6 [+ or -] 1.1      2.7 [+ or -] 1.2
              Female       2.6 [+ or -] 1.9      3.8 [+ or -] 2.7
              Both         2.6 [+ or -] 1.6      3.4 [+ or -] 2.4
              Min-Max           0.5-8.0              0.5-11.3
Total         Male        92.0 [+ or -] 33.1    93.3 [+ or -] 53.8
              Female      118.3 [+ or -] 41.5   135.2 [+ or -] 57.4
              Both        106.6 [+ or -] 40.0   122.5 [+ or -] 59.2
              Min-Max         49.2-200.1            47.7-280.1

                                             Point C
Layers        Sex
                               Right eye             Left eye

Epithelial    Male         6.3 [+ or -] 3.0      4.2 [+ or -] 1.5
              Female       5.6 [+ or -] 3.8      7.1 [+ or -] 3.5
              Both         5.9 [+ or -] 3.5      6.5 [+ or -] 3.4
              Min-Max          1.1-16.8              1.0-14.3
Middle        Male        171.5 [+ or -] 62.6   167.9 [+ or -] 62.4
              Female      160.4 [+ or -] 78.8   206.0 [+ or -] 71.6
              Both        165.3 [+ or -] 71.8   197.7 [+ or -] 71.1
              Min-Max         65.1-347.9            64.2-325.3
Endothelial   Male         2.6 [+ or -] 1.9      2.1 [+ or -] 1.1
              Female       2.1 [+ or -] 1.4      2.9 [+ or -] 1.6
              Both         2.3 [+ or -] 1.6      2.7 [+ or -] 1.6
              Min-Max           0.7-9.4               0.7-6.4
Total         Male        167.9 [+ or -] 63.9   180.1 [+ or -] 58.1
              Female      184.2 [+ or -] 82.0   216.6 [+ or -] 72.6
              Both        173.3 [+ or -] 74.3   210.2 [+ or -] 72.4
              Min-Max         85.0-361.0            70.3-352.3

Table 2. Mean values, standard deviation, minimum and maximum values
of retina, choroid and sclera thickness ([micro]m) at points 1 to 6
of the right and left eyeballs in male and female free-living
kestrels.

                                   Retina

Points Sex             Right                  Left

1
 Male           53.7 [+ or -] 24.8     58.1 [+ or -] 19.1
 Female         61.4 [+ or -] 20.3     53.8 [+ or -] 23.8
 Both sexes     57.4 [+ or -] 22.5     55.6 [+ or -] 21.9
 Min-Max            32.5-115.3             26.7-110.8

2
 Male           81.6 [+ or -] 31.5     73.6 [+ or -] 20.2
 Female         87.5 [+ or -] 34.9    115.7 [+ or -] 55.0
 Both sexes     84.7 [+ or -] 33.2     96.4 [+ or -] 47.2
 Min-Max            35.9-169.2             42.5-178.0

3
 Male           101.5 [+ or -] 42.7    68.8 [+ or -] 19.8
 Female         194.9 [+ or -] 72.5   159.8 [+ or -] 105.8
 Both sexes     129.8 [+ or -] 68.1   112.9 [+ or -] 87.0
 Min Max            53.6-313.0             38.5-394.8

4
 Male           107.7 [+ or -] 44.6    65.5 [+ or -] 11.5
 Female         105.3 [+ or -] 82.5   151.0 [+ or -] 51.6
 Both sexes     106.9 [+ or -] 58.9   121.9 [+ or -] 58.8
 Min-Max            37.4-242.3             43.5-263.6

5
 Male           72.2 [+ or -] 31.1     62.6 [+ or -] 27.3
 Female         110.2 [+ or -] 40.8   114.3 [+ or -] 49.9
 Both sexes     99.2 [+ or -] 40.2     96.5 [+ or -] 49.8
 Min-Max            39.2-179.8             37.5-195.3

6
 Male           45.8 [+ or -] 20.4     60.2 [+ or -] 29.6
 Female         69.8 [+ or -] 37.6     73.7 [+ or -] 24.0
 Both sexes     61.1 [+ or -] 32.8     71.1 [+ or -] 25.4
 Min-Max            19.6-123.4             34.6-110.5

                                Choroid

Points Sex            Right                 Left

1
 Male           17.0 [+ or -] 15.9   28.8 [+ or -] 22.1
 Female         24.0 [+ or -] 10.7   20.6 [+ or -] 19.9
 Both sexes     20.3 [+ or -] 13.9   26.2 [+ or -] 23.9
 Min-Max             5.8-71.4             3.5-94.1

2
 Male           14.7 [+ or -] 10.7   20.2 [+ or -] 19.9
 Female         13.8 [+ or -] 4.9    18.9 [+ or -] 10.1
 Both sexes     14.3 [+ or -] 7.1    19.2 [+ or -] 15.1
 Min-Max             3.2-42.5             6.1-75.2

3
 Male           22.2 [+ or -] 13.9   26.1 [+ or -] 23.9
 Female         28.4 [+ or -] 6.0    24.5 [+ or -] 8.5
 Both sexes     24.7 [+ or -] 9.7    25.3 [+ or -] 12.0
 Min Max             8.4-36.6             9.0-53.4

4
 Male           15.5 [+ or -] 6.8    20.2 [+ or -] 9.5
 Female         11.4 [+ or -] 5.8    21.8 [+ or -] 8.7
 Both sexes     14.3 [+ or -] 6.7    21.1 [+ or -] 8.9
 Min-Max             5.5-34.0             6.5-41.1

5
 Male           22.6 [+ or -] 14.8   16.6 [+ or -] 9.7
 Female         21.9 [+ or -] 9.7    17.1 [+ or -] 10.3
 Both sexes     22.3 [+ or -] 9.4    16.9 [+ or -] 9.9
 Min-Max             7.1-61.1             5.4-40.1

6
 Male           19.5 [+ or -] 8.9    21.7 [+ or -] 11.3
 Female         19.1 [+ or -] 5.8    28.0 [+ or -] 24.0
 Both sexes     19.3 [+ or -] 7.2    25.0 [+ or -] 27.6
 Min-Max             5.0-39.5             4.4-90.7

                                 Sclera

Points Sex             Right                 Left

1
 Male           115.4 [+ or -] 19.9   104.2 [+ or -] 19.2
 Female         116.4 [+ or -] 17.3   105.3 [+ or -] 31.3
 Both sexes     115.6 [+ or -] 19.0   104.8 [+ or -] 27.7
 Min-Max            72.3-161.1            63.5-149.2

2
 Male           97.4 [+ or -] 48.7    84.1 [+ or -] 16.7
 Female         79.4 [+ or -] 21.8    75.0 [+ or -] 19.5
 Both sexes     85.8 [+ or -] 38.1    78.9 [+ or -] 23.7
 Min-Max            38.4-185.5            31.7-117.0

3
 Male           115.0 [+ or -] 42.2   99.9 [+ or -] 33.6
 Female         91.5 [+ or -] 28.7    118.4 [+ or -] 75.8
 Both sexes     109.2 [+ or -] 40.0   107.8 [+ or -] 55.3
 Min Max            51.0-190.3            40.9-270.1

4
 Male           77.4 [+ or -] 30.0    68.5 [+ or -] 13.2
 Female         70.2 [+ or -] 30.1    83.3 [+ or -] 33.7
 Both sexes     74.3 [+ or -] 30.0    74.1 [+ or -] 26.4
 Min-Max            45.8-165.1            36.1-150.8

5
 Male           83.3 [+ or -] 11.3    117.7 [+ or -] 28.2
 Female         93.1 [+ or -] 28.8    96.3 [+ or -] 31.6
 Both sexes     88.5 [+ or -] 22.8    101.1 [+ or -] 31.8
 Min-Max            51.3-154.2            38.6-144.6

6
 Male           87.2 [+ or -] 20.3    74.7 [+ or -] 20.6
 Female         104.4 [+ or -] 33.9   82.7 [+ or -] 28.4
 Both sexes     94.1 [+ or -] 27.7    79.7 [+ or -] 25.8
 Min-Max            41.4-146.3            44.2-155.7
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Title Annotation:Original Study
Author:Werther, Karin; Candioto, Cinthia Graziela; Korbel, Rudiger
Publication:Journal of Avian Medicine and Surgery
Date:Dec 1, 2017
Words:5665
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