Zbl. Vet. Med. C. Anat. Hist. Embryol. 5,193-205 @ 1976 Verlag Paul Parey, Berlin und Hamburg ISSN 0044-4294/ASTM-Coden : AHEMA 5

(1976)

Department of Veterinary Anatomy, University of Glasgow Veterinary School, Bearsden, Glasgow

Studies on the Appearance of the Centres of Ossification of the Axial Skeleton in the Feline Foetus BY JOHN

S. BOYD

With 9 figures and 4 tables (Received for publication February 24, 197J)

Introduction I n the literature of the study of osteogenesis of the cat there is comparatively little to be found concerning the foetal stage of development. In all thc earlier works, the findings were from observations made on gross dissection material and light microscopy. STRAUSS-DURCKHEIM (1845) described the centres of ossification for the skeleton as did ST. GEORGEMIVART(1881) whc also revealed a sequence of growth but omitted any precise dates of appearance of the centres. Further contributions on the patterns of ossification were presented by LESBRE (1897) and JAYNE (1898) gave a comprehensive description of the centres of ossification of the complete post natal feline skeleton. Later researchers SCHAEFFER (1932) and DREWS (1933) using alizarin red staining were able to ascribe dates for times of appearance of the centres of ossification in the appendicular skeleton and skull of the feline foetus. Radiographic studies have been used to provide a description of the development of the manus and pes in the cat at birth (BRESSOU et al., 1959) and the appearance of the adult cat skull (HARE,1959). The most recent radiographic work of SMITH(1968, 1969) gave the progressive development of the appendicular skeleton of the kitten from birth, both as individual bones and as part of the skeleton as a whole. A similar description of the centres for the foetal appendicular skeleton has been described by BOYD(1968) but there has been no such description of the radiographic appearance of the axial skeleton, until the thesis of BOYD(1974). The history of the use of alizarin red S has been well narrated by NOBACK/NOBACK (1944) and that of radiographic studies by O’RAHILLY/ MEYER(1956). The latter authors criticised the lack of contrast to be found in radiographic studies. However, impregnation with heavy metal salts as described by HODGES (1953) has improved the contrast by enhancing the radiopacity of the foetal skeleton. This was produced by a partial replacement of calcium by silver. Although it was known that silver nitrate is not strictly Zbl. Vet. Med.. Reihe C. Rd. 5 . Heft 3

14

194

JOHN

S. BOYD

specific for calcium (CAMERON, 1930), O’RAHILLY/MEYER (1956) justified the use of this technique in their work on human foetuses by showing that soft tissue impregnation did not interfere with the detection of the skeleton. They further found that, in foetal material, the most critical method of detecting osseous tissue was histological but that the difference in time of detection using alizarin staining and silver impregnation with radiography was not great. In a later report MEYER/~’RAHILLY (1958) observed that when an initial positive response was obtained with alizarin red S or silver nitrate this coincided fairly closely with the formation of the periosteal collar. They observed that silver nitrate was deposited not only in the circumferential osseous areas but also in the calcified cartilage in the centre of the shaft. The deposition of alizarin red S appears to be similar in nature, according to the description of ZAWISCH (1956).

Materials and Methods The foetuses were from 90 litters and the total number of individuals was 288. The foetuses were mainly obtained from the uteri of fresh cadavers while others arrived at the department in either 10 O/o formalin or 75 O/a alcohol. Others, yet again, were obtained by caesarian section from pregnant cats which had unknown mating dates. The foetuses were measured for crown-rump length. Average crown-rump (c. r.) measurements for each litter and the assessed ages (i. e. time since mating) are shown in Table 1. Any individual which was obviously malformed or grossly smaller than its litter mates was discarded. The measurements of crown-rump compared to time since mating, given by FARRIS(1950) are used in this study to give a n approximate age to the foetuses under investigation.

Table 1 Correlation of crown-rump length measurement to estimated day of gestation

The foetuses of each litter were radiographed in both lateral and dorso-ventral positions. I n order to increase the radiopacity of the developing centres, 5 1 foetuses from 42 litters were impregnated with an aqueous solution of silver nitrate as described by HODGES (1953). After radiographing the entire foetus, the heads were removed and radiographed separately in lateral and dorso-ventral positions. The heads were then either sectioned in the median plane and the t w o halves radiographed or had the mandible and dome of the cranium removed to allow clearer dorso-ventral images to be obtained. If the number of foetuses in a litter allowed, both these sections were carried out in representatives from each litter. Where numbers permitted, a foetus from each litter which was received in the fresh state was stained by the alizarin red S technique (HOOD/NEIL, 1948) and examined under a dissection microscope. The specimens were photographed either directly or through the microscope depending on the size of the structure examined. The staining technique was that described by HOOD/NEIL (1948).

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195

MEYER/O’RAHILLY (1958) state that the first positive reaction with the alizarin method and the first signs of appearance of increased opacity on radiographs coincide fairly closely with the laying down of the periosteal collar which is detected histologically. Therefore these methods do not demonstrate the onset of true endochondral ossification, i. e. rhe appearance of a centre of ossification which is said to be constituted only when the osteogenic cells, osteoblasts and capillaries invading from the periosteal collar reach the interior of the midsection of the cartilage model (HAM,1965). To clarify this point and to enable establishment of the time difference between the first positive reaction with the alizarin red method, the silver nitrate impregnation method and the true onset of a centre of ossification, foetuses from 35 litters were examined histologi(1972) emphasiscally after decalcification and staining with H. and E. O’RAHILLY/GARDNER ed the need for histological examination in such studies and stated that as a method it was superior to alizarin and radiographic examination. Where the number of foetuses per litter allowed, the sections were made in three planes, i. e. transverse, frontal and saggital. Histological examination helped to determine the type of ossification and the time of onset of that process, except in the skull where only the type of ossification was observed due to insufficient suitable specimens being available for judging the time of onset by histological

Table 2 List of centers noted and their times of appearance with corresponding C. R. Lengths R Radiography of foetus, S Silver nitrate impregnated radiography, A Alizarin red staining of foetus, H Histology Table 2, contd. AXiAL SKELETON

Centre

Vertebrae Cervicales 111 V I I

C. R. Method length

mm,

Centrurn

R

L9

OaY Of gestation

36

-

Laminae

Atlas

j

Laminae

AXIAL SKELETON Vertebrae Sacrales

;;

Centrurn

Method

mm, length

Day gestation Of

R

h9 t o 66

36 to LO

Laminae

L9

1 ;1 I

C. R. Centre

66

35

q;

Ventral body

130 121

58 56 52

58 L3 55

38 3.5 36

73 67 66

LO LO

S

108

Post-partum 53

A H

8L

LL

R

38 to 39

s

35 35

35

I

: 63

Lh

Ventral body (Arch)

I ;I 1 R

105

;;1

H

35 : 39 51 51 L7

Vertebrae Caudales ICoccygeael

Centrurn

s A H

H Axis

Laminae

Centrum

R

L9

36

s

L3

A H

39 LL : 63

3L 33 35 : 39

R 5 A H

L9 56

39 LL : 63

Laminae

A H

0s Arcus Haemalis

36 37 33 35 : 39

BL 8L

82

LL LL 1.3

Costae

A

R

L9

36

Sternum

S

L3 t o 56 35 to 39 LL : 63

3L to 37 31 to 33 35 : 39

Corpus

Centrum

A H

ilertebrae

Laminae

R 5 A H

L9 56 39

36 37 33

4L : 63

35 : 39

Centrurn

R

L9

36

5

L3 to 56

3 L to 37

A H

39 LL : 63

35 : 39

R

69 56

36 37

-urnbales

Laminae

5

L3

A

H

LL

: 63

R

Corpus

11

H

35 : 38

33 to 36 31 31 31 : 33

R

58 to 66 56 to 66 L9 to 66 LL : 63

38 to LO 37 to LO 36 to LO 35 : 39

A

n Vertebrae Thoracicae

R

S

s

R

Rostra\ body (Dens)

R

S A H

33

31

35 : 39 14‘

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JOHN

S. BOYD

methods. Thus in this study a positive reaction with either the alizarin red technique or first sign of opacity on a radiograph either with or without silver impregnation, is taken t o represent the onset of ossification, the nature of the type of ossification, where possible, having been observed on histological section. The development of the feline skull has been described using alizarin red staining (DREWS, 1933) but his number of litters used was limited t o 25. The number of litters studied in this work is 90 of whim 60 were stained with alizarin red.

Results concerning the vertebrae column, ribs and starnum The lists of centres from which the vertebrae developed is given in Table 2. The time during gestation for each centre to make its appearance is given for each technique used. In the case of appearance on histological section both the times of appearance of primary calcification and a true centre of ossification are given. The cervical vertebrae in general were seen to develop from three principal centres, with the atlas and axis presenting extraordinary features. The mode of ossification was endochondral in type. The three centres were two for the laminae and one for the centrum. The axis was formed from the three principal centres but there also appeared immediately cranial to the centrum a further rounded centre which became more relative to the centrum of the second vertebrae as gestation progressed. This centre was for the dens but remained separate from the centrum of the second vertebra a t birth (Fig. .I). The atlas developed from two centres for the laminae which were flrst to appear of all the laminae of the cervical vertebrae and they were followed

B

Fig. 1. Ventro-dorsal view of an alizarin red stained specimen of the cranial cervical region of the developping foetal vertebral column. C. R. 130 mm, assessed age 58 days. A Lamina of atlas, B Transverse bar-like centre of atlas, C Lamina of axis, D Centre for corpus of axis, E Centre for corpus of 3rd cervical vertebra, F Centre for dens

Fig. 2. Ventro-dorsal view of an alizarin red stained specimen of the sacral region of the developing foetal vertebral column. C. R. 130 mm., assessed age 58 days. A Ilium, B Ischium, C Pubis, D Lamina of sacral vertebrae 1, E Corpus of sacral vertebra 1, F Centre on lateral mass

I

II 1

*i

Ib

Studies on the Appearance of the Centres of Ossification of the Axial Skeleton

197

by the development of a third, more ventrally placed, transverse bar like centre (Fig. 1). The thoracic, lumbar and sacral vertebrae all developed in foetal life from the three basic centres of ossification, again by endochondral ossification. The centra made their appearance before the laminae in these regions and the thoracic elements were in advance of both the cervical and lumbar regions. The elements for the sacral and coccygeal vertebrae (vertebrae caudales) were later t o develop (Table 2). The sacral vertebrae appeared to develop in general from three principal centres but in addition there appeared to be other additional paired centres developing in the transverse masses of the sacral elements (Fig. 2 and 3). The centres in the lateral masses were a constant feature of only the first sacral vertebra but other individuals did have them at the second and even the third sacral vertebra. The coccygeal vertebrae differed in their foetal development from the other vertebrae as the more caudal of the group developed from only one centre of ossification, that being for the centrum. The cranial three coccygeal vertebrae developed from three centres, i. e. one for the centrum and two for the laminae. The succeeding five vertebrae produced from the centrum dorsal projections of varying degree which remained attached to the centrum. The most caudal of the group remained cartilaginous at birth. There appeared also in the coccygeal region two small centres ventral to the centre of some of the vertebrae and these were taken as indications of development of the chevron bones or ossa arcus haemalis (Figs. 2 and 3). The list of centres from which the costae and sternum developed is given in Table 2 . There would seem t o be only a diaphyseal centre present for each rib in foetal life but that ossifies early, even before the vertebrae. The mode of ossification for both the ribs and sternum was endochondral. I n the foetuses examined which had ribs in evidence, there were found to be some anomalies in the number of ribs. This was observed in four litters and affected nine individuals. The incidence of these supernumerary ribs in littermates is also of note. The variations in rib numbers are listed in Table 3 which gives details of concomitant anomalies in the vertebral column and sternum. Each sternal segment appeared to be from a single separate centre. The common number of sternal segments was eight but variations did occur and are recorded in Table 3. Table 3 Numbers of individuals variations in body elements of thorax and vertebral column Estimated Litter

Individuals

Number of ribs

a b

1L : 1L 13 : 13

a b

13 : 12 13 : 12

a b

1L : 1L 1L : 1L

C

1L : 1L

a b

1L : 1L 1L : 1L

[days)

54

59

57

65

70

I

61

Number of cervical vertebrae

Number of thoracic vertebrae 13 13

13 I

13

7

13

I

13 13 1L 1L

1 Number of lumbar vertebrae

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JOHN

S. BOYD

Discussion of vertebrae column, ribs and starnum The view that the basic vertebra is formed from three principal centres (ST. GEORGE MIVART,1881; STRAUSS-DURCKHEIM, 1845; LESBRE,1897 and JAYNE,1898) would appear to be in agreement with these findings but in: foetal development only four centres were detected for the axis and three for the atlas. The odontoid process would seem to derive from one main centre which is in line with LESBRE’S (1897) description. There was no evidence of the two centres described by STRAUSS-DURCKHEIM (1845), and ST. GEORGE MIVART’S(1881) and JAYNE’S(1898) description of two principal centres placed side b y side, was not substantiated by these findings. There is, however, agreement with the listed authors as to the development of the atlas from three centres. STRAUSS-DURCKHEIM (1845) mentions the first sacral vertebra as being original in that it has an additional centre on each transverse mass, as was found in this work, whilst the presence of the small centres ventral to some of the coccygeal vertebrae is as described by CROUCH (1969), the chevron bones, and FREWEIN (1970), the ossa arcus haemalis. The finding that the sternebrae appear to be developed from single centres of ossification concurs with the views of both STRAUSS-DURCKHEIM (1845) and JAYNE (1898) but the latter author qualifies this by narrating that there are grounds for believing that these centres are derived from paired primary centres. The significance of the finding of variations in the number of ribs and sternebrae is discussed by LINDSAY/BOYD (1968) where it is also noted that the anomalies are seen to occur in littermates in both foetal and post-natal life.

c Fig. 3. Lateral view of an alizarin red stained specimen of the sacral region of the developing foetal vertebral column. C . R. 130 mm., assessed age 58 days, A Ilium, B Ischium, C Pubis, D Lamina of the 7th lumbar vertebra, E Vertebrae caudales with ossa arcus haemalis evident related to centra, F Centre on lateral mass

Results concerning the skull The skull has been divided for convenience of description into (A) Ossa faciei including mandible and (B) Ossa cranii. The relevant literature for each bone of the skull is given in its corresponding section. A list of centres of ossification of the skull with times of first appearance using radiography, radiography with silver nitrate impregnation and alizarin red staining is given in TDhlP 4

Studies on the Appearance of the Centres of Ossification of the Axial Skeleton

195

Table 4 List of centers noted and their times appearance with corresponding C . R. Lengths R Radiography of foetus, S Silver nitrate impregnated radiography, A Alizarin red staining of foetus Table 4, contd. OSSA F A C E Maxilla

Centre

Method

C. R. length

mm,

C. R. Day Of gestation

Centre

OSSA CRANll

05

Centre Corpus

0.5

Centre

lncisivum A

28

38 29 26

33 30

Ala

0s pterygoideum

0s

Centre

Mandibula

Centre A

29 26

30

35 29 25

31 30 28

Pars Tympanica

Pars Petrosa

OSSA CRANll DS

0s Ternporale Pars Squanwsa

Basioccipital

Occipitale

l : l :: I :,"I

1-1

Centre

1 l*l j

33 R

s

L9

13

31 31

R

L9

5

L3

37

36 3L

8L tQ 9L LL to L8 0s Parietale

Centre

R S A

58 56 35

38 37 31

0s Frontale

Centre

R S A

38 31 25

33 30 28

R

85

s

8L 35

15 L3 31

s

L9 13

36 3L

S A

31 35

30 31

0s Lacrimale

Centre

36 3L

A

0s Nasale

3s

56 35 35

LO

4 Centres

Supraoccipital

Centre

A

R

51 LL

Ectotympanic

Exoccipital

0s lnterparietale

39 38

s Centre

Of

gestation

66 63 58

R

A

05

Day

L3

S

28

length

mm.

105 8L 82

A

Palatinum

Zygomaticum

R

s

Praesphenoidale

25

Method

Centre

R

3asisphenoidale

66 Ala

36 35

Maxilla: Histologically, the centres for the maxilla were seen to develop in membrane. There appeared to be two prinicpal centres, one for the maxilla of each side. O n each side the foramen infrarobitale was developing a t the beginning of the 31-40 day phase to become enclosed by 35 days (C.R. 44.2mm.) and the maxillary sinus was becoming evident as a cavity in the centre by 43 days (C. R. 82.5 mm.) (Fig. 4). The presence of the primordia of the teeth became evident in the 5 1-60 day period (Fig. 7). 0 s incisivum: Histologically, the 0 s incisivum developed in membrane. The development was from two centres, one for the bone of each side, placed rostrally and to each side of midline. The proccessus palatinus of each side was seen developing in the later part of the 31-40 day period as was the processus nasalis. The primordia of the incisor teeth were not in evidence till after 60 days (C. R. 138 mm.) but the arcus alveolaris was seen developing in the 51 to 60 day period (Fig. 7). 0 s palatinum: Histologically it was seen that the palatine centres of ossification were developed from membrane. The development of the palatine canals was seen commencing in the first part of the 51-60 day period (Fig. 7 and 8) and the foramen sphenopalatinum was seen developing at the beginn-

200

JOHN

S. BOYD

Fig. 4. Dorsal view of an alizarin stained skull of a foetus, C. R. 95 mm., estimated age 48 days. A Maxilla, B Infraorbital foramen, C Developing maxillary sinus, D and E Initial centres for praesphenoid, F. Centre for 0 s nasale, G Foramen rotundum and foramen ovale on alae of basisphenoid, H Body of basisphenoid Fig. 5. Dorsal view of an alizarin stained skull of a foetus, C. R. 95 mm, estimated age 48 days. A Precursor of condylus occipitalis of exoccipital centre, B Centres formed from cartilage. 0 s temporale, C Centre for vomer, D Canales optici of praesphenoid, E Body of basisphenoid, F Foramen rotundum and foramen ovale on alae of basisphenoid

C

F

Fig. 6 . Dorsal view of the mandible stained with alizarin from a foetus, C. R. 95 mm., estimated age 48 days. A Primordia of tooth in alveolus, B Canalis mandibulae, C Processus condylaris, D Processus coronoideus, E Processus angularis Fig. 7. Ventral view of an alizarin stained skull of a foetus, C. R. 125 mm., estimated age 57 days. A Primordia of teeth in developing maxilla, B Arcus alveolus in 0s incisivum, C Developing palatine canal, D 0 s pterygoideum, E Petrous section of temporal bone, F Promontory of the uvramid with round window. 0 s temuorale

Studies on the Appearance of the Centres of Ossification of the Axial Skeleton

201

ing of the 45-50 day period but remained incomplete throughout gestation (Fig.. 8). 0 s zygomaticum: Histologically, the 0 s zygomaticum was seen to develop from membrane and there were two primary centres, one for the bone of each side. The primordium of the processus frontalis became evident during the 41-50 day period (Fig. 9). Mandibula: Histologically, the mandible was seen to develop in membrane by the laying down of ossified tissue around a cartilaginous precursor. The corpora of the mandibulae were the first to develop but the rami were appearing in the second phase of the 31-40 day period. The alveoli dentales were forming in this period also by the growth of a separate medial wall but the primordia of the teeth were not in evidence till after 40 days (C. R. 66 mm.), (Fig. 6). In fact those of the incisors did not appear till after 60 days (C. R. 136 mm.). The canalis mandibulae was seen developing during the 41-50 day phase (Fig.6) and was converted to an enclosed canal by the second half of the 51-60 day period with the formation of the foramen mandibulae. The differentiation of the precursors of the processus coronoideus, condylaris and angularis was becoming, noticeable at the end of the 31-40 day period (Fig. 6). 0 s occipitale: The histological findings indicated that the original centres for this bone developed in cartilage. There were four centres, one each for the basi- and supraoccipital and two for the paired exoccipitals (Fig. 8 and 9). The precursor of each condylus occipitalis was becoming evident by the second half of the 41-50 period being seen as a thickening of the exoccipita1 centres (Fig. 5). \

"

I

G

Fig. 8. Dorso-oblique view of an alizarin stained skull of a foetus, C. R. 125 mm., estimated age 57 days. A Foramen sphenopalatinum, B Supraoccipital centre, C Basi-occipital centre, D Optic foramen, E Petrous section of 0 s temporale Fig. 9. Lateral view of an alizarin stained skull of a foetus, C. R. 127 mm., estimated age 57 days. A Processus frontalis, 0 s zygomaticum, B Supra-occipital centre, C Exoccipital centre, D Petrous section, 0 s temporale, E Processus tentoricus, 0 s parietale, F Supra-orbital process of 0 s frontale of opposite side

202

JOHN

S. BOYD

0 s interparietale: Histologically, the interparietal bone was seen to be preceded by cartilage which later ossified. The first evidence of bone was the appearance of two centres stained with alizarin red in foetus of 33 days (C. R. 39 mm.) followed by signs of union of the centres by 35 days (C. R. 44.2 mm.) (Fig. 8). 0 s sphenoidale: Histologically, the development of the 0s sphenoidale was seen t o be by ossification of existing cartilage. There were two main areas of development i. e., the area for the praesphenoid and that for the basisphenoid. The former involved four separate centres, developing as two placed apart to either side of midline initially, followed by two further centres placed a t midline and between the two initial centres (Fig. 4). The two centres at midline united almost immediately forming a single structure (Fig. 5). Thus from this point, the development was from three regions of ossifiction, the single midline structure, and two more laterally placed centres. The merging of the lateral centres with the midline structures resulted in the formation of the canales optici, this occurring in the middle of the 41-50 day period (Fig. 5 and 8). The second main area for the development was formed of two laterally placed centres for the alae of the basisphenoid which were placed one to either side of midline and a centre for the body of the basisphenoid. There were seen developing in the alae two foramina for each side, being seen as early as the end of the 31-40 day period (Fig. 4 and 5). They were the foramen rotundum and ovale. 0 s pterygoideum: The histological picture was of ossification from a cartilaginous precursor, there being two centres, one for the bone of each side. It was found that in the feline the centres for the pterygoids closed with the alae of the basisphenodis around the end of the gestation period and remained separated from the palatine by a fine sutural line, producing a developmental situation individual to the feline (Fig. 7). 0 s tempovale: The nature of the development of the centres for this bone was both endochondral and intramembranous when viewed histologically. A single centre each for the squamous part of the temporal bone, the ectotympanic ring and the malleus appeared to develop in membrane appearing earlier than the other temporal centres. The centres formed from cartilage were involved in the development of the petrous portion of the bone. There were 4 such centres for each temporal bone, appearing first in alizarin stained specimens a t between 44 and 48 days (C. R. 84 and 94 mm.) (Fig. 5). The most ventrally placed centre continued to develop to produce the promontory of the pyramid with the round window in evidence, the centres above it becoming confluent to form the petrous section of the temporal bone. The internal acoustic meatus was seen on the dorsal surface at 57 days (C. R. 125 mm.) (Fig!. 7-9). The gap between the squamous and tympanic centres and the exoccipital centres was still evident a t birth (Fig. 9). No development of the processus mastoideus of the pars petrosa was observed during foetal development. Auditory ossicles: No detailed study was made of the auditory ossicles during this investigation. 0 s parietale: Histologically, the centres were seen to develop from membrane. T h e development was from two primary centres, one for each side. The development of the processus tentoricus was seen in the alizarin stained foetus in the 41-50 day period (Fig. 9). 0 s frontale: Histologically, the ossa frontalia were seen to develop in membrane, several days in advance of the appearance of the parietal centres.

Studies on the Appearance of the Centres of Ossification of the Axial Skeleton

203

There were two centres, one for each side. The supraorbital process became evident in the latter part of the 51 to 60 day period (Fig. 9). 0 s ethmoidale: EWER(1973) describes the skull of Canoidea as having turbinals comprising a single maxillary, a nasal and a primary series of ethmoturbinals, the latter differentiating originally form the median nasal septum. These are sometimes collectively referred to as endoturbinals. They are supplemented by later developing outgrowths from the side walls of the nasal passages, forming an ectoturbinal series. In a foetus from a litter obtained at birth, there was evidence of alizarin red staining of the primary series of the endoturbinalia. Ossu turbinaliu: In a foetus from a litter obtained at birth, there was evidence of alizarin red staining of the ventral conchae (maxillary or ventral turbinalia). This is similar to the findings of DREWS (1933). 0 s lacrimale: The centre developed from membrane as was observed histologically, there being one centre for each side. 0 s nasale: Histologically, the centres were seen to develop in membrane. There were two primary centres, one for the bone of each side (Figs. 4 and 5). Vomer: Histologically, the vomer developed from membrane being constructed alongside the more caudo-ventral part of the cartilage of the nasal capsule which lay in midline. The alizarin red stained specimens demonstrated a centre which appeared to have two wings unified at midline (Fig. 5). There was no histological or alizarin stained evidence of pairing of the centres. 0 s hyoideum: No ' detailed study was made of the hyoid apparatus during this investigation.

Discussion of the skull The description of the numbers of centres for the development of the skull corresponds closely with the work of DREW(1933) except in the case of the origins of the vomer. DREWS describes two centres for the vomer whilst the evidence found in this series was for a single centre with paired wing-like development. The finding that the centres for the pterygoids close with the alae of the basisphenoids around the termination of gestation and remain separated from the palatine centres by a fine sutural line is contrary to the report of DREWS (9133) who describes the centres as completely merging with their neighbouring bones during the intrauterine life of the cat. However the unification with the basisphenoid would justify the illustration of a kitten skull by CROUCH (1969) which demonstrates the pterygoid as just a process of the alisphenoid (ala of the basisphenoid). It is hoped that the record of the different centres of ossification of the bones of the skull and their approximate times of appearance may serve as a guide to assessing the maturity and normal progression of development of foetal kittens.

Summary Ossification of the vertebral column, ribs, sternum and skull of the foetuses of cats was studied radiographically. All individuals from 90 litters were radiographed both fresh and after impregnation with silver nitrate. Others were subjected to histologically examination and alizarin red staining. The ages of the litters were estimated using crown-rump length. The range of ages was from day 24 after mating to day 63. The times of observation of the first appearance of the centres of ossification were noted using various techniaues and both these times and all the

204

JOHN

S. BOYD

centres for the axial skeleton appearing during foetal life were tabulated. A survey of the relevant literature is also given. Zusammenf assung Studien uber das Erscheinen von Verknocherungszentren im Ahsenskelett von Katzenfeten Die Verknocherung von Wirbelsaule, Rippen, Brustbein und Schadel bei Katzenfeten wurde radiographisch untersucht. Alle Einzeltiere von 90 Wurfen wurden sowohl frisch als auch nach Impregnierung mit Silbernitrat gerontgt. Einige wurden auch histologisch untersucht und mit Alizarin-Rot gefarbt. Das Alter der Tiere wurde auf Grund der Scheitel-Steii3lange geschatzt. Die Altersspanne reichte vom 24. bis 63. Tag nach der Kopulation. Die Zeiten, an denen das Auftreten der Verknocherungszentren zum erstenmal beobachtet wurde, konnten mittels verschiedener Techniken festgestellt werden. Diese Zeiten und alle Zentren fur die axiale Skelettbildung, die wahrend der fetalen Periode auftreten, wurden tabellarisch erfai3t. Ein Uberblick uber die relevante Literatur wird vermittelt.

Resume Etudes sur I’apparition des centres d’ossification dans le squelette axial de foetus de Chat L’ossification de la colonne vertkbrale, des cbtes, du sternum et du crine a ktk ktudike A la radiographie sur des foetus de Chat. La totalitk des sujets de 90 portkes ont ktk radiographiquikes A la fois 2i l’ktat frais et aprks imprkgnation au nitrate d’argent. Quelques spkcimes furent aussi soumis A examen histologique a p r b traitement au Rouge d’alizarine . L’Sge des portkes a ktk dktermink d’aprh la longueur vertex-coccyx; les tranches d’Sge s’ktendaient du 24e au 63e jour aprks la copulation. A l’aide de diffkrentes techniques, on a relevk les dates d’apparition des centres d’ossification. La chronologie des tous les noyaux d’ossification du squelette axial a kttk ktablie pour toute la durke de la vie foetale. Un a p e r p bibliographique sur le sujet est kgalement donnk.

Resumen Estudio sobre la aparici6n de centros de osificacihn en el esqueleto axial de fetos del gat0 La osificaci6n de la columna vertebral, de las costillas, del estern6n y del crineo se estudi6 radiogrificamente en fetos del gato. Todos 10s animales individuales de 90 partos se sometieron a la radiografia, tanto en estado fresco como despuks de su impregnaci6n con nitrato de plata. Algunos se examinaron tambikn histoMgicamente, colorindose con rojo de alizarina. La edad de 10s animales se calcul6 s e d n su tamaiio ipico-caudal, correspondiento a un margen entre 10s 24 y 63 dias despuks de la copulaci6n. La kpoca de la aparici6n de 10s centros de osificaci6n se determin6 mediante diferentes tecnicas y tanto la fecha exacta como les nLcleos para el desarrollo del esqueleto axial durante el period0 fetal, se anotaran sin6pticamente en una tabla. Ademas, se revisa la bibliograffa correspondiente.

Studies on the Appearance of the Centres of Ossification of the Axial Skeleton

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References BOYD,J. S., 1968 : Radiographic appearance of the centres of ossification of the limb bones in the feline foetus. Br. vet. J., 124, 365-370. BOYD,J. S., 1974: Ph. D. Thesis. Patterns of Ossification in the Feline Foetus. Univ. of Glasgow. BRESSOU,C., N. A. POMRIASKINSKY-KOBOZIEFF et N. KOBOZIEFF, 1959: Etude radiologique de l’ossification du squelette de la main du chat. Rec. Med. Vet., 131, 547-563, 611. CAMERON, G., 1930: The staining of calcium. J. Path. and Bact. 33, 929-55. CROUCH,J. E., 1969: Text-Atlas of Cat Anatomy. Lea and Febiger, Philadelphia. DREWS,M., 1933: Uber Ossifikationsvorgange an Katzen und Hundeschadel. Morph. Jb., 73. 185-237. EWER,R. F., 1973: The Carnivores. Weidenfield and Nicolson, London. FARRIS,E. 1.. 1950: The Care and Breeding of Laboratorv Animals. New York: Wilev. FREWEIN,$,.1970: Die Haemapophysen & den Schwanzwirbeln von Katze, Hund ;nd Rind. Zbl. Vet. Med., A, 17, 565-572. HAM, A. W.. 1965: Histolow. Philadeluhia: T. B. Liouencott. HARE,W. C. D., 1959: Gdiographi; anatomy of’the feline skull. J. A. V. M. A., 134, 349-356. HODGES, P. C., 1953: Ossification in the foetal pig. Anat. Rec. 116, 315-325. HOOD, R. C., and W. NEIL, 1948: A modification of alizarin red S technic for demonstrating bone formation. Stain Tech., 23, 209-218. JAYNE, H., 1898: Mammalian Anatomy. Vol. I. J. B. Lippincott, Philadelphia. LESBRE,F.-X., 1897: Contribution A I’ktude de l’ossification du squelette des mammiferis domestiques. Annales de la SociCtC d’Agriculture. Sciences et Industrie de Lyon, SCries VII, V O ~V, . 1-106. LINDSAY,F. E. F., and J. S. BOYD,1968: Variations in number of ribs in the domestic cat. Vet. Rec. 82, 471. MEXER,D. B., and R. O’RAHILLY,1958: Multiple tedmiques in the study of the onset of prenatal ossification. Anat. Rec. 132, 181-193. MIVART,ST. GEORGE,1881: The Cat: An Introduction to the Study of Back-Boned Animals, especially Mammals. Chas. Scribner & Sons. New York. NOBACK, C. R., and E. NOBACK, 1944: Demonstrating the Osseous Skeleton of Human Embryos and Fetuses. Stain Tecfi., 19, 51-54. O’RAHILLY,R., and E. GARDNER, 1972: The initial appearance of ossification in staged human embryos. Amer. J. Anat., 34, 291-307. O’RAHILLY,R., and D. B. MEYER, 1956: Roetgenographic investigation of the human skeleton during early foetal life. Amer. J. of Roentgenology. 76, No. 3, 455-458. SCHAFER,H., 1932: Die Ossifikationsvorgange im Gliedmanenskelett der Hauskatze. Morph. Jb. 70, 548-600. SMITH,R. N., 1968: Appearance of ossification centres in the kitten. J. small Anim. Pract., 9, 497-51 1. SMITH, R. N., 1969: Fusion of ossification centres in the cat. J. small Anim. Pract. 10, 523-530. STRAUSS-DURCKHEIM, H., 1845 : Anatomie DCscriptive et Comparative du Chat. Chez PAuteur, 4, Rue Copeau. Paris. ZAWISCH,C., 1956: Minverhaltnis zwischen den am aufgehellten Ganzembryo und den aus histologisch-embryologischen Schnittserien gewonnenen Ossifikationsdaten. Anat. Anz., 102, 305-316. Author’s address: JOHN S. BOYD, B. V. M. S., M. R. C. V. S., Veterinary School and Hospital, University of Glasgow, Great Britain.

Studies on the appearance of the centres of ossification of the axial skeleton in the feline foetus.

Zbl. Vet. Med. C. Anat. Hist. Embryol. 5,193-205 @ 1976 Verlag Paul Parey, Berlin und Hamburg ISSN 0044-4294/ASTM-Coden : AHEMA 5 (1976) Department...
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