Paper - The sternum - its early development and ossification in man and mammals

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Paterson The sternum - its early development and ossification in man and mammals. (1900) J Anat Physiol. 35(1): 21-32 PMID 17232454

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This historic 1900 paper by Paterson is an early description of the development of the sternum.


See also: Paterson AM. Development of the Sternum and Shoulder Girdle in Mammals (1902) Brit. Med. J. 2:777

Whitehead RH. and Waddell JA. The early development of the mammalian sternum (1911) Amer. J Anat. 12: 89-106.

Modern Notes: sternum | bone | bone timeline | Axial Skeleton Development

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1853 Bone | 1885 Sphenoid | 1902 - Pubo-femoral Region | Spinal Column and Back | Body Segmentation | Cranium | Body Wall, Ribs, and Sternum | Limbs | 1901 - Limbs | 1902 - Arm Development | 1906 Human Embryo Ossification | 1906 Lower limb Nerves and Muscle | 1907 - Muscular System | Skeleton and Limbs | 1908 Vertebra | 1908 Cervical Vertebra | 1909 Mandible | 1910 - Skeleton and Connective Tissues | Muscular System | Coelom and Diaphragm | 1913 Clavicle | 1920 Clavicle | 1921 - External body form | Connective tissues and skeletal | Muscular | Diaphragm | 1929 Rat Somite | 1932 Pelvis | 1940 Synovial Joints | 1943 Human Embryonic, Fetal and Circumnatal Skeleton | 1947 Joints | 1949 Cartilage and Bone | 1957 Chondrification Hands and Feet | 1968 Knee
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Pages where the terms "Historic Textbook" and "Historic Embryology" appear on this site, and sections within pages where this disclaimer appears, indicate that the content and scientific understanding are specific to the time of publication. This means that while some scientific descriptions are still accurate, the terminology and interpretation of the developmental mechanisms reflect the understanding at the time of original publication and those of the preceding periods, these terms and interpretations may not reflect our current scientific understanding.     (More? Embryology History | Historic Embryology Papers)

The Sternum - Its Early Development and Ossification in Man and Mammals

By Professor Paterson (1900)

Liverpool. (PLATES II., III.)

(Preliminary Communication).

  • Read at the Manchester meeting of the Anatomical Society of Great Britain and Ireland,1900.


In the following pages the record is given of some recent observations upon the early development and ossification of the sternum in man and certain mammals (chiefly rodents). The morphological problems associated with the anatomy and development of this bone are so numerous and important, that it has seemed desirable to make, in the first place, a brief statement of certain facts of development, so as to clear the way for future discussion and consideration of the more general anatomical questions in which the sternum is implicated.

I. Early Development

The following observations upon the early development of the sternum were made on rat and human embryos.

(a) In a series of continuous sagittal sections through a human embryo in the second month, prepared and placed at my disposal by Professor Paul, the first anlage of the sternum (fig. 1) is to be seen as a dense conglomeration of mesoblastic cells, occupying the anterior part of the thoracic wall in the middle line, and tapering off posteriorly: disappearing as a separate structure about the middle in length of the thoracic wall.


There is no indication of any bilateral arrangement of this cellular tissue. The inner end of the clavicle and the costal cartilages are composed of cartilage. The first three costal cartilages join the cellular median sternum; the fourth and fifth A cartilages join those above them; the sixth and seventh have free pointed ends.


In rat embryos of 9 mm. in length, a very similar condition is found (figs. 2, 3. 4). In the angle between the jaw and the thoracic wall (praecervical sinus) there is a conglomeration in the middle line of mesoblastic cellular tissue; traceable laterally into association with the shoulder girdle, and concerned with the formation of the clavicles; thinning off as it passes backwards in the thoracic wall on the ventral aspect of the bulging heart.


At this stage this cellular mass is not connected with any of the costal cartilages, which are extending in a ventral direction, and ending distally in tapering points (fig. 4). There is, moreover, no indication of bilateral subdivision of the mass, except at its cephalic end; there the cells are consolidated into two horns, which are concerned with the formation of the -clavicles and sterno-clavicular articulations, and with the anterior parts of the pre-sternum.

(b) In rat embryos, 10 mm in length, an advance in development has occurred (figs. 5-8). The sternum is still cellular. The pre-sternum is single and median (fig. 9), and at its cephalic end the component cells are more distinctly massed together on each side to produce the sterno-clavicular joints, and the inner ends of the clavicles. The cellular meso-sternum (figs. 10-12) consists of two definitely separate strands of mesoblastic cells, which are separated in the middle line by a layer of sparser and more loosely arranged cells. The cellular sternum is now joined by the first six costal cartilages (the seventh is still separate on each side), but there is an obvious distinction in the character of the cells composing sternum and costal cartilages (figs. 11, 12). The eighth costal cartilages are not in any way related to the sternum, and there is no indication of a meta-sternum.


In rat embryos, 13 mm in length, the process of development has perceptibly advanced. Though the sternum is still cellular, and not yet converted into cartilage, the median separation between the two halves of the meso-sternum has disappeared, and the meso-sternum consists of a single median band of cellular tissue (fig. 14). The meta-sternum (fig. 15) has appeared; cellular in character, and tapering off in the angle between the chest wall and the diaphragm. The clavicle in its outer part is undergoing ossification, and its inner end is cartilaginous. It is clearly demarcated from the pre-sternum, although no joint cavity has yet appeared in the sterno-clavicular articulation (fig. 13). All the seven costal cartilages are now connected with the sternum; but there is still an obvious distinction between the character of the tissues composing the sternum on the one hand and the costal cartilages on the other (fig. 16).


(c) The third stage in the development of the sternum is associated with the conversion of its cellular tissue into cartilage,—at first cellular, afterwards hyaline. The process begins in the pre-sternum in the upper lateral angles, along with the formation of the clavicle (fig. 11). In the mesosternum, cartilage cells first appear at the periphery of the band, in the intervals between the attachments of the costal cartilages (fig. 16). The parts of the sternumopposite the costal attachments remain longest in a cellular condition. In the meta-sternum, cartilage formation begins at the anterior end.


Ultimately the sternum is laid down—a model of the future bone—as a simple median band of hyaline cartilage, separated at this stage from the clavicles by cellular connective tissue, but in complete fusion with the costal cartilages on each side, and presenting absolutely no differentiation of its component parts.


Three human sterna of the third month, measuring respectively 8, 9, and 10 mm., show clearly this condition (figs. 17, 18, 19). The demarcation of sternal elements and of costal cartilages is shown in the special arrangements of the cartilage cells in lines, along which, later on, the joint cavities will be formed. In all three sterna the sterno-clavicular joint is completely formed, with its inter-articular fibro-cartilage. But in only one case is there a definite costo-sternal joint cavity (between the mesosternum and the right second costal cartilage) (fig. 18)

  • Figures 19 (A-J) show the existence of a sternal foramen. In several sections it presented the appearance of fissura sterni. The perforation contained vessels, one of which was of considerable size.

(d) The further changes in the cartilaginous sternum preceding ossification occur in rodents (rat, mouse) Without cleavage of the parts of the sternum or separation of costal cartilages. Opposite to the costal attachments the cartilage is distinctly hyaline, poorer in cells, and stained less deeply than in the intervals between the costal cartilages. In these intervals the cells are massed together, stain deeply, and the process of ossification is foreshadowed by the ‘formation of “ primary areolze,” which occur in the centre of the pre-sternum, in the meta-sternum, and in the first four so-called segments of the meso-sternum (figs. 20, 21, 22).


These areolae increase in size, while at the same time the perichondrium becomes enormously thickened, followed by the formation of periosteal temporary bone in the usual way (fig. 22).


Thus at birth (in the mouse, fig. 23), while there is complete fusion of the sternal elements together, and of the costal cartilages with them, there is a distinct differentiation of elements entering into the constitution of the sternum. Bone formation has begun, and cartilage only exists at the extremities of the pre-sternum and meta-sternum, in the meso-sternum opposite the costal attachments, and in the interval between the attachments of the sixth and seventh costal cartilages (fig. 24).

II. Ossification

The following facts have been derived from an examination of 236 sterna of human embryos between the foetal ages of three to nine months. 2

(A) Dates of ossification

The approximate periods of ossification in the component parts of the sternum are shown in Table I., which essentially corroborates the accepted account of the dates at which the several centres appear. The first nuclei appear generally in the sixth month for the pre-sternum and the first piece of the meso-sternum. In the seventh month centres appear for the second and third pieces of the mesosternum. N 0 further addition to the number of centres occurs during the eighth and ninth months ; and in full-time foetuses (of which 122 examples were examined) the fourth piece of the meso-sternum and the meta-sternum are usually cartilaginous.

(B) Position and number of centres of ossification

In Table II. a summary is given of the situation and number of centres of ossification in the component parts of the sternum. A more intimate analysis did not appear necessary; and for the sake of brevity and clearness, reference has been omitted to the separation or fusion of double centres, and to obliquity in their position (such oblique double nodules being grouped as lateral). The results tabulated, it should be noted, are reached from an examination of specimens of which the large majority are fulltime foetuses. The cases of younger sterna are not only fewer in number, but are also less advanced in ossification.

Table I. Ossification of the Sternum (percentages)
Table to be formatted.

l CENTRE PRESENT. CENTRE ABSENT. I _ m 1 N Z l “J 2".“ as ‘6 0 , § Meso-sternum. g 2 E Meso-sternum. 2 ,3 Z :3 :5 E In E I-1 2 '25 2 5 . 2 ' -if - 2 $9 4 I ‘ Q 33 g <" E 1st 1 2nd 7 3rd 4th .3 5 1st 2nd 3rd 4th «E

2 :5: 2 . mm. 1 1 IX. 122 64'4 96-7 99-2 99-2 2 83-3 29 , 8-1 3-3 3 -8 -8 16-6 71 91-8. VIII. 21 52-3- 81 81 1 76-2 47'6l 9-5i 14-3 l 19 19 23'8 52-3 90-5 85-7 I l VII. 16 49-1 93-3 87-5 3 87-5 62-5 37-5 12-5 6-6% 12-5 12-5 37-5 62-5| 87-5 VI. 3! 40'7 80'6 83'8 77'4 1 54'8 6'4 I 0 l9'3 16'1 22‘5 45'1 93'5 100 V. 7'4 36‘5 62'5 66'6 * 4I‘6 l2°5 4'1 l 0 37'5 33'3 58’3 87'5 958 100 IV. 1 29'6 15'3 23 15'3 7'7 H 77 1 0 84'6 77 8-1'6 92'3 92'3 100 III. ; 23'9 2'2 2'2 2‘2 , 1'1 1 0 0 77'7 77'7 77'7 88'8 100 100 a 4 ,


While there is considerable variability both in number and position, the centres of ossification are, as a general rule, single and median, and are six in number; one for the pre-sternum, one each for the first four elements of the meso-sternum, and one for the meta-sternum. Exceptions to this rule are found in all situations except in the meta-sternum, which in the few cases in which bone formation has begun, is invariably provided with a single median centre.


The pre—sternum is generally formed by a single centre (79 per cent.). When there are two centres, they are generally vertica.1ly placed. Three or more centres occur quite rarely (26 per cent.).


The first centre for the meso-sternum is, as a rule, also single (785 per cent.); when there are two, they are usually laterally placed. The second and third centres of the meso-sternum are less frequently single than the above-named centres (593 per cent.: 60'5 per cent.). When there are two centres, they are in most cases laterally placed. The fourth centre in the mesosternum is not generally present. When it occurs it is nearly as often double ‘as single; and when two centres are present, they are as often vertical as lateral in position.


Table II. Median and Lateral Ossification
Table to be formatted.

MONtrHs,. . . . .* IX. VIII. I VII. i VI. ’ v. Iv. III. '.ro1uu.. H Pmnonnuens.

5 1 —-L -r ‘ocunj -1:-T .-:——j-—::

14 }9 1 24 3}12 3 4 1 3

1 0} 3 '0 4 0} } 0 }

I27 0 3 }5 .0 1 0 3 17 25 ' 1

I i I

Centre Single, . . _ . . 84 » Double X::~':::::," : 23 }2s ,, Three or more, . . 4

1.

G‘?!

147 179

3g}3: }39 l 209

<1 —¢14—

186 .. ..

78'5

5 147 2 6 .. 30 }35 16.0} 186 _

5}4o 2.6 21 3

137 ,.. ..

7 108 ] 3_8.. 59-3 b.:}74 33 }3::: 40-6

-Lee-nj u-

182 . . . . l 60-5

5 3-5 " 42 } 47 -29-5} 33 . 9}56 6.3 39 3

Pre-sternum.

O rJ"~. 00

7*: CO

1 Total Ossified , . . . . 111 g

Centre Single, . . _ . . Meso-sternum. Double Vertncal, .

so 15 0 12 1 2 12 1 1 FirstPiece. » Lateral, . 25}25}30,1} 2}2 1}1}2 2} 3}3 1} 3}3 4 o 1 o no 17 — 15

,, Three or more, . .

14 26

Total ossined, . . . .

Centre Single, . V .ti . 5 59 0 12 1] 9 #1 0 5

- er ca .

SecondP1ece. ,, Double Lateral,’ _ 47}52 4} 4}4 I 31 «i}5 4} 5}5 1} (1)}1 _ 14 __

61!-(O r-’% Q1-I

,, Three or more, . . 6} 58 0

1-__.—. T — en;

N963 (N I 1-! 24% b

I O9

17:ta1ossined,. . . . 117 16 24 A 6

Centre Single, . . . 59 7 4 14 1

Third Piece. ,, Double ; 33}33}41 g} 3}3 5}6 ‘ g} 3}3 i (1, 1}_l ,, Three or more, . . 8 1

Q1 55% r"’% CW

.. 5- — :3. -2- an.

Total Ossifled, . . . . 100 10 , 10 ‘ 17 2

Centre Single, .{v .t_ . 7 18 0 1 I 2 3 1 0 th P’ . - "'°‘‘ ° }14 1 } 3 1 } 1 Four 1ece ,, Double ‘Lateral,’ . 7 }u 1 }1 1 }3 1 }1 0 0}1 .1..- .

ONOCN

N 9% 6061930 9% ON

,, Three or more, . . 0

1 -.—_ j us. -7

Total Ossified, . . . . 32 2 i 6 .1

OOOO cl o I l I O

Meta-sternum. Single Centre, .' . . . 10 3 2 V 1 1


The part of the sternum between the attachments of the sixth and seventh costal cartilages is cartilaginous at birth, and the question of its ossification is deferred for the present. It appears that it may be ossified by extension from the fourth piece, though there is reason for believing that in some cases at least it may possess a separate and independent centre.

(C) Fissures Grooves Foramina

One remarkable negative feature characterises the series of foetal sterna examined. In all there is a complete median plate of cartilage, grooved it may be . on one or both sides, perforated in some instances by one or more holes, but in no single instance is there a fissum storm; A longitudinal groove (Table III.) is characteristic of the foetal meso-sternum, occurring in 158 out of 222 examples, or 7 0'1 percent., a proportion which obtains generally for all ages. It may be faint or obvious ; it may be found on one or both aspects of the meso-sternum, and implicate it in the whole or part of its length, but it never appears in the pre-sternum. This grooving of the meso-sternum is probably associated with the method of early development of the cartilage, but it is at the same time plain that it is not necessarily coincident with a bilateral asymcation of the meso-sternum.

Table III. Grooves
Table to be formatted.

1' Per Cent. I Months. , lases. Present. Absent.

Present. Absent. l IX. 113 75 38 66-3 I 336 1' VIII. 17 6 11 35'2 6467 I VII. 16 13 3 ' 812 18'?

2 VI. 30 24 6 80-0 20-0 V. 24 19 5 79'1 208 IV. A 13 13 0 100 III. 9 8 1 88'8 ll°l Total 222 158 a 64 70'1 29'0 1


Table IV. Sternal Foramina
Table to be formatted.

. 4-; ——u—

PRESENT.

ABSENT. . . . r more N°- One 1n Two In One 1n TWO 0

M°nth3- » °f - Meta-sternum Meta-sternum Meso-sternum in Lfisfigiand TOTAI“ e . ,

Per

,——-jj ———. 1-: 1-: n-g—- jj:—.jn-g-———_——:_—.._——-———n———

Percent No. P“ No. P“ No.

cent. cent.

I Per No. cent. No.

.00

IX. .120 81 67'5 23 VIII. 2o 14 70

VII. 16 10 62-5

VI. 30 20 66'6

I Present :H 1 in meta-sternum 2 in meta-sternum 1 in meso-sternum 2 or more in mesosternum and meta 2 sternum 0

Absent . . . 164 = 69 '4 per cent.

u-100

moo II II II

IV. 13 7 53 '9 5

III. 9 7 77'7

.;:e—-———:u-:a-j-T1-ajjj.-———-——.———-——:——jo

Total present 7;=30‘5 per cent.


V0

I '."

N

v-4 K:

00

‘P

' GO

to H O O O v-I O 00

Sternal foramina (Table IV.) occur only occasionally (in 72 out of 236 cases, or 30'5 per cent.). The number and situation of the perforations are as follows :— 9 Cases. Per cent.

One foramen in the meta-sternum . . . 54 22'8 Two foramina in the meta-sternum . ' . 5 2'1 One foramen in the meso-sternum . . . 8 3'3

Two or more foramina (in the meso-sternum and meta-sternum) . . . . . 5 2'1 7 2 . . . 30'5

The great majority thus occur singly in the meta-sternum, and the pre-sternum is never perforated. From an examination of a human embryonic sternum 9 mm. in length (third month) (fig. 19), one is led to believe that the perforation is due to the persistence of vessels, preventing the conversion of the embryonic connective tissue into cartilage in the middle line.


Like the grooves, these foramina are not improbably causally associated with the mode of early development of the sternum, and it is therefore noteworthy that neither grooves nor foramina occur in the pre-sternum.


(D) Union of sternal elements and costal cartilages

An examination of the mode of union of the parts of the sternum with one another and with the costal cartilages brings out the fact that the connections are much the same in the earlier and later months of foetal life (Table V.).

The pre-sternum and meso-sternum are usually connected together by a fibrous lamina (764 per cent.) opposite the attachments of the second costal cartilages. More rarely they are fused together by cartilaginous union (23'6 per cent.). I have only met with one example (in a 9 months foetus) of a case of alteration in position of the junction to the point opposite the attachments of the third costal cartilages.

The meso-sternum and meta-sternum are usually (77°9 per cent.) united by cartilage, and only exceptionally (221 per cent.) by a fibrous lamina.

The costal cartilages in the centre of the series are generally fused with the lateral borders of the sternum, and are not united to it by a. fibrous lamina. The first costal cartilage is also, as a rule (813 per cent.) continuous with the pre-sternum. Occasionally on one side or both the union is fibrous.

The condition of the seventh and eighth costal cartilages has been particularly noted. It is not uncommon for the pair of seventh cartilages to articulate together in front of the sternum (34 cases—14°4 per cent.). (In still fewer cases the same occurs with the sixth costal cartilage.) In 8 per cent. of the cases the seventh cartilage fails to reach the sternum on one side or both. On the other hand, the eighth cartilage on one side or both is connected with the sternum in still fewer cases (48 per cent.). In rare cases, the 5th, 6th, or 7th cartilage reaches on one side to the middle line of the sternum, its distal end pushing its way forwards through the body of the sternum.


Table V. Ossification of Sternal Elements and Costal
Table to be formatted.


0a~rtt'lage3. _ - ‘ 3 Months . . . . . . IX. VIII. VII. VI. v. IV. III. 01;; . "" ’ -"'" ' '__’ T 1- '—""' -"—' '"-" ""_" Prggiggnfifm {Fibrous . . . I 75-1 73-9 99-9 37 583 69-2 66-6 =76-4 F Mesojsggrnumj Cartilaginous . . 24-7 21 O . 12-9 41-6 36-7 33-3 =23'6 Meggggrggm Fibrous . . . 31 31-5 31-2 46 9 6 11-1 =22-1 1 Memgfigmum Cartilaginous . . J 63-9 63-4 63-7 66 96-9 166 33-3 =77-9 V Fibrous . . . I 14 25 6'6 0 0 153 111 Fggftflgzgal Cartilaginous . . 76 63-7 80 100 73-2 76-9 33-3 =31-3 Dissimilar . . . 9'9 187 133 0 21°6 7'6 0 Sgvepflh {Separate from sternum 6'6 5'8 18 '7 15-3 0 9 0 :92 OS Cartilage United . . . 93-4 94-2 31-3 34-7 100 91 166 = 3 Eighth costal Separate from sternum 90 100 100 967 100 909 88°8 =95'2 ‘ Cartilage United . . . 99 0 6 3-5 6 9 11-1 = 4-3

1- 4-} r if r I I


(E) Shape of the meta-sternum

Out of 189 cases, the metasternum is present in 182 (963 per cent.); absent in seven instances (37 per cent.). I have been as careful as possible to discard all examples in which there was the slightest indication that the meta-sternum had been accidentally lost in maceration.

While the shape is extremely variable, it is more often single and median than bifurcated. An undivided meta-sternum occurs in 107 cases (57 '6 per cent.); a bifid meta-sternum in 77 cases (423 per cent.).

=(F) Anomalies - Epi-sternal cartilages

One of the most striking features of the series of embryonic sterna examined is the absence of anomalous conditions, and the regularity and symmetry of development. N 0 case of fissum sterml is recorded. One example occurs of transference of the pre-meso-sternal junction to the level of the third costal cartilages. A few instances are found in which one or more costal cartilages (usually the 5th, 6th, or 7th) force their way through the cartilaginous sternum to the middle line. Absence of the meta-sternum, asymmetry in the attachment of costal cartilages, and fusion of contiguous costal cartilages together, also occurred in a few examples.

Epi-sterna! cartilages. — In two cases supra-sternal cartilages have been found, situated at the cephalic border of the pre-sternum, between the clavicular articular surfaces. In one case the cartilages are separated from the pre-sternum and fused together; in the other case, they are separate from one another, but continuous with the cartilaginous pre-sternum.


It is not my desire to make any general deductions, or attempt to draw any definite conclusions from these observations at present. The subject is a large one, and is only very partially dealt with in this communication. I have ventured to make this bare statement of fact to the Anatomical Society, partly in order to clear the way for further work on the same subject, and partly to draw attention to some of the general morphological problems associated with a study of the human and mammalian sternum.

Description Of Plates

Plate 2

Paterson1900 plate2.jpg

Fig. 1. Human embryo (sagittal section).

Fig. 2. Rat 9 mm. Section across bottom of praecervical sinus.

Fig. 3. ,, ,, Sagittal section through chest wall.

Fig. 4. ,, ,, Transverse section through middle of chest wall, showing ossifying ribs and absence of sternum.

Fig. 5. Rat 10 mm’ 1 Magnified seven times, showing clavicles,

7' ” ” }- pregslizernum, meso-sternum, and costal . ' ' ” 1 ” cartilages.

Fig. 8.

Fig. 9. Rat 10 mm’ acteristic features of pre-sternum and

Fig 10' ” ” meso-sternum.

Fig. 11. Bat 10 mm. { Higher magnification, to show differentiation

Fig. 12. ,, ,, of tissue in sternum and costal cartilages.

{ Magnified twenty-eight times, to show char

Rat 13 mm Magnified seven times, to show structure and connections of sternal elements.

Plate 3

Paterson1900 plate3.jpg

Fig. 15. ” ” , connections of sternal elements. ' ' 3! 3)

{ Magnified twenty—eight times, to show general

Fig. 16. Rat 13 mm. structure of sternum and connections of costal cartilages.

Fig. 17. Human sternum, 3rd month, 8 mm. long, magnified twenty eight times.

Fig. 18. Human sternum, 3rd month, 10 mm. long, magnified twenty one times.

Fig. 19. A-I. Sections of human sternum, 3rd month, 9 mm. long, possessing sternal foramen and 8 costal cartilages, - magnified 18 times. J. Reconstruction of same.

Fig. 20. Rat embryo. Coronal section of cartilaginous sternum, showing primary areolae, — magnified seven times.

Fig. 21. Coronal section of older rat’s sternum, showing primary areolae and absence of ossification in last piece of mcso-sternum, magnified seven times.

Fig. 22. Coronal section of older rat’s sternum, showing primary areolae, thickened perichondrium, and absence of bone formation between 6th and 7th costal cartilages.

Fig. 23. Coronal section of sternum of mouse a few days after birth, showing bone formation and cartilages.

Fig. 24. Sternum (lower end) of rat 9 days old, showing ossification.

15' a’ ma W/7502:,/1'//2. Cam br/'a’_qe ../ou/5/1.0/'/Irzart. &Pfiy.s*. Uct. 7900.


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