the thickness and collagen content of tendon relative to the cross-sectional area of muscle during...

The Thickness and Collagen Content of Tendon Relative to the Cross-Sectional Area of Muscleduring GrowthAuthor(s): D. H. Elliott and G. N. C. CrawfordSource: Proceedings of the Royal Society of London. Series B, Biological Sciences, Vol. 162, No.987 (Apr. 13, 1965), pp. 198-202Published by: The Royal SocietyStable URL: http://www.jstor.org/stable/75509 .

Accessed: 04/05/2014 16:11

Your use of the JSTOR archive indicates your acceptance of the Terms & Conditions of Use, available at .http://www.jstor.org/page/info/about/policies/terms.jsp

.JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range ofcontent in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new formsof scholarship. For more information about JSTOR, please contact [email protected].

.

The Royal Society is collaborating with JSTOR to digitize, preserve and extend access to Proceedings of theRoyal Society of London. Series B, Biological Sciences.

http://www.jstor.org

This content downloaded from 130.132.123.28 on Sun, 4 May 2014 16:11:15 PMAll use subject to JSTOR Terms and Conditions

http://www.jstor.org/action/showPublisher?publisherCode=rsl

http://www.jstor.org/stable/75509?origin=JSTOR-pdf

http://www.jstor.org/page/info/about/policies/terms.jsp


The thickness and collagen content of tendon relative to the cross-sectional area of muscle during growth

BY D. H. ELLIOTT* AND G. N. C. CRAWFORD

Department of Human Anatomy, University of Oxford

(Communicated by G. W. Harris, F.R.S.-Received 23 July 1964)

The tendon of peroneus brevis is thinner than that of tibialis anterior in the foetal and three- week old rabbit but thicker in the adult. At three weeks there is no difference between these muscles in the ratio of the thickness of collagen in their tendons to the cross-sectional area of their muscle fasciculi. Thereafter the growth of tendon collagen is such that this ratio increases in peroneus brevis but decreases in tibialis anterior, diverging towards their separate adult values.

INTRODUCTION

The ratios of tendon thickness to muscle strength and to fascicular cross-sectional area differ between the fusiform and pennate groups of muscles in the adult rabbit

(Elliott & Crawford I965). This difference might be present at birth but, alterna-

tively, if related to muscle function might develop post-natally as does differen- tiation into the slow or fast types of muscle (Denny-Brown I929; Buller, Eccles & Eccles I960). An attempt has been made to resolve this point by relating the thickness of collagen in the tendons of the fusiform tibialis anterior and the

pennate peroneus brevis to the cross-sectional area of their muscle fasciculi

during growth of the rabbit. Fascicular cross-sectional area was the muscle di- mension of choice because it is independent of any change in the internal architecture of the muscle belly which may occur after birth (Alder, Crawford & Edwards 1958).

METHODS

Muscles and their tendons from two foetal litters at full-term and from young rabbits of mixed stock were examined at various ages up to sixteen weeks. The limbs were fixed in mid-flexion by perfusing formaldehyde solution through the thoracic aorta in a similar manner to that already described for the adult (Elliott & Craw- ford 1965). The muscles and tendons of young rabbits are very small and this

investigation had to be restricted to tibialis anterior and peroneus brevis, the

largest of the fusiform and pennate groups. The methods used were similar to those described for the adult except that in the

smaller specimens muscle and tendon length had to be measured with a travelling microscope whose vernier scale was calibrated to 0-02 mm, and dry weight with an

Oertling balance calibrated to 0-002 mg. It was also necessary to pool several of the smaller specimens in order to provide sufficient material for the estimation of

hydroxyproline content.

Comparison of the indices of muscle fascicular cross-sectional area during growth depends upon the assumption that the sarcomere has the same length at all ages.

* Present address: Royal Naval Medical School, Alverstoke, Gosport, Hants.

[ 198 ]



Growth of tendon collagen 199

In order to test this the tibialis anterior in each of seven three-week old and ten adult rabbits was fixed in full plantar-flexion and the mean sarcomere length determined. There was no significant difference between the young (3.16 + 0-02 [Km) and the adult (3-11 + 0-03 jcm).

RESULTS

Foetal rabbits

The tendon of peroneus brevis was thinner than that of tibialis anterior in eight full-term foetal rabbits (table 1), but during growth it increases in thickness from ca. 75 % of that of the tibialis anterior in the foetal to ca. 140% in the adult.

TABLE 1

(a) Eight full-term foetal rabbits

tibialis anterior peroneus brevis

dry belly weight (mg) 2.14 + 0.23 0.60 ? 0-06 belly length (mm) 11.2 + 0-7 9.8 + 0-3 belly weight as approx. per cent of that of the 0-3 0.3

adult belly length as approx. per cent of that of the 15 15

adult tendon thickness (pg/mm) 18-9 + 2-0 14.3 + 1-2 tendon thickness as approx. per cent of that of 4-4 2-4

the adult

(b) Ten three-week-old rabbits

index of muscle fascicular cross-sectional area 4.07 + 0.15 3.24 ? 015 (/xg/sarcomere)

tendon thickness (/Lg/mm) 100 + 5 71 + 3 tendon thickness (pg/mm) per unit index of muscle 24-7 + 1.1 22.0 + 0.9

cross-sectional area thickness of tendon collagen (,tg/mm) per unit 10-88 ? 0-52 9.67 ? 0-37

index of muscle cross-sectional area

(c) Fifteen adult rabbits

index of muscle fascicular cross-sectional area 38-9 ? 1-0 37-6 + 1-0

(/ig/sarcomere) tendon thickness (mg/mm) 0-43 + 0-01 0-59 + 0-01 tendon thickness (pg/mm) per unit index of muscle 11-00 + 0-29 15-82 + 0-50

cross-sectional area thickness of tendon collagen (tg/mm) per unit 7-59 + 0-15 11-85 + 0-37

index of fascicular cross-sectional area

(The estimate of variation is the standard error of the mean.)

The fasciculi of macerated foetal muscles were too small to be measured with

accuracy but the weight and length of the foetal tibialis anterior belly were the same proportion of its adult dimensions as were those of the foetal peroneus brevis. This indicates that the ratio of their belly girths remains constant during growth and thus that the ratio of tendon girth to belly girth in peroneus brevis gradually increases relative to that of tibialis anterior. If the internal architecture of the two

muscles remained constant this would imply a similar change in the ratio of tendon

girth to muscle fascicular cross-sectional area. However, inspection of peroneus



200 D. H. Elliott and G. N. C. Crawford

brevis in the foetus suggests that it is more fusiform and less pennate than in the adult and the ratio of its fascicular cross-sectional area to belly girth would then increase with age. The change in the ratio of tendon girth to fascicular cross-sectional area between foetus and adult in peroneus brevis relative to that of tibialis anterior would therefore be reduced.

F A

40 + A A

I : A A A A

o r

_

AA A

.?= X A~~~~~~~A o.0

a) 4- x A

2 0- X

OsxX A A x A

X

I . . . t I . 1 - I I .,J..t. -

0 0-2 0-4

x thickness of collagen in tendon (mg/mm) A dry weight of tendon (mg/mm)

FIGURE 1. The growth of tibialis anterior tendon relative to that of its muscle. The horizontal and vertical lines through the greatest (mean of fifteen adult) and the least point (mean of ten three-week old) on the tendon collagen curve represent twice the standard error of the mean.

Three-week-old rabbits As in the foetus the tendon of peroneus brevis in ten rabbits, 21 days old and

weighing between 250 and 350 g, was about 70 % of the thickness of that of tibialis anterior (table 1). It was possible to measure the length of the fasciculi of the three- week-old rabbit and then calculate their index of cross-sectional area. There was no significant difference between the two muscles in the thickness of tendon per unit index of fascicular cross-sectional area and in both the values were greater than in the adult. However, they change relative to each other during growth and fiducial limits suggest that in the three-week-old rabbit this ratio for peroneus brevis is between 70 and 110% of that for tibialis anterior, whereas in the adult it ranges from 130 to 160%.



Growth of tendon collagen 201

The hydroxyproline content of the tendons was determined and converted into

collagen content on the assumption that it formed a constant proportion of collagen throughout growth (Elliott I964). 44 + 3 mg collagen were thus estimated to be present in 100 mg dry tendon in both peroneus brevis and tibialis anterior as

opposed to the 71 + 1 % present in these tendons in the adult. As a result of the

30-

A

A

A 0

CD

v

c8

0

sq

0

0 -1

0

.3

0

0

0

0

A

0

0

A A

A

0

co A

ot A

o0 '

A

0

0

0

0

0-2 0-4

dry weight of tendon (mg/mm)

06

FIGURE 2. Tendon thickness relative to muscle cross-sectional area in rabbits between the

ages of three and sixteen weeks. A, Tibialis anterior; 0, peroneus brevis.

alteration of collagen content being the same in the two tendons, the amount of

collagen per millimetre of each tendon changes less than its dry weight per millimetre relative to the cross-sectional area of its muscle during growth (table 1; figure 1). However, in each muscle there is a significant difference between the young and adult values (P = 0-01), the ratio of collagen thickness to fascicular cross-sectional area decreasing in tibialis anterior but increasing in peroneus brevis.



D. H. Elliott and G. N. C. Crawford

Four- to sixteen-week-old rabbits

The thickness of the tendons of peroneus brevis and tibialis anterior and their

collagen thickness relative to the cross-sectional area of their muscles gradually diverge from their common three-week-old value towards their separate adult values after the first month of post-natal growth (figure 2).

DISCUSSION

During growth the decrease in the ratio of tendon thickness to muscle cross- sectional area is partly explicable by the simultaneous decrease in the density of cells (Inglemark 1945, I948) and increase in the concentration of collagen. How-

ever, in both muscles there is also a significant change in the ratio of the thickness of collagen in the tendon to fascicular cross-sectional area. This cannot be ascribed to a difference in the maximum tension which the two muscles transmit since it has

already been shown that there is no general relationship between tendon girth and muscle strength (Elliott & Crawford 1965). The growth of collagen in the tendon, although perhaps related to the cross-sectional area or strength of muscle in

utero, may be determined after birth only partly, if at all, by this and might be influenced rather by some other factor such as the frequency and duration of the

average tension transmitted.

REFERENCES

Alder, A. B., Crawford, G. N. C. & Edwards, R. G. 1958 Proc. Roy. Soc. B, 148, 207. Buller, A. J., Eccles, J. L. & Eccles, R. M. 1960 J. Physiol. 150, 399. Denny-Brown, D. E. 1929 Proc. Roy. Soc. B, 104, 371. Elliott, D. H. 1964 D. Phil. thesis (Oxford). Elliott, D. H. & Crawford, G. N. C. 1965 Proc. Roy. Soc. B, 162, 137. Inglemark, B. E. 1945 Acta Soc. Med. upsalien, 50, 357. Inglemark, B. E. 1948 Acta anat. 6, 113.

202



the thickness and collagen content of tendon relative to the cross-sectional area of muscle during...

Documents