The Position of the Nutrient Foramen and Direction of the Nutrient Canal in the Long Bones of the Madder-Fed Pig by Carrick G

THE POSITION OF THE NUTRIENT FORAMEN AND DIRECTION OF THE NUTRIENT CANAL IN THE LONG BONES OF THE MADDER-FED PIG BY CARRICK G. PAYTON, M.D. Lecturer and Senior Demonstrator in Anatomy, University of Birmingham

INTRODUCTION THE external opening of the nutrient canal, usually referred to as the nutrient foramen, has a particular position and the canal a certain direction constant for each bone. Because of confusion of these two points in the literature on the subject, I wish to stress the fact that the position of the foramen and the direction of the canal are two distinct and separate phenomena of the nutrient artery, and may be the result of independent mechanisms. The literature available is small in amount, deals mainly with direction of the canal, and gives the impression that investigators have assumed that both phenomena are caused by this direction. In this account the position of the nutrient foramen and the direction ofthe canal will be dealt with separately. Throughout this paper use has been made of the data contained in two previous papers on the growth of the diaphyses and epiphyses of the long bones in the madder-fed pig (1, 2). MATERIAL AND METHODS Observations and measurements are made from the limb bones of a dozen madder-fed pigs used in my recent publication on diaphysial growth(1). The age of the pigs varied from 80 to 587 days. These pigs had been treated by the "indirect madder method," whereby the madder is withheld for a period before killing, and consequently the new bone of this non-madder period shows up white against a background of maddered bone. Particulars of age, madder period and non-madder period are noted in Table I.

Table I. Duration in days with and without madder feeding. Age at death Madder period Non-madder period Pig No. days days days 14 80 72 8 15 91 77 14 16 108 84 24 17 126 105 21 12 140 61 28 1 169 68 29 2 197 97 28 3 225 125 28 4 279 153 54 6 362 207 84 9 475 271 126 8 587 394 116 Position ofNutrient Foramen and Direction ofNutrient Canal 501 Longitudinal sections were cut through the long axes of the diaphyses and the plane of the section was chosen to pass through the nutrient foramen.

HISTORY BWrard (3), almost 100 years ago, noticed that the direction of the nutrient canals in the human being was constant for a given bone. He noticed that in the upper limb the canals were directed towards the elbow and in the lower limb away from the knee. He advanced no theories concerning these observations, but remarked that the nutrient artery entering the bone divided into two branches, ascending and descending, the branch continuing in the direction of the main artery was the larger, and therefore, because of the better blood supply, caused union to occur first of all between the diaphysis and epiphysis towards which it flows. Thus the canal is slanted towards that end at which the epiphysis is first united to the shaft. In this series of pig bones the direction of the nutrient canal has been noted and this is considered with regard to the end of the diaphysis which first unites with its epiphysis (Table II).

Table II. The direction of the nutrient canal in relation to the end of the diaphysis which unites with its epiphysis first. In humerus canal directed away from distal. end ofdiaphysis which unites with its epiphysis first

,, radius ,, towards proximal ,. VP .. ,, ulna ,, towards proximal ,. .. ..

femur ,, away from proximal ,. VP Pt tibia ,, towards distal ,. ., .. fibula ,, towards distal ,. .J. 9 It is to be noted from Table II that for the bones of the pig the humerus and femur disagree with Berard's statement. In contrast with Berard's idea, Humphry (4) demonstrated, by means of madder staining in the pig's bones, the unequal growth of the two ends of the diaphysis, and stated that the obliquity of the canal was not the cause but the effect of the unequal growth. This unequal growth at the two ends would cause an unequal drag on the periosteum which is fixed to the two ends of the bone. Humphry's dragging theory is disputed by Piollet(5), who states that in the human foetus the nutrient arteries are directed first perpendicularly to the bone's long axis and then later all proceed distally in the bone, while still later the arteries of the radius, ulna and femur change their direction, so that in the adult all the arteries are found directed away from the growing ends as the result of unequal growth of the diaphysis in which growth is peripheral, while growth of soft parts is interstitial. Thus both Humphry and Piollet associate the obliquity of the nutrient canal with the unequal growth of the diaphysis. In Table III the direction of the canal in respect to the greater growing end of the diaphysis is noted for this series of bones. 502 Carrick G. Payton Table III. To show the relation between the direction of the nutrient canal and the end of the diaphysis with the greater growth. In humerus canal directed proximally and proximal end of diaphysis is greater growing end radius ,, proximally ,, distal , . ulna ,, proximally ,, distal femur ,, distally ,, distal ,.9 pi- tibia ,, distally ,, proximal ,. .. fibula ,, distally ,, proximal ,. .. It is seen from Table III that the nutrient canals in the pig's humerus and femur are directed towards the end of the diaphysis with the greater growth, in contrast to Piollet's and Humphry's statements. Various authors, in addition to the foregoing, have supported (6) or dis- agreed (7) with these statements without, however, adding to our knowledge. The text-books of anatomy generally quote either 1Wrard's (8) orHumphry's and Piollet's (9) theories. A few of them remark that the reason for the obliquity seems obscure. Since the nutrient canals as observed in the long bones of the pig do not agree with any of the above theories, is it just possible that this apparent agreement for the human long bones is one of mere coincidence?

GENERAL OBSERVATIONS In the pig's humerus the nutrient foramen is situated on the posterior surface near the junction of the middle and distal thirds of the shaft. The canal is directed proximally into the bone. The outer end of the canal comes into relation with the lower edge of a layer of new bone which is being laid down on the exterior of the posterior part of the shaft (fig. 1). It will be noticed that the nutrient canal of the humerus does not enter the shaft so obliquely as is the case in the other bones, because the canal is involved in a modelling process at the distal end of the diaphysis. It has been shown (l) that new bone is added to the distal end of the diaphysis and that most of this new bone is rapidly absorbed on the anterior and posterior aspects of this extremity to form the coronoid and olecranon fossae. Owing to the distal extremity growing downwards and forwards the olecranon fossa becomes the deeper of the two fossae and requires to be filled in on its proximal aspect to enable the shaft of the humerus to extend in a distal direction. Conse- quently a layer of new bone is found on the posterior part of the olecranon fossa extending proximally on the posterior surface of the shaft as far as the nutrient foramen. In this way the nutrient foramen is sandwiched between two edges of new bone-one, the distal edge of new bone added to the shaft, and the other, the proximal edge of new bone added to the olecranon fossa. This peculiar position of the canal between two layers of new bone in addition to lessening the obliquity of the canal may also modify any movement of the canal in respect to the layer of new bone round the shaft; but reference to this point is made later. In the radius the nutrient foramen is situated on the posterior surface of the shaft near the junction of the proximal and middle thirds. The canal is i .

Fits. 3;.

ltAl

L. 4. I'iL. .5. Jg ja . Figs. 1-6 are respectively longitudinal sections cut through the nutrient canals of humeral, radial, ulnar, femoral, tibial and fibular diaphyses of Pig. No. 4. Age 279 days. The areas of bone unstained by madder are represented white and indicate new bone laid down during the non-madder period of 54 days. Bone stained by madder is black or stippled. 504 Carrick G. Payton directed proximally into the bone. The external end of the canal lies at the lower edge of new bone which is being added to the outside of the posterior part of the shaft (fig. 2). In the ulna the nutrient foramen is situated on the anterior surface of the shaft near the middle. The canal is directed proximally into the bone. The inner end of the canal lies in relation to the upper margin of new bone which is being added to the inside of the anterior part of the shaft (fig. 3). In the femur the nutrient foramen is situated on the anterior surface of the shaft near the junction of the proximal and middle thirds. The canal is directed distally into the bone. The outer end of the canal lies in relation to the proximal margin of new bone which is being added to the outside of the shaft (fig. 4). In the tibia the nutrient foramen is situated on the posterior surface of the shaft near the junction of the proximal and middle thirds. The canal is directed distally into the bone. The outer end of the canal lies in relation to the proximal margin of new bone which is being added to the outside of the shaft (fig. 5). In the fibula the nutrient foramen is situated on the medial surface near the junction of the proximal and middle thirds. The canal is directed distally into the bone. The outer end of the canal lies in relation to the proximal margin of new bone which is being added to the outside of the shaft (fig. 6).

Position It is generally agreed that the vessels which occupy the nutrient canal are derived from those that took part in the initial invasion of the ossifying cartilage, so that the nutrient foramen was at the site of the original centre of ossification. It is known that the diaphysis increases in length unequally at its two ends, so that it is not surprising to find the foramen nearer one end of the diaphysis. But when it is found that the position of the foramen bears no mechanical relation to the growing ends of the diaphysis a problem is raised. The following observations go to show that the canal moves inde- pendently of the growth in length of the diaphysis. Observations of the appearance of the bone immediately surrounding the foramen and especially of the appearance of sections through the foramen show that absorption is taking place on one side and addition of new bone on the other. These observations are noted for all the long bones in Table IV. Table IV. To show the position of absorption and addition of bone round-the nutrientforamen. In humerus absorption occurs on the distal* and addition on the proximal side of foramen ,, radius ,, distal ,, proximal ,, ulna ,, distal ,, proximal ,, ,,femur , proximal ,, distal IV ,, tibia ,, proximal ,, distal ,, fibula ,, proximal ,, distal , * This absorption is slight for humerus, as explained on p. 502. Position ofNutrient Foramen and Direction ofNutrient Canal 505 This observation gives an indication that the foramen may move inde- pendently of the growth of the diaphysis. Further support of this independent movement could be obtained if a landmark on some bone from which measurements could be taken could be shown to remain stationary so far as diaphysial increments are concerned. Such a guide was found on the ulna, in which bone the proximal articular surface is carried by the diaphysis. On this articular surface is a groove dividing the sigmoid notch into olecranon and coronoid parts. The following calculations show that the groove is constant in position so far as growth in a proximal and distal direction is concerned. Measurements from this groove to the proximal end of the diaphysis in a young and an old bone give the following results: No. 14 (80 days old), 28 mm., No. 9 (475 days old), 42*5 mm. This gives an increase in the length of this section of the ulna of 14*5 mm. in No. 9 which is 395 days older than No. 14. Now the amount of new bone added to the proximal end of the diaphysis can be measured by means of the madder staining. These measurements have already been published. From these measurements it is seen that the upper end of the diaphysis grows in relation to the lower end as 0 5: 1-0. The length of No. 14 diaphysis is 100 mm. as compared with No. 9 which is 143 mm. Therefore No. 9 is 43 mm. longer than No. 14. The upper end of the diaphysis adds one-third of this, namely 14*3 mm. Thus it is apparent that only the proximal end of the section of bone grows and that the groove in the sigmoid notch remains stationary, so far as alteration in a proximo-distal direction is concerned. Measurements have been made of the distance between this groove on the sigmoid notch of the ulna and the nutrient foramen (Table V). Table V. Measurements of distance between groove on sigmoid notch ofulna and nutrientforamen. Measurements in mm. Ulna No. 14 15 16 17 12 1 2 3 4 6 Age (days) 80 91 108 126 140 169 197 225 279 362 Distance, groove to foramen 25-5 27-5 28-7 27-0 31-0 27-5 27-0 36-0 33-3 35.5 From these measurements it is seen that the foramen travels distally as one passes from the younger to the older bones. Further evidence of the independent movement of the nutrient foramen can be got by measuring the distance between the nutrient foramen and the proximal end of the diaphysis (Table VI) and using these measurements to mark the position of the nutrient foramen on the graphs (already published) where the diaphyses are in such a position that they can be superimposed so far as growth in length is concerned (figs. 7, 8). If the older theories that the position of the foramen was dependent upon unequal growth of the diaphysis held good these foramina should be in a horizontal line on the graphs, and should be situated in that half of the bone 506 Carrick C. Payton Table VI. Measurements in mm. of the distance between the nutrient foramina and the proximal end of the diaphyses. Pig No. 14 15 16 17 12 1 2 3 4 6 9 8 Humerus 58-0 60*0 50 3 68-8 70 5 70-2 76-0 80-5 84-2 79 0 85-3 100-2 Radius 16-5 20-5 21-0 20-2 28-7 20-0 25-0 30-2 34 0 23-2 29-0 32-3 Ulna 55-3 58-1 58-3 60-0 65-0 62-0 70 0 80-5 75-8 75 0 80-2 100 0 Femur 34*2 30*5 35*1 38-6 35 0 34 0 35 0 38&2 38-0 43-2 40-3 47-2 Tibia 38-0 38-0 44 0 50 0 47-7 47 0 54-0 60-4 54-3 60-2 62-0 70 3 Fibula 46-0 400 28-5 40 0 40-8 44-5 40 5 48-0 55-6 55-0 42-3 66-2

LEFT DIAPHYSES OF +t; d C0 o0 40t FEMORA. Cl d _d _o z 30 6~~~~ _ .f...lT, 'V0-

Fig. 7. Graphic representation of the relative rates and amounts of growth at the ends of the humeral, radial and ulnar diaphyses as previously published(l), with the position of the nutrient foramina indicated as explained in the text. Position ofNutrient Foramen and Direction ofNutrient Canal 507

80 l0o 15O 200aco 46o 500 600. Fig. 8. Graphic representation of the relative rates and amounts of growth at the ends of the femoral, tibial and fibular diaphyses as previously published(l), with the position of the nutrient foramina indicated as explained in the text. remote from the end with the greater increment. It is seen, however, that in none of the graphs except the humerus are the foramina in a horizontal line. Further, the foramina of the ulna, tibia and fibula are situated in that half of the bone with the greater increment. It is also observed that the foramina of these last-mentioned bones move towards the end with the greater increment as the age of the bones increases. The exception of the humerus has already been anticipated (p. 502) owing to the peculiar position of the canal which is situated between two layers of new bone which would tend to keep it stationary. 508 Carrick G. Payton Direction The direction of the nutrient canal is constant for a given adult bone. It has been pointed out, however, that in the case of the pig bones, the direction bears no constant relationship to the epiphysis which unites first with the shaft, nor is the direction a mechanical result of unequal growth at the two extremities. By means of the madder method the following observations are made possible: the nutrient foramen is seen to enter the shaft close to the margin of the band of new bone added to the circumference of the diaphysis, for the purpose of keeping this part of the bone in proportion to the growing ends.

Further, in some of the younger bones this nutrient .. canal is seen to enter the medullary cavity close to the oldest part of the shaft. In the majority of the bones, if the canal is at the upper end of the bone, it enters the shaft proximodistally, while if at the lower end, it enters in the reverse direction, disto- proximally. At whichever end of the shaft the canal enters it will be found to run parallel to the nearest edge of new bone which is being added to the shaft (fig. 9). This holds good with all the long bones except the ulna, the foramen of which is exactly the reverse in direction, i.e. it lies near the upper end of the bone and enters disto-proximally. In this bone, however, it can be seen that the shaft is convex anteriorly and shows no layer of new bone Fig. 9. Fig. 10. on the A section Figs. 9 and 10 respectively show surface. longitudinal (fig. 3) through the directions which the nu- the anterior wall of the shaft of this bone shows that trenticnatrient canal may taketaewhewhen the layer of new bone added to the shaft is being newbone is added to the outer deposited on the internal surface, and the direction and inner aspects ofthe shaft; of the bevel at the upper and lower ends ofthis band the new bone is represented of new bone is the reverse of that met with in white. the other long bones. At the upper end the bevel slopes upwards and inwards and at the lower end downwards and inwards (fig. 10). The nutrient canal of the ulna is parallel with the bevel at the upper end and runs upwards into the bone. The band of new bone round the shaft of the diaphysis is regarded as secondary to the growth at the ends of the diaphysis (1). It keeps the thickness of the shaft in proportion to the size of the diaphysial ends. The growth of the diaphysial ends slows down with the age of the bone, so the band of new bone round the shaft requires to extend less at its margins and the margins become less acute. Now if the nutrient canal bears relationship to the margin of new bone, a change in the obliquity of the canal will occur with the age of the bone. Position ofNutrient Foramen and Direction ofNutrient Canal 509 The actual degree of obliquity of the nutrient canal has been measured in all the tibiae of the series by the following method: A line is taken through the middle of the maximum side to side diameter of each end of the diaphysis. A straight wire rod is inserted into the nutrient canal and the angle is measured between this wire and the first line (fig. 11). The measurements of the angles thus obtained are set out in Table VII. Table VII. Measurements of the angles between the long axis and nutrient canal of tibiae as described in the text. PigNo. 14 15 16 17 12 1 2 3 4 Angle 160 170 17-50 180 170 17.50 200 190 20.50

Fig. 11. To show the method of measuring the angle between the planes of the nutrient canal and the long axis of the diaphysis as described in the text. The angle is observed to increase with the age of the bone, and the greater this angle the less oblique is the nutrient canal to the long axis of the bone.

SUMMARY AND CONCLUSIONS The position of the nutrient foramen bears no relationship to the unequal growth at the diaphysial ends-it has actually been shown to approach the diaphysial extremity with the greater increment in some bones. There is a considerable amount of evidence that the foramen moves inde- pendently of diaphysial growth as shown by: 510 Carrick G. Payton (1) observations of absorption and addition of bone round the margins of the nutrient foramen; (2) measurements from a fixed point on the ulna indicating that the nutrient foramen travels distally with the increasing age of the bone; (3) the position of the nutrient foramen (plotted upon graphs in which the diaphyses can be superimposed) moving with the age of the bone, except in the case of the humerus, for which an explanation is given. The direction of the nutrient canal is not dependent upon the union of epiphyses or the unequal growth at the diaphysial extremities. It is shown that the canal follows the bevel of the edge of new bone added to the shaft. The bevel at the end of this new bone becomes blunt as the general rate of growth slows with age, and correspondingly the nutrient canal decreases in obliquity. This decrease in obliquity is not accompanied by a shortening, but by an increase in length, because, as pointed out previously(1), the absorption generally on the inside of the shaft does not balance the addition generally on the outside, a process resulting in an increase in the thickness of the wall of the shaft.

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