DIAPHYSEAL NUTRIENT FORAMINA IN HUMAN UPPER AND LOWER LIMB LONG BONES
A Thesis Submitted for the Partial Fulfillment of the Requirement for the Master Degree in Anatomy Department of Anatomy College of Medicine
By:
SAMEERA YASSIN SHAHEEN MBBS
King Saud University 2009
I
Table of contents III
Acknowledgment List of Tables
V
List of Figures
VIII
List of Diagrams
IX
Summary
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1. Introduction
1
2. Literature Review
3
2.1. Number of nutrient foramina.
3
2.2. Position of nutrient foramina.
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2.3. Size of nutrient foramina.
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2.4. Direction of nutrient foramina.
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2.5. Obliquity of nutrient foramina.
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3. Aim of the study
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4. Material and Methods
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4.1. Number. 4.2. Position.
16 17
4.2.1. Calculation of the foraminal index.
17
4.2.2. Determination of total length of bone.
17
4.2.3. Subdivisions of position of foramina according to FI. 18
II
4.3. Size.
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4.4. Direction and Obliquity.
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4.5. Photographs.
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4.6 Statistical Analysis.
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5.Results
20 5.1.Humerus.
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5.2. Radius.
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5.3.Ulna. 5.4. Femur. 5.5. Tibia. 5.6. Fibula. 6. Discussion
22 23 24 26 54
6.1. Number of Nutrient Foramina.
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6.2. Position of Nutrient Foramina.
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6.3. Size of Nutrient Foramina.
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6.4. Direction of Nutrient Foramina.
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6.5. Obliquity of Nutrient Foramina.
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6.6. Clinical Anatomy.
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7. Conclusion and Recommendation
67
8. References
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9. Arabic Summary
73
III
Acknowledgment
I would like to express my sincere appreciation to Dr. Jamila H. Elmedany, Associate Professor of Anatomy, College of Medicine, King Saud University, because she suggested this point of research and for her help and guidance throughout the study. My deepest gratitude and thanks to Dr. Ahmed Fathalla Ibrahim, Associate Professor of Anatomy, College of Medicine, King Saud University, who spared no effort to guide me on day-to-day basically since the beginning of thesis. I am very grateful to him. May God bless him with peace, health and happiness throughout his life. I am also thankful to Professor Dr. Ashry J. Mohammad for his assistance in the statistical analysis of the data. Special thanks to Dr. Hassem Darwish for his advice, information and ideas. I would like to thank Mr. Eid A. G. Abdu for his technical assistance throughout this study. I am indebted to Mr. Mohammad Khedr for his generous support and excellent assistance. I also express special thanks to Dr. Abdullah Al-Dahmash, chairman of the Department of Anatomy, College of Medicine, King Saud University. I owe particular thanks to Dr. Musaed Al-Fayez, Assistant Professor of Anatomy, College of Medicine, King Saud University, for his substantial support throughout my master study.
IV
Finally, special thanks to my husband, Dr. Abdullah M. Al-Shaier for his patience and good humour and to my parents and my family members for their encouragement for my own benefit and success.
V
List of Tables Table # 1
Number of nutrient foramina observed in the long bones of the upper limb.
2
Position and number of dominant and secondary nutrient foramina
Page 28
observed in the humerus.
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3 Position and number of dominant and secondary nutrient foramina observed in the radius.
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4 Position and number of dominant and secondary nutrient foramina observed in the ulna.
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5 Position and direction of the nutrient foramina in the long bones of the upper limb.
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6 The Range, mean and standard deviation of foraminal indices of the humerus.
33
7 The Range, mean and standard deviation of foraminal indices of the radius.
34
VI
8 The Range, mean and standard deviation of foraminal indices
9
of the ulna.
35
Number of nutrient foramina observed in the long bones of the lower limb.
36
10 Position and number of dominant and secondary nutrient foramina observed in the femur.
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11 Position and number of dominant and secondary nutrient foramina observed in the tibia.
38
12 Position and number of dominant and secondary nutrient foramina observed in the fibula.
39
13 Position and direction of the nutrient foramina in the long bones of the lower limb.
40
14 The Range, mean and standard deviation of foraminal indices of the femur.
41
VII
15 The Range, mean and standard deviation of foraminal indices of the tibia.
42
16 The Range, mean and standard deviation of foraminal indices of the fibula.
43
VIII
List of Figures Fig # 1
Page
A photograph of the anterior surface of a left humerus showing a single nutrient foramen on the anteromedial surface of the shaft.
44
2
A photograph of a shaft of a humerus showing double nutrient foramina.
45
3
A photograph of the anterior surface of a right radius showing a single nutrient foramen on the anterior surface close to the interosseous border of its shaft.
4
A photograph of the anterior surface of a right ulna showing a single nutrient foramen on the middle of the anterior surface of the shaft.
5
48
A photograph of the posterior surface of a femoral shaft showing double nutrient foramina.
7
47
A photograph of the posterior surface of a right femur showing a single nutrient foramen medial to the medial lip of linea aspera.
6
46
49
A photograph of the posterior surface of a left tibia showing a single nutrient foramen on the posterior surface midway between the interosseous border and soleal line.
8
50
A photograph of a right fibula showing double nutrient foramina on the posterior surface of its shaft lateral to the medial crest.
51
IX
List of Diagrams
Diagrams #
Page
1 Position of the nutrient foramina, irrespective of the surface on which the foramen is located, for the humerus, radius and ulna: The range given is determined from the foraminal index.
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2 Position of the nutrient foramina, irrespective of the surface on which the foramen is located, for the femur, tibia and fibula: The range given is determined from the foraminal index.
53
X
Summary
Diaphyseal Nutrient Foramina in Human Upper and Lower Limb Long Bones The aim of the present study was to study the diaphyseal nutrient foramina in human upper and lower limb long bones. The material of the present study consisted of 180 adult human long bones of the upper (30 humeri, 30 radii, 30 ulnae) and lower (30 femora, 30 tibiae, 30 fibulae) limbs. For each bone, the number, position, size, direction and obliquity of their nutrient foramina were studied. With the exception of femur, the majority of nutrient foramina in all bones studied were single in number and were secondary in size. Most of the nutrient foramina were concentrated in the middle third of the bone with the exception of tibia in which nutrient foramina were predominantly observed in its proximal third. Nutrient foramina were mostly located on the anterior surface of the shaft of bones of upper limb and on the posterior surface of the shaft of bones of lower limb. The direction of nutrient foramina followed the growing end theory, with variations in the direction observed in some fibulae. The results of the present study confirmed previous findings regarding the number and position of nutrient foramina in the long bones of the limbs and provided clinical information concerning the nutrient foramina which could be useful as reference for surgical procedures.
INTRODUCTION
1- Introduction
Bones are structures that adapt to their mechanical environment, and from a fetal age adapt to the presence of naturally occuring holes. These holes or nutrient foramina, allow blood vessels to pass through the bone cortex (Gotzen et al., 2003). The nutrient artery is the principal source of blood supply to a long bone and is particularly important during its active growth period in the embryo and fetus, as well as during the early phase of ossification (Lewis, 1956). During childhood, the nutrient arteries provide 70-80% of the interosseous blood supply to long bones: when this supply is compromised, medullary bone ischemia occurs with less vascularization of the metaphysis and growth plate (Forriol Campos et al., 1987). The diaphyseal nutrient arteries obliquely penetrate in the diaphysis of the long bones, their entrance point and angulations being relatively constant, dividing in ascending and descending branches, once they reach the medullary cavity. (Collipal et al., 2007). It has been suggested that the direction of the nutrient foramina is determined by the growing end of the bone. The growing end is supposed to grow at least twice as fast as the other end. As a characteristic, the diaphyseal nutrient vessels move away from the growth extremity dominant in the bone (Mysorekar, 1967). Variations have been described in the direction of nutrient foramina only in the lower limb bones (Longia et al., 1980). However, variations in the direction of nutrient foramina in long bones of the upper limb have never been reported.
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A considerable interest in studying nutrient foramina resulted not only from morphological, but also from clinical aspects. Nutrient foramina reflect to a certain degree the bone vascularization. Some pathological bone conditions such as developmental abnormalities, fracture healing or acute hematogenic osteomyelities are closely related to the vascular system of the bone (Skawina and Wyczolkowski, 1987). Detailed data on the blood supply to the long bones and the association with the areas of bone supplied has been continued to be a major factor in the development of new transplantation and resection techniques in orthopaedics (Kirschner et al., 1998; Kizilkanat et al., 2007). However, there is still a need for a greater understanding of the direction, location and number of nutrient foramina in bones such as the humerus, radius, ulna, femur, tibia and fibula.
LITERATURE REVIEW
3
2-Literature Review
2.1-Number of nutrient foramina Lutken (1950) studied the number of the nutrient foramina in the diaphyses of humerus and femure. He reported a single nutrient foramen in almost all of the humeri and up to triple foramina in the rest. In the femora, he reported a single foramen in half of the femora, double in 44.4% and triple in 2.19% of the bones examined. Shulman (1959) studied the number of the nutrient foramina in human radii and ulnae. He reported that a single nutrient foramen was present in almost all bones. The less had duplication of foramina (8.6%) and the least had no nutrient foramen (0.6%). Carroll (1963) examined the number of nutrient foramina in seventy-one adult humeri and observed a single nutrient foramen in two-thirds of the humeri, two foramina in 20.6% and three in 3.09% of the bones examined. Mysorekar (1967) studied the number of diaphysial nutrient foramina of long bones in upper and lower limbs. He stated that nearly half of humeri had a single nutrient foramen and the rest had more than one foramen. Regarding radii and ulnae, he observed that, in the majority, there was a single nutrient foramen, and reported few specimens with no foramina. He found that half of femora had more than one nutrient foramen, while the majority of tibiae and fibulae had a single nutrient foramen. He did not detect nutrient foramina in 3.9% of fibulae.
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Longia et al. (1980) calculated the number of nutrient foramina in the human long bones. They observed a single foramen in more than half of the humeri, two in 13% and none in 2%. Almost all of radii were observed to have a single nutrient foramen. They stated that majority of all ulnae examined had a single foramen except fewer with double and triple foramina. In the femora, they observed double nutrient foramina in less than half of specimens; the majority of tibiae and fibulae studied had a single nutrient foramen. Mckee et al. (1984) studied the number of the nutrient foramina in the shaft of the fibula and stated that the most frequent result was a single nutrient foramen. Forriol Campos et al. (1987) analyzed the number of diaphysial nutrient foramina in long bones of limbs. They found a single nutrient foramen in most of the humeri (75%) and two nutrient foramina were in the rest, while in all radii and ulnae examined they found only a single nutrient foramen. They also observed a single nutrient foramen in less than half of the examined femora. In 10% of femora, there were three nutrient foramina. They reported a single nutrient foramen in the majority of tibiae (90%), and rarely double foramina. However, a single nutrient foramen was observed in all fibulae examined. Sendemir and Cimen (1991) examined the number of the diaphysial nutrient foramina of the lower limb bones. They observed that 46% of the femora had two nutrient foramina. They reported individual femora having as many as six, eight and nine nutrient foramina on their shafts which were dominant in size. One nutrient foramen was almost constant in the tibia; only 5.2% had foramina. They observed
5
a single nutrient foramen in 74% of the fibulae and reported the absence of nutrient foramina in 18.9% of specimens examined. Nagel (1993) recorded the number of the nutrient foramina of human long bones and described the clinical relevance of avoiding injury to the nutrient artery during operative procedures. In the majority of humeri (80%), he found a single nutrient foramen; double foramina in remaining. He recorded a single nutrient foramen in all radii and ulnae and reported that there were double nutrient foramina in 80% of femora examined. In 10% of the femora, a single foramen was located while triple foramina were identified in the other 10%. There was a single nutrient foramen in almost all of the tibiae examined. Gumusburun et al. (1994) studied the number of nutrient foramina in human lower limb long bones. They stated that 60% of femora had more than one foramen and the rest had a single nutrient foramen. They reported individual femora having five, or six nutrient foramina. The majority of tibiae examined had a single nutrient foramen. They stated that fibula with a single foramen was the commonest. Skawina et al. (1994) investigated the number of nutrient foramina present in the humerus and femur. The majority of the investigated bones had a single nutrient foramen. Occasionally, double foramina were observed in humerus and double or triple nutrient foramina in the femur. Bridgeman and Brookes (1996) found double nutrient foramina in 53.2% of femora examined and one foramen in the remaining bones.
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Gumusburun et al. (1996) studied the number of the nutrient foramina on the fibulae and reported that almost all fibulae had a single nutrient foramen. They also noticed the absence of nutrient in 3.9% of fibulae examined. Al-Motabagani (2002) studied the arterial supply of the femoral diaphysis. He noticed that femora had a single nutrient foramen as equal as those having double foramina. He also noticed that, in four cases, nutrient foramina were absent. Collipal et al. (2007) investigated the number of diaphyseal foramina in the lower limb long bones. They found double nutrient foramina in more than half of the femora (52%), and a single nutrient foramen in the rest. The majority of the nutrient foramina of tibiae had a single nutrient foramen. In the fibula, they found that three quarters of the bones presented with a single nutrient foramen. Kizilkanat et al. (2007) studied human long bones of the upper and lower limbs to determine the number of their nutrient foramina. They reported a single foramen in almost all the studied humeri. The greatest number of radii and ulnae were observed to have a single nutrient foramen. Regarding all long bones of lower limbs, they observed that the majority had a single nutrient foramen. 2.2-Position of the nutrient foramina Payton (1934) observed that the position of the nutrient foramen beared no relationship to the unequal growth at the diaphyseal ends, and reported remarkable evidence that the foramen moved independently of the growth of the diaphysis. And reported that the vessels which occupy the nutrient canal are derived from those that
7 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. Lutken (1950) stated that the position of the nutrient foramina on the shaft of the humeri was so variable that he could not determine a typical one. In the femur, he observed that the majority of the foramina were found in the proximal half of the linea aspera. Shulman (1959) studied the position of nutrient foramina in radius and ulna. He reported that the majority of nutrient foramina were on the anterior surface of the shaft of the radius while less than half of nutrient foramina were on the proximal third the radial shaft. Regarding the ulna, he stated that the majority of foramina were found in the proximal half of the diaphysis with a low incidence within its proximal third. Carroll (1963) examined the position of the nutrient foramina of the humeral diaphysis and found that most of them were concentrated on the medial aspect of the distal half of the middle third of the shaft. Mysorekar (1967) had studied the position of diaphyseal nutrient foramina of long bones of limbs. He observed that the nutrient foramina of the humerus were present just below the middle of the bone and reported that they were almost equally distributed on the anteromedial surface and on the medial border. In both radius and the ulna, more than half of foramina were located in the middle third of the bones, especially on the anterior surface of the diaphysis. He pointed out that, in the femur, the nutrient foramina were restricted to the linea aspera or adjacent zones, locating
8 itself in the middle third of the bone. He also stated that all nutrient foramina in the tibia were above the middle of the bone and particularly in the upper third. Regarding the fibula, almost all the foramina were observed on the medial crest in the middle third of the bone. Longia et al. (1980) studied the position of the nutrient foramina of long bones. They observed that 90.99% of the foramina were located in the middle third of the shaft of humerus and reported that most of them were on the medial part of the anteromedial surface. In the majority of radii, the foramina were located on the anterior surface of middle third of the shaft. They stated that the nutrient foramina in the ulna were found more in the proximal third than in the middle third of the bone and were located most frequently on the middle of the anterior surface of the ulnae. Regarding the femur, they reported that nearly half of the nutrient foramina were in the middle third of the shaft and was restricted to the linea aspera or adjacent zones. In most of the tibiae, the foramina were in the proximal third lateral to the vertical line, and in fibulae 85.19% of the foramina were located in the middle third of its shaft. Mckee et al. (1984) studied the position of the nutrient foramina in fibulae and observed that almost all the fibular foramina were located in the middle third of the bone and were distributed mainly on its posterior surface either on the medial crest or on the medial surface of the fibula. Forriol Campos et al. (1987) described the position of the diaphysial nutrient foramina in human long bones. They stated that the nutrient foramina of the upper extremity were located closer to the elbow than the shoulder or wrist and they were
9 placed on the anteromedial surface of the humeral diaphysis in 80% of the bones, less often on the posterior surface. They reported that most of the nutrient foramina in radial bones were located closer to the elbow than the wrist. They added that all the nutrient foramina were located on the anterior surface of the shaft. Regarding the ulna, they reported that all the foramina were on the anterolateral surface of the bone. In the femora, they stated that the nutrient foramina were closer to the hip. The nutrient foramina in tibiae were situated at the junction of the proximal and middle third of the bone, and were always distal to the soleal line in the posterior surface of the bone. In fibulae, most of the foramina were in the middle third of the bone with an equal distribution of the foramina on the medial and posterior surfaces. Sendemir and Cimen (1991) examined the position of the diaphysial nutrient foramina of the human lower limb long bones. They pointed out that the nutrient foramina of the femur were almost distributed equally on the linea aspera and the medial lip. In the tibiae, the nutrient foramina were concentrated on the posterior surface, with few foramina on the lateral surface of the tibia. They also observed that most of the nutrient foramina were on the medial surface of the fibula, less on the posterior and on the lateral surfaces. Nagel (1993) recorded the point of nutrient artery entrance to the bony surface of human long bones. He stated that the majority of the radial and ulnar foramina were located in the proximal third of the bone. He reported that the entrance to the femoral diaphysis in all cases was posteriorly along the linea aspera. He also stated that, in all specimens of studied tibia, the foramina were located posterolaterally.
10 Gumusburun et al. (1994) studied the position of the diaphysial nutrient foramina of the lower limbs. They reported that more than half of the foramina in the femur were found on linea aspera and its medial and lateral lips. In tibia 77% of nutrient foramina were in the upper third, 46% in the middle third but no foramen was observed in the lower third. The majority of the foramina were observed on the posterior surface of the bone. They reported that 92.3% of the fibular foramina were in the middle third of the bone and that the foramina were seen primarily on the posterior surface and secondarily on the medial crest of the bone. Gumusburun et al. (1996) studied the location of the nutrient foramina on the fibulae and reported that the foramina were seen primarily on the posterior surface and secondarily on the medial crest of the bone. Most of the foramina were in the middle third of the shaft of the fibula. Collipal et al. (2007) investigated the location of the diaphyseal nutrient foramina in the lower limb long bones. The nutrient foramina of the femur were located in the linea aspera in more than half of specimens. The nutrient foramina of the tibiae were found under the soleal line in the proximal third of the bone. In the fibula, the most frequent location of nutrient foramina being in the middle third of the posterior surface of the bone. Kizilkanat et al. (2007) studied the position of nutrient foramina in human long bones of upper and lower limbs. They observed that 62.3% of the nutrient foramina were located on the anteromedial surface of the humerus. They reported that the radial nutrient foramina were generally located on the anterior aspect in 98.1% of radii; and
11 that the majority of nutrient foramina of ulna were lying on the anterolateral surface of the bone. In both, radius and ulna, the foramina were limited to the proximal half of the diaphysis. They pointed out that, in the femur, the nutrient foramina were restricted to the linea aspera or adjacent zones, locating themselves to the middle third of the bone. They added that most of the tibial foramina were on the posterior surface of the middle third of the shaft, while the nutrient foramina of the fibula were limited to the posterior surface of the bone. 2.3-Size of nutrient foramina Carroll (1963) mentioned that about one-third of the nutrient foramina in the humerus belonged to the dominant type. A significantly greater proportion of large foramina were demonstrated on the right side. Also, he noticed no dominant foramina were found in the proximal third of the shaft of the humerus. Longia et al. (1980) observed in their studies on the size of nutrient foramina of long bones of upper and lower limbs, that most of the foramina were of the dominant type. Mckee et al (1984) stated that the size of the foramina in the fibula was variable and 44.6% of the foramina were dominant. Bridgeman and Brookes (1996) and Al-Motabagani (2002) examined the nutrient arteries of the diaphysis of the aging human femur and stated that nutrient foramina in the same bones were not necessarily equal in size. Such observation was also applicable to the sizes of their nutrient arteries.
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Kizilkanat et al. (2007) stated that in all cases where a single nutrient foramen in a long bone was noticed, it was always dominant. 2.4-Direction of nutrient foramina Berard (1835) was the first to correlate the direction of the nutrient canals with the mode of bone’s ossification and growth. Humphrey (1861) was the first to offer an explanation for the variations in direction of the nutrient foramina in long bones. Schwalbe (1876) and Langer (1876) discussed and worked out on Humphrey’s theory stating that the direction of the canals was determined by the tension of the periosteum produced by the longitudinal growth of the diaphysis. Digby (1916) suggested that by a change in the direction of the nutrient artery at its origin, the obliquity of the nutrient canal might be decided and the form of their surrounding tissues might be determined. Harris (1933) put forward the theory that the nutrient foramen had a constant position during the growth of the bone. Payton (1934) stated that the direction of the nutrient canal was not dependent upon the union of epiphyses or the unequal growth at the diaphysial extremities. Lutken (1950) findings proved that Harris conception could not be maintained and that the theory of external resorption during growth could not depend on it.
13 Shulman (1959) studied the direction of the nutrient foramina in radii and ulnae and found that all were directed towards the elbow. Hughes (1952) found anomalous canals most frequently in the femur. He attributed this to the unequal arterial growth of an artery close to a long bone. However, Mysorekar (1967) studied human long bones and found anomalous directed canals only in the fibula. He attributed this to the peculiar ossification pattern in that bone. Patak and Mysorekar (1977) stated that the direction of the foramen was always away from the growing end, thus favoring the growing end theory. Longia et al. (1980) found anomalous canals in femora, tibiae and fibulae. 2.5- Obliquity of nutrient foramina Humphrey (1861) demonstrated 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. Piollet (1905) stated that, in the human foetus, the nutrient arteries were directed first perpendicularly to the long axis of the bone and then later all proceeded distally in the bone. In the adult all the arteries were found directed away from the growing ends. Digby (1916) measured the diaphyseal growth in the proximal and distal directions and assumed that the obliquity of the nutrient canals resulted from the fact that whilst
14 a bone grew in length chiefly from one end, the vessel from which the nutrient artery arose, grew equally throughout its length. The nutrient canal always pointed towards the oldest part of the shaft of a long bone. Payton (1934) observed that a change in the obliquity of the canal would occur with the age of the bone. He stated that as the general rate of growth decreased with age, the nutrient canal decreased in obliquity. This decrease was not accompanied by shortening, but by an increase in length. Mysorekar (1967) and Longia et al. (1980) studied the obliquity of nutrient foramina in long bones of limbs and observed that there was no change in the obliquity of the foramina, whether they were in the centre of the bone or nearer to the ends. Bridgeman and Brookes (1996) studied the obliquity of femoral nutrient foramina and found that they always pointed proximally, and related this to the rate of osteogenesis being faster at the lower growth cartilage. Al-Motabagani (2002) stated that the femoral nutrient foramina pointed obliquely upwards as it lay away from the faster growing lower end.
AIM OF THE STUDY
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3-Aim of the study
The aim of the present study is:
1- Determination of the number and position of the nutrient foramina in the human upper and lower limb long bones. 2- Determination of the size, the direction and the obliquity of the nutrient canals running from them.
MATERIAL AND METHODS
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4- Material and Methods
The material of the present study consisted of 180 adult human cleaned and dried bones of the upper and lower limbs. They were divided into six groups 30 bones of each. They were obtained from the osteology collection held in the Department of Anatomy, Faculty of Medicine, King Saud University. The groups were arranged as follows: Group 1: 30 humeri. Group 2: 30 radii. Group 3: 30 ulnae. Group 4: 30 femora. Group 5: 30 tibiae. Group 6: 30 fibulae.
All selected bones were normal with no appearance of pathological changes. The specific age and sex characteristics of the bones studied were unknown. The nutrient foramina were observed in all bones with the help of a hand-lens. They were identified by their elevated margins and by the presence of a distinct groove proximal to them. Only well-defined foramina on the diaphysis were accepted. Foramina at the ends of the bone were ignored. The following data were studied on the diaphyseal nutrient foramina of each bone:
4.1.Number: Bones were examined for the number of nutrient foramina.
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4.2.Position: 4.2.1. Calculation of the foraminal index: The position of all nutrient foramina was determined by calculating a foraminal index (FI) using the formula: FI = (DNF/TL) x 100
(Hughes, 1952; Shulman, 1959).
DNF = the distance from the proximal end of the bone to the nutrient foramen. TL = total bone length.
4.2.2. Determination of the total length of bone: Determination of the total length of the individual bone was taken as follows: - Humerus: the distance between the proximal margin of the head of the humerus and the most distal aspect of trochlea. - Radius: the distance between the most proximal margin of the head of the radius and the tip of the radial styloid process. - Ulna: the distance between the most proximal margin of the olecranon and the tip of the ulnar styloid process. - Femur: the distance between the proximal aspect of the head of the femur and the most distal aspect of the medial condyle. - Tibia: the distance between the proximal margin of the medial condyle and the tip of the medial malleolus.
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- Fibula: the distance between the apex of the head of the fibula and the tip of the lateral malleolus.
4.2.3. Subdivisions of position of foramina according to FI : The position of the foramina was divided into three types according to FI as follow: Type 1: FI up to 33.33, the foramen was in the proximal third of the bone. Type 2: FI from 33.33 up to 66.66, the foramen was in the middle third of the bone. Type 3: FI above 66.66, the foramen was in the distal third of the bone.
All measurements were taken to the nearest 0.1 mm using an INOX sliding caliper (Kizilkanat et al, 2007).
4.3.Size: Nutrient foramina smaller than the size of 24 hypodermic needle (0.56 mm in diameter) were considered as being secondary nutrient foramina (S.F) while those equal or larger were accepted as being dominant nutrient foramina (D.F) (Kizilkanat et al; 2007).
4.4.Direction and Obliquity: A fine stiff wire was used to confirm the direction and obliquity of the foramen.
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4.5.Photographs: Photographs were taken by a cannon digital camera (12 mega pixels). Each photograph had a definition of 16x12 cm.
4.6.Statistical analysis: The results were analyzed and tabulated using the Statistical Package of Social Sciences (SPSS) 8.0 windows. The range, mean and standard deviation of FI were determined.
RESULTS
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5-Results
5.1. HUMERUS (Figs. 1&2) 5.1.1. Number:
In the whole series of 30 humeri examined, 18(60%) had a single foramen, 10(33.3%) had double foramina and 2(6.6%) had three foramina (Table-1).
5.1.2. Position:
The nutrient foramina were located along the whole middle third of the humerus with the foramen index ranging between 33 and 68.68% of the bone length (Table-6; Diagram-1). Of the total 44 foramina, 2(4.5%) were in the proximal third (Type-1), 40(90.9%) in the middle third (Type-2), and 2(4.5%) were in the distal third (Type-3) (Table-5). Of all humeral foramina, 26(59.09%) were on the anteromedial surface, 7(15.9%) on the medial border, 6(13.6%) on the posterior surface close to the lateral border, 3(6.8%) on the middle of the posterior surface and 2(4.5%) on the posterior surface close to the medial border (Table - 2).
5.1.3. Size:
Of the 44 foramina, 11(25%) were dominant and 33(75%) were secondary foramina (Table -2).
21 5.1.4. Direction:
The nutrient foramina in all humeri examined were directed distally (Table-5; Fig.1).
5.1.5. Obliquity:
There was no change in the obliquity of the foramina, whether they were in the centre of the bone or nearer to the ends.
5.2. RADIUS (Fig.3) 5.2.1. Number:
In the whole series of 30 radii examined, (100%) had a single nutrient foramen (Table-1).
5.2.2. Position:
The total 30 foramina were located closer to the elbow than to the wrist with the foramen index ranging between 27.82 and 48.57% of the bone length (Table-7; Diagram-1). Of the total 30 foramina, 13(43.3%) were in the proximal third (Type-1), and 17(56.6%) in the middle third (Type-2). There were no foramina in the distal third (Type-3) (Table-5). Of all radial foramina, 10(33.3%) were on the anterior surface midway between the interosseous and anterior borders, 10(33.3%) on the anterior surface closer to anterior border, 7(23.3%) on the anterior surface closer to the interosseous border and 3(10%) on the posterior surface closer to the interosseous border (Table-3).
22 5.2.3. Size:
Of the 30 foramina, 6(20%) were dominant and 24(80%) were secondary foramina (Table-3).
5.2.4. Direction:
The nutrient foramina in all radii examined, were directed proximally (Table-5; Fig.3).
5.2.5. Obliquity:
There was no change in the obliquity of the foramina, whether they were in the centre of the bone or nearer to the ends.
5.3. ULNA (Fig.4) 5.3.1. Number:
In the whole series of 30 ulnae examined 28(93.3%) had a single nutrient foramen, 2(6.6%) had double foramina (Table-1).
5.3.2. Position:
The nutrient foramina were located closer to the elbow than to the wrist with the foramen index ranging between 27.00 and 47.59% of the bone length (Table-8; Diagram-1). Of the total 32 foramina, 12(37.5%) were in the proximal third (Type-1) and 20(62.5%) in the middle third (Type-2). There were no foramina in the distal third (Type-3) (Table-5). Of all ulnae foramina, 18 (56.2%) were on the anterior surface
23 closer to the anterior border, 9(28.12%) on the anterior surface closer to the interosseous border and 5(15.6%) on the middle of the anterior surface (Table-4).
5.3.3. Size:
Of the 32 foramina, 12(37.5%) were dominant and 20(62.5%) were secondary foramina (Table-4).
5.3.4. Direction:
The nutrient foramina of all ulnae examined, were directed proximally (Table-5; Fig.4).
5.3.5. Obliquity:
There was no change in the obliquity of the foramina, whether they were in the centre of bone or nearer to the ends.
5.4. FEMUR (Fig.5) 5.4.1. Number:
In the whole series of 30 femora examined, 12(40%) had a single foramen and 18(60%) had double foramina (Table-9).
5.4.2. Position:
The nutrient foramina were located along the middle third of the femur with the foramen index ranging between 29.81 and 62.65% of the bone length (Table-14;
24 Diagram-2). Of the total 48 foramina, 8(16.6%) were in the proximal third (Type-1) and 40(83.3%) in the middle third (Type-2). There were no foramina in the distal third (Type-3) (Table-13). Of all femoral foramina, 12(25%) were on the medial lip of the linea aspera, 9(18.75%) on the lateral lip of linea aspera, 8(16.6%) on the posteromedial surface, 7(14.5%) between the two lips of linea aspera. 6(12.5%) on the gluteal tuberosity, 4(8.3%) medial to spiral line and 2(4.16%) on the posterolateral surface (Table-10).
5.4.3. Size:
Of the 48 foramina, 35(72.9%) were dominant and 13(27.08%) were secondary foramina (Table-10).
5.4.4. Direction:
The nutrient foramina in all femora examined, were directed proximally (Table-13; Fig.5).
5.4.5. Obliquity:
There was no change in the obliquity of the foramina, whether they were in the centre of the bone or nearer to the ends.
5.5. TIBIA (Fig.7) 5.5.1. Number:
The whole series of 30 tibiae examined had a single nutrient foramen (Table-9).
25 5.5.2. Position:
The nutrient foramina were situated with the foramen index ranging between 26.49 and 35.54% of the bone length (Table-15; Diagram-2). Of the total 30 foramina, 27(90%) were in the proximal third (Type-1) and 3(10%) were in the middle third (Type-2). There were no foramina in the distal third (Type- 3) (Table13). All foramina were located on the posterior surface of the tibiae, 19(63.3%) were closer to the interosseous border, 9(30%) were midway between interosseous border and soleal line and 2(6.66%) were on the posterior surface closer to the soleal line (Table-11).
5.5.3. Size:
Of the 30 foramina, 11(36.6%) were dominant and 19(63.33%) were secondary foramina (Table-11).
5.5.4. Direction:
The nutrient foramina of all tibiae examined, were directed distally (Table-13; Fig.7).
5.5.5. Obliquity:
There was no change in the obliquity of the foramina, whether they were in the center of the bone or nearer to the ends. Compared to those on femur and fibula, the nutrient foramina of the tibia appeared to be the most vertically located foramina (Fig.7).
26
5.6. FIBULA (Fig.8) 5.6.1. Number:
Out of 30 fibulae examined, 24(80%) showed a single foramen while 6(20%) possessed double foramina (Table-9).
5.6.2. Position:
The nutrient foramina of fibulae were situated in the middle third of the bone with a foramen index ranging between 35.17 and 67.78% of the bone length (Table16; Diagram-2). Of the total 36 foramina, 35(97.2%) existed in the middle third (Type-2) and 1(2.7%) were in the distal third (Type-3). There were no foramina in the proximal third (Type-1) (Table-13). Of the whole fibular foramina, 24(66.6%) were on the medial crest of the posterior surface, 11(30.5%) on the posterior surface between medial crest and interosseous border and 1(2.7%) on lateral surface (Table12).
5.6.3. Size:
Of all fibular foramina, 4(11.1%) were dominant foramina while 32(88.8%) were secondary (Table-12).
5.6.4. Direction:
Of the total 36 nutrient foramina observed in the fibulae, 28 (77.71%) was directed distally; while the direction of 8(22.2%) was proximally (Tabe-13; Fig.8).
27 5.6.5. Obliquity:
There was no change in the obliquity of the foramina, whether they were in the centre of bone or nearer to the ends.
28
Table – 1:
Number of nutrient foramina observed in the long bones of the upper limb.
Bone
Humerus (n=30)
Radius (n=30)
Ulna (n=30)
Number of bone
Number of Foramina
Percentage
18
1
60%
10
2
33.3%
2
3
6.6%
30
1
100%
28
1
93.3%
2
2
6.66%
29
Table – 2: Position and number of dominant (DF) and secondary (SF) nutrient foramina observed in the humerus.
Position
Anteromedial surface
Total number of foramina
Number of foramina %
Single
Two
Three
DF
SF
DF
SF
DF
SF
26
59.09
5
9
2
6
-
4
3
6.8
-
-
1
2
-
-
2
4.5
-
-
-
1
-
1
6
13.6
-
-
-
5
-
1
7
15.90
3
1
-
3
-
-
Posterior surface ( in the middle of surface ) Posterior surface ( close to medial border ) Posterior surface ( close to lateral border ) Medial border
30
Table – 3: Position and number of dominant (DF) and secondary (SF) nutrient foramina observed in the radius.
Position
Total number of foramina
%
10
Number of foramina Single
Two
Three
DF
SF
DF
SF
DF
SF
33.3
1
9
-
-
-
-
7
23.3
2
5
-
-
-
-
10
33.3
3
7
-
-
-
-
3
10
-
3
-
-
-
-
Anterior surface ( midway between interosseous and anterior borders )
Anterior surface ( close to interosseous border )
Anterior surface ( close to anterior border )
Posterior surface ( close to interosseous border )
31
Table – 4: Position and number of dominant (DF) and secondary (SF) nutrient foramina observed in the ulna.
Number of foramina Position
Anterior surface
Total number of foramina
%
Single
Two
Three
DF
SF
DF
SF
DF
SF
5
15.6
3
2
-
-
-
-
9
28.12
2
5
-
2
-
-
18
56.2
7
9
-
2
-
-
( in the middle of surface )
Anterior surface ( close to interosseous border )
Anterior surface ( close to anterior border )
32
Table – 5: Position and direction of nutrient foramina in the long bones of the upper limb.
Position
Bone
Direction
Type-1
Type-2
Type-3
Humerus
2(4.5%)
40(90.9%)
2(4.5%)
Distally
Radius
13(43.3%)
17(56.6%)
–
Proximally
Ulna
12(37.5%)
20(62.5%)
–
Proximally
33
Table – 6: The range, mean ± standard deviation (SD) of foraminal indices of the humerus.
Position
Side
Range
Mean ± SD
Anteromedial surface
R
50.18 – 63.38
56.72 ± 4.30
L
49.06 – 67.35
57.27 ± 5.13
Posterior surface
R
36.14 – 42.44
39.29 ± 4.45
( in the middle of surface )
L
–
–
Posterior surface
R
(close to lateral border)
L
38.45 – 44.56
41.34 ± 2.34
R
53.59 – 68.68
59.85 ± 5.85
L
55.33 – 56.21
55.77 ± 0.62
–
–
Medial border
34
Table – 7: The range, mean ± standard deviation (SD) of foraminal indices of the radius.
Position
Side
Range
Mean ± SD
Anterior surface
R
29.95 – 43.92
34.51 ± 5.2
L
29.68 – 48.57
39.13 ± 13.36
Anterior surface
R
34.45 – 37.10
35.34 ± 1.51
(close to interosseous border)
L
30.80 – 38.78
35.78 ± 3.54
Anterior surface
R
31.81 – 35.94
34.02 ± 1.47
(close to anterior border)
L
27.82 – 32.63
30.00 ± 1.99
Posterior surface
R
31.22 – 38.13
34.67 ± 4.88
(close to interosseous border)
L
_
–
( in the middle of surface )
35
Table – 8: The range, mean ± standard deviation (SD) of foraminal indices of the ulna.
Position
Side
Range
Mean ± SD
Anterior surface
R
38.13 – 47.59
42.54 ± 4.76
L
35.93 – 46.74
41.3 ± 7.6
Anterior surface
R
27.00 – 45.62
37.42 ± 6.91
(close to interosseous border)
L
31.31 – 45.05
40.38 ± 7.86
Anterior surface
R
27.90 – 40.17
33.58 ± 3.48
(close to anterior border)
L
31.39 – 36.12
33.59 ± 1.85
( in the middle of surface )
36
Table – 9: Number of nutrient foramina observed in the long bones of the lower limb.
Bone
Number of bone
Number of Foramina
Percentage
Femur (n = 30)
12
1
40%
18
2
60%
30
1
100%
24
1
80%
6
2
20%
Tibia (n = 30)
Fibula (n = 30)
37
Table – 10: Position and number of dominant (DF) and secondary (SF) nutrient foramina observed in the femur.
Position
Total number of foramina
Number of foramina %
Single foramen
Two foramina
DF
SF
DF
SF
Between the two lips of linea 7
14.5
3
–
4
–
Medial lip of linea aspera
12
25
2
–
5
5
Lateral lip of linea aspera
9
18.75
4
–
5
–
Posteromedial Surface
8
16.6
1
–
3
4
Posterolateral Surface
2
4.16
–
–
2
–
Medial to spiral line
4
8.3
1
–
1
2
Gluteal tuberosity
6
12.5
1
–
3
2
aspera
38
Table – 11: Position and number of dominant (DF) and secondary (SF) nutrient foramina observed in the tibia.
Number of foramina Position
Total number of foramina
%
Single foramen DF SF
Two foramina DF SF
Posterior surface (midway between interosseous
9
30
2
7
–
–
19
63.3
8
11
–
–
2
6.66
1
1
–
–
border and soleal line) Posterior surface (closer to the interosseous border). Posterior surface (closer to soleal line).
39
Table – 12: Position and number of dominant (DF) and secondary (SF) nutrient foramina observed in the fibula.
Position
Posterior surface
Total number of foramina
Number of foramina %
Single foramen
Two foramina
DF
SF
DF
SF
24
66.66
1
19
2
2
11
30.55
–
4
–
7
(on the medial crest )
Posterior surface (between medial crest and interosseous border) – Lateral surface
1
2.77
–
–
1
40
Table – 13: Position and direction of nutrient foramina in the long bones of the lower limb.
Position
Bone
Direction
Type-1
Type-2
Type-3
8(16.6%)
40(83.3%)
–
Tibia
27(90%)
3(10%)
–
Fibula
–
35(97.2%)
1(2.7%)
Femur
Proximally
Distally
28 distally 8 proximally
41
Table – 14: The range, mean ± standard deviation (SD) of foraminal indices of the femur.
Position
Between the two lips of linea aspera
Side
Range
Mean ± SD
R
36.06 – 62.65
46.00 ± 11.55
L
37.09 – 38.49
37.63 ± 00.75
R
37.37 – 60.38
52.54 ± 9.48
L
44.05 – 59.17
54.93 ± 7.27
R
35.30 – 61.14
46.25 ± 10.16
L
35.87 – 51.53
41.70 ± 8.55
R
45.20 – 59.06
55.47 ± 5.81
L
55.11 – 60.67
57.18 ± 3.03
R
29.81 – 31.90
31.12 ± 00.91
L
–
–
R
31.73 – 34.25
33.07 ± 1.26
L
31.87 – 37.31
34.06 ± 2.87
Medial lip of linea aspera
Lateral lip of linea aspera
Posteromedial Surface
Medial to spiral line
Gluteal tuberosity
42
Table – 15: The range, mean ± standard deviation (SD) of foraminal indices of the tibia.
Position
Side
Range
Mean ± SD
Posterior surface
R
27.95 – 31.52
29.47 ± 1.43
( Midway between interosseous border and soleal line)
L
27.82 – 34.17
31.24 ± 2.62
Posterior surface
R
28.53 – 32.17
30.25 ± 1.45
(closer to interosseous border)
L
26.49 – 35.54
30.56 ± 3.06
43
Table – 16: The range, mean ± standard deviation (SD) of foraminal indices of the fibula.
Position
Side
Range
Mean ± SD
Posterior surface
R
35.17 – 61.77
44.99 ± 8.04
L
36.31 – 50.15
43.17 ± 4.05
Posterior surface
R
36.08 – 65.38
52.71 ± 13.00
(between medial crest and
L
40.25 – 67.78
55.02 ± 12.74
(on the medial crest)
interosseous border)
44
Fig.1: A photograph of the anterior surface of a left humerus showing a single nutrient foramen (NF) on the anteromedial surface of the shaft. The foramen is located in the middle third of the bone (Type-2) and is directed downward.
45
Fig.2: A photograph of a shaft of a humerus showing double nutrient foramina (NF). Both foramina are directed downward.
46
Fig.3: A photograph of the anterior surface of a right radius showing a single nutrient foramen (NF) on the anterior surface close to the interosseous border of its shaft. The foramen is located in the middle third of the bone (Typ-2) and is directed upward.
47
Fig.4: A photograph of the anterior surface of a right ulna showing a single nutrient foramen (NF) on the middle of the anterior surface of the shaft. The foramen is located in the middle third (Type-2) and is directed upward.
48
Fig.5: A photograph of the posterior surface of a right femur showing a single nutrient foramen (NF) medial to the medial lip of linea aspera (ML). The foramen is located at the proximal third (Type-1) and is directed upward.
49
Fig.6: A photograph of the posterior surface of a femoral shaft showing double nutrient foramina (NF). Both foramina are directed upwards as shown by the needles inserted. The upper foramen is located between the two lips of linea aspera; the lower foramen is located on the medial lip (ML). (LL): lateral lip of linea aspera.
50
Fig.7: A photograph of the posterior surface of a left tibia showing a single nutrient foramen (NF) on the posterior surface midway between the interosseous border (IB) and soleal line (SL). The foramen is located in the proximal third (Type-1) and is directed downward.
51
Fig.8: A photograph of a right fibula showing double nutrient foramina (NF) on the posterior surface of its shaft lateral to the medial crest (MC). Both foramina are located in the middle third (Type-2); the upper foramen is directed downward while the lower foramen is directed upward as shown by the needles inserted.
52
53
DISCUSSION
54
6. Discussion
6.1. Number of Nutrient Foramina: In the present study, a single nutrient foramen has a higher percentage (60%) in the humeral bones, compared to that of double (33.3%) and triple foramina (6.6%) respectively. Many studies reported a percentage approximately similar to that of the present result (Lutken, 1950; Carroll, 1963; Mysorekar, 1967; Forriol Campos et al., 1987). Other studies reported a higher percentage of a single nutrient foramen (8088%) (Longia et al., 1980; Nagel, 1993; Kizilkanat et al., 2007).The range of occurrence of double foramina varied from 13% (Longia et al., 1980) to 42% (Mysorekar, 1967). According to Kizilkanat (2007), the percentage of occurrence of triple foramina in the humeri did not exceed 1-7%. The latter observations were in accordance to those reported in the present study. Moreover, Kizilkanat et al. (2007) reported the presence of four nutrient foramina in 1% of the humeri studied. Such number was not observed in the present study. On the other hand, the absence of nutrient foramina in some humeri was also reported by other authors (Lutken, 1950; Patake et al., 1977; Longia et al., 1980; Kizilkanat et al., 2007) they stated that in such cases, the periosteal vessels were entirely responsible for the blood supply of the bone. In the present study all the radii examined had a single nutrient foramen. The same finding was reported by Forriol Campos et al. (1987) and Nagel (1993). In other studies, the majority of radii (more than 90%) were found to possess a single nutrient
55 foramen (Shulman, 1959; Mysorekar, 1967; Longia et al., 1980; Kizilkanat et al., 2007). In such studies, radii possessing double nutrient foramina were also observed. Furthermore, Shulman (1959) reported the absence of nutrient foramina in 1.2% of radii examined. In the present study 93.3% of ulnae examined had a single nutrient foramen. Double nutrient foramina were observed in the rest of the ulnae examined. With the exception of Nagel (1993) who recorded a single nutrient foramen in all specimens examined, other authors reported a single nutrient foramen in more than 91% of ulnae (Shulman, 1959; Mysorekar, 1967; Longia et al., 1980; Forriol Campos et al., 1987; Kizilkanat et al., 2007). Furthermore, Longia et al. (1980) observed three nutrient foramina in 1% of ulnae examined, while Shulman (1959) and Mysorekar (1967) reported the absence of nutrient foramina in 0.6% and 1.1% of ulnae, respectively. In this study, 60% of the femora examined possessed double nutrient foramina, while 40% had only one nutrient foramen. In the previous literatures, a discrepancy was noticed regarding the number of nutrient foramina in the femora. Many authors stated that the majority of femora studied had double nutrient foramina (Mysorekar, 1967; Forriol Campos et al., 1987; Nagel, 1993; Gumusburun et al., 1994; Collipal, 2007), while others reported the presence of a single foramen in most specimens (Lutken, 1950; Laing, 1953; Longia et al., 1980; Sendemir and Cimen, 1991; Motabagani, 2002; Kizilkanat et al., 2007). Three nutrient foramina were observed in a small number of femora (2.19% - 10.7%) by many authors (Lutken, 1950; Longia et al., 1980; Forriol Campos et al., 1987; Nagel, 1993; Gumusburun et al., 1994;
56 Collipal, 2007). It was interesting to find studies reporting a number of nutrient foramina as high as six (Gumusburun et al., 1994) and up to nine (Sendemit and cimen, 1991), while others confirmed the absence of nutrient foramina in some femora (Mysorekar, 1967; Gumusburun et al., 1994; Motabagoni, 2002). In this study, the whole series of tibiae examined had a single nutrient foramen. Previous studies reported the presence of a single nutrient foramen in at least 90% of the tibiae. But, in contradiction with the present results, they also reported the presence of double nutrient foramina in some of the tibiae (Mysorekar, 1967; Longia et al., 1980; Forriol et al., 1987; Sendemir and Cimen, 1991; Nagel, 1993; Gumusburun et al., 1994; Collipal et al., 2007). It was interesting to notice that, in the present study, both the preaxial bones of the limbs, namely radius and tibia, possessed only a single nutrient foramen. Further studies will be needed to clarify such observations. In the fibulae studied, 80% of the bones presented a single nutrient foramen, while 20% of the bones possessed double nutrient foramina. Similar data had been reported by Mysorekar (1967), Longia et al. (1980), Guo (1981), Mckee et al. (1984), Forriol Campos et al (1987) and Sendemir and Cimen (1991), while Mckee et al. (1984) reported fibulae with three nutrient foramina. On the other hand, Mysorekar (1967), Mckee et al. (1984), Gumusburun et al. (1994) and Kizilkanat et al. (2007) reported fibulae with no nutrient foramina. 6.2. Position of Nutrient Foramina: In this study, 90.9% of the nutrient foramina were located along the whole middle third of the humerus, with the foramen index ranging between 33% and 68.68% of the bone length. In accordance with the present results, previous studies reported the
57
position of the nutrient foramina within the middle third of the bone (Carroll, 1963; Mysorekar, 1967; Longia et al., 1980; Forriol Campos et al., 1987; Nagel, 1993; Kizilkanat et al., 2007). In this study, 60% of all humeral nutrient foramina were observed on the anteromedial surface of the bone. Similar findings had been reported by Carroll (1963), Longia et al. (1980), Forriol Campos et al. (1987) and Kizilkanat et al. (2007). On the other hand, Mysorekar (1967) reported an equal percentage of foramina on both the anteromedial surface and the medial border. The site of entrance of the main artery into the humerus makes it vulnerable to be damaged in cases of exposure and plating of the medial column in supracondylar fractures of the humerus. So it had been advocated to plating these fractures both medially and laterally with fixation extending up to the diaphysis (Nagel, 1993). In the present study, 56.6% of the total nutrient foramina were distributed most often in the middle third of the radius and 43.3% were in the proximal third, with the foramen index ranging between 27.82 % and 48.57% of the bone length. The ratios of the present study were close to those reported by Mysorekar (1967) who found 62% of foramina located in the middle third of the bone and 36% in the proximal end. On the other hand, some reports such as those of Shulman (1959), Forriol Campos et al. (1987), Nagel (1993) and Kizilkanat et al. (2007) stated that the majority of nutrient foramina were located in the proximal third of the bone. In the present study, 90% of all radial foramina were on the anterior surface of the bone. Such results were in accordance with the previous studies (Shulman, 1959; Mysorekar, 1967; Longia et al., 1980; Forriol Campos et al., 1987) who stated that the majority of nutrient foramina were located on the anterior surface of the bone.
58
Regarding the ulna, the majority of nutrient foramina (62.5%) were in the middle third while 37.5% were in the proximal third of the bone, with the foramen index ranging between 27 and 47.59% of the bone length. No nutrient foramina were detected in the distal third of the ulnae. Reviewing the literatures, some authors reported that the majority of nutrient foramina were located in the middle third (Mysorekar, 1967) while others stated that most of foramina were in the proximal third (Shulman, 1959; Longia et al., 1980). However, all authors agreed that there were no nutrient foramina in the distal third of the ulna. In the present study, 99.92% of the nutrient foramina were located on the anterior surface of the ulnae. In all previous studies, and in accordance with the present results, the nutrient foramina were mostly observed on the anterior surface of the ulna (Shulman, 1959; Mysorekar, 1967; Longia et al., 1980; Forriol Campos et al., 1987; Kizilkanat et al., 2007). The blood supply to the sites of muscle attachment to the proximal half of the radius and ulna is directly reinforced by the nutrient arteries. There are, however, no significant muscle attachments to the distal half of the radius and ulna, corresponding to a general lack of nutrient foramina. Delayed or nonunion in the middle or lower diaphysis following trauma may be directly related to the absence of the nutrient arteries entering the bones in these areas (Kizilkanat et al., 2007). The posterior surface of both radius and ulna often lack nutrient foramina especially in the middle and dorsal diaphysis. That is why the dorsal localization for the plate is preferred during operative procedure (Giebel et al., 1997).
59
In the present study, most of the nutrient foramina (83.33%) were located along the middle third of the femur; the rest were in the proximal third, with no foramina detected in the distal third of the femur. These results were in accordance with those of Laing (1953), Mysorekar (1967), Forriol Campos et al. (1987), Sendemir and Cimen (1991), Gumusburun et al. (1994) and Kizilkanat et al. (2007). However, these findings did not coincide with those of Lutken (1950) and Ferriol Campos et al. (1987) who stated that the nutrient foramina were closer to the hip joint. Laing (1953) attributed the lack of the nutrient foramina in the lower third of the femur to the absence of vessels entering this part of bone. In this study, 58.33% of the nutrient foramina of the femora were located mainly around the linea aspera and along a narrow strip on either side of it. These results were similar to those of Lutken (1950), Laing (1953), Longia et al. (1980), Sendemir and Cimen (1991) and Gumusburun et al. (1994) who stated that most of nutrient foramina where concentrated along the linea aspera. In the present study, 90% of the nutrient foramina in the tibiae were in the proximal third, with the foramen index ranging between 26.49 and 35.54% of the bone length. Nutrient foramina were located in the middle third in the rest of the tibiae examined (10%). There were no foramina in the distal third. Similarly, many authors reported the presence of the majority of nutrient foramina in the proximal third of the tibia (Mysorekar, 1967; Longia et al., 1980; Gumusburn et al., 1994; Collipal et al., 2007). On the other hand, Kizilkanat et al. (2007) stated that most of nutrient foramina were located in the middle third with the foramen index ranging between 27 and 63% of the bone length.
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In the present series, all nutrient foramina studied were located on the posterior surface of the tibiae. Similar results were reported by Mysorekar (1967), Longia et al. (1980), Forriol et al. (1987), Sendemir and Cimen (1991), Nagel (1993), Gumusburun et al. (1994), Kizilkanat et al. (2007) and Collipal et al. (2007). The rate of healing of a fracture is related to the vascular supply of the bone. The areas or regions with a good blood supply are more rapidly healed than those with a poor blood supply. The tibia is a good example of such process. Because of the absence of nutrient foramina in the distal third of the tibia, fractures in that region tend to show delayed union or malunion (Trueta, 1974). In the present series, most of the nutrient foramina of the fibula were situated in the middle third of the bone (97.2%), with a foramen index ranging between 35.17% and 67.78% of the bone length. The rest of the nutrient foramina (2.8%) were located in the distal third of the bone. These results were in agreement with most of the previous studies (Mysorekar, 1967; Mckee et al., 1984; Forriol Campos et al., 1987; Sendemir and Cimen, 1991; Gumusburun et al., 1994; Collipal et al., 2007). On other hand, Guo (1981) reported that the majority of foramina were located in the proximal third of the fibula. In this study, 66.66% of the fibular foramina were located on the medial crest and 30.55% on the posterior surface. Similarly, Mysorekar (1967) reported that 56% of nutrient foramina were located on the medial crest while 33% lied on the posterior surface of fibula. However, some authors observed more nutrient foramina on the posterior surface compared to those on the medial crest (Mckee et al., 1984; Forriol Campos et al., 1987; Gumusburun et al., 1994; Kizilkanat et al., 2007; Collipal et al.,
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2007). Others, (Sendemir and Cimen, 1991) reported that the majority of foramina were on the medial surface of the fibula. Knowing the variations in the distribution of the nutrient foramina is important preoperatively, especially regarding the fibula used in bone grafting. In the majority of the specimens, the nutrient foramina were located in the middle third of the fibula which is the segment that must be used for the transplant, if one desires that the implant include endosteal vascularization and peripheral vascularization (Mckee et al., 1984; Collipal et al., 2007). It is very important that the nutrient blood supply is preserved in free vascularized bone grafts so that the osteocytes and osteoblasts in the graft survive, and the healing of the graft to the recipient bone is facilitated with the usual replacement of the graft by creeping substitution (Gumusburun et al., 1996). The present study proved that most of the nutrient foramina were observed to lie on the flexor surface of the bones. Thus, on the humerus, radius and ulna they were mostly on the anterior surface while on the femur, tibia and fibula, they were located on the posterior surface. Kizilkanat et al. (2007) stated that the position of the nutrient foramina was directly related to the requirements of a continuous blood supply to specific aspects of each bone, for example where there were major muscle attachments. It might be that, being more bulky, stronger and more active, flexors need more blood supply compared to extensors of limbs. 6.3. Size of Nutrient Foramina: The present results showed that, with the exception of the femur in which most of the foramina studied were dominant, all long bones of upper and lower limb possessed a majority of secondary nutrient foramina.
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These results were in agreement with those of Carroll (1963) and Longia et al. (1980) who reported that about two third of the nutrient foramina were secondary. The present results contradicted with those of kizilkanat et al. (2007) who stated that most foramina were of the dominant type. They added that wherever a single nutrient foramen was observed, it was always dominant. This was not the case in the present study. Sendemir and Cimen (1991) stated that there was no femur without a dominant nutrient foramen. Such statement was applicable in the present study, only in case of femora with a single nutrient foramen. 6.4. Direction of Nutrient Foramina: In this study, all the nutrient foramina in humerus were directed distally (away from the growing ends). Similar observations were reported by Lutken (1950) who stated that all canals which were found in humerus were directed distally. In the radii examined, the direction of the nutrient foramina was proximal. Similar observations were reported by Shulman (1959) and Mysorekar (1967) who stated that all nutrient foramina on the diaphysis of radius entered obliquely and were directed towards the elbow. The nutrient foramina of all ulnae examined had a proximal direction. Similar observations were reported by Shulman (1959) and Longia et al. (1980) who stated that all nutrient foramina on the shaft of the ulna entered obliquely and all were directed towards the elbow. In the current work, all nutrient foramina in the femur were directed proximally, away from the growing ends. Lutken (1950) and Longia et
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al. (1980) reported foramina having a distal direction in 1% and 0.5% of femora, respectively. Hughes (1952) stated that anomalous canals were found frequently in the femur, which might be the cause of the latter findings. The present study confirmed the previous reports suggesting that the nutrient foramina in the tibiae were directed away from the knee (Mysorekar, 1967; Hughes, 1952). On the other hand, Longia et al. (1980) observed nutrient foramina directed towards the knee in 3.5% of tibiae examined. Regarding the fibula, the direction of 77.71% of nutrient foramina was distal, while 22.2% had a proximal direction. In accordance with the present results, Longia et al. (1980) reported nutrient foramina having a proximal direction in 9.5% of fibulae examined. Mysorekar (1967) added that variations, in the direction of nutrient foramina were found only in the fibula. 6.5. Obliquity of Nutrient Foramina: In all long bones of upper and lower limbs examined, there were no changes in the obliquity of the foramen whether it was in the centre of the bone or nearer the ends. Such results were in agreement with those of Mysorekar (1967). Many theories had been put forward to account for the generally constant direction of the canals, and also the anomalously directed ones. Among these were the 'periosteal slip' theory of Schwalbe (1876), the vascular theory of Hughes (1952) and the muscular theory of Lacroix (1951), the ‘vascular theory’ appeared to offer the most comprehensive explanation but, instead of only one theory explaining the
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anomalous foramina, all factors may be appropriately and proportionately responsible in individual bones. 6.6. Clinical Anatomy: An understanding of the position and number of the nutrient foramina in long bones is important in orthopaedic surgical procedures such as joint replacement therapy, fracture repair, bone grafts and vascularized bone microsurgery (Kizilkanat et al., 2007). Longitudinal stress fractures are more commonly associated with the tibia, but occasionally occur in the femur and fibula. Knowing the position of nutrient foramina is important in longitudinal stress fractures, as they can either initiate from the nutrient foramen or its superomedial aspect. The foramen may be a potential area of weakness in some patients and, when under stress because of increased physical activity or decreased quality of the bone, the foramen may allow development of a fracture. Position of the fracture relative to the nutrient foramen of the long bone and the patterns of edema are the secondary signs in the key of the diagnosis of this type of fracture (Craig et al., 2003). Investigations on the vascular anatomy of long bones are important to human because it is relevant to fracture treatment (Bridgeman and Brookes, 1996; AlMotabagani, 2002). There may be instances in which the vascular integrity of a long bone is vital, and knowledge of the nutrient anatomy may be of value to the orthopaedic surgeon. The surgical exposure and periosteal stripping in open reduction internal fixation
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procedures of diaphyseal fractures present further vascular insult to existing osseous injury. Depending upon the desired effect of internal fixation, its devices often require different bony surface exposures. Some of these extensiles exposure may involve dissection in regions of the nutrient artery. It must be borne in mind that any injury to the nutrient arteries of the bones must be avoided. This will entail careful consideration as to their origin from the main trunks and situation where they enter the bones (Nagel, 1993). The healing of fractures, as of all wounds, is dependent upon blood supply, Injury to the nutrient artery at the time of fracture, or at subsequent manipulation, may be a significant factor predisposing to faulty union. If surgeons could avoid a limited area of the cortex of the long bone containing the nutrient foramen, particularly during an open reduction, an improvement in the management of this problem might be attained (Carroll, 1963). Recent results confirmed the hypothesis that vascularized bone and joint allograft survival depends strongly on the blood supply and control of rejection. Anatomical factors were suspected to be responsible for this phenomenon. To improve the surgical technique for the transplantation of femoral diaphyses and knee joints in human, one must consider the number and position of nutrient foramina. The entry of the nutrient vessels must be considered, especially the most distal nutrient foramen, which can occur about 12 cm above the femoral condyles. Further details are needed about the course of the arteries supplying the femoral shaft and the corresponding nutritive areas so better resection techniques could be developed for the transplantation of femoral diaphyses (Kirschner M, 1998).
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Similarly, the anatomical facts are also necessary for the success of free vascularized elbow allografts. In order to really vascularized elbow joint allograft, the exact topography of nutrient foramina of the humerus, radius, and ulna must be specified to preserve diaphyseal vascularization of the recipient. The levels of osseous section are selected according to the localization of the diaphyseal nutrient foramina of the three bones in order to preserve diaphyseal vascularization of the recipient to support the consolidation with the osseous graft (Wavreille, 2006).
CONCLUSION AND RECOMMENDATION
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7. Conclusion and Recommendation
The study confirmed previous reports regarding the number and position of the nutrient foramina in the long bones of the limbs. It also provided important information to the clinical significance of the nutrient foramina. Accordingly, a well understanding of the characteristic morphological features of the nutrient foramina by orthopaedic surgeons is recommended. Exact position and distribution of the nutrient foramina in bone diaphysis is important to avoid damage to the nutrient vessels during surgical procedures.
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8. References
Al-Motabagani (2002). The arterial architecture of the human femoral diaphysis. J. Anat. Soc. India 51(1): 27 - 31. Berard, A. (1835). Mẻmoire sur le rapport qui existe entre la direction des condits nourriciers des os longs et l’ordre suivant lequel les epiphysis see soudent au corps de l’os. Archives gẻnẻrales de mẻdicine.7: 176 - 183 (cited by Nagel, A., 1993). Bridgeman, G., Brookes, M. (1996). Blood supply to the human femoral diaphysis in youth and senescence. J. Anat. 188: 611 - 621. Carroll, S.E. (1963). A study of the nutrient foramina of the humeral diaphysis. J. Bone Jt. Surg. 45: 176 - 181. Collipal, E., Vargas, R., Parra, X., Silva, H., Sol, M. (2007). Diaphyseal nutrient foramina in the femur, tibia and fibula bones. Int. J. Morphol. 25 (2): 305 - 308. Craig, J.G., Widman, D., van Holsbeeck, M., (2003). Longitudinal stress fracture: patterns of edema and the importance of the nutrient foramen. Skeletal Radiol. 32: 22 - 27.
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Digby, K., H. (1916). The measurement of diaphysial growth in proximal and distal directions. J. Anat. 50: 187 – 188. Emine Kizilkanata, Neslihan Boyana, Esin T. Ozsahina, Roger Soamesb, Ozkan Oguza (2007). Location, number and clinical significance of nutrient foramina in human long bones. Ann. Anat. 189: 87 - 95. Forriol Campos, F., Gomez Pellico, L., Gianonatti Alias, M., FernandezValencia, R. (1987). A study of the nutrient foramina in human long bones. Surg. Radiol. Anat. 9: 251 - 255. Giebel, G., D., Meyer, CH., Koebke, J., Giebel, G.(1997). Arterial supply of forearm bones and its importance for the operative treatment of fractures. Surg. Radiol. Anat.19: 149 - 153. Gotzen, N., Cross, A., Ifju, P., Rapoff, A. (2003). Understanding stress concentration about a nutrient foramen. J. Biomech.36: 1511 - 1521. Gumusburun, E., Adiguzel, E., Erdil, H., Ozkan, Y., Gulec, E.(1996). A study of the nutrient foramina in the shaft of the fibula. Okajimas Folia Anat. Jpn.73 (2-3): 125 - 128. Gumusburun, E., Yucel, F., Ozkan, Y., Akgun, Z. (1994). A study of the nutrient foramina of lower limb long bones. Surg. Radiol. Anat. 16: 409 - 412. Guo, F. (1981). Fibular blood supply. Chin. Med. J. 94: 396 - 400.
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Guo, F. (1981). Observation of the blood supply to the fibula. Arch. Orthop. Traumat. Surg. 98: 147 - 151. Harris, H. A. (1933). Bone growth in health and disease. London: Humphrey Milford, pp. 239. Hughes, H. (1952). The factors determining the direction of the canal for the nutrient artery in the long bones of mammals and birds. Acta anat. 15: 261 - 280. Humphrey, G. M. (1961). Observations on the growth of the long bones. Med. chir. Trans., 44: 117 - 134. Kirschner, M. H., Menck, J., Hennerbichler, A., Gaber, O., Hofmann, G.O., (1998). Importance of arterial blood supply to the femur and tibia for transplantation of vascularized femoral diaphyses and knee joints.World J. Surg. 22: 845 - 852. Lacroix, P. (1951). The organization of bones. London: J. & A. Churchill p.75. Laing, P. G. (1953). The blood supply of the femoral shaft. J. Bone Jt. Surg. 35: 462 - 466. Langer, K. (1876). Uber das Gefässsystem der Röhrenknochen, mit Beitragen zur Kenntnis des Baues und der Entwicklung des Knochengewebes. Denkschr. Akad. Wiss. Wien, 36: 1 - 40 (cited by Skawina et al., 1994).
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Lewis, O.J. (1956). The blood supply of developing long bones with special reference to the metaphyses. J. Bone Jt. Surg. 38: 928 - 933. Longia, G.S., Ajmani, M.L., Saxena, S.K., Thomas, R.J. (1980). Study of diaphyseal nutrient foramina in human long bones. Acta Anat. (Basel) 107: 399 - 406. Lutken, P. (1950). Investigation into the position of the nutrient foramina and the direction of the vessel canals in the shafts of the humerus and femur in man. Acta anat. 9: 57 - 68. McKee, N. H., Haw, P., Vettese, T. (1984). Anatomic study of the nutrient foramen in the shaft of the fibula. Clin. Orthop. Rel. Res.184:141 - 144. Mysorekar, V.R. (1967). Diaphysial nutrient foramina in human long bones. J Anat.101: 813 - 822. Nagel, A. (1993).The clinical significance of the nutrient artery. Orthop. Rev.22: 557 - 561. Patake, S.M., Mysorekar, V.R. (1977). Diaphysial nutrient foramina in human metacarpals and metatarsals. J. Anat.124: 299 - 304. Payton, C., G. (1934). The position of the nutrient foramina and direction of the nutrient canal in the long bones of the madder-fed pig. J. Anat. Lond. 68: 500 - 510.
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Piollet, P. (1905). Recherches expẻrimentales sur le mode d’accroissement des os. Arch. Physiol. Norm. 5: 5 - 42 (cited by Payton, C., G., 1934). Schwalbe, G. (1876). Uber die Ernährungskanäle und das knochenwachstum. Zeitschr. F. Anat. U. Entwgesch., 1: 307 - 352 (cited by Shulman, S.S., 1959). Sendemir, E., Cimen, A. (1991). Nutrient foramina in the shafts of lower limb long bones: situation and number. Surg. Radiol. Anat. 13: 105 - 108. Shulman, S.S. (1959). Observations on the nutrient foramina of the human radius and ulna. Anat. Rec.134: 685 - 697. Skawina, A., Litwin, J.A, Gorzyca, J., and Miodonski, A.J. (1994). The vascular system of human fetal long bones: A scanning electron microscope study of corrosion casts. J. Anat.185: 369 - 376. Skawina, A., Wyczolkowski, M. (1987). Nutrient foramina of humerus, radius and ulna in Human Fetuses. Folia Morphol. 46: 17 - 24. Trueta, J. (1974). Blood supply and the rate of healing of tibial fractures. Clin. Orthop. Rel.Res. 105: 11 - 26. Wavreille, G., Remedios, Dos, C., Chantelot, C.(2006). Anatomic bases of vascularized elbow joint harvesting to achieve vascularized allograft. Surg. Radiol. Anat. 28: 498 - 510.
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اﻟﻤﻠﺨﺺ اﻟﻌﺮﺑﻲ
ﺛﻘﻮب اﻟﺘﻐﺬﯾﺔ اﻟﺪﻣﻮﯾﺔ ﻓﻲ ﺟﺴﻢ اﻟﻌﻈﺎم اﻟﻄﻮﯾﻠﺔ ﻟﻠﻄﺮﻓﯿﻦ اﻟﻌﻠﻮي واﻟﺴﻔﻠﻲ ﻓﻲ اﻹﻧﺴﺎن اﻟﻐﺮض ﻣﻦ ھﺬا اﻟﺒﺤﺚ ھﻮ ﺑﯿﺎن ﻋﺪد وﻣﻜﺎن ﺛﻘﻮب اﻟﺘﻐﺬﯾﺔ ﻓﻲ اﻟﻌﻈﺎم اﻟﻄﻮﯾﻠﺔ ﻟﻠﻄﺮﻓﯿﻦ اﻟﻌﻠﻮي واﻟﺴﻔﻠﻲ ﻟﻺﻧﺴﺎن، وﻛﺬﻟﻚ ﺑﯿﺎن ﺣﺠﻢ واﺗﺠﺎه وﻣﯿﻞ ﻗﻨﻮات اﻟﺘﻐﺬﯾﺔ اﻟﻤﻤﺘﺪة ﻣﻨﮭﺎ .وﻗﺪ ﺗﻤﺖ اﻟﺪراﺳﺔ ﺑﺎﺳﺘﺨﺪام ١٨٠ﻋﻈﻤﺔ آدﻣﯿﺔ ﻣﻦ ﻋﻈﺎم اﻟﻄﺮﻓﯿﻦ اﻟﻌﻠﻮي و اﻟﺴﻔﻠﻲ ﻷﺷﺨﺎص ﺑﺎﻟﻐﯿﻦ .وﻗﺪ ﻗﺴﻤﺖ اﻟﻌﻈﺎم إﻟﻰ ﺳﺘﺔ ﻣﺠﻤﻮﻋﺎت ﺗﻜﻮﻧﺖ ﻛﻞ ﻣﻨﮭﺎ ﻣﻦ ﺛﻼﺛﯿﻦ ﻋﻈﻤﺔ ﻟﻜﻞ ﻣﻦ اﻟﻌﻀﺪ واﻟﻜﻌﺒﺮة و اﻟﺰﻧﺪ وذﻟﻚ ﺑﺎﻟﻨﺴﺒﺔ ﻟﻌﻈﺎم اﻟﻄﺮف اﻟﻌﻠﻮي ،وأﯾﻀﺎ ﺛﻼﺛﯿﻦ ﻋﻈﻤﺔ ﻟﻜﻞ ﻣﻦ اﻟﻔﺨﺬ و اﻟﻘﺼﺒﺔ واﻟﺸﻈﯿﺔ ﺑﺎﻟﻨﺴﺒﺔ ﻟﻌﻈﺎم اﻟﻄﺮف اﻟﺴﻔﻠﻲ .وﻗﺪ ﺗﺒﯿﻦ وﺟﻮد ﺛﻘﺐ واﺣﺪ ﻟﻠﺘﻐﺬﯾﺔ ﻏﺎﻟﺒﺎ ﻓﻲ ﻛﻞ اﻟﻌﻈﺎم ﺑﺎﺳﺘﺜﻨﺎء ﻋﻈﻤﺔ اﻟﻔﺨﺬ ،ﻛﻤﺎ ﻛﺎﻧﺖ ﻣﻌﻈﻢ اﻟﺜﻘﻮب ﺛﺎﻧﻮﯾﺔ ﻓﻲ ﻗﯿﺎﺳﮭﺎ .وﻗﺪ وﺟﺪ أن ﻣﻌﻈﻢ ھﺬه اﻟﺜﻘﻮب ﻛﺎﻧﺖ ﻓﻲ اﻟﺜﻠﺚ اﻷوﺳﻂ ﻣﻦ اﻟﻌﻈﺎم ﺑﺎﺳﺘﺜﻨﺎء ﻋﻈﻤﺔ اﻟﻘﺼﺒﺔ ،واﻟﺘﻲ وﺟﺪت ﻓﯿﮭﺎ اﻟﺜﻘﻮب ﻓﻲ ﺛﻠﺜﮭﺎ اﻟﻌﻠﻮي .ﻛﻤﺎ ﻟﻮﺣﻆ أن ﺛﻘﻮب اﻟﺘﻐﺬﯾﺔ وﺟﺪت ﻋﻠﻰ اﻟﺴﻄﺢ اﻷﻣﺎﻣﻲ ﻟﻌﻈﺎم اﻟﻄﺮف اﻟﻌﻠﻮي ﺑﯿﻨﻤﺎ وﺟﺪت ﻋﻠﻰ اﻟﺴﻄﺢ اﻟﺨﻠﻔﻲ ﻟﻌﻈﺎم اﻟﻄﺮف اﻟﺴﻔﻠﻲ .وﻛﺎن اﺗﺠﺎه اﻟﺜﻘﻮب ﻣﺘﻮاﻓﻘﺎ ﻣﻊ ﻧﻈﺮﯾﺔ اﻟﻨﮭﺎﯾﺔ اﻟﻨﺎﻣﯿﺔ ﻣﻊ وﺟﻮد ﺑﻌﺾ اﻹﺧﺘﻼﻓﺎت ﺑﺎﻟﻨﺴﺒﺔ ﻟﻌﻈﻤﺔ اﻟﺸﻈﯿﺔ. وﻟﻘﺪ ﺗﻮاﻓﻘﺖ ﻧﺘﺎﺋﺞ ھﺬه اﻟﺪراﺳﺔ ﻣﻊ اﻟﺒﺤﻮث اﻟﺴﺎﺑﻘﺔ اﻟﻤﺘﻌﻠﻘﺔ ﺑﻌﺪد وﻣﻮﻗﻊ ﺛﻘﻮب اﻟﺘﻐﺬﯾﺔ ﻓﻲ اﻟﻌﻈﺎم اﻟﻄﻮﯾﻠﺔ ،ﻛﻤﺎ أﻛﺪت أھﻤﯿﺔ ھﺬه اﻟﺜﻘﻮب ﻣﻦ اﻟﻨﺎﺣﯿﺔ اﻹﻛﻠﯿﻨﯿﻜﯿﺔ ﺣﯿﺚ ﯾﻤﻜﻦ أن ﺗﻌﺪ ﻣﺮﺟﻌﺎ ﻣﻔﯿﺪا ﻟﺠﺮاﺣﺎت اﻟﻌﻈﺎم.
