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 Table of Contents  
Year : 2021  |  Volume : 10  |  Issue : 3  |  Page : 160-163

Variations in nutrient foramina of clavicle – A descriptive study

1 Associate Professor, Department of Anatomy, Burdwan Medical College, Bardhaman, West Bengal, India
2 Assistant Professor, Department of Anatomy, Burdwan Medical College, Bardhaman, West Bengal, India

Date of Submission17-Jan-2021
Date of Decision22-Jun-2021
Date of Acceptance21-Jul-2021
Date of Web Publication30-Jul-2021

Correspondence Address:
Prerana Aggarwal
3rd Floor, 185.Garfa Main Road, Kolkata - 700 078, West Bengal
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/NJCA.NJCA_13_21

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Background: Human clavicle, an important bone of the pectoral girdle connects the upper appendicular skeleton to the axial skeleton. The nutrition and growth of the bone depend mainly on the nutrient artery. It enters the bone through the nutrient foramen. Hence this study aimed to study the number, position, location, direction, and distance of nutrient foramina of the clavicle from the sternal end. Methodology: In a descriptive study 79 dry adult human clavicles (40 right, 39 left) were studied, and mean foramen index (FI) was calculated. The data obtained were tabulated, results obtained and the inference was drawn. Results: The mean length of clavicles studied was 141.36 ± 11.11 mm (right 140.51 ± 11.10 mm, left 142.36 ± 11.14 mm). The average distance of foramina (DNF) from the sternal end was 61.48 ± 15.82 mm (right 62.88 ± 16.28 mm, left 59.96 ± 15.12 mm). Nutrient foramen was found in all the studied bones. The total foramina observed are 120. Forty-four bones have single (55.70%), 29 double (36.71%), and 6 triple (7.59%) foramina. Foramina were distributed on all four surfaces of the clavicle, predominantly on the posterior surface (52.50%). Most foramina were present on the middle third (67.50%) with an average FI% of 43.82 ± 11.85 (right 44.99 ± 12.09, left 42.43 ± 11.41). The foramina were directed toward the acromial end in all cases. Conclusion: The nutrient artery of the clavicle needs to be preserved for maintaining its vitality. Hence, the morphometric and topographic knowledge related to nutrient foramen and its variations is of immense importance to orthopedic surgeons and radiotherapists while treating clavicular pathologies.

Keywords: Clavicle, foramen index, nutrient foramen

How to cite this article:
Aggarwal P, Ghorai S. Variations in nutrient foramina of clavicle – A descriptive study. Natl J Clin Anat 2021;10:160-3

How to cite this URL:
Aggarwal P, Ghorai S. Variations in nutrient foramina of clavicle – A descriptive study. Natl J Clin Anat [serial online] 2021 [cited 2022 Sep 25];10:160-3. Available from: http://www.njca.info/text.asp?2021/10/3/160/322799

  Introduction Top

Clavicle, a modified long bone, is horizontally placed across the root of the neck. Clavicle keeps the arm away from the trunk.[1] Clavicle is the most common bone in the body which is susceptible to fracture. The weakest point of the clavicle is the junction of the middle and outer third. This is the most common site to get fractured when a person falls on the outstretched hand.[2] This is also the position of the nutrient foramen.[3]

Recent studies depict that patients with untreated clavicular fracture show a higher rate of nonunion and specific deficits of shoulder function. These cases have shown good results with external or internal fixations with nails, plates, screws, or surgical bone grafting[4] for which the knowledge of the nutrient arterial supply is important. Preservation of nutrient vessels is essential for proper fracture healing,[5],[6] failing which neurovascular complications may occur even after surgical repair of fractures.

More recently, microsurgical vascularized bone transplantation is another technique which is becoming popular. It also requires information related to the anatomy of nutrient foramina for the preservation of circulation of the affected bony structure.[6] Moreover, preservation of nutrient blood flow is crucial for the osteocytes survival in cases of resection of tumor, traumas, and congenital pseudoarthrosis.[6],[7]

There are no data available relating to the nutrient foramina of the clavicle from West Bengal, especially the Bardhaman district, hence a comprehensive study related to the same was conducted.

  Methods Top

This is a descriptive study conducted on 79 (41 right and 38 left) unpaired, cleaned, and dried adult human clavicles in the anatomy department of Burdwan Medical College, Bardhaman, West Bengal for more than 1 year (September 2019–August 2020 (Since study included dry bones exemption was sought from IEC)). The exact age and sex of the bones were not known. Damaged and deformed bones were excluded. The bones were studied for the number, direction, length-wise location, and positions of the foramina with respect to the surface. The nutrient foramina were identified using a magnifying glass by the presence of a well-marked groove and slightly raised margin at the commencement of the canal. The direction of the canal was determined by using a 24G needle. The foraminal distance from the sternal end (DNF) and the total length of the clavicle (TL) were measured in millimeters using Vernier caliper, ignoring curves of the clavicle.

The Hughes formula was used for calculating the foramen index (FI):[8]

FI = (DNF/TL) ×100

DNF = Distance of nutrient foramen from the proximal end (sternal end) of the clavicle

TL = Total length of clavicle

The data were tabulated, analyzed, compared with the already available data from similar studies done in the past and the inference was drawn.

Paired t-test was used to compare the FI of the two sides.

  Results Top

A total of 120 nutrient foramina were found in 79 clavicles studied. In all the studied clavicles at least one nutrient foramen was found (100%). Double and triple foramina were also found, in 29 bones (36.71%) and 6 bones (7.59%), respectively [Figure 1] and [Figure 2]. Most of the bones studied had single nutrient foramen 44 (55.70%). The foramina were predominantly found on the posterior surface 63 (52.50%) and on the middle third of the clavicle 81 (67.50%). All the 79 (100%) foramina were directed toward the acromial end. Observations are tabulated in [Table 1] and [Table 2].
Figure 1: Double nutrient foramen in a left clavicle

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Figure 2: Triple nutrient foramen in a right clavicle

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Table 1: Morphometry of nutrient foramina of clavicle

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Table 2: Topography of nutrient foramen in clavicle

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The range of FI% on the 2 sides was noted. On the right side, it was 23.65–70.73 with the mean value 44.99 ± 12.09. On the left side, the range and the mean values were 22.73–68.18 and 42.43 ± 11.41 respectively. On comparing the two sides, “t” test value of FI was 0.24. “P” > 0.05, thus the result found was not significant.

  Discussion Top

Nutrition of a long bone depends on its blood supply which is also a major factor determining the union after a fracture. Prognosis of surgical treatment for traumatic and nontraumatic pathologies or radiotherapy also depends on the maintenance of proper vascularity of the bone for which the anatomical knowledge related to the nutrient foramen is essential.

Professor Trueta has mentioned that the blood supply of the outer third of the compact bone of shaft comes from the periosteal arteries and that for inner two-third from nutrient arteries.[9] Kizilkanat et al. also said that for long bones major blood supply comes from the nutrient arteries, especially during the bone growth and the early phases of ossification.[10] Nutrient artery and nerve pierce the cartilage or the mesenchyme of the growing long bone and enter its shaft. During ossification the areas around the vessels and nerves get ossified and form a nutrient canal, the entry point remains as nutrient foramen. As stated by Khundsen, the nutrient artery of clavicle is either the branch of suprascapular, thoracoacromial, or internal thoracic artery.[11]

Most textbooks mention the presence of a single nutrient foramen in clavicle.[12] In the present study also, we had found most clavicles with single foramen 44 (55.70%) as also found by Sinha et al.,[13] Sowmiya et al.,[14] Suma et al.[15] and Kumar et al.[16] However, studies done by B. Murlimanju et al.,[17] Rahul et al.[18] and Sahu Santosh and Dali[12] show that most clavicles had double foramina [Table 3]. Clavicles with double 29 (36.71%) and triple 6 (7.59%) foramina were also found in the present study, but no clavicle studied here showed the absence of foramen or foramina more than three. Textbook of Gray's anatomy mentions that initially, ossification starts in the shaft of the clavicle in condensed mesenchyme from two primary centers, medial and lateral. The junction of these two centers lies at the junction of the middle and lateral third of the clavicle.[19] In addition to the primary nutrient artery, the presence of two or more arteries separately invading these masses can explain the presence of multiple foramina in the clavicle.
Table 3: Comparision of data between present and previous studies

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Malukar and Joshi states that the nutrient foramen is present at the original center of ossification as the nutrient vessels occupying the nutrient foramina usually come from the vessels which have initially invaded the cartilage during ossification.[20] Therefore the site of the foramen and nutrient canal may be a weak point and prone to fractures.[1] Carroll has mentioned in his study that any damage either traumatic or iatrogenic, to the nutrient foramen or nutrient canal may cause delayed union or nonunion of the bone following a fracture as the healing process is dependent on the maintenance of vascularity of a bone.[21] These complications are not rare after clavicular fractures involving the mid-shaft region. So we looked for the length-wise location of the foramina and found that the most common site of the nutrient foramen, seen in 81 clavicles (67.5%) was the middle third of the shaft followed by medial one-third, found in 31 clavicles (25.83%). The mean DNF was 61.48 ± 15.82 and mean FI% 43.82 ± 11.85 [Table 2]. The result was comparable to most of the studies mentioned in [Table 3].

Pereira et al.[22] in their study found that the clavicles show more variations as to the surface on which the foramina were present as was also evident in the present study. Foramina were found on all four surfaces (anterior, posterior, superior, and inferior), though it was found predominantly on the posterior surface as also found by Rahul et al., Kumar et al., Sowmiya et al. [Table 3]. The result differs from Gray's anatomy textbook according to which inferior surface is the most common location of the nutrient foramen.[19]

A nutrient artery as stated earlier comes from the initial vessels that are present at the site of primary ossification. Schwalbe G explained that before the appearance of epiphyses, there is equal growth at the two ends of a long bone. Hence, the direction of the nutrient foramen should be horizontal' in a vertical long bone before birth.[18] Gradually as the bone grows faster at one end known as the growing end (ends of a growing bone develop from secondary centers of ossification and are supplied by epiphyseal and juxta-epiphyseal arteries), the nutrient canal containing the nutrient artery becomes slanted and is directed away from that end. Hence the direction of the nutrient artery follows the general rule of “growing end theory' and is opposite to the growing end.[20] Berard was the first one who correlated the direction of the nutrient canal with ossification and bone growth.[18] Humphrey worked on the direction and obliquity of the nutrient canals and postulated “periosteal slipping theory” which also states that the canal points away from the growing end.[23] The sternal end being the growing end in the clavicle, we found that the nutrient foramina in all the clavicles studied were directed towards the acromial end as also found in other studies [Table 3].

Studies done in the different parts of the world and within the country show variations in the number, location, position, and direction of the clavicular foramina. Since no such data is available from our part of the country, a study like ours will be of great help to the radiotherapist and surgeons over here.

  Conclusion Top

All of the clavicles studied had at least one foramina. Most of the clavicles had single foramen. The foramina were predominant on the posterior surface and on the middle one-third of the shaft. The mean DNF was 61.48 mm and the mean FI was 43.82%. All the nutrient foramina were directed towards the acromial end. Awareness about these foramina is essential to preserve the blood circulation during radiation therapy given for treating malignant bone metastasis, internal fixation surgery as well as bone grafting done for treatment of nonunion of clavicular fractures. Further with the advent of microvascular bone graft transfer, the anatomical data about nutrient foramina has become essential.

Hence, the data from the present study can be used alike by anatomists for further research work on the same topic, radiotherapists for treating clavicular malignant deposits/tumors, and surgeons for the treatment of fracture clavicle and its related complications.

Limitations of the study

The study sample size was small. Only 79 bones were studied due to the unavailability of bones in the department. Larger sample size and multicentric studies would give more accurate results. Age- and gender-specific results could be obtained if the age and sex of the individual bones studied were known. The results were not co-related radiologically.

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Conflicts of interest

There are no conflicts of interest.

  References Top

Snell Richard S. Clinical Anatomy by Regions. 8th ed. USA: Lippincott Williams and Wilkins; 2008. p. 432-3.  Back to cited text no. 1
Khan K, Bradnock TJ, Scott C, Robinson CM. Fractures of the clavicle. J Bone Joint Surg Am 2009;91:447-60.  Back to cited text no. 2
Kumar R, Madewell JE, Swischuk LE, Lindell MM, David R. The clavicle: Normal and abnormal. Radiographics 1989;9:677-706.  Back to cited text no. 3
Huang HK, Chiang CC, Hung SH, Su YP, Chiu FY, Liu CL, et al. The role of autologous bone graft in surgical treatment of hypertrophic nonunion of midshaft clavicle fractures. J Chin Med Assoc 2012;75:216-20.  Back to cited text no. 4
Longia GS, Ajmani ML, Saxena SK, Thomas RJ. Study of diaphyseal nutrient foramina in human long bones. Acta Anat 1980;107:399-406.  Back to cited text no. 5
Gùmùsburun E, Yucel F, Ozkan Y, Akgun Z. A study of the nutrient foramina of lower limb long bones. Surg Radiol Anat 1994;16:409-12.  Back to cited text no. 6
Sendemir E, Çimen A. Nutrient foramina in the shafts of lower limb long bones: Situation and number. Surg Radiol Anat 1991;13:105-8.  Back to cited text no. 7
Hughes H. The factors determining the direction of the canal for the nutrient artery in the long bones of mammals and birds. Acta Anat (Basel) 1952;15:261-80.  Back to cited text no. 8
Brookes M. Blood supply of long bones. Br Med J 1963;2:1064-5.  Back to cited text no. 9
Kizilkanat E, Boyan N, Ozsahin ET, Soames R, Oguz O. Location, number and clinical significance of nutrient foramina in human long bones. Ann Anat 2007;189:87-95.  Back to cited text no. 10
Knudsen FW, Andersen M, Krag. The arterial supply of the clavicle. Surg Radiol Anat 1989;11:211-14.  Back to cited text no. 11
Sahu Santosh K, Dali M. Morphological and topographical anatomy of nutrient foramina in human clavicles of Eastern Odisha. Int J Appl Res 2017;3:521-3.  Back to cited text no. 12
Sinha P, Mishra SJ, Kumar P, Singh S, Sushobhana K, Passey J, et al.Morphometric & Topographic Study Of Nutrient Foramen In Human Clavicle In India. Int J Biol Med Res 2015;6:5118-21.  Back to cited text no. 13
Sowmiya G, Sundarapandian S, Nithya V. Neurovascular foramina of the human clavicle and their clinical significance. Res J Pharm Biol Chem Sci 2016;7:2634.  Back to cited text no. 14
Suma MP, Veera U, Srinivasan S. The study of nutrient foramina in human clavicle. J Evid Based Med Healthc 2018;5:107-9.  Back to cited text no. 15
Kumar D, Raichandani L, Kataria SK, Singh J. Variation in number and position of nutrient foramen of clavicle – A morphological study in western Rajasthan. Indian J Anat Surg Head Neck Brain 2019;5:67-71.  Back to cited text no. 16
Murlimanju BV, Prabhu LV, Pai MM, Yadav A, Dhananjaya KV, Prashanth KU, et al. Neurovascular foramina of the human clavicle and their clinical significance. Surg Radiol Anat 2011;33:679-82.  Back to cited text no. 17
Rahul R, Shrestha S, Kavitha B. Morphological and topographical anatomy of nutrient foramina in human clavicles and their clinical importance. IOSR J Dent Med Sci 2014;13:37-40.  Back to cited text no. 18
Standring S, Healy JC, Johnson D, Collins P, et al., editors. Gray's Anatomy: The Anatomical Basis of Clinical Practice. 40th ed. London: Elsevier Churchill Livingstone; 2008. p. 792-3.  Back to cited text no. 19
Malukar O, Joshi H. Diaphysial nutrient foramina in long bones and miniature long bones. Natl J Integr Res Med 2011;2:23-26.  Back to cited text no. 20
Carroll SE. A study of the nutrient foramina of the humeral diaphysis. J Bone Joint Surg Br 1963;45-B: 176-81.  Back to cited text no. 21
Pereira GA, Lopes PT, Santos AM, Silveira FH. Nutrient foramina in the upper and lower limb long bones: Morphometric study in bones of southern Brazilian adults. Int J Morphol 2011;29:514-20.  Back to cited text no. 22
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  [Figure 1], [Figure 2]

  [Table 1], [Table 2], [Table 3]


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