Abstract
The human clavicle provides the bony connection between the upper extremity and the axial skeleton and it is reported to be among the first bones ossified and the last bone to fuse. Clavicle development of the studied mammals shows a combination of intramembranous and endochondrial ossification. The covering of its joints in adult humans differs from other joints of long bones. The rat clavicle pattern morphologically appears to be partly different in comparison with the human one. These differences partially restrict the use of the rat as a model for the study of human articular cartilage but on the other hand they can provide some valuable possibilities for application in medical research and practice.
Similar content being viewed by others
Abbreviations
- ACJ:
-
acromioclavicular joint
- BM:
-
bone marrow
- CF:
-
collagenic fibers
- Ch:
-
chondrocytic cell layer
- F:
-
fibrous layer
- H:
-
hypertrophic cell layer
- HE:
-
hematoxylin and eosin
- M:
-
mitotic figs
- O:
-
ossification zones
- P:
-
proliferative cell layer
- SCJ:
-
sternoclavicular joint
- TMJ:
-
temporomandibular joint
References
Andersen H (1963) Histochemistry and development of the human shoulder and acromioclavicular joints with particular reference to the early development of the clavicle. Acta Anat 55:124–165
Barbaix E, Lapierre M, Van Roy P, Clarijs JP (2000) The sternoclavicular joint: variants of the discus articularis. Clin Biomech 15:3–7
Barrow AE, Pilia M, Guda T, Kadrmas WR, Burns TC (2014) Femoral suspension devices for anterior cruciate ligament reconstruction: do adjustable loops lengthen? Am J Sports Med 42:343–349. https://doi.org/10.1177/0363546513507769
Bendele AM (2001) Models of osteoarthritis. J Musculoskelet Neuronal Interact 1:363–376
Beresford WA (1981) Chondroid bone, secondary cartilage, and metaplasia. Urban & Schwarzenberg, New York 454 pp
Brossmann J, Stabler A, Preidler KW, Trudell D, Resnick D (1996) Sternoclavicular joint: MR imaging -anatomic correlation. Radiology 198:193–198
Calixto LF, Penagos R, Jaramillo L, Gutiérrez ML, Garzón-Alvarado D (2015) A histological study of postnatal development of clavicle articular ends. Univ Sci (Bogota) 20:361–368. https://doi.org/10.11144/Javeriana.SC20-3.ahso
David CM, Elavarasi P (2016) Functional anatomy and biomechanics of temporomandibular joint and the far-reaching effects of its disorders. Journal of Advanced Clinical & Research Insights 3:101–106. https://doi.org/10.15713/ins.jcri.115
Delatte M, Von den Hoff JW, Maltha JC, Kuijpers-Jagtman AM (2004) Growth stimulation of mandibular condyles and femoral heads of newborn rats by IGF-I. Arch Oral Biol 49:165–175
Ellis E, Carlson DS (1986) Histologic comparison of the costochondral, sternoclavicular, and temporomandibular joints during growth in Macaca mulatta. J Oral Maxillofac Surg 44:312–321
Emura K, Arakawa T, Terashima T, Miki A (2009) Macroscopic and histological observations on the human sternoclavicular joint disc. Anat Sci Int 84:182–188. https://doi.org/10.1007/s12565-009-0014-5
Emura K, Arakawa T, Miki A, Terashima T (2014) Anatomical observations of the human acromioclavicular joint. Clin Anat 27:1046–1052. https://doi.org/10.1002/ca.22410
Fang J, Hall BK (1997) Chondrogenic cell differentiation from membrane bone periostea. Anat Embryol 196:349–362
Fraser-Moodie JA, Shortt NL, Robinson CM (2008) Injuries to the acromioclavicular joint. J Bone Joint Surg 90:697–707. https://doi.org/10.1302/0301-620X.90B6.20704
Gardner E (1968) The embryology of the clavicle. Clin Orthop Relat Res 58:9–16
Gardner E, Gray DJ (1953) Prenatal development of the human shoulder and acromioclavicular joints. Am J Anat 92:219–276
Groh GI, Wirth MA (2011) Management of traumatic sternoclavicular joint injuries. J Am Acad Orthop Surg 19:1–7
Ha AS, Petscavage-Thomas JM, Tagoylo GH (2014) Acromioclavicular joint: the other joint in the shoulder. Am J Roentgenol 202:375–385. https://doi.org/10.2214/AJR.13.11460
Hall BK (2001) Development of the clavicles in birds and mammals. J Exp Zool 289:153–161
Hall BK (2005) Bones and cartilage: developmental and evolutionary skeletal biology. Elsevier Academic Press, London
Harrington MA, Keller TS, Seiler JG, Weikert DR, Moeljanto E, Schwartz HS (1993) Geometric properties and the predicted mechanical behavior of adult human clavicles. J Biomech 26:417–426
Herring SW (1994) Development of functional interactions between skeletal and muscular systems pp165–191. In: Bone: differentiation and morphogenesis of bone. Volume 9. Hall BK (ed). Boca Raton
Higginbotham TO, Kuhn JE (2005) Atraumatic disorders of the sternoclavicular joint. J Am Acad Orthop Surg 13:138–145
Hirouchi H, Kitamura K, Yamamoto M, Odaka K, Matsunaga S, Sakiyama K, Abe S (2018) Developmental characteristics of secondary cartilage in the mandibular condyle and sphenoid bone in mice. Arch Oral Biol 89:84–92. https://doi.org/10.1016/j.archoralbio.2017.12.027
Huang L-H, Fukai N, Selby PB, Olsen BR, Mundlos (1997) Mouse clavicular development: analysis of wild-typeand cleidocranial dysplasia mutant mice. Dev Dyn 210:33–40
Inthasan C, Mahakkanukrauh P (2017) Age estimation from clavicle by Histomorphometry method: a review. Med & Health 12:4–17. https://doi.org/10.17576/MH.2017.1201.02
Joseph PR, Rosenfeld W (1990) Clavicular fractures in neonates. Am J Dis Child 144:165–167
Kantomaa T (1984) The role of the mandibular condyle in the facial growth. Thesis, Oulu. Proceedings of the Finnish Dental Society 80, Suppl. IX
Koski K (1974) The first Sheldon Friel memorial lecture. The mandibular complex Trans Eur Orthod Soc:53–67
Lippert LS (2006) Clinical kinesiology and anatomy, 4th edition; 95-96, https://doi.org/10.2522/ptj.2006.86.12.1715.1
Matsuoka T, Ahlberg PE, Kessaris N, Iannarelli P, Dennehy U, Richardson WD, McMahon AP, Koentges G (2005) Neural crest origins of the neck and shoulder. Nature 436:347–355. https://doi.org/10.1038/nature03837
Mazzocca AD, Arciero RA, Bicos J (2007) Evaluation and treatment of acromioclavicular joint injuries. Am J Sports Med 35:316–329
Mérida-Velasco JR, Rodríguez-Vázquez JF, De la Cuadra Blanco C, Campos López R, Sánchez-Montesino I, Mérida-Velasco JA (2009) Development of the human mandibular condylar cartilage in human specimens of 10–15 weeks’ gestation. J Anat 214:56–64. https://doi.org/10.1111/j.1469-7580.2008.01009.x
Mescher AL (2016) Junqueira's basic histology text and atlas. Fourteenth edition, McGraw-hill education chpt 8 bone 138–160
Mizoguchi I, Toriya N, Nakao Y (2013) Growth of the mandible and biological characteristics of the mandibular condylar cartilage. Japanese Dental Science Review 49:39–150. https://doi.org/10.1016/j.jdsr.2013.07.004
Montenegro M, Rojas M, Domingue S (2004) Comparative osteogenesis of the clavicle secondary cartilages and epiphyseal cartilages of long bones. Int J Morphol 22:201–206
Moore, K.L., Dalley, A.F., Agur, A.M.R. (2011) Upper limb. In clinically oriented Anatomy.Baltimore: Lippincott Williams and Wilkins pp 673-688
Moore, KL, Persaud, TVN, Torchia MG (2013) Before we are born: essentials of embryology and birth defects. Saunders, 8th edition
Moriyama H, Yoshimura O, Kawamata S, Takayanagi K, Kurose T, Kubota A, Hosoda M, Tobimatsu Y (2008) Alteration in articular cartilage of rat knee joints after spinal cord injury. Osteoarthr Cartil 16:392–398. https://doi.org/10.1016/j.joca.2007.07.002
Nagashima et al (2016) Developmental origin of the clavicle, and its implications for the evolution of the neck and the paired appendages in vertebrates. J Anat 229:536–548. https://doi.org/10.1111/joa.12502
Nishida T, Kubota S, Kojima S, Kuboki T, Nakao K, Kushibiki T, Tabata Y, Takigawa M (2004) Regeneration of defects in articular cartilage in rat knee joints by CCN2 (connective tissue growth factor). J Bone Miner Res 19:1308–1319
Noble JS (2003) Degenerative sternoclavicular arthritis and hyperostosis. Clin Sports Med 22:407–422
O’Rahilly R, Gardner E (1972) The initial appearance of ossification in stages human embryos. Am J Anat 134:291–230
Oppenheim WL, Davis A, Growdon WA, Dorey FJ, Davlin LB (1990) Clavicle fractures in the newborn. Clin Orthop Rel Res 250:176–180
Phadnis J., Bain GI (2015) Clavicle Anatomy. In : Bain GI, Itoi E, Di Giacomo G, Sugaya H (eds) Normal and Pathological Anatomy of the Shoulder. Publisher: Springer, pp71–80
Piel MJ, Kroin JS, van Wijnen AJ, Kc R, Im HJ (2014) Pain assessment in animal models of osteoarthritis. Gene 537:184–188. https://doi.org/10.1016/j.gene.2013.11.091
Pingsmann A, Patsalis T, Michiels I (2002) Resection arthroplasty of the sternoclavicular joint for the treatment of primary degenerative sternoclavicular arthritis. J Bone Joint Surg 84:513–517
Precious DA, Hall BK (1994) Repair of fractured membrane bones. In: Hall BK, (ed.) Bone, Vol. 9: Differentiation and morphogenesis of bone. Boca Raton, FL: CRC Press. 145–163
Ramirez-Yañez GO (2004) The mandibular condylar cartilage: a review. Ortop Rev Int Ortop Func 1:85–94
Reid D, Polson K, Johnson L (2012) Acromioclavicular joint separations grades I–III a review of the literature and development of best practice guidelines. Sports Med 42:681–696. https://doi.org/10.2165/11633460-000000000-00000
Ren Y, Maltha JC, Kuijpers-Jagtman AM (2004) The rat as a model for orthodontic tooth movement: a critical review and a proposed solution. Eur J Orthod 26:483–490
Renfree KJ, Wright TW (2003) Anatomy and biomechanics of the acromioclavicular and sternoclavicular joints. Clin Sports Med 22:219–237
Reuler JB, Girard DE, Nardone DA (1978) Sternoclavicular joint involvement in ankylosing spondylitis. South Med J 71:1480–1481
Robinson CM, Jenkins PJ, Markham PE, Beggs I (2008) Disorders of the sternoclavicular joint. J Bone Joint Surg 90:685–696. https://doi.org/10.1302/0301-620X.90B6.20391
Rojas MA, Montenegro MA (1995) An anatomical and embryological study of the clavicle in cats (Felis domestus) and sheep (Ovis aries) during the prenatal period. Acta Anat (Basel) 154:128–134
Rönning O, Kantomaa T (1988) The growth pattern of the clavicle in the rat. J Anat 159:173–179
Rönning O, Koski K (1974) The effect of periostomy on the growth of the condylar process in the rat. Proc Finn Dent Soc 70:28–29
Ross MH, Pawlina W (2016) Histology. A text and atlas: with correlated cell and molecular biology 7th edition chpt bone 214–258
Schneider MM, Balke M, Koenen P, Fröhlich M, Wafaisade A, Bouillon B, Banerjee M (2016) Inter- and intraobserver reliability of the Rockwood classification in acute acromioclavicular joint dislocations. Knee Surg Sports Traumatol Arthrosc 24:2192–2196. https://doi.org/10.1007/s00167-014-3436-0
Shen G, Darendeliler MA (2005) The adaptive remodeling of condylar cartilage: a transition from chondrogenesis to osteogenesis. J Dent Res 84:691–699. https://doi.org/10.1177/154405910508400802
Shimizu, K, , Awaya G, Matsuda F, Wakita S, Mayekawa M (1991) Friedrich's disease: a case report. Nihon geka hokan. Archiv für japanische Chirurgie 60: 184
Shirazian H, Chang EY, Wolfson T, Gamst AC, Chung CB, Resnick DL (2014) Prevalence of sternoclavicular joint calcium pyrophosphate dihydrate crystal deposition on computed tomography. Clin Imaging 38:380–383. https://doi.org/10.1016/j.clinimag.2014.02.016
Spar I (1978) Psoriatic arthritis of the sternoclavicular joint. Conn Med 42:225–226
Suezie K, Blank A, Strauss E (2014) Management of Type 3 acromioclavicular joint dislocations current controversies. Bulletin Hospital Joint Diseases 72:5360
Tran S, Hall BK (1989) Growth of the Clavicle and Development of Clavicular Secondary Cartilage in the Embryonic Mouse. Acta Anat 135(3):200–207
Valasek P, Theis S, DeLaurier A, Hinits Y, Luke GN, Otto AM, Minchin J, He L, Christ B, Brooks G, Sang H, Evans DJ, Logan M, Huang R, Patel K (2011) Cellular and molecular investigations into the development of the pectoral girdle. Dev Biol 357:108–116. https://doi.org/10.1016/j.ydbio.2011.06.031
van Riet RP, Bell SN (2011) Clinical evaluation of acromioclavicular joint pathology: sensitivity of a new test. J Shoulder Elb Surg 20:73–76. https://doi.org/10.1016/j.jse.2010.05.023
Walton J, Mahajan S, Paxinos A, Marshall J, Bryant C, Shnier R, Quinn R, Murell GAC (2004) Diagnostic values of tests for acromioclavicular joint pain. The Journal Of Bone & Joint Surgery 86-A:807–812
Willlems W.J. (2015) Comparative Anatomy of the Shoulder. In : Bain GI, Itoi E, Di Giacomo G, Sugaya H (eds) Normal and pathological anatomy of the shoulder. Publisher: Springer, pp 3–14
Wohlgethan JR, Newberg AH, Reed JI (1988) The risk of abscess from sternoclavicular arthritis. J Rheumatol 15:1302–1306
Yoo Yon-Sik (2015) Acromioclavicular Joint. In : Bain GI, Itoi E, Di Giacomo G, Giacomo G, Sugaya H (eds) Normal and Pathological Anatomy of the Shoulder. Publisher: SPRINGER, pp 159–169
Acknowledgments
The authors thank Mrs. Lubica Bošmanska and Alexandra Machova for assistance during the preparation of histological specimens. This work was partly supported by the APVV-15-0372 and by theVEGA-2/0129/15 grants.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
We declare that we have no conflict of interest.
Ethical approval
The bone sample of human clavicle originates from donor cadaver for science purposes at the Institute of Anatomy of Medical Faculty of Comenius University Bratislava, Slovak Republic and it was provided by a staff member of mentioned institution - co-author of this publication.
Rights and permissions
About this article
Cite this article
Líška, J., Zamborský, R., Maženský, D. et al. Comparison of clavicular joints in human and laboratory rat. Biologia 73, 1247–1254 (2018). https://doi.org/10.2478/s11756-018-0130-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.2478/s11756-018-0130-6