Introduction

Development of the upper limb (Fig. 1.1) can best be understood as a series of ectodermal and mesodermal interactions controlled by a complex system of signalling during embryogenesis. The development starts as a limb bud in the ventrolateral wall of the embryo on the ‘Wolff crest’ 28 days after fertilization. Differentiation of the limb buds occur between the 5th and 8th week.^1–4 The formation of limb buds is induced by the adjacent somites. The bones are formed as mesenchymal condensations that first chondrify then ossify. Limb muscles are formed from myogenic precursor cells that originate in mesodermal somites. The peripheral nerves arise from the neural crest. They migrate and extend their axons later in response to trophic cues, such as ephrins, produced by the muscles and connective tissues.^5,6

Figure 1.1 The development of the upper limb with particular reference to the elbow. The external appearance of the right arm is shown (A, I–IV), with the internal development of the left arm (B, I–IV): I, 32 days; II, 36 days; III, 42 days; IV, 48 days.

Redrawn from Stanley D and Kay NRM (eds). Surgery of the elbow. Hodder Arnold 1998 (fig 1.2, p 2).

Elbow joint development

Table 1.1 Elbow joint development

Prenatal development

The ectodermal covering at the site of each putative limb thickens to form the apical ectodermal ridge (AER). This together with the somatopleuric mesenchyme is called the progress zone. The orientation and progression of limb development are controlled by the progress zone. The differentiation occurs in a proximodistal, craniocaudal and dorsoventral axis. The proximodistal axis is regulated by the progress zone, which is controlled by factors including fibroblast growth factor (FGF), bone morphogenic protein (BMP) and Hox genes.⁷

Craniocaudal polarization is regulated by a small population of mesenchymal cells on the postaxial border of the limb bud termed the zone of polarizing activity, which produces the peptide, sonic hedgehog (Shh).⁸ BMPs and Gremlin, a secreted inhibitor of BMPs, also participate in this pathway; the BMPs produced throughout the limb mesenchyme and in the AER inhibit production of FGFs by the AER.⁵ A key role of Shh is to activate expression of the BMP antagonist Gremlin, thereby preventing this inhibition of FGF expression (Fig. 1.2). The dorsoventral axis (radio-ulnar axis in upper limb) is controlled by the ectoderm of the limb.

Figure 1.2 Positive and negative feedback loops control limb outgrowth and cessation of growth. This model explains how the two loops are used first to promote and then to terminate signals. Arrows indicate activation; the T-shaped red line indicates inhibition. Dashed lines represent diminished regulation. During promotion of outgrowth, the positive regulatory loop increases all signals; Shh produced in the ZPA (green zone) promotes FGF expression in the AER (blue zone). This effect of Shh is mediated through its ability to induce Gremlin. Gremlin in turn antagonizes bone morphogenetic proteins (BMPs), which inhibit FGF action (not shown). The overall effect is thus to promote FGF expression in the AER. The trigger to cessation of growth occurs when AER FGFs are produced at a sufficiently high level that they repress expression of Gremlin (represented by a T-shaped line in the figure). By this stage of development, the limb mesenchyme has grown, which leads to a larger domain of Gremlin expression (red zone). Once Gremlin expression declines, cessation of limb growth occurs (last panel in figure). Gremlin is no longer present to repress BMP signals, and thus BMPs are able to repress FGF expression. Loss of FGF leads to an inability of FGF to maintain Shh expression. Thus growth along all limb axes ceases. (FGFs, fibroblast growth factors; Shh, sonic hedgehog, AER, apical ectodermal ridge; ZPA, zone of polarizing activity; Grem, Gremlin.)

Redrawn from Lyons K and Ezaki M. Molecular regulation of limb growth. J Bone Joint Surg (Am) 2009; 91:47–52.

While the exact mechanism of chondrogenesis is unclear, the Hox genes, BMP, Sox9, Indian hedgehog (Ihh) and parathyroid hormone-related protein (PTHrP) play an important role.^9,10 The elbow joint develops from mesenchymal interzones.¹¹ The mesenchymal interzone between the chondrifying bone ends differentiates into fibroblastic tissue (Fig. 1.3). This further differentiates into three layers. The outer layers form the cartilage layer. Vacuoles appear within the central layer, which coalesces to form the synovial cavity. The capsule is formed from the mesenchymal sheath surrounding the entire interzones.

Figure 1.3 Formation of the elbow joint. Cartilage, ligaments, and capsular elements of the joints develop from the interzone regions of the axial mesenchymal condensations that form the humerus and radius and ulna.

Redrawn from Larson WJ (ed). Essentials of human embryology. Churchill Livingstone 1998 (fig 11.6, p 215). © Elsevier 1998.

These developmental changes that lead to formation of the elbow joint occur progressively. Chondrification of the humeral, radial and ulnar shaft is present by the 6th intrauterine week in embryos of 12 mm and by this stage there has also been enlargement of the distal humerus, which will develop into the future condyles. The shape of the coronoid and olecranon processes can be seen in the 13 mm embryo.

At 7.5 weeks (20 mm embryo) the epiphyses are identifiable in precartilage and by the 8th week the interzone between the humerus and radius and between the humerus and ulna can be recognized as the future elbow joint. Cavitation begins during the 9th week (27 mm embryo) and is complete by the end of the 10th week (39 mm embryo).

Also by this stage muscles and tendons are well developed and have obtained a nerve supply from the developing limb bud (Fig. 1.4).

Figure 1.4 The development of the upper limb dermatomes. The axial line indicates where there is no sensory overlap: (A)35 days; (B), 41 days; (C) adult dermatomal pattern.

Redrawn from Stanley D and Kay NRM (eds). Surgery of the elbow. Hodder Arnold 1998 (fig 1.3, p 3).

By 30 weeks the shafts of the humerus, radius and ulna are well ossified and there is cartilaginous cover of the distal humerus and proximal radius and ulna. By this time all elements required for elbow movement are present.

Postnatal development

After birth the most important anatomical changes that occur at the elbow relate to ossification of the lower humeral and upper radial and ulnar epiphyses.

The distal humerus ossifies by four ossific centres: the capitellum and lateral part of trochlea, the medial epicondyle, the medial two-thirds of the trochlea and the lateral epicondyle (Fig. 1.5). The distal humerus is cartilaginous at birth. This is important as trauma to the distal humerus in the first 6 months of life can displace the whole of the distal humerus, which can be difficult to diagnose by plain radiographs. In addition, it is essential to be aware of the sequence in which the ossific centres appear at the elbow in order to appropriately recognize and manage paediatric elbow injuries.

Figure 1.5 The time of appearance of the ossific centres at the lower end of the humerus.

Redrawn from Stanley D and Kay NRM (eds). Surgery of the elbow. Hodder Arnold 1998 (fig 1.7, p 5).

The ossific centre for the capitellum and the lateral one-third of the trochlea appears first. This occurs early in females at between the 1st and 11th month and between 1st and the 26th month in males. The narrower medial portion of the lozenge-shaped epiphysis forms the lateral part of the trochlea, while the lateral portion is closely associated with the lateral epicondyle. This anatomical arrangement is called the lateral condylar epiphysis. If, therefore, the capitellar epiphysis is displaced due to trauma, it almost invariably displaces as one piece including the lateral epicondyle, irrespective of whether or not the lateral epicondyle epiphysis is ossified. This arrangement of the capitellar ossific centre explains the classification of lateral condyle fracture as described by Milch. Milch type 1 is the same as Salter–Harris type IV and Milch type 2 as Salter–Harris type II (Fig. 1.6). The capitellar ossification centre fuses with the trochlear and the lateral epicondylar epiphyses at puberty and to the humerus shaft at 14–16 years.

Figure 1.6 Lateral humeral condylar fractures. (A) Milch type 1 fracture, which is a Salter–Harris type IV epiphyseal fracture. (B) Milch type 2 fracture, which is a Salter–Harris type II epiphyseal fracture.

Redrawn from Canale ST (ed). Campbell’s operative orthopaedics (10th edn). Mosby 2002 (fig 33.47, p 1426). © Elsevier 2002.

The medial epicondyle is the second ossification centre to appear. It is apparent between the 5th and 8th year in females and between the 7th and 9th year in males. It is completely extracapsular and is always separate from the remainder of the lower humeral epiphysis. It serves as an origin for the common flexor origin and has the ulnar nerve running immediately posterior. It can become completely detached and incarcerated in the elbow joint after dislocation of the elbow and must be carefully evaluated following this injury. It fuses to the rest of the humerus at the age of 20.

The ossific centre for the medial two-thirds of the trochlea appears third. This becomes apparent between the 7th and 11th year in females and between 8th and 13th year in males. It forms in two parts, each with its own blood supply. The lateral part from the metaphysis and the medial part from structures attached to the medial epicondyle, a feature which may affect the pattern of avascular necrosis. It fuses with the capitellum at puberty and the rest of the humeral shaft at 14–16 years.

The lateral epicondyle ossific centre appears last, between the 8th and 11th year in females and between the 9th and 13th year in males. Like the medial epicondyle, it is also extracapsular. It serves as the attachment for the common extensor origin. It fuses with the capitellum at 6 months and to the humerus at puberty. As a result of early fusion fracture displacement of the lateral epicondyle is rare.

The ossification centre of the head of the radius appears at 4 years in females and at 5 or 6 years in males. It is entirely intracapsular and is liable to develop avascular necrosis (AVN). It fuses with the radial shaft at 14 and 17 years of life. The ossification centre of the tip of olecranon appears, usually in two parts, at the 9th year of life in females and the 11th year in males. It fuses with the rest of the shaft between the ages of 14 and 16 (Fig. 1.7).

Figure 1.7 Stages in the ossification of the radial and ulna epiphyses.

Redrawn from Stanley D and Kay NRM (eds). Surgery of the elbow. Hodder Arnold 1998 (fig 1.8, p 6).

Ossification at the elbow

Table 1.2 Ossification centres at the elbow

Knowledge of the normal epiphyseal ossification times is essential in the diagnosis of paediatric elbow injuries. The order of appearance of the centres can be remembered using the useful mnemonic CRITOE (Capitellum, Radial head, Internal (medial) epicondyle, Trochlea, Olecranon, External (lateral) epicondyle).When doubt exists it is appropriate to undertake radiographs of the contralateral elbow. Abnormalities of development and their management will be dealt with in Chapter 15.