Anatomy and Growth

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Anatomy and Growth

It is impossible to separate the anatomy from the growth of the physis. Each is dependent upon the other. They live together and they die together. When the physis ceases to exist, growth is completed and vice versa. In this chapter an attempt is made to discuss anatomy and growth separately. In chapters of the various anatomic sites (Part II) they will be discussed together.

This chapter is offered as a basic understanding of the growth plate as it pertains to fracture. It is not a comprehensive work on the anatomy, growth, and development of the physis. The aspects of physiology, biochemistry, endocrinology, and metabolism of the physis are not included. A representative portion of the extensive literature on the physical aspects of anatomy and growth of the physis is documented here. The advent of MR imaging has introduced new perspectives in studying anatomy of the physis [3, 20–22].

Contents

History. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. ... 7 AnAtomy.. . . 7 Physis ... .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 8 Zone.of.Ranvier. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. ... 9 Epiphysis. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. ... 9 Blood.Supply. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 11 Epiphysis.Versus.Apophysis. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 11 Stress.and.Fracture.Patterns.... .. .. .. .. .. .. .. .. .. .. .. .. .. . 12 GrowtH ... .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. . 12 Growth.Assessment.... .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. . 13 Blood.Supply. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 13 Nerve.Supply. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 14 Physeal.Strength.. . . 14 Growth.Disturbance... .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. . 16 Physeal.Closure. ... .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. . 17 references. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. .. 17

History

The word epiphysis appeared in the English language as early as 1634. The first suggestion of the impor- tance of the structure now known as the physis began when Hales, in 1727, noted that bones grew in length only at their ends. This was verified by Duhamel in 1742, John Hunter in 1837, and by numerous subse- quent investigators. The microscopic anatomy of the physis was described by Müller in 1858. Basic effects of injury to the physis, both experimental and clinical, were recorded by Ollier, Vogt, and Hutchinson between the years 1867 and 1894 and by Hass in 1917 [31, 46, 52, 56, 68, 70, 71].

AnAtomy

All long bones of a growing child consist of an epiphysis, physis, and metaphysis at each end separated by the diaphysis (Fig. 2.1). Physis is a Greek word (phy- ein) which means nature, or to generate. In English it means something that grows or becomes. English medical dictionaries designate the physis as the seg- ment of bone responsible for growth in length of the bone.

Fig. 2.1

Anatomy.of.a.prototype.long.bone.(excluding.metacarpals,.metatarsals,.and.phalanges).in.children

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Dia means between {the physes}. The diaphysis is the initial and primary center of ossification (PCO).

It becomes the central shaft of a long bone and is composed of mature, lamellar bone with a strong cortical exterior. It enlarges circumferentially by periosteal, membranous osseous tissue apposition on the original enchondral model, but does not grow longi- tudinally. All long bones (humerus, radius, ulnar, femur, tibia, fibula, clavicle, metacarpals, metatarsals, phalanges, and ribs) have one PCO, located in the diaphysis. Flat bones (scapula and innominate) and vertebrae have multiple primary centers of ossification (Fig. 5.1).

Meta means adjacent to {the physis}. The metaphyses denote the flaring ends of the central shaft of a long bone and are composed of endosteal, spongy, trabecular bone surrounded by the exterior thin cortical bone, both of which are prone to crush or torus fractures.

Epi means upon {the physis}. The chondro-osseous epiphysis rests upon the physis and articulates with the adjacent bone. At birth all epiphyses, except the distal femur, consist only of cartilage and therefore are not visible on routine roentgenographs. Most, but not all, epiphyses contain at least one secondary center of ossification (SCO).

Physis

The physis is the reference point of a growing bone and differentiates immature bone from mature bone, which has no physis but retains the other anatomic nomenclature.

The physis is a complex structure, discoidal in form and often referred to as a “plate,” i.e., the epiphyseal growth plate. Its cellular anatomy is defined in terms of layers: germinal, proliferative, columnar, hypertrophic, and provisional calcification (Fig. 2.2), each with a designated function. Various authors have grouped these into three, four, or five zones. The germinal zone is also called the resting or reserve zone.

Its functions include storage of nutrients and accu- mulation of stem cells. The proliferative and columnar zones provide for cell division, differentiation of chondrocytes oriented in columns, and matrix production. In the hypertrophic zone the cells enlarge in size and show enhanced metabolic activity with an established program of apoptosis. At the zone of provisional calcification vascular channels invade the dead columnar cells and mineralization of the inter- cellular matrix occurs, later to be replaced by osteoblasts and bone. The metaphyseal bone adjacent to the zone of provisional calcification is sometimes re-

Fig. 2.2

Anatomy. and. blood. supply. of.

the.physis .The.physis.has.been.

artificially. expanded. to. detail.

its.individual.zones

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ferred to as primary spongiosa [6, 7, 10, 12–14, 16, 17, 23, 24, 33, 37, 41–43].

The physis is also composed of noncellular compo- nents, the matrix, through which the cell columns traverse. It is the dominant structural feature in- fluencing the strength of the physis [10]. Since this physis is interposed between the epiphysis and the primary center of ossification of the diaphysis-metaphysis it could be called the primary physis. At birth the primary physis is smooth and typically flat or gently dome-shaped (proximal femur, Fig. 26.1; proximal humerus, Fig. 17.1). With growth some physes, e.g., the distal femur, develop gentle undulations.

The physis is avascular. Its supply of oxygen and nutrients is provided by epiphyseal vessels [6, 7]. Small arterial branches arise at right angles to the main epiphyseal artery (arteries) in the SCO and pass through small cartilage canals in the resting zone to terminate at the top of the cell columns in the proliferative zone [7].

Primary physes (between epiphyses and metaphyses), secondary physes (surrounding the SCO), and the apophyseal physes have all similar structure and function. Knowledge of structure and function of these physes is being rapidly expanded by MR imaging [3, 20–22].

Zone of ranvier

The periphery of the growth plate, the periphysis, surrounds the physis of tubular bones (Fig. 2.3). It contains fibrovascular tissue, undifferentiated mesenchymal tissue, differentiated epiphyseal and physeal cartilage (the zone of Ranvier), and the osseous ring of Lacroix. The zone of Ranvier is responsible for latitudinal growth and Lacroix’s perichondral ring provides mechanical support for the physis [81]. Mi- toses occur in the periphysis in both longitudinal and transverse directions, allowing both longitudinal and latitudinal (circumferential) growth [6, 7, 9, 12, 18, 25, 26, 30, 32–34, 56]. The surface periosteum is continu- ous with the perichondrium. The periosteum contributes significantly to the strength of the physis [2], but does not provide appreciable appositional growth [18].

Epiphysis

The epiphysis includes the whole of the cartilage at the end of a long bone except for the physis. A SCO usually develops within it. This ossified nucleus is a miniature metaphysis surrounded by a physis which enlarges by enchondral ossification globally or spher-

ically into the epiphyseal cartilage (Figs. 2.1, 2.4) in all directions until it approximates the shape of the pre- existing cartilage mass that makes up the epiphysis (Figs. 2.5, 2.6) [4, 7, 15, 21, 56, 58, 81]. Since this physis is wholly within the secondary center of ossification it could be called the secondary physis.

All long bones have an epiphysis and a physis at each end. Usually a SCO develops within the epiphysis at each end of the bone. However, some long bones (metacarpals, metatarsals, phalanges of the hands and feet, clavicles, and ribs) develop a SCO at only one end. Growth occurs from the physis at each end re- gardless of whether or not the epiphysis develops a SCO [73, 94].

A few long bone epiphyses develop multiple secondary centers of ossification. The most extreme example is the humerus which has two secondary ossification centers proximally (Fig. 17.1) and four distally (Fig. 15.1), all of which ossify at different ages.

Flat bones (scapula and innominate) and vertebrae have multiple secondary centers of ossification (Fig. 5.1).

Fig. 2.3

Anatomy. and. blood. supply. of. the. periphery. of. the.

physis,.the.zone.of.Ranvier

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Fig. 2.4

Anatomy. and. blood. supply. of.

the. epiphysis,. and. its. secondary.center.of.ossification

Fig. 2.5

Growth.patterns.of.a.typical.enchondral.bone .a.In.addition.to.longitudinal.growth,.the.flat.primary.physis.(PP).initially.

also.grows.latitudinally.(circumferentially) .The.developing.secondary.center.of.ossification.enlarges.globally.from.its.

own.spherical.secondary.physis.(SP) .b.Once.the.secondary.center.of.ossification.(SCO).is.relatively.mature,.latitudinal.

growth.of.the.physis.is.essentially.appositional.growth,.supplied.by.the.zone.of.Ranvier.(open arrows) .c.Bone.remodeling.occurs.in.the.metaphysis.by.subperiosteal.osteoclasts.and.osteoblasts.(shaded arrows) .(Adapted.from.Ogden.[33],.

with.permission)

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To complicate matters further, some epiphyses begin as one large cartilaginous mass and develop into two separate secondary ossification centers (for example the proximal femoral capital epiphysis and greater trochanter apophysis, and the proximal tibial epiphysis and the tibial tubercle apophysis). The two proximal tibial ossification centers eventually coalesce into one. These and other vagaries will be discussed in the chapter for each epiphysis.

Blood Supply

The blood supply of the physis derives from three in- dependent sources: epiphyseal arteries, intramedul- lary metaphyseal arteries, and the periosteal arteries of the circumferential zone of Ranvier (Fig. 2.2). In late fetal and early postnatal periods the cartilaginous epiphysis contains numerous vessels some of which cross the physis. However, no vessels have been found passing from the metaphyseal to the epiphyseal side across the physis in normal fully developed physes (for example after the first 3 years of life) [6, 8, 28, 35, 40, 42, 45, 46]. Epiphyseal arteries penetrate the epiphysis and form branches which provide nutrition to the germinal, proliferating, and columnar cell zones (Fig. 2.2). The epiphyseal vessels are therefore

responsible for longitudinal growth. The pattern of vessels within the epiphysis changes with maturity. In the unossified epiphysis, the vascular canals are mainly parallel in a longitudinal direction. After development of the SCO, the vascular canals are radial [3].On the metaphyseal side the major interosseous artery combines with arteries penetrating the metaphysis peripherally from the periosteum to form loops which penetrate into the enlarging spaces of the dying hypertrophic cells. The metaphyseal vessels nourish osteoprogenitor cells which produce bone on the cartilage matrix scaffold, called the primary spongiosa metaphyseal bone. Thus the metaphyseal vessels influence on growth is indirect.

A third blood supply consisting of additional periosteal branches supply the specialized zone of Ran- vier, where undifferentiated mesenchymal cells give rise to chondroblasts (Fig. 2.3).

Epiphysis Versus Apophysis

Differences between epiphyses and apophyses may have been first distinguished by Galen [83], and are clearly defined. The primary physis of an epiphysis is perpendicular to the longitudinal axis of a long bone.

Its main function is longitudinal growth. The epiphysis forms the articular surface with the adjacent bone and typically has no musculo-tendinous attachments.

It is sometimes referred to as a “pressure epiphysis”

[33, 34, 36, 83]. The bones containing epiphyses are detailed in Part II.

The primary physis of a long bone apophysis (apo

= “from,” “away,” “off,” “asunder”) is parallel or oblique to the axis of the long bone. Apophyses nei- ther participate in longitudinal growth nor articulate with adjacent long bones. Apophyses of flat bones (scapula, innominate) are on the periphery, contrib- uting to circumferential growth, and those on the tip of vertebral processes contribute to growth of these projecting processes. The major function of an apophysis is for the attachment of musculotendinous struc- tures which provide motion or stability to the long bone, the flat bone, or the vertebra. It is sometimes referred to as a “traction epiphysis” [33, 36, 83]. The apophyses are not discussed in this text.

The cartilaginous mass at the end of some long bones have features of both an epiphysis and an apophysis. The most notable are the proximal ulna, the proximal tibia, proximal femur, and the distal humerus. These vagaries are discussed in their respec- tive chapters. In addition, there are anomalies of both epiphyses and apophyses which, though uncommon,

Fig. 2.6

Spherical.growth.of.secondary.center.of.ossification . Growth.arrest.line.(arrows).in.the.distal.femoral.epiphysis.of.a.10.year.3.month.old.girl,.1.year.4.months.following.a.distal.femoral.fracture

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can be a cause for confusion in evaluating roentgenographs following trauma. These occur most notably on the hands [1, 38], feet [38], and tibial medial mal- leolus (Chapter 11A).

Stress and Fracture Patterns

There is a strong correlation between the orientation of the epiphyseal plates and the related stress patterns (compressive stress, tensile stress, and shear stress).

The greater portions of most epiphyseal primary physes lie at right angles to the longitudinal axis of the bone and are most often subjected to compression between the epiphysis and metaphysis [98].

Fracture patterns of the physis are determined by the nature and direction of the applied force as well as by regional variations of physeal anatomy, and will usually occur through the weakest structure [110].

This is the zones of hypertrophy and provisional calcification, where the nonstructured cell spaces are the largest and the supporting cartilaginous matrix is the smallest (Fig. 2.2). Thus, fractures of the physis commonly occur transversely in the hypertrophic zone of the physis (type 3 fracture) (Fig. 30.1). The fracture often, however, wanders into other zones of the physis (Fig. 30.2) or into the metaphysis (type 2) or epiphysis (type 4). The noncellular matrix contains small collagenous fibrils. There may be a relationship between these fibrils and the vertical or oblique direction of fractures within the physis as seen in type 4 and 5 fractures [11, 39].

GrowtH

The phenomenon of growth is the paramount differ- ence between pediatric and adult orthopaedics [77].

The rate of growth, the size (area), and the contour of each physis changes as the chondro-osseous skeleton progressively matures. Growth is the evolution of the organism, from embryo to adult. It is influenced by gender, genetics, health, disease, injury, environment, and possibly exercise [42, 58, 61, 67, 77, 81, 85]. The exact effect of functional stimulus on bone growth needs further study. It may be that longitudinal growth of bone is predetermined in embryonic life, and unless there is disturbance to its vascular supply or injury to the physeal cartilage, it will continue to grow until maturity [70]. Growth occurs at the physis by the process of enchondral (“within cartilage”) ossification.

The physiologic mechanisms governing or control- ling physeal growth are not well known. Agents

known to influence physeal growth may be divided into systemic or general factors, which affect many or all physes, and local factors, which affect a single physis. Systemic factors include genes, hormones, nutrition, and general health. Local factors or forces that may affect physeal growth include the blood supply, the physiologic mechanical forces acting on the physis, trauma, and infection [13, 56]. Growth of the physis is also influenced by precise and complex biological controls including chemical, metabolic, hormonal, nutritional, and physical factors. Scores of articles, both observational and experimental, a few of which are referenced here [19, 50, 51], have been written on each of these aspects of growth. Since this text con- cerns fracture of the growth plate, only the physical factors are presented.

The gradual lengthening (growth) of the extremities and spine occurs solely in the primary physes and the secondary physes of epiphyses of long bones and vertebrae [19, 52, 68, 81]. Longitudinal growth begins when cells in the germinal zone divide and line up in columns. Mitotic cells are observed only in the germinal and adjacent part of the proliferative zones [4, 5].

These sensitive layers, the germinal and proliferative zones, are the areas of primary concern in any injury involving the growth plate. Damage to cells in these layers, in contradistinction to the columnar, hypertrophic, and provisional calcification zones, may have serious, long-term consequences of growth patterns [66, 80, 81]. Most of the actual bone elongation occurs in the proliferative, columnar, and hypertrophic layers of the physis by enlargement of the cells (Fig. 2.2).

Selective deactivation of membrane transporters responsible for volume regulation contributes to the enlargement of chondrocytes and plays an important role in long bone growth [84].

On the cellular level growth is a controlled matura- tion process beginning with cell division in the proliferative zone [80] through completion of cell hypertrophy. Kember [80] suggests that within a single individual the rates of cell proliferation in all growth plates are the same while the sizes of the proliferation zones are different and are specific to each plate. The primary mechanism of cell enlargement is cytoplas- mic and nuclear swelling [59]. During growth, growth plate chondrocytes increase their volumes tenfold.

Longitudinal growth is linearly related to the final volume reached by the hypertrophic chondrocytes [84]. Selective deactivation of membrane transporters that are responsible for volume regulation contributes to the enlargement of chondrocytes and plays an important role in physeal growth [57, 85]. Thus the rate of growth is regulated primarily by modulation of

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chondrocytic activity [19, 79] and depends primarily on the age of the individual and the inherent potential for growth of each plate [42].

Circumferential (latitudinal, transverse, diametric) growth of the physis occurs initially from latitudinal growth of the physis itself (Fig. 2.5)and later as appositional growth from the zone of Ranvier (Fig. 2.3) [18, 34, 43, 99]. Bone remodeling occurs as subperiosteal osteoclasts in the metaphysis reduce the thickness of the cortical bone and osteoblasts in the diaphysis increase the thickness of the cortical bone of the diaphysis.

A small amount of longitudinal growth occurs within the epiphysis itself, by the same process from a miniature physis situated spherically around the SCO (Figs. 2.1, 2.4, 2.5, 2.6, 3F.8b) [58, 81, 87, 97]. A super- ficial layer of epiphyseal cartilage is destined to serve as articular cartilage and is incapable of ossification (Fig. 2.5c) [87]. For most long bones the primary physis accounts for at least 95% of longitudinal growth.

The secondary physis of the epiphysis, as it enlarges, accounts for the remaining 5% or less of longitudinal growth (Fig. 2.6). Since the growth of the epiphysis accounts for relatively little longitudinal growth [97]

only the ossified portion is usually considered when calculating growth and bone length discrepancy on growth charts.

In addition to differences of growth of the primary physis versus the secondary physis, there are also variations in the amount of growth from the primary physis at one end of a bone versus the other end (Fig. 2.7). This was first observed by Ollier in 1867 [52] and first estimated by Digby in 1915 [62]. Al- though Digby’s methods of measurement have been questioned [76] his figures have been accepted in the ensuing decades. For example, overall the distal femur contributes 70%, and the proximal end 30% of total length. This ratio of growth is not, however, con- stant throughout the growth period. Growth from each end is proportionally equal before birth and during the first portion of postnatal life [65]. For example, in the newborn the large cartilaginous proximal femoral epiphysis contributes 50% of the length. As growth proceeds the proximal end contributes a progressively smaller percentage of the longitudinal growth, i.e., 40, 30, 20, 10%, etc. At the conclusion of growth the aggregate overall growth is 30% at the proximal end, 70% at the distal end.

Growth Assessment

Growth assessment provides a reference for normal development, and in abnormal states a guideline for treatment [63, 81]. The knowledge of time (patient age) and pattern of ossification of both the primary and secondary centers of ossification is necessary in evaluating both growth and growth injury (Chap- ter 5, Fig. 5.1). Patterns of growth are very similar for boys and girls despite the different ages at which each gender achieves certain milestones [90]. The annual growth of the limbs and trunk are related to the skeletal age of each child, and the increments of growth per skeletal year are subject to statistical analysis.

Methods of growth prediction of leg length and mature height have been derived [49, 69, 108]. When as- sessing an injured growth plate it is essential to know not only the percentage of bone growth from each end of the bones, but how much growth remains at each end at that age. Treatment decisions depend on it.

Tables, charts, and graphs [49, 52, 53, 62, 64, 69, 86, 88, 92, 101] are valuable aids in these assessments and predictions. This phenomenon will be discussed in more detail in chapters at each site (Part II), when data are available.

Blood Supply

Most of the factors which effect physeal growth in- volve, in one way or another, the vascular supply which brings nutrients to the physis [15, 54, 60, 70, 71, 78, 100, 102–107]. If there is ischemia on the metaphy- seal side of the physis the metaphyseal vascular loops do not invade the hypertrophic zone and those cells continue to accumulate (Fig. 2.8). Since the epiphyseal vessels continue to supply the germinal and proliferating layers of the physis, cell production, and longitudinal growth continues.

Ischemia of the epiphyseal vessels deprives the germinal and proliferating layers of nutrition (Fig. 2.9).

The metaphyseal vascular loops continue to invade the hypertrophic zone causing the physis to narrow.

Longitudinal growth ceases in the areas affected, pro- ducing angular deformity and diminished growth. If the entire physes is affected growth ceases completely.

Since the periosteal vessels which supply the zone of Ranvier are rarely selectively and circumferentially compromised, loss of circumferential growth does not occur as an isolated event.

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nerve Supply

Little is unknown concerning the influence of the nervous system on growth of the physis. Abnormali- ties of bone growth produced by disturbances of in- nervation appear to be slight. The initial effect of sud- den paralysis produces increased lengthening of the affected bone. It is speculated that this lengthening is due to the hyperemia of disuse. In the presence of per- sistent paralysis growth of the limb is ultimately de- pressed [93].

Physeal Strength

The qualitative mechanical strength of the physis is generally greater in female rats and increases with age [30, 55]. At the onset of puberty, however, the increase in tensile strength slows down significantly in females and moderately in males. Although these gender and age factors may influence fracture statistics in rats, there is no evidence to suggest that human male physes are weaker than female physes as an explanation for more physeal fractures in males than females.

Fig. 2.

Relative.growth.from.each.end.of.the.major.long.bones .The.horizontal line.represents.birth .The.numbers.represent..

the.final.percentage.of.growth.supplied.by.each.end.of.the.bone .(Adapted.from.Pritchett.[92],.with.permission)

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The peak incidence of physeal fractures usually corresponds with the timing of the growth spurt in both genders (Fig. 4.2) [48]. The increase in growth rate is accompanied by four changes: increase in rate of cell division, increase in the length of replicating columns, increase in the number of columns, and an increase in size of the hypertrophied cells. Increased cell size in the hypertrophic zone reduces the amount of matrix available to resist fracture. An increase in weakness is thus predictable. The shear strength of the physis varies with anatomic location and is a function of modulus, inclination, and thickness [47], and possibly the interdigitation of undulations known as pegging or mammillary processes present at the physeal-metaphyseal junction of some physes (Fig. 2.10) [33]. There is no study documenting the sites or ages at which these papillae occur, or their effect on the shear strength of the physis.

A transverse fracture of the physis may run across various layers. Usually, however, the fracture travers-

es through the hypertrophic zone and zone of provisional calcification and is therefore on the metaphyseal side of the physis (Fig. 30.1).

As a child grows, the physis becomes progressively thinner until its complete obliteration [81]. Although experimental work in heifers suggests that thicker growth plates are weaker [110], the rate of physeal fractures is definitely greater in humans in adolescence (Fig. 4.2) when the physis is thinner, than at earlier ages. Thus, physeal fracture statistics are influenced by these growth/age factors. The type of mechanical loading (compression, tension, shear, and torque) applied to the physis also influences the histologic zone of failure in a predictable pattern [89].

However, the more important factors are the size of the patient and the activities of participation at the time of fracture (mass × velocity = force).

The amount of growth remaining in any bone depends more on skeletal maturity and bone age than on chronologic age. Knowledge of the expected age of

Fig. 2.

Temporary. ischemia. of. the. metaphysis. impedes. the.

enchondral.ossification.process,.but.not.growth.of.the.

germinal.and.columnar.layers.of.the.physis

Fig. 2.

Temporary. ischemia. of. the. epiphyseal. blood. supply.

results. in. death. of. the. germinal. cells. and. loss. of.

growth

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normal growth cessation of each physis helps deter- mine both the appropriate treatment and the antici- pated length of follow-up. Physeal union may be defined as beginning with the first mineralized bridge from epiphyseal bone to metaphyseal bone and end- ing with the complete disappearance of the cartilaginous physeal plate and its replacement by bone and marrow [73]. This process may take months to years.

The peripheral parts of the plate are the last to close [73]. This cessation of growth varies not only between males and females, but also within each gender, and occasionally from right to left side within the same individual. These aspects are discussed and referenced in Chapter 6 and in each site chapter (Part II).

Growth Disturbance

Hefti et al. [74] identified four types of growth disturbance following fractures in children. In type I, the overall growth activity of the physis is increased (overgrowth). In type II growth activity of the physis is severely impaired or completely arrested. In type III growth is stimulated in a portion of the physis creat- ing an angular deformity. Type IV is asymmetric growth arrest (a bone bridge). Longitudinal overgrowth of bone (type I), as sometimes occurs following diaphyseal fracture, is an interesting phenomenon. The most plausible explanation is increased vascular supply to the physis due to the hyperemia of fracture healing. When this occurs with a physeal fracture, the amount of increased growth is usually modest (Fig. 11A.2c) as compared with a metaphyseal or diaphyseal fracture. Type II fractures occur when fractures traverse into the germinal and cell division

areas. This is more likely to occur when the physeal

“plate” is anatomically irregular, rather than in a smooth flat plane [16, 17, 27, 29, 30, 44]. Growth following fracture of the physis will progress unabated if the fracture is confined to the columnar and hypertrophic layers and the blood supply to the epiphysis remains intact.

When one physis of an extremity long bone is irreversibly injured, the physis at the other end of the bone is frequently exhibits increased growth. This could be called compensational growth or true overgrowth. This phenomenon has received little scien- tific study [75]. It may occur to a significant amount of some cases, and not at all in others. A similar phenomenon occurs with the proximal (humerus and femur) and distal (radius/ulna and tibia/fibula) long bones of the extremities. For example, when a tibial physis is irreversibly injured the femur may exhibit true overgrowth (Fig. 8J.1). Again, the amount of compensatory overgrowth of the adjacent bone may be significant or nonexistent.

Spontaneous correction of angular deformity following fracture occurs by vector pressure changes on the physes of the injured bone and by remodeling by means of increased periosteal appositional bone formation in the concavity of the deformity and removal of bone on the convexity. It occurs with greater rapid- ity and on a considerably larger scale in a child than in an adult, through physeal growth [82]. The longitudinal vector compression forces result in asymmetric physeal growth. The growth rate of the physis is faster on the concave side of the deformity than on the convex side [91, 95]. Spontaneous correction of post fracture rotational deformity also occurs associated

Fig. 2.10

CT. scan. of. the. distal. fibial.

epiphyses.in.a.13.year.2.month.

old. boy. shows. undulations. . of. mammillary. processes . (AP.

roentgenographs. are. shown.

on.Fig .11B 4a)

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with growth, but to a lesser degree and perhaps only in the first year after fracture [72, 96, 109].

Physeal Closure

Little is known concerning closure of the growth plate other than anatomic observations. There is no research suggesting that a diminution of blood supply to the epiphysis is responsible for the reduction of germinal cells. Initially proliferating chondrocytes in the germinal and proliferating zones become less in number, and chondrocytes in the zone of cell columns form into groups rather than columns. In the zone of hypertrophy the large vacuolated cells also decrease in number. The physis becomes progressively thinner.

Capillary tufts invade from the metaphysis, pass through the physis to reach the secondary center of ossification. As physeal cartilage is removed bone is laid down around the capillary tufts until bone unites the metaphysis to the epiphysis. The plate is now ef- fectively closed, as all remains of the growth plate are slowly obliterated. A narrow transverse line of roent- genographic increased density, the so-called “epiphyseal scar,” marks the site of the former physis. This line may persist for life [56, 66].

Premature (abnormal) cessation of growth may occur with any injury to the physis (e.g., radiation, infection, vascular deprivation, frostbite, burn, etc.), but most commonly occurs following fracture. Injuries other than fracture which have been found to cause premature growth arrest are not presented in this text.

references Anatomy

1. Adams CO: Multiple epiphyseal anomalies in the hands of a patient with Legg-Perthes’ disease. J Bone Joint Surg 19:814-816, 1937

2. Amamilo SC, Bader DL, Houghton GR: The periosteum in growth plate failure. Clin Orthop 194:293-305, 1985 3. Barnewolt CE, Shapiro F, Jaramillo D: Normal gadolini-

um enhanced MR images of the developing appendicular skeleton: Part 1. Cartilaginous epiphysis and physis. Am J Roentgenol 169:183-189, 1997

4. Brashear HR Jr: Epiphyseal fractures of the lower extremity. Southern Med J 51:845-851, 1958

5. Brashear HR Jr: Epiphyseal fractures: a microscopic study of the healing process in rats. J Bone Joint Surg 41A:1055- 1064, 1959

6. Brighton CL: Structure and function of the growth plate.

Clin Orthop 136:22-32, 1978

7. Brighton CT: The growth plate. Orthop Clin N Am 15:571- 595, 1984

8. Brookes M, Landon DH: The juxta-epiphyseal vessels in the long bones of fetal rats. J Bone Joint Surg 46B:336-345, 9. Burkus JK, Ogden JA: Development of the distal femoral 1964 epiphysis: a microscopic investigation of the zone of Ran- vier. J Pediatr Orthop 4:661-668, 1984

10. Cohen B, Chorney GS, Phillips DP, Buckwalter JA, Rat- cliffe A, Mow VC: The microstructural tensile properties and biomechanical properties of the bovine distal femoral growth plate. J Orthop Res 10:263-275, 1992

11. Dallek M, Mommsen U, Jungbluth KH, Sauer HD: Injuries of the collagenous fibres and the epiphyseal plate [Ger- man]. Z Kinderchir 36:123-124, 1982

12. Delgado-Baeza E, Miralles-Flores C: The growth plate.

Mapfre Med 4 (suppl II):1-5, 1993

13. Farnum CE, Wilsman NJ: Growth plate cellular function.

In: Buckwalter JA, Ehrlich MG, Sandell LJ, Trippel SB (eds).

Skeletal Growth and Development: Clinical Issues and Ba- sic Science Advances. American Academy of Orthopaedic Surgeons, Rosemont, IL, 1997, Chapter 13, pp 203-223 14. Fazzalari NL, Wilsdon CA, Byard RW, Byers S, Foster B:

Morphology of the growth plate and trabecular bone (abstr). J Bone Joint Surg 76B(suppl):107, 1994

15. Floyd III W E, Zaleske DJ, Schiller AL, Trahan C, Mankin HJ: Vascular events associated with the appearance of the secondary center of ossification in the murine distal femoral epiphysis. J Bone Joint Surg 69A:185-190, 1987 16. Fujii T, Takai S, Arai Y, Kim W, Amiel D, Hirasawa Y: Mi-

crostructural properties of the distal growth plate of the rabbit radius and ulna: Biological, biochemical, and morphological studies. J Pediatr Orthop 18:87-93, 2000 17. Harris WR: Epiphyseal injuries. AAOS Instruct Course

Lect 15:206-214, 1958

18. Heřt J: Growth of the epiphyseal plate in circumference.

Acta Anat 82:420-436, 1972

19. Hunziker EB: Growth plate formation, structure, and function. In Skeletal Growth and Development: Clinical Issues and Basic Science Advances. Buckwalter JA, Ehrlich MG, Sandell LJ, Trippel SB (eds): Rosemont, IL, Ameri- can Academy of Orthopaedic Surgeons, 1997, Chapter 12, pp 187-202

20. Jaramillo D, Connolly SA, Mulkern RV, Shapiro F: Devel- oping epiphysis: MR imaging characteristics and histologic correlation in the newborn lamb. Radiology 207:637-645, 21. Jaramillo D, Hoffer A: Cartilaginous epiphysis and growth 1998 plate: Normal and abnormal MR image findings. Am J Roentgenol 158:1105-1110, 1992

22. Jaramillo D, Shapiro F: Growth cartilage: normal appearance, variants, and abnormalities. MRI Clin N Am 6(3):455-471, 1998

23. Kember NF: Cell division in enchondral ossification.

J Bone Joint Surg 42B:824-839, 1960

24. Kumar R, Madewell JE, Swischuk LE: The normal and abnormal growth plate. Radiol Clin N Am 25:1133-1153, 25. Langenskiöld A: The growth mechanism in the periph-1987

eral part of the normal growth plate. In: de Pablos J (ed).

Surgery of the Growth Plate. Ediciones Ergon, S.A., Ma- drid,1998, Chapter 5, pp 29-30

26. Langenskiöld A: Role of the ossification groove of Ranvier in normal and pathologic bone growth: A review. J Pediatr Orthop 18:173-177, 1998

(12)

27. Lee FY, Rho JY, Harten R Jr, Parsons JR, Behrens FF: Mi- cromechanical properties of epiphyseal trabecular bone and primary spongiosa around the physis: An in situ na- noindentation study. J Pediatr Orthop 18:582-585, 1998 28. Lewis OJ: The blood supply of developing long bones with

special reference to the metaphyses. J Bone Joint Surg 38B:928-933, 1956

29. Moon BS, Williams JL, Schmidt TL: Fracture toughness of growth plate cartilage. In: Puzas JE (ed). Transactions of the 46th Annual Meeting of the Orthopedic Research Society, Orthopedic Research Society, Chicago, IL, 2000;25:988 30. Morscher E: Strength and morphology of growth cartilage

under hormonal influence of puberty. Reconstr Surg Trau- mat 10:3-104, 1968

31. Nicholson JT, Nixon JE: Epiphyseal fractures. J Pediatrics 59:939-950, 1961

32. Oestreich AE, Ahmad BS: The periphysis and its effect on the metaphysis: I. Definition and normal radiographic pattern. Skel Radiol 21:283-286, 1992

33. Ogden JA: Anatomy and physiology of skeletal development. In: Ogden JA. Skeletal Injury in the Child. 3rd edn.

Springer, New York, 2000, Chapter 1, pp. 1-37

34. Ogden JA, Rosenberg LC: Defining the growth plate. In:

Uhthoff HK, Wiley JJ (eds). Behavior of the Growth Plate.

Raven Press, New York, 1988, pp 1-15

35. Oni OOA: Chondrocyte hypertrophy in the growth plate is a vascular phenomenon. J Bone Joint Surg 80B (Supp I):84, 36. Parsons FG: On pressure epiphyses. J Anat Phys 39:402-1998

412, 1905

37. Robertson Jr WW: Basic science and pathology: Newest knowledge of the growth plate. Clin Orthop 253:270-278, 38. Roche AF, Sunderlund S: Multiple ossification centres in 1990 the epiphyses of the long bones of the human hand and foot. J Bone Joint Surg 41B:375-383, 1959

39. Scott BA, Pease DC: Electron microscopy of the epiphyseal apparatus. Anat Rec 126:465-495, 1956

40. Shapiro F: Epiphyseal disorders. New Engl J Med 317:1702- 1710, 1987

41. Shapiro F, Holtrop ME, Glimcher MJ: Organization and cellular biology of the perichondral ossification groove of Ranvier: A morphological study in rabbits. J Bone Joint Surg 59A:703-723, 1977

42. Siffert RS: The growth plate and its affections. Instr Course Lect 18:J1 1962-1969, Chapter 5:26-40, 1973

43. Siffert RS: The growth plate and its affections. J Bone Joint Surg 48A:546-563, 1966

44. Smith DG, Geist RW, Cooperman DR: Microscopic exam- ination of a naturally occurring epiphyseal growth plate fracture. J Pediatr Orthop 8:306-308, 1985

45. Spira E, Farin I: The vascular supply to the epiphyseal plate under normal and pathologic conditions. Acta Orthop Scand 38:1-22, 1967

46. Trueta J, Morgan JD: The vascular contribution to osteo- genesis. I. Studies by the injection method. J Bone Joint Surg 42B:97-109, 1960

47. Williams JL, Varni JN, Eick JD, Petersen EC, Schmidt TL:

Shear strength of the physis varies with anatomical location and is a function of modulus, inclination and thickness. J Pediatr Orthop 17:214-222, 1999

Growth

48. Alexander CJ: Effect of growth rate on the strength of the growth plate-shaft junction. Skel Radiol 1:67-76, 1976 49. Anderson M, Green WT, Messner MB: Growth and predic-

tions or growth in the lower extremities. J Bone Joint Surg 45A:1-14, 1963

50. Armstrong PF: Cell kinetics and control of physeal growth.

In: Uhthoff HK, Wiley JJ (eds). Behavior of the Growth Plate. Raven Press, New York, 1988, pp 233-236

51. Bentley G, Greer RB: The fate of chondrocytes in en- dochondral ossification in the rabbit. J Bone Joint Surg 52B:571-577, 1970

52. Bisgard JD, Bisgard ME: Longitudinal growth of long bones. Arch Surg 31:568-578, 1935

53. Blais MM, Green WT, Anderson M: Lengths of the growing foot. J Bone Joint Surg 38A:998-1000, 1956

54. Brashear HR Jr: Epiphyseal avascular necrosis and its relation to longitudinal bone growth. J Bone Joint Surg 45A:1423-1438, 1963

55. Bright RW, Richmond V, Burstein AH, Elmore SM: Epiph- yseal-plate cartilage. A biomechanical and histological analysis of failure modes. J Bone Joint Surg 56A:688-703, 56. Brighton CT: Clinical problems in epiphyseal plate growth 1974

and development. Instruct Course Lect 7:105-122, 1974 57. Breuer GJ, VanEnkevort BA, Farnum CE, Wilsman NJ:

Linear relationship between volume of hypertrophic chondrocytes and the rate of longitudinal bone growth in growth plates. J Orthop Res 9:348-359, 1991

58. Buckwalter JA, Ehrlich MG, Sandell LJ, Trippel SB: Skeletal Growth and Development: Clinical Issues and Basic Sci- ence Advances. American Academy of Orthopaedic Sur- geons, Rosemont, IL, 1998

59. Buckwalter JA, Mower D, Ungar R, Schaeffer J, Ginsberg B: Morphometric analysis of chondrocyte hypertrophy.

J Bone Joint Surg 68A:243-255, 1986

60. Cameron DA: Erosion of the epiphysis of the rat tibia by capillaries. J Bone Joint Surg 43B:590-594, 1961

61. Dickerman Z, Loewinger J, Laron Z: The pattern of growth in children with constitutional tall stature from birth to age 9 years. Acta Paediatr Scand 73:530-536, 1984 62. Digby KH: The measurement of diaphyseal growth in

proximal and distal directions. J Anat Phys 50:187-188, 63. Dimeglio A: Growth in pediatric orthopaedics. J Pediatr 1915

Orthop 21:549-555, 2001

64. Diméglio A, Bonnel F: Growth and development of the knee. In: dePablos J (ed). The Immature Knee. biblio stm, Barcelona, 1998, Chapter 1, pp 4-8

65. Editorial u: J Am Med Assoc 105:1935

66. Eeg-Larsen N: An experimental study on growth and glycolysis in the epiphyseal cartilage of rats. Acta Physiol Scand 38 (suppl 128):1-77, 1956

67. Fahmy A: Correlation between growth rate and changes in the epiphyseal plate (abstr). J Bone Joint Surg 37B:731, 68. Gatewood, Mullen BP: Experimental observations on the 1955

growth of long bones. Arch Surg 15:215-221, 1927 69. Green WT, Anderson M: Skeletal age and the control of

growth. Instr Course Lect 18:199-217, 1962

70. Haas SL: The localization of the growing point in the epiphyseal cartilage plate of bones. Am J Orthop Surg 15:563-586, 1917

(13)

71. Haas SL: The relationship of the blood supply to the longitudinal growth of bone. Am J Orthop Surg 15:157-171, 305-316, 1917

72. Hagglund G, Hansson L, Normal O: Correction by growth of rotational deformities after femoral fracture in children.

Acta Orthop Scand 54:858, 1983

73. Haines RW: The histology of epiphyseal union in mam- mals. J Anat 120:1-25, 1975

74. Hefti F, vonLaer L, Morscher E: Principles and pathogen- esis of post-traumatic axial malalignment in the growth years [German]. Orthopade 20:324-330, 1991

75. Hellstadius A: An investigation, by experiments on ani- mals, of the role played by the epiphyseal cartilage in longitudinal growth. Acta Chir Scand 95:156-166, 1947 76. Hendryson IE: An evaluation of the estimated percentage

of growth from the distal epiphyseal line. J Bone Joint Surg 27:208-210, 1945

77. Hensinger RN: The challenge of growth: The fourth di- mension of pediatric care (Editorial). J Pediatr Orthop 18:141-144, 1998

78. Jaramillo D, Laor T, Jaleske DJ: Indirect trauma to the growth plate: Results of MRI imaging after epiphyseal and metaphyseal injury in rabbits. Radiology 187:171-178, 79. Kember NF, Sissons HA: Quantitative histology of the hu-1993

man growth plate. J Bone Joint Surg 58B:426-435, 1976 80. Kember NF: Watching cells divide: A computer animated

film of bone growth. Cell Tissue Kinet 11:201-202, 1978 81. Krauspe R, Raab P: The role of the growth plate (physis).

Normal growth. J Bone Joint Surg 81B (abstr):130-131, 82. Kwon DJ, Moon MS: The influence of physeal injury upon 1999 growth correction of deformed rat tibia. Int Surg 65:341- 345, 1980

83. Lewin P: Epiphyses. Their growth, development, injuries, and diseases. Am J Dis Child 37:141-178, 1929

84. Liow RYL, Bowden G, Urban JPG, Murray DW: Chondro- cyte hypertrophy at the growth plate–the role of cell volume regulation in long bone growth (abstr). J Bone Joint Surg 81B (suppl II):51, 1999

85. Malina RM: Exercise as an influence upon growth: Re- view and critique of current concepts. Clin Pediatr 8:16-26, 86. Maresh MM: Linear growth of long bones of extremities 1969 from infancy through adolescence. Am J Dis Child 89:725- 742, 1955

87. McKibbon B, Holdsworth FW: The dual nature of epiphyseal cartilage. J Bone Joint Surg 49B:351-361, 1967 88. Meredith HV: Length of the upper extremities in homo-

sapiens from birth through adolescence. Growth 11:1-50, 89. Moen CT, Pelker RP: Biomechanical and histological cor-1947

relations in growth plate failure. J Pediatr Orthop 4:180- 184, 1984

90. Moseley CF: Normal growth and patterns of growth. In: de Pablos J (ed). Surgery of the growth plate. Ediciones Ergon, S.A., Madrid, 1998, Chapter 1, p 3-5

91. Murray DW, Wilson J: Bone growth and remodeling after fracture. J Bone Joint Surg 77B (suppl I):91, 1995 92. Pritchett JW: Practical Bone Growth. Seattle, WA, 1993,

pp 163

93. Ring PA: The influence of the nervous system upon the growth of bones. J Bone Joint Surg 43B:121-140, 1961 94. Roche A: The sites of elongation of human metacarpals

and metatarsals. Acta Anat 61:193-202, 1965

95. Ryöppy S, Karaharju EO: Alteration of epiphyseal growth by an experimentally produced angular deformity. Acta Orthop Scand 45:490-498, 1974

96. Schneider M: The effect of growth on femoral torsion. An experimental study in dogs. J Bone Joint Surg 45A:1439- 1449, 1963

97. Siegling JA: Growth of the epiphyses. J Bone Joint Surg 23:23-36, 1941

98. Smith JW: The relationship of epiphysial plates to stress in some bones of the lower limb. J Anat 96:58-78, 1962 99. Solomon L: Diametric growth of the epiphyseal plate.

J Bone Joint Surg 48B:170-177, 1966

100. Spira E, Farin I, Karplus H: Blood supply of the epiphyseal plate in growing rabbits (abstr). J Bone Joint Surg 48B:391, 101. Trotter M, Gleser GC: Estimation of stature from long 1966 bones of American whites and Negroes. Am J Phys An- thropol 10:463-514, 1952

102. Trueta J: The blood supply adjacent to the epiphyseal plate and its influence on growth (abstr). J Bone Joint Surg 41B:206, 1959

103. Trueta J: The influence of growth on the sequelae of bone and joint injuries (abstr). J Bone Joint Surg 40B:154-155, 104. Trueta J, Amato VP: The vascular contribution to os-1958

teogenesis. III. Changes in the growth cartilage caused by experimentally induced ischaemia. J Bone Joint Surg 42B:571-587, 1960

105. Trueta J, Buhr AJ: The vascular contribution to osteogen- esis. V. The vasculature supplying the epiphyseal cartilage in Rachitic rats. J Bone Joint Surg 45B:572-581, 1963 106. Trueta J, Little K: The vascular contribution to osteogen-

esis. II. Studies with the electron microscope. J Bone Joint Surg 42B:367-376, 1960

107. Trueta J, Trias A: The vascular contribution to osteogen- esis. IV. The effect of pressure upon the epiphyseal cartilage of the rabbit. J Bone Joint Surg 43B:800-813, 1961 108. Tupman GS: A study of bone growth in normal children

and its relationship to skeletal maturity. J Bone Joint Surg 44B:42-63, 1962

109. Verbeek HOF: Does rotation deformity, following femur shaft fracture, correct during growth? Reconstr Surg Traumat 17:75-81, 1979

110. Williams JL, Do PD, Eick JD, Schmidt TL: Tensile properties of the physis vary with anatomic location, thickness, strain rate, and age. J Orthop Res 19:1043-1048, 2001