Classification Of Limb Malformations On The Basis Of Embryological Failures
Alfred B. Swanson, M.D.
Many complexities face the scientist when he attempts to classify the variable congenital malformations of the limbs. Numerous writers have attempted to categorize the established clinical entities into some order, but to date none have been completely successful.
In the past, the use of strange-sounding expressions to describe some common deficiencies has further confused the picture. Terms such as adactyly, arachnodactyly, brachydactyly, brachyphalangia, clinodactyly, camptodactyly, ectrodactyly, ectrosyndactyly, macrodactyly, Polydactyly, symbrachydactyly, syndactyly, hypodactyly, arthrogryposis, cleft hand, split hand, lobster-claw hand, central aplasia, perodactyly, peromanus, peropus, perochirus, talipomanus, clubhand, meromelia, hemimelia, amelia, ectromelia, phocomelia, hypertrophy, macrodactylia, arachnodactylia, gigantism, proximal femoral focal deficiency, intercalary, clinarthrosis, and synostosis have been used to describe various anomalous conditions. It is our belief that a terminology which would be more descriptive and which would help to clarify the relationship of the defects is very much needed. However, there should be no objection to authors' using existing terms in the subclassification of certain descriptive conditions.
A workable classification must use simple, easily remembered terminology. It must be concise enough to receive clinical entities with minimal confusion, but at the same time broad enough to permit the full categorization of complex cases. An ideal classification could be made by grouping cases according to etiology, but unfortunately the etiology of many of these defects is still obscure. Enough basic evidence has been collected, nonetheless, to group cases according to the parts that have been primarily affected by certain embryological failures. This approach has been used in the classifi-cation system to be presented.
Early Limb Development
Study of the early development of limbs in the human embryo demonstrates the fact that limb differentiation occurs in a definite sequential order. The upper and lower limbs are recognizable first as small buds of tissue on the lateral body wall at the fourth postovulatory week. These buds grow and differentiate rapidly in the ensuing three weeks. The various regions of the limbs grow in a proximodistal sequence. The arm and the forearm, for example, appear before the hand. The skeletal elements of the limbs are found within the limb buds. These condensations soon chondrify in a definite order and ossification follows. The differentiation of the soft tissue elements of the limb usually follows an order similar to that of the skeletal elements unless a disorder of development or differentiation occurs.
Occurrence of Defects
Most limb defects occur during the embryonic phase of differentiation. Environmental factors inhibit the rate of orderly differentiation of the part which is most rapidly changing. Certain common congenital defects can be predicted consistently by disturbing the embryo at precise stages of development. It is possible to observe the clinical manifestations of arrest of development and of differentiation, and to determine at which time during the embryonic stage and at which site on the limb the defect occurred.
The degree of severity and the place at which the insult occurs on the fashioning limb bud can be compared to that of abscess formation in adult tissues. In the abscess there is an area of central destruction surrounded by an area of cellular infiltrate, with resulting scar tissue formation and structural deformity. The same destructive process occurring in embryological life before structural formation had occurred would certainly lead to disorganization of the developing tissue about the area of destruction. The various clinical pictures are felt to represent varying degrees of destruction within this organization of the limb mesenchyma. The time at which the insult occurs and the sequential development of the part are also important, as is the location of the destructive process, and will determine the type of ensuing deformity.
Common Environmental Agents
Anoxia, irradiation, antivitamins, hormones, drugs, and some viral infections are the most common environmental agents in the production of these defects. The mother's ability to metabolize or handle these agents and the individual's genetic pattern can be important factors in modifying the final configuration of the deformity. The anatomist, the biochemist, the embryologist, and the geneticist, along with the clinician, continue to make important advances in understanding these problems.
Comprehensive and useful classifications of congenital limb deficiencies, which have proved valuable to those working with child amputees, have been published recently. These classifications are based on a description of absent skeletal parts. A classification useful to those interested in congenital malformations of the hand has also been published and includes provision for the evaluation of the total anatomy of the limb.
Although the embryological insult to the limb is usually not so specific as to result in a sharp line of demarcation, certain patterns of these deficiencies can be grouped. Experience in classifying 300 cases of congenital upper-limb malformations has shown us that the cases may involve a total part-i.e., both the skeletal and the associated soft parts-or may involve only the dermomyofascial structures. A classification which considers all limb elements, both skeletal and soft tissue, would best answer the needs of the clinician and surgeon. Many cases involving soft tissue deficiencies only are milder manifestations of certain general deficiency patterns- for example, a case in which parts of the thumb only were deficient. This should be categorized with the radial longitudinal deficiencies or radial clubhand cases, as they represent a mild deficiency of the preaxial or radial radical of the limb.
The Proposed Classification
Experience with this classification, which was designed primarily for use with hand anomalies, has shown that it also lends itself to use for the entire upper limb and for the lower limb as well.
This classification takes note of the similarities in certain pathological entities. Subclassification of the groups recognizes the differences and expresses the mildness or the severity of the type. An example is clubhand (arrest of radial longitudinal development) . In addition to the fact that the radius is either partially or totally absent, the condition can be associated with hypoplasia or aplasia of the thumb or carpal bones or of the musculature on the preaxial or radial side of the limb. Each group can be subclassified into its degrees of severity as desired for completeness.
Occasionally the insult to the limb may result in mixed involvement. As an example, the severe central longitudinal arrest of development (cleft hand) may be manifested as an almost transverse arrest of the entire hand with only rudimentary radial and ulnar digits present. The judgment of the clinician will be required to categorize these relatively rare cases appropriately. In certain cases where mixed involvement prevents the examiner from establishing a specific classification, he may want to group this rare case into a mixed-type category. This type of categorization should occur very infrequently, and in our experience has not been necessary.
Use of Silhouette Drawings
Each case reviewed should be recorded on a silhouette drawing which shows an outline of the extremity and of the skeletal parts (Fig. 1 ). Shading out of absent parts and labeling associated defects can facilitate the subclassification of deficiency categories. Further description of deficient parts can be facilitated by anatomical division of the limb into shoulder girdle, arm, forearm, and hand, or pelvic girdle, thigh, leg, and foot. These can be broken down further into carpus, digits (1, 2, 3, 4, and 5), phalanges (1, 2, and 3), proximal, middle, and distal parts of long bones. Description of muscle loss, skin and nail variations, nerve, motor, or sensory deficits, associated contractures or relaxations, and such conditions as the subluxation or dislocatio of joints, range of motion of joints, vascular anomalies associated with spinal, visceral, or other soft tissue defects, can be listed for completeness.
Cases of transverse arrest of the limb may be categorized easily by using the well-known amputation level. As an example, a certain type of transverse arrest of the forearm might also be described as a transverse arrest, short below-elbow type.
Note: The dark and stippled areas in the illustrations represent varying degrees of insult to the embryological limb anlage.
This classification categorizes the malformations of limbs as follows:
I. Arrest of development of parts
(Shoulder: S; arm: A; forearm: F; hand: H)
A. Transverse. The deficiencies in this group represent the so-called congenital amputations, ranging from aphalangia to amelia. Usually the stump is well padded with soft tissue and may show rudimentary digits or a dimpling at the end of the stump. It represents a transverse arrest in the limb anlage (Fig. 2 ).
1. Classical phocomelia, in which the hand is attached directly to the trunk, demonstrating the failure of development of intermediate segments of the limb (Fig. 3 ).
2. Other intercalary segmental defects-S, A, F, H (i.e., incomplete phocomelia).
C. Longitudinal (pre- and post-axial deficiencies)
1. Radial: The absence of parts or deficiencies on the radial or preaxial side of the limb vary from deficient thenar muscles to a short floating thumb, and from deficient carpals, metacarpals, and radius to the classical radial clubhand (Fig. 4 ).
2. Central: The middle finger or metacarpal may be missing, as in the cleft hand. The second, third, and fourth metacarpals and the so-called central rays of the hand are noted to be embryolog-ically differentiated at a separate time from the radial and ulnar rays. In severe central deficiencies, these digits may be reduced to nubbins. In an extreme case, the defect may result in complete suppression, similar to a transverse arrest and resulting in an aphalangia (Fig. 5 ).
3. Ulnar: The little and ring fingers may be deficient, with or without associated deficiencies in the ulna and carpal bones (Fig. 6 ).
II. Failure of differentiation of parts
A. Shoulder. Undescended scapula, absence of pectoral muscles, etc.
B. Arm. Synostosis of elbow.
C. Forearm. Synostosis of the proximal radius and ulna with or without dislocation of the radial head (Fig. 7 ).
1. Syndactyly, from simple skin bridging to fusion of parts (Fig. 8 ).
2. Contracture secondary to failure of differentiation of muscle, ligaments, and capsular structures. From simple trigger thumb to flexion contracture of the little finger (camp-todactyly) to severe arthrogryposis of the hand.
3. Lateral deviation or displacement due to asymmetrical abnormalities of the digits (clinodactyly).
III. Duplications (S, A, F, H)
Duplication of parts probably occurs as a result of a particular insult to the limb bud and ectodermal cap at a very early stage of their development, so that splitting of the original embryonic part occurs. These defects may range from Polydactyly to twinning or mirror hands (Fig. 9 and Fig. 10 ).
IV. Overgrowth (S, A, F, H)
In digital gigantism, the abnormality usually is greatest at the periphery. The whole limb may be affected. Some cases appear to be due to skeletal overgrowth with normal-appearing soft parts. Others show excess fat, lymphatic and fibrous tissue. Neurofibromata, lymphangioma, or angioma may be present. During growth, the enlarged part may increase in size at a relatively greater rate than the normal parts. However, in some cases the size difference remains relatively unchanged (Fig. 11 ).
V. The congenital circular constriction band syndrome
Faulty focal development along the course of the limb may be the result of necrosis of the developing mesenchymal tissues. The theory that extrinsic amniotic bands cause these defects seems less attractive than that intrinsic circumferential necrosis occurs on the developing limb. Annular constriction bands or rings may represent an area of necrosis of the superficial tissue. When these constriction bands are severe, they may result in intrauterine gangrene, and true fetal amputations may occur. The circumscribed proximal scar on the limb usually is just deep enough to cut off normal vascular and lymph return and results in chronic edema of the limb. If a circumferential focal necrosis occurs distally in the early stages of hand development, the differentiation pattern may become disorganized, re>sulting in syndactyly, Polydactyly, synostosis, and constriction bands with or without amputation of digits. The necrosis of tissue and its resultant fusion of parts is not unlike an untreated third-degree burn with bridges of scar.
VI. Generalized skeletal defects
Defects in the limb may be manifestations of a generalized defect, such as appear in dyschondroplasia, achondroplasia, arachnodactyly, dia-strophic dwarfism, etc. Certain generalized skeletal defect syndromes are characterized by distinct abnormality patterns, as in diastrophic dwarfism (Fig. 13 and 14 ).
(Pelvic girdle: P; thigh: T; leg: L; foot: F)
I. Arrest of development of parts
A. Transverse. The hip joint is classed with the pelvis, the knee joint with the thigh, and the ankle joint with the leg. The deficiencies in this group represent the so-called congenital amputations ranging from aphalangia to amelia (Fig. 15 ).
1. Classical phocomelia (Fig. 16 ).
2. Other intercalary segmental defects, i.e., proximal femoral focal deficiency (Fig. 17 ) or incomplete phocomelia.
1. Tibial: The absence of parts on the tibial or preaxial side of the lower limb may vary from partial to complete absence of the tibia and deficiencies on the medial aspect of the foot (Fig. 18 ).
2. Central: Cleft foot with the absence of the central rays is the typical entity (Fig. 19 ).
3. Fibular: The fibular deficiency represents the postaxial side of the limb and may present as partial or complete absence of the fibula and the associated lateral aspect of the foot (Fig. 20 ).
II. Failure of differentiation of parts
A. Pelvic girdle. Congenitally dislocated hip is a classical example of this group (Fig. 21 ).
B. Thigh. For example, congenital dislocation of the knee (Fig. 22 ).
C Leg. For example, congenital pseudarthrosis of the tibia and fibula (Fig. 23 ).
D. Foot. For example, congenital clubfoot (Fig. 24 ).
V. The congenital circular constriction band syndrome
VI. Generalized skeletal defects
The author is grateful to Dr. Akira Fujiwara, Dr. Charles H. Frantz, Richard Rae, and Shirley Furgerson for their assistance and suggestions in preparing the material for this article.
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Alfred B. Swanson, M.D. is the Medical Consultant Area Child Amputee Center Grand Rapids, Michigan