AVIAN BASIC and CLINICAL ANATOMY and COMMON MUSCULOSKELETAL PROBLEMS

Patrick T. Redig DVM, PhD

Department of Small Animal Clinical Sciences

Avian Core CVM 6880

1. Introduction: This discussion on avian clinical anatomy will deal with the musculoskeletal adaptation for flight and an overview of the structures that are of importance for recognition of clinical problems and as landmarks for surgical approaches.
2. Background: Birds evolved from therapod dinosaurs and in fact may be their living descendants. Consequently they bear strong anatomical relationships to dinosauran ancestors although aerodynamics and energetics of flight have resulted in much unique modification of soft tissue and skeletal structures. Though there are some 9,500 species of birds currently living (compared to about 4,000 mammals), the demands of flight have limited the extent to which large differences in skeletal structures have developed. At first glance such a statement may seem off the mark since there appears to be a bewildering array of sizes, shapes, and colors among birds. Yet, in fact, there is less variability in skeletal detail among the entire class Aves than there is within the mammalian order of just Carnivora. The bulk of the alterations in birds have been in "peripheral" structures such as beaks, feet, shape of wing, and so on.
3. Specific modifications evolved to meet the demands of flight:
   1. The beginnings -- bipedal dinosaurs (e.g. velociraptors) (figure 1)
      
      1. Derivations leading toward flight in birds occurred during the Jurassic period - 160 million years ago. Current theories suggest that the motions and machinery for flight evolved from the ground up rather than down from the trees.
      2. Retained dinosauran features include:
         1. egg-laying (figure 1a.)
         2. specialized skin modifications -- scales
         3. air sacs
         4. Warm-bloodedness?
   2. New Developments
      1. Extensive modifications of axial and appendicular skeleton for flight
         
         1. Shifting of center of gravity forward through loss of heavy dinosauran tail--larger forelimbs took over balancing activity relieving the need for the counterbalance of the heavy tail (figure 2, skeleton of a merlin -- a small falcon).
            
         2. Reduction in weight of head structures and modifications of mouth parts to take over many of the manipulative functions of the forelimbs such as food handling, nest material manipulation, and grooming (figure 2).
            
         3. Centralization of heavy muscles on appendicular skeleton
            
         4. Reduction in skeletal weight through pneumatization of large bones
            
         5. Reinforcement of skeleton through trussing (figure 3 -- cutaway of avian humerus showing trussing of trabecular bone for internal strengthening -- similar to concept of bicycle spokes).
            
         6. Weight reduction through vertebral fusion which eliminates the need for heavy lumbar muscles - (figure 4 -- skeleton of great horned owl in dorsal recumbency showing fusion of vertebral column elements)
            
      2. More powerful muscles, more efficient heart and respiratory systems
         
         1. e.g. Birds can maintain sustained flight of more than 8 hours at altitudes over 20,000 feet (how high can humans go without oxygen support?).
            
         2. e.g. On a gram for gram basis, avian muscle is five times stronger than mammalian muscle.
            
      3. Feathers -- modified scales
         
   3. The results -- skeletal features of the modern bird
      1. Axial Skeleton
         1. Shortened body axis -- among vertebrates, only the frog has a shorter body trunk. Heavy muscles for flight and ground propulsion (thighs) are placed under the center of gravity and the center of lift (shoulder joint) (figure 2).
            
         2. Head modifications -- major ones are for:
            -Eyesight -- up to 50% of the head by volume is filled by eyeballs (figures 5a,b); scleral oscicles support large eyeballs; additionally there is extensive development within the brain of the visual lobes to provide integrating network -- done at the expense of olfaction -- a necessary modification for high speed locomotion. Birds can detect electromagnetic radiation in the ultraviolet range viz-a-viz they can see if the ultraviolet spectrum
            -Jaw modifications are for lightnesss and manipulative functions formerly carried out by the forelimbs. Both upper and lower jaws articulate; most birds have a "synovial" or membranous joint between the rostrum and the cranium. Some, especially parrots, have an actual articulating joint and exhibit "cranial kinesis" (figure 7)
            -Skull articulates on 1st cervical vertebral body via a single condyle rather than 2 -- increases mobility of head (figure 8)
            
         3. Cervical vertebrae
            1. Variable numbers -- 11 in a parakeet, 25 in swans, 7 in either a man or a giraffe.
               
            2. Heterocoelus condition -- saddle-shaped articular surfaces -- increases mobility of the neck.
               
            3. Dorsal, lateral, and ventral spinous processes are present for attachment of ligaments that support the neck in place of a ligamentum nuchae (figure 8)
               
            4. Birds such as herons have specially modified cervical vertebrae -- articular facets are arranged so as to cause a sharp "Z" kink -- allows the the neck to be folded in flight and provides a a mechanical accelerator for hurling the head or beak at prey objects.
               
         4. Thoracic vertebrae -- the ribs are borne on these
            
            1. Vary in number from 3-10.
               
            2. The first 3-5 are fused (notarium) except in penguins. Fusion is necessary to provide rigidity to the column for flight; lack of fusion in penguins facilitates swimming mode of locomotion (figure 9a).
               
            3. The last 2-3 are usually not fused -- clinically significant because this is the usual site of a back injury -- signs are loss of use of pelvic appendages (figure 10).
               
            4. Ribs -- composed of two segments, joined nearly at right angles--the dorsal segment is directed caudally, the ventral segment is directed anteriorly, hinged at the junction (figure 9a,b,c)
               
            5. Uncinate processes -- boney processes that overlap adjacent ribs to give greater rigidity to skeleton (figure 9a,b,c)
               
         5. Lumbar and Pelvic Vertebrae
            
            1. Fused into a bony cover called the synsacrum
            2. Elements of illeum, ischium, pubic bones, and acetabulum are present.
            3. Sacral vertebrae are fused into a bony structure called the pygostyle -- tail feathers are attached to this.
      2. Appendicular skeleton (be able to identify the following bones on a radiograph)
         1. Bones of the pectoral girdle
            1. Scapula -- varying degrees of development -- attachment of flexors and elevators of the wing (figure 8)
            2. Sternum with keel (carina) -- flight muscle attachment -- keel well- developed in strong flyers -- flat in ostriches (figure 9a,c)
            3. Coracoid bone (figure 9a,c)
               -support pillar for shoulder
               -opposed contractile force when major pectorals contract
               -fractures and dislocates with frontal impact (e.g. windows or mirrors)
               
            4. Furcula or Clavicle (wishbone) (figure 11)
               - a strut to hold wings apart
               -limits medial collapse of body cavity when the pectoral muscles contract for the downstroke of the wing
               -widest angle in the strongest flyers
               -hypocleideum -- point of fusion of two clavicles
               
            5. At the juncture of the coracoid, scapula and clavicle, a natural opening forms through which the tendon of the supracoracoideus muscle passes to insert on the dorsal aspect of the humerus
               -known as the foramen triosseum (triosseal canal) (figure 8)
               -creates a pulley arrangement thereby reversing the direction of pull of the tendon so as to serve as an elevator of the wing.
               
         2. Anatomy of the Pectoral Limb proper (figure 12)
            
            1. Humerus (figure 13)
               -deltoid (pectoral) crest
               -bicipital crest - pneumatic foramen on posterior margin
               - Projections distally, proximal to the condyles for attachment of tendons of origin for the antebrachial flexors and extensors (see below)
               - pneumatized -- air sac extending from the cranial thoracic group fills the central cavity.
               - the humerus typically has a pronounced "S" shape which allows placement of intramedullary pins for fracture repair without interfering with joint integrity (figure 14).
               
            2. Radius and Ulna -- Antebrachium (figure 12)
               -ulna is the larger bone -- may be strongly curved in the anterior-posterior plane
               -secondary flight feathers are attached here to the periosteum on the dorsal surface of the ulna; they form the flying or lifting surface of the wing -- this section is strongly cambered or curved.
               -the radius serves as part of the extensor apparatus of the carpus
               
            3. Metacarpus -- (figure 12) hand --consists of :
               -2 vestigial carpal bones (radialcarpal and ulnarocarpal)
               - 2 metacarpals (major and minor)
               - 3 phalanges. 1st phalanx forms the alula, 2nd is the largest and has 3 primaries attached, and #3 is a single digit to which is attached the 10th primary.
               
      3. Muscles of the pectoral limb -- show the greatest modifications for flight. May comprise 35% of the body weight -- shifted craniad under the center of lift and have long tendons reaching distally to the portion of the limb controlled by them.
         
         1. Superficial pectoral (pectoralis) (figure 15)
            -Origin: keel, clavicle, coracoid and sternal ribs
            -Insertion: ventral pectoral crest, proximal humerus
            -Innervation: pectoral nerves
            -Action: downstroke of the wing, depresses leading edge of pars longus of the propatagialis tendon.
            (Lab note) Detach the pectoralis muscle from its mutliple sites of origin along the keel, beginning distally, and reflect it towards its point of insertion. The supracoracoideus lies deep and medial to the pectoralis -- note airsac that lies between the two muscles.
            
         2. Supracoracoideus (figure 15)
            -Origin: sternum, clavicle and coracoid
            -Insertion: by means of a prominent tendon upon the lateral tubercle of the humerus. The tendon passes through the triosseal foramen.
            -Action: elevates the wing
            (Lab Note) Examine the lateral surface of the coracoid and locate the coracobrachialis caudalis muscle.
            
         3. Coracobrachialis caudalis (ventralis) (figure 16)
            -Origin: lateral surface of the coracoid
            -Insertion: medial (ventral) tubercle of the humerus
            -Action: depresses the wing along with the pectoralis muscle
            -Clinically: frequently torn with shoulder dislocations rendering the bird significantly impaired for flight.
            
         4. Propatagialis (pars brevis and pars longus) (figure 17)
            -Origin: Distal end of the coracoid bone
            -Insertion: 2 parts
            
            1. Pars longus: inserts on the carpo-metacarpus and forms the leading edge of the wing. The patagium is attached to it.
               
            2. Pars brevis: attaches to apeunerosis arising from dorsal musculature in the proximal 1/3 of the antebrachium.
               
            -Actions:
            
            1. Tenses the patagium (elastic web)
               
            2. Extends the carpus
               
            3. Serves as a check ligament to prevent overextension of the elbow joint.
               
            -Clinically: frequently contracts following humeral fractures which limits extension of the wing.
            
         5. Deltoideus major (figure 18)
            Origin: scapula and clavicle
            Insertion: dorsal surface of humerus
            Action: elevates the wing
            
         6. Triceps brachii: two - three heads (figure 18)
            -Origin: One head from scapula, the other from proximal humerus
            -Insertion: olecranon of the ulna
            -Action: extension of the elbow joint
            -Clinically: must be preserved when fixation hardware is applied to the humerus and ulna.
            
         7. Biceps brachii (figure 18)
            -Origin: distal end of coracoid and bicipital crest of humerus
            -Insertion: radius and ulna -- dorsal aspect
            - Actions: flexes the elbow joint and extends the shoulder
            - Note location of radial nerve relative to this muscle
            
         8. Brachialis
            -Origin: distal end of the humerus
            -Insertion: proximal portion of the ulna
            - Action: flexes the elbow joint
            There are four muscles of the antebrachium that are important; all are located on the dorsal or lateral aspect:
            
         9. Extensor metacarpi radialis (figure 19)
            -Origin: lateral epicondyle of the humerus
            -Insertion: dorsal surface of the carpometacarpus
            -Action: extends the metacarpus
            
         10. Extensor digitorum communis (common digital extensor)
             -Origin: lateral epicondyle of the humerus
             -Insertion: dorsal surface of the proximal phalanx of digit III with a short link to the alula.
             -Action: extends the carpus, metacarpus, and alula
             -Clinical: is sutured to edge of triceps tendon to stabilize dislocated elbows.
             
         11. Extensor metacarpi ulnaris (ulnaris lateralis) (figure 19)
             -Origin: lateral epicondyle of the humerus
             -Insertion: carpometacarpus
             -Action: flexes the metacarpus -- when wing is extended -- only flexor located on lateral (dorsal) surface of the wing.
             
         12. Supinator
             -Origin: lateral epicondyle of the humerus (deep)
             -Insertion: cranial surface of the radius
             -Action: elevates the cranial border of the antebrachium and supinates (rotates upward) the cranial edge of the wing
             Clinical: tendon of origin may have to be cut in some procedures to reduce a radial luxation.
             
         Musculature of the ventral surface of the antebrachium, while important for locomotion, does not feature in any of the surgical approaches to the wing, hence will not be dealt with here. See Orosz et al for details.
         
      4. Pelvic limb: Osteology -- still used largely for walking, so there is less modification than seen in the wing.
         
         1. Femur
            - variably pneumatized -- from abdominal airsac group
            -articulates with pelvis in a modified ball and socket joint -- gliding joint
            - projects forward in normal perching position (figure 9)
            - externally attached to the body wall by a web of skin, abduction very limited. This web is a regularly used site for subcutaneous injection of fluids.
            
         2. Tibiotarsus / fibula (figures 24,25)
            - most frequent site of fractures
            - Cnemial crest is highly modified in strong swimmers such as loons
            - Fibula is greatly reduced -- limits amount of rotation and sideways stepping ability
            - Tarsal bones are fused with the tibia to form the tibiotarsus
            
         3. Hock joint (intertarsal joint)
            
         4. Tarsometatarsus
            - fusion of 3 metatarsal bones -- can see unfused bones in radiographs of juveniles
            -No marrow cavity
            -Digital tendons run in deep groove on caudal aspect
            -Most, but not all birds have four digits
            -Rear projecting toe is called the hallux (DI).
            -Forward projecting digits are numbered DII, DIII, and DIV
            -The number of bones in each toe is one more than the number of the digit.
             
            
      5. Pelvic Limb Myology: : movement to center of mass with long tendons going to extemities; tendons are often ossified. (Femur: figures 20,21,22,23)
         
         
         1. Iliotibialis cranialis (sartorious)
            -Origin: cranial portion of the iliac crest
            -Insertion: medial aspect of patella and tibiotarsus
            -Action: flexes the hip joint and extends the stifle
            -Clinical: cranial edge serves as a landmark for endoscopic entry point for sexing and general abdominal examination.
            
         2. Iliotibialis lateralis
            -Origin: most of the length of the iliac crest
            -Insertion: joints the fascia of the femorotibilais and inserts with that muscle upon the patella and tibiotarsus
            -Action: flexes the hip and extends the stifle
            -Clinical: large muscle in vultures and fowl, small in psittacines and raptors. Surgical approach to femur lies along its caudal border
            
         3. Iliofibularis
            -Origin: iliac crest caudal to the acetabulum
            -Insertion: proximal end of the fibula
            -Action: flexes the stifle
            -Clinical: Surgical approach to the femur lies between this muscle and iliotibialis lateralis. A large neurovascular bundle lies deep and must be preserved
            
         4. Femorotibialis externus
            -Origin: adherent to most of the length of the craniolateral femur
            -Insertion: patella and proximal tibiotarsus
            -Action: extends the stifle
            -Clinical: typically needs to be periosteally elevated from shaft of femur during surgical approaches.
            Muscles of the tibiotarsal region (figures 24, 25)
            
         5. Fibularis longus (peroneus longus)
            -Origin: patella, cranial and lateral cnemial crests and the lateral fibula
            -Insertion: caudal tarsometarsus and tendon of the flexor perforatus digiti III.
            -Action: extends the intertarsal joint (hock)
            
         6. Tibialis cranialis: lateral and medial heads
            -Origins: lateral head- lateral condyle of the femur, medial head - lateral and medial cnemial crests and rotular crest
            -Insertion: two heads unite to form a common tendon inserting on the dorsal metatarsal groove.
            -Actions: flexes the hock
            
         7. Extensor digitorum longus
            -Origin: cranial surface of the tibiotarsus between the medial and lateral cnemial crests
            -Insertion: the dorsum of the distal-most phalanx of digits II-IV
            -Action: extends the forward digits
            
         8. Gastrocnemius complex (3 heads)
            -Origins:
            1) lateral head -- lateral femoral condyle
            2) intermediate head -- area near medial femoral condyle
            3) medial head -- popliteal area fascia and medial femoral condyle
            -Insertion: All three heads form a common tendon that inserts on the prominent hypotarsal protuberance
            -Action: strong extender of the hock joint
            -Clinical: medial surgical approach to tibiotarsus occurs along cranial edge of medial grastroc.
            
            
            

1. Know radiographic appearance of fractures and soft tissue aberrations
   
2. Know infectious, non-infectious and metabolic musculoskeletal problems in birds
   

1. Fractures and injuries to the vertebral column (figures 29-35): Fractures of the vertebral bodies from impact injuries (collisions with windows, mirrors, vehicles) are difficult to detect radiologically. However, there are often other clinical and radiological signs that lead a clinician to make a presumptive diagnosis.
   
2. Fractures and luxations of the Shoulder Girdle
   
   1. Scapula
      
   2. Coracoid (figures 36 and 37)
      
   3. Keel
      
   4. Shoulder separations/humeral luxations (figure 38)
      
3. Fractures and Luxations of the humerus (figures 39 - 42)
   
   1. Proximal sub-condylar fractures
      
   2. Deltoid and sub-deltoid fractures and avulsions
      
   3. Diaphyseal humeral fractures
      
   4. Distal sub-condylar fractures
      
4. Forearm Injuries (figures 43 - 46)
   
   1. Elbow Luxations -- caudal-dorsal
      
   2. Fractures
      
5. Metacarpal Fractures (figure 47)
   
   1. Major and/or minor metacarpal
      
   2. Digits
      
6. Pelvic Fractures: (figures 48,49,50)
    
   
7. Femoral Injuries
   
   1. Coxofemoral Luxations (figures,51,52,53)
      
   2. Stifle luxations and Diaphyseal Fractures (figure 54,55a,b)
      
   3. Subcondylar Fractures
      
8. Tibiotarsal
   
   1. Stifle Joint luxations and proximal tibiotarsal fractures
      
   2. Diaphyseal and Distal Tibiotarsal Fractures (figures 56a,b)
      
9. Metabolic Musculoskeletal Problems
   
   1. Secondary Nutritional Hyperparathyroidism (juvenile rickets) (figures 57,58,59a,b)
      
   2. Choline-Manganese Deficiency (perosis)
      
   3. Vitamin E/Selenium (with sulfur amino acid deficiency): white muscle disease
      
   4. Vitamin B-complex deficiencies (biotin, riboflavin, thiamine)
      
   5. Excess protein in diet of growing bird, fast feather growth, weights the wings and causes them to fold; may have a genetic factor also.
      
   6. Ionophore toxicity -- muscle necrosis and toxicity -- coccidiostats e.g. Monensin -- growth promoter in cattle and sheep. Horses are most sensitive, chickens are least. Turkeys are more so than chickens. Problems arise when feeds are mixed.
      
   7. Calcium Depletion in laying hens (figures 60,61)
      
10. Infectious Bone Disease Problems (no images)
    
    1. Osteomyelitis -- general
       
    2. Osteopetrosis (chickens): lymphoid leukosis/sarcoma virus -- lymphoid leukosis -- retrovirus -- egg transmitted -- causes tumors in bursa and elsewhere -- usually in adult birds
       
    3. Marek's Disease: Herpes virus -- causes tumors in nerves, and elsewhere, but not in bursa -- usually young birds -- producers vaccinate for this.
       
11. Neoplastic Musculoskeletal Problems (no images)
    
    1. Osteosarcomas (long bones)
       
    2. Rhabdomyosarcoma
       
    3. Hemangiosarcoma
       
    4. Squamous Cell Carcinoma
       
    5. Renal Carcinoma
       
12. Miscellany
    
    1. Vertebral column scoliosis of unknown etiology (figures 62a,b)
       
    2. Maxillary luxation (figure 63)
       
    3. Rupture of the extensor tendon of the m. Hallucis longus (figure 64)
       
    4. Trumpeter Swan with egg in abdomen (figure 65)
       

1. Unique Characteristics of Avian Eyes compared to Mammalian Eyes
   
   1. Much greater resolving power: 2 - 8 times that of mammals
      
   2. All birds have color vision and UV perception is common -- up to 680 nm
      
   3. Visual field is 360 degrees in some birds
      
   4. Complete decussation of the optic nerve at the chiasma
      
   5. Iris is controlled by skeletal muscle rather than smooth muscle -- rapid accomodation to changing light -- essential for high speed locomotion.
      
2. Size: The avian eye is very large; much of it protrudes outside the orbit. Its shape is maintained in part by a series of internal bones known as the scleral oscicles.
   
   1. Range of axial length:
      
      1. Kiwi: 8 mm
         
      2. Ostrich: 50 mm
         
3. Shape: determined by anulus ossicularis sclerae (scleral oscicles)
   
   1. Flat: diurnal birds with narrow heads: e.g. columbiformes
      
   2. Conical: diurnal birds with broad head: e.g. falconiformes
      
   3. Tubular: nocturnal birds: e.g. Strigiformes
      
4. Relative Weight compared to head
   
   • Human: 1%
     
   • Fowl: 7%
     
   • Owl: 30%
     
5. External Features
   
   1. Dorsal and ventral palpebra
      
   2. Nictatating membrane (3rd eyelid): transparent in birds that swim underwater.
      
   3. Large lacrimal gland at base of nictatating membrane
      
   4. Nasal salt gland present adjacent to orbit -- some of its secretions lubricate the eye also.
      
   5. Two large lacrimal puncta that communicate with nasal passages are present in the medial canthus.
      
6. Anterior Chamber
   
   1. Two parts to the lens: dense central portion (optical portion) surrounded by the "annular pad" or ringwulst to which is firmly attached the ciliary process and ciliary body.
      
   2. Large ciliary body in contact with lens -- can change shape of the lens for accomodation.
      
   3. Iris: contains striated rather than smooth muscle -- provides for rapid accomodation -- non-responsive to atropine for creating mydriasis.
      
7. Vitreous Chamber Features
   
   1. Pecten: large, fan-folded structure
      
      1. Obscures the optic disc
         
      2. 30 different functions hypothesized
         
         • nourish the retina
           
         • screen against bright light
           
         • motion detector
           
         • regulator of intraocular pressure
           
   2. Central fovea, plus additional temporal fovea in some birds (raptors, hummingbirds, swifts, swallows).
      
   3. Three layers to posterior portion of globe
      
      1. Sclera or fibrous coat -- outer
         
      2. Choroid layer -- highly vascularized
         
      3. Retina: non-vascularized, pigmented in diurnal birds
         
8. What do you see when eye examination is conducted?
   
   1. Cornea: abrasions, ulcers, infections, synechia (attachement of a fibrous strand between edge of iris and the cornea -- anterior synechia)
      
   2. Anterior Chamber: hyphema (blood) -- may lead to fibrin clots and synechia
      
   3. Lens
      
      • Luxations
        
      • Cataracts
        
      • Synechia (attachment of a fibrous strand between edge of iris and the lens - posterior synechia)
        
   4. Retina
      
      • Pigmentation
        
      • Choroid cascade
        
      • Edema
        
      • Tears, Detachments, colobomas
        

1. Basilic: ventral humerus
   
2. Cutaneous Ulnar: overlying proximal portion of antebrachium on the ventral aspect
   
3. Jugular: Right (left one is 4x smaller)
   
4. Medial Saphenous or metatarsal vein: located on medial aspect of leg just anterior to the intertarsal (hock) joint
   

1. Smith, SA and BJ Smith. Atlas of Avian Radiographic Anatomy. Saunders, Philadelphia. 1992. Pp. 226.
   
2. Evans, HE Anatomy of the Budgerigar, Chapter 5 in Diseases of Cage and Aviary Birds, 2nd edition (M. Petrak ed.). Lea and Febiger, Philadelphia. 1982. Separate chapter on reserve in Vet Med Library
   
3. Williams, D. Ophthalmology, chapter 26 in Avian Medicine: Principles and Application (Ritchie, B. G Harrison, L Harrison, eds). Wingers Publ. Lake Worth, Florida 1994. 1384pp.
   
4. McMillan, MC. Imaging Techniques, Chapter 12 in Avian Medicine: Principles and Application (Ritchie, B. G Harrison, L Harrison, eds). Wingers Publ. Lake Worth, Florida 1994. 1384pp.