RAPIDLY PROGRESSIVE CHARCOT ARTHROPATHY FOLLOWING MINOR JOINT TRAUMA IN PATIENTS WITH DIABETIC NEUROPATHY
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1 ~ _ BRIEF REPORT RAPIDLY PROGRESSIVE CHARCOT ARTHROPATHY FOLLOWING MINOR JOINT TRAUMA IN PATIENTS WITH DIABETIC NEUROPATHY SALLY D. SLOWMAN-KOVACS, EI'HAN M. BKAUNSTEIN, and KENNETH D. BRANDT Neuropathic (Charcot) arthropathy is a slowly progressive, chronic, destructive form of joint degeneration seen in patients with a neurosensory deficit. Attempts to produce neuropathic joint disease experimentally with a variety of deafferentation procedures have generally been unsuccessful. However, if the knee is rendered unstable by anterior cruciate ligament transection (ACLT), breakdown of the joint occurs rapidly in dogs that have previously undergone dorsal root ganglionectomy (DRG) for deafferentation of the ipsilateral limb. In contrast, ACLT in neurologically intact dogs produces only nonprogressive changes that are characteristic of mild osteoarthritis. This report describes 3 patients with longstanding insulin-dependent diabetes mellitus in whom neuropathic arthropathy developed within weeks after minor trauma to the foot or ankle. In these patients, diabetic neuropathy served as the functional equivalent of dorsal root ganglionectomy, and the minor trauma served as the functional equivalent of ACLT. Together, they illustrate the phenomenon From the Indiana University School of Medicine and the Indiana University Specialized Center of Research in Osteoarthritis, Indianapolis. Supported in part by grants AR-20582, AR-7448, and AR from the National Institute of Arthritis and Musculoskeletal and Skin Diseases, and an award from the Arthritis Foundation. Sally D. Slowman-Kovacs, MD: Clinical Assistant Professor of Medicine, Indiana University School of Medicine; Ethan M. Rraunstein, MD: Professor of Radiology, Indiana University School of Medicine; Kenneth D. Brandt, MD: Professor of Medicine and Head, Rheumatology Division, Indiana University School of Medicine, and Director, Indiana University Specialized Center of Kesearch in Osteoarthritis. Address reprint requests to Kenneth D. Brandt, MD, Indiana University School of Medicine, 541 Clinical Drive, Room 492, Indianapolis, IN Submitted for publication June 19, 1989; accepted in revised form October 3, of neurogenic acceleration of joint degeneration in humans. Neuropathic arthropathy (NA; Charcot joint) is a severe, generally chronic, destructive arthropathy complicating conditions associated with neurosensory loss (1,2). Attempts to create NA experimentally by various limb deafferentation procedures have met with only limited success (3-5). For example, in dogs that had undergone unilateral L4-S 1 dorsal root ganglionectomy (DRG) to produce extensive hind limb deafferentation, no gross, histologic, biochemical, or metabolic abnormalities developed in the knees during a 16-month observation period (6). However, when the deafferentation procedure was followed by transection of the anterior cruciate ligament (ACLT), a striking degeneration of the unstable knee developed within 3 weeks, with osteochondral fracture, fibrillation of the articular surface, full-thickness cartilage ulcers, and extensive areas of chondrocyte death (6). In contrast, ACLT in neurologically intact dogs produces only mild nonprogressive osteoarthritis, with minimal morphologic changes in the articular cartilage even after months of joint instability (7). That NA may also develop acutely following joint trauma in patients with underlying neurologic defects is rarely emphasized in the rheumatology literature. For this reason, we herein describe 3 patients with diabetic neuropathy in whom minor trauma to the foot or ankle resulted in acute NA in only 3-6 weeks. We believe that these cases illustrate neurogenic acceleration of degenerative joint disease, and are analogous to the canine model described above. Arthritis and Rheumatism, Vol. 33, No. 3 (March 1990)
2 BRIEF REPORTS 413 A Figure 1. A, Oblique view of the left foot of patient I. Mild cartilage loss and a periosteal reaction are present at the first tarsometatarsal joint, but there is no fracture or dislocation at the tarsometatarsal joints. B, Oblique view of the same foot 6 weeks later. A Lisfranc fracturedislocation of the foot is apparent. Note the gap between the first and second metatarsal shafts and the collapse of cuneiform I (arrow). B CASE REPORTS Patient 1. Patient I, a 50-year-old white woman with a 24-year history of insulin-dependent diabetes mellitus, was successfully treated with antibiotics and a cast for an ulcer of the left big toe. She was in good health for 9 months until she stepped in a hole in her lawn, spraining her left ankle. She presented to her family physician with marked swelling of the left foot, but with minimal pain. A radiograph showed soft tissue swelling, a mild periosteal reaction, subcortical osteopenia, and joint space narrowing, all of which were confined to the first tarsometatarsal joint (Figure IA). Despite therapy with naproxen, diffuse swelling of the left foot persisted, and an examination 6 weeks later revealed warmth and erythema of the skin over the left ankle, with minimal tenderness and limited range of motion of the tibiotalar joint. Nerve conduction studies confirmed the presence of moderately severe sensorimotor peripheral neuropathy in both lower extremities. A second radiograph of the left foot (Figure 1B) now showed extensive soft tissue swelling, a Lisfranc fracturedislocation of the tarsometatarsal joints, and bony fragmentation of cuneiforms 1-111, findings that are consistent with a diagnosis of NA. Patient 2. Patient 2 was a 59-year-old white woman who presented with an %year history of insulin-dependent diabetes mellitus and severe peripheral neuropathy, manifested by a 5-year history of lancinating pain in the legs and severe hypesthesia from the knees to the toes bilaterally. She also had an
3 414 BRIEF REPORTS A B C Figure 2. A, Anteroposterior (AP) view of the right foot of patient 2. The bones appear essentially normal. B, AP view of the same foot 3 weeks later. A fracture of cuneiform 1 is apparent (arrow), with collapse of subcortical bone. C, AP view of the same foot 5 weeks after the initial radiograph. Further collapse of cuheiform I has developed (arrow), and a Lisfranc dislocation of tarsometatarsal joints 11-V is present. A new gap is present between the first and second metatarsals (open arrow). 18-month history of Charcot arthropathy of the left foot. Radiographs of her left foot showed a periosteal reaction, cystic changes, and narrowing of the tarsometatarsal joints. While undergoing treatment for a nonhealing cutaneous ulcer over the first cuneiform of her left foot, she tripped and stumbled over her right foot. During the following week, she developed progressive pain in the right foot, with swelling and tenderness of the right lateral midfoot. A radiograph showed only soft tissue swelling over the navicular and cuneiform bones (Figure 2A). The patient was subsequently treated with a non-narcotic analgesic. A second radiograph (Figurc 2B), which was obtained 3 weeks later because of persistent pain in her right foot, initially revealed only soft tissue swelling. However, subsequent review of this radiograph also revealed a fracture of cuneiform I, which was not apparent on the initial radiograph. Because of persistent pain, swelling, and tenderness, a third radiograph of the right foot was obtained 5 weeks after the initial radiograph (Figure 2C). It now showed collapse of cuneiform I and a Lisfranc fracture-dislocation of the tarsometatarsal joints. Patient 3. Patient 3, a 30-year-old white woman with a 12-year history of poorly controlled insulindependent diabetes mellitus complicated by nephropathy, retinopathy, and neuropathy, was hospitalized for control of her diabetes. In addition to her usual chronic mild, dependent edema, she presented with marked painless swelling of the left foot, which was attributed to either autonomic neuropathy or hypoalbuminemia. Despite her use of support stockings and diuretics, an examination 2 months later revealed persistent swelling of the left foot with edema, erythema, and warmth of the skin overlying the left ankle. A radiograph showed soft tissue swelling, a loose body or talar osteophyte, and a possible talar fracture (Figure 3A). She was given a 1-week regimen of cephalexin for presumptive cellulitis. Three weeks later, the patient stumbled and twisted her left foot. Two weeks after the stumble, she presented with mild pain in the left foot and ankle. Examination revealed moderate edema, warmth, and tenderness of the left ankle and foot, and bony enlargement of the left ankle. A second radiograph, taken 5% weeks after the initial radiograph, now revealed soft
4 BRIEF REPORTS 415 A Figure 3. A, Lateral view of the left ankle of patient 3. It shows an anterior talar osteophyte and a possible talar fracture (arrow). B, Lateral view of the same ankle 5V2 weeks later. There has been resorption of the talar neck. Loose ossific debris scattered anteriorly (arrow) and posteriorly (arrowhead) within the ankle joint, and a calcaneal stress fracture (open arrow) are now present. A periosteal reaction has developed anterior to the tibia1 shaft. B tissue swelling, osteoporosis, marked periosteal reaction, and remarkable soft tissue calcification, with destruction of the neck of the talus and a stress fracture of the calcaneus (Figure 3B). These findings are consistent with a diagnosis of NA. DISCUSSION Diabetic neuropathy is the most common cause of NA in the western world, outranking other deafferentation disorders, such as tabes dorsalis, syringomyelia, and leprosy (I). In patients with diabetes mellitus, the sites most often affected by NA are the tarsometa- tarsal, metatarsophalangeal, and tibiotalar joints (60%, 30%, and lo%, respectively) (8). The differential diagnosis of diabetic neuropathic arthropathy includes cellulitis, pyarthrosis, osteornyelitis, osteoarthritis, and reflex symptomatic dystrophy. Plain radiographs should prove helpful in differentiating osteoarthritis from the neuropathic process. Soft tissue infections are diagnosed by appropriate cultures and responses to antibiotics. Initially, the bony margins produced by osseous fragmentation in neuropathic joint disease are sharply defincd, whereas osteomyelitis produces osteoporotic bone with ill-
5 416 BRIEF REPORTS defined edges. Subsequently, the development of Lisfranc fracture dislocations or hypertrophic destructive changes with paraarticular debris and periosteal reaction are so typical of NA that they make other considerations highly unlikely. Bone scintigraphy with technetium-labeled diphosphonate may not be helpful in the differential diagnosis. Scans of diabetics with neuropathy, with or without arthropathy, will reveal a markedly abnormal uptake within 2 minutes after injection of the radionuclide, indicating increased local blood flow (9). Reflex sympathetic dystrophy, in which similar findings may be seen on bone scintigraphy, produces patchy bone demineralization, but will not result in Lisfranc dislocations or paraarticular debris with osteophytosis and sclerosis, as is seen in NA. Although NA is generally considered to be a slowly progressive condition, the findings in these patients emphasize that even minor trauma may lead to extremely rapid development of Charcot arthropathy in individuals with a preexisting neurosensory disorder. In addition, although many people with diabetic neuropathy presumably incur minor trauma to the lower extremities, only a minority of them develop NA. Essentially no dose-response data exist with regard to the development of NA. If ligaments were strained or weakened as a result of the minor trauma, recurrent mechanical damage to intraarticular structures could occur with subsequent joint usage. In any event, a clear temporal relationship was shown to exist between the incidents of minor trauma and the subsequent neuropathic joint changes observed in our group of patients. The presence of longstanding diabetes mellitus, peripheral neuropathy, and a history of relatively minor trauma to the foot or ankle was common to all 3 patients. In this clinical setting, as a result of the peripheral neuropathy, protective muscular reflexes normally initiated by input from nociceptors or mechanoreceptors in the extremity may be impaired, so that the normal range of joint excursion is exceeded, leading to damage of the articular and periarticular tissues. In a previous study of the pathogenesis of NA (6), superimposition of knee instability on a limb that had undergone extensive deafferentation by DRG led to a very rapid breakdown of the joint. This contrasted sharply with the mild joint degeneration that results from knee instability following ACLT in neurologically intact dogs (7). Deafferentation of the knee by transection of the major articular nerves (rather than by DRG), however, did not markedly affect the rate or severity of degenerative changes in the knee following ACLT (10). In addition, deafferentation of the knee by either procedure did not result in joint disease if joint stability was maintained (6,lO). Since DRG results in much more extensive deafferentation of the limb than articular nerve transection, these results suggest that DRG may accelerate the breakdown of joints that are predisposed to damage ligamentous insufficiency, by reducing sensory input into the central nervous system from muscles, tendons, ligaments, or skin, rather than from the joint itself. In the patients described above, diabetic neuropathy presumably served as the functional equivalent of DRG in the canine model, and the patients stumble represented the functional equivalent of ACLT. Neuropathic arthropathy in humans may exhibit predominantly atrophic or predominantly hypertrophic features. The atrophic form, which rarely affects the lower extremities, is characterized by extensive bone resorption, with little evidence of accompanying bone orjoint repair. It usually evolves in 2 4 weeks, and has therefore been termed the acute neuropathic joint (11). Although the changes seen in the patients described herein developed with great rapidity, radiographs indicated that they did not have the atrophic form, but rather, the hypertrophic form of NA. Although it generally evolves over many months or years (12), the hypertrophic form of NA typically involves weight-bearing joints of the lower extremity. It is characterized by a combination of new bone growth and destructive, degenerative changes. Fibrillation, erosion, and calcification of the articular cartilage, subchondral sclerosis, exuberant marginal osteophytes, metaplastic ossification at sites of attachment of ligaments and tendons, intraarticular loose bodies, intraarticular and juxtaarticular fractures, and joint subluxation (all of which were noted in our 3 patients) are characteristic features of NA. Clotisy and Thompson (13) have recently emphasized the importance of fractures in adults with juvenile-onset diabetes. The calcaneal fracture and subsequent NA of patient 3 is a good example of neuropathic skeletal disease. The pathophysiology of the joint lesions in patients with diabetic neuropathy is still unclear. However, it is important to recognize the rapidity with which a Charcot joint may develop after minor trauma in the patient with diabetic neuropathy, since prompt
6 BRIEF REPORTS 417 treatment of the injury (e.g., immobilization following sprains and strains) may minimize the frequency or severity of this serious complication (13~4). Acknowledgments. We are indebted to Drs. Lowell B. Robison and Clyde B. Kernek for allowing us to study their patients. We also thank Julie Dodt and Donna Faulkner for preparation of the manuscript REFERENCES Ellman MH: Neuropathic joint disease (Charcot joints), Arthritis and Allied Conditions. Edited by DJ McCarty. Philadelphia, Lea & Febiger, 1989 Resnick D, Sartoris D, Cone KO 111: Imaging, Textbook of Rheumatology. Edited by WN Kelley, ED Harris Jr, S Ruddy, CB Sledge. Philadelphia, WB Saunders, 1989 Eloesser L: On the nature of neuropathic affections of the joints. Ann Surg 66: , 1917 Finsterbush A, Friedman B: The effect of sensory denervation on rabbits knee joints: a light and electron microscopic study. J Bone Joint Surg 57A: , 1975 Johnson JTH: Neuropathic fractures and joint injuries: pathogenesis and rationale of prevention and treatment. J Bone Joint Surg 49A:1-30, 1967 O Connor BL, Palmoski MJ, Brandt KD: Neurogenic acceleration of degenerative joint lesions. J Bone Joint Surg 67A: , Palmoski MJ, Brandt KD: Proteoglycan depletion, rather than fibrillation, determines the effects of salicylate and indomethacin on osteoarthritic cartilage. Arthritis Rheum 28:54%553, Sinha S, Munichoodappa CS, Kozak GP: Neuroarthropathy (Charcot joints) in diabetes mellitus. Medicine (Baltimore) 51: , Edmonds ME, Clarke MB, Newton S, Barrett J, Watkins PJ: Increased uptake of bone radiopharmaceutical in diabetic neuropathy. Q J Med , O Connor BL, Visco DM, Brandt KD: The development of experimental osteoarthritis in dogs with extensively deafferented knee joints. Arthritis Rheum 32 (suppl 4):S106, Brower AC: The acute neuropathic joint. Arthritis Rheum 31: , Bruckner FE, Howell A: Neuropathic joints. Semin Arthritis Rheum 2:47-69, Clotisy DR, Thompson RC: Fractures associated with neuropathic arthropathy in adults who have juvenileonset diabetes. J Bone Joint Surg 70A: , Brooks AP: Neuropathic foot in diabetes. 11. Charcot s neuroarthropathy. Diabetic Med 3: , 1986
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