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Metastatic carcinoma presenting as monarticular arthritisa case report and review of the literature.

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95
METASTATIC CARCINOMA PRESENTING AS MONARTICULAR
ARTHRITIS: A CASE REPORT AND REVIEW OF THE LITERATURE
GARVIN C. MURRAY and ROBERT H. PERSELLIN
Arthritis resulting from metastatic carcinoma involving juxtaarticular bone or synovial tissue is a poorly
recognized and rarely reported occurrence. It has received only brief mention in the current standard tests
of rheumatology (1,2). Consequently, when it occurs, it
usually presents a diagnostic dilemma leading to unfortunate delays and errors in medical management.
We present here an unusual case of the heretofore unreported occurrence of sternoclavicular arthritis as the presenting manifestation of metastatic carcinoma. The pertinent literature is reviewed, and the
clinical characteristics of this form of arthritis are discussed.
Case Report. In December 1977, a 69-year-old
Mexican-American man presented to the Bexar County
Hospital emergency room with a 3-week history of
painful swelling of the right sternoclavicular joint. An
anteroposterior radiograph of the right clavicle and sternoclavicular joint revealed only soft tissue swelling
without bony abnormalities; however, a small infiltrate
was noted in the apex of the right lung associated with
pleural thickening. Because of this finding, he was admitted for further evaluation.
He had an 80-pack a year smoking history but
From the Division of Rheumatology, Department of Medicine, The University of Texas Health Science Center at San Antonio.
Supported in part by an Arthritis Clinical Research Center
grant from the Arthritis Foundation and by grants from the South
Central Texas Chapter of the Arthritis Foundation and the Ruth and
Vernon Taylor Foundation.
Garvin C. Murray, MD: Fellow in Rheumatology; Robert H.
Persellin, MD: Professor of Medicine, Head, Division of RheumatolOgY.
Address reprint requests to Robert H. Persellin, MD, Department of Medicine, Division of Rheumatology, The University of
Texas Health Science Center, 7703 Floyd Curl Drive, San Antonio,
TX 78284.
Submitted for publication June 14, 1979; accepted July 31,
1979.
Arthritis and Rheumatism, Vol. 23, No. 1 (January 1980)
denied chronic cough or hemoptysis. There was no history of fever, chills, night sweats, weight loss, or exposure to tuberculosis. The sternoclavicular symptoms
were first noted 3 weeks prior to admission and had
gradually become more severe. There was no history of
trauma associated with the onset of the joint pain. No
other arthritic complaints were elicited. The patient had
been hospitalized in 1971 for medical problems associated with chronic alcoholism, including Wernicke’s syndrome, Korsakoff s psychosis, peripheral neuropathy,
muscle atrophy, and hepatic cirrhosis.
On examination the patient appeared chronically
ill and debilitated with clinical features of an organic
brain syndrome. His vital signs and cardiorespiratory
findings were normal. The liver was slightly enlarged
but nontender. No lymphadenopathy or prostatic nodules were present. Prominent clubbing of the fingers was
noted, but other manifestations of hypertrophic pulmonary osteoarthropathy were not apparent. Overlying the
right sternoclavicular joint was a 3 x 4 cm area of swelling which was mildly erythematous, warm, and tender
to palpation. There were no other signs of arthritis.
Laboratory studies revealed a hematocrit of 42%
and a leukocyte count of 5,100/mm3 with a normal differential. The alkaline phosphatase was moderately elevated at 196 units/liter (normal, 35-125 units/liter) and
a Westergren erythrocyte sedimentation rate was 30
=/hour. Normal values were obtained for serum electrolytes, urea nitrogen, glucose, bilirubin, creatinine,
SGOT, LDH, and urinalysis.
Tomography of the right lung revealed multiple
thick and thin-walled cavitary lesions involving the
greater portion of the right apex associated with irregular pleural thickening. Sputum cytology was negative;
however, fluorochrome smears for Mycobacterium tuberculosis documented active infection.
In view of the finding of pulmonary tuberculosis,
96
CASE REPORTS
the possibility of tuberculous arthritis was considered,
and an evaluation of the sternoclavicular lesion was undertaken. Except for soft tissue swelling, results of
tomograms of the right clavicle and sternoclavicular
joint were normal. Arthrocentesis of the involved joint
yielded only 0.3 ml of serosanguinous fluid, which subsequently proved to be culture-negative for aerobic bacteria and M tuberculosis. In addition to occasional polymorphonuclear leukocytes, a Wright's stain of the joint
aspirate surprisingly revealed clumps of darkly staining
neoplastic cells (Figure 1). An open biopsy provided additional tissue which was histologically consistent with
metastatic clear cell carcinoma infiltrating the sternal
head of the right clavicle.
A search for the primary carcinoma, including
bronchoscopy, intravenous pyelogram, upper gastrointestinal series, barium enema, and a liver-spleen scan,
was negative. A 99"technetiumpyrophosphate bone scan
demonstrated areas of increased uptake in the regions of
the right sternoclavicular joint and proximal femur, left
shoulder, and iliac crest (Figure 2). In view of the re-
sults of the clinical evaluation, it was thought that the
neoplasm had probably originated in the bronchioles.
Although the patient was treated with a chemotherapeutic regimen, as well as with isoniazid and ethambutol, he died 4 weeks later. An autopsy was not performed.
Discussion. A broad spectrum of rheumatologic
disorders is known to occur in association with malignant diseases. These are listed in Table 1 and include
such diverse syndromes as hypertrophic osteoarthropathy (3), gout (4), dermatomyositis (5), Sjogren's
syndrome (6), carcinomatous polyarthritis (7), and arthritis associated with lymphoproliferative and myeloproliferative diseases (8,9). Although less well recognized, arthritis due to metastatic carcinoma involving
juxtaarticular structures or synovium can also occur
(10-19) and on rare occasions may be the presenting
manifestation of the malignant process. Diagnosis in
these cases can be difficult, often resulting in unfortunate delays and errors in medical management.
Figure 1. A cluster of poorly differentiated malignant cells seen in the sternoclavicular joint aspirate. (Wright's stain, original
magnification X 1200.)
CASE REPORTS
Figure 2. 99"Technetium pyrophosphate scan of the patient demonstrating areas of increased uptake in the regions of the right sternoclavicularjoint and proximal femur, left shoulder, and iliac crest.
97
case was there a polyarticular onset (case 2). Importantly, inflammation of the affected joints was observed
in all 11 patients in which physical findings were reported. Effusions were present in six. The knee was
most commonly involved with the hip being the second
most likely site. Involvement of the ankle, wrist, and the
joints of the hands and feet was less frequent. No previous cases of sternoclavicular involvement have been
reported. This distribution of arthritis parallels the incidence of osseous metastases involving the appendicular skeleton which diminishes with increasing distance
from the central axis of the body (20,21). Not surprisingly, carcinoma of the breast and lung were the primary neoplasms in the majority of cases (64%). These
malignancies are the most common to occur in women
and men, respectively, and both commonly metastasize
to bone (22). Although metastases to distant peripheral
sites are rare, this review concurs with previous observations that metastatic osseous invasion distal to the knee
or elbow most frequently results from bronchogenic carcinoma (23,24).
Arthrocentesis, performed on 6 patients, was often valuable in establishing the appropriate diagnosis.
In the majority (83%) the synovial fluid was bloody or
serosanguinous and usually noninflammatory. Cytologic evaluation utilizing either Papanicolaou or
Wright's staining revealed neoplastic epithelial cells in
four instances. As illustrated by the present case, an
evaluation of even a seemingly insignificant quantity of
aspirated fluid may prove fruitful. Based on observations in four synovial fluid aspirates with characteristics
similar to those reported above, Naib suggested that the
presence of an hemorrhagic, noninflammatory effusion
should arouse suspicion of a primary or secondary neoplasm (25).
Percutaneous or surgical synovial biopsies were
performed in 5 instances and proved diagnostic in 4 patients. Bone biopsy was diagnostic in 4 others, whereas
the diagnosis was made at autopsy in 2. The presence of
neoplastic epithelial cells was the most striking feature
of the synovial histology in the majority of patients. La-
Table 1. Rheumatic disorders associated with malignant diseases
Our experience with the patient presented here
was in many ways comparable to other reported cases of
arthritis resulting from metastatic carcinoma (10-19). A
summary of the clinical features of these patients together with the Dresent case is presented in Table 2.
The arthritis associated with metastatic carcinoma was most commonly monarticular. In only one
Y
Hypertrophic osteoarthropathy
Gout
Dermatomyositis
Sjogren's syndrome
Carcinomatous polyarthritis
Arthritis associated with lymphoproliferativeand
myeloproliferative diseases
Arthritis associated with metastatic carcinoma
CASE REPORTS
Table 2. Summary of the clinical features of 14 cases of arthritis caused by metastatic carcinoma
Case no. Age/
(Ref.) sex
Initial
diagnosis*
History of
previous
Joint
malignancy involved
Duration of
symptoms to
final
diagnosis
Initial
radiologic
findings
Radiologic
findings
at final
diagnosis
Procedure
diagnostic of
articular
lesiont
Final
diagnosis
l(l0)
66/F
RA
Yes
Ankle
24
months
Mild deminerali- Diffuse deminerzation
alization
BBx
Breast
carcinoma
2(11)
59/M
RA
No
Knee, PIP
joints
5
weeks
Numerous
osteolytic
lesions
AUT
Squamous cell
carcinoma, lung
3(12)
66/M
MA
Yes
Knee
4
weeks
Demineralization Extensive lysis
of patella
ARCT, SBx
Squamous cell
carcinoma, lung
4(13)
63/M
TA or
TbA
No
Knee
3
months
Not reported
Lysis, lower
pole of patella
AUT
Epidermoid
carcinoma, lung
5 (14)
62/F
OA
Yes
Knee
4
weeks
Not reported
Degenerative
changes
ARCT, SBx
Adenocarcinoma,
colon
6 (15)
54/F
MA
Yes
Knee
12
months
Mild degenerative Osteolytic
changes
and blastic
lesions
ARCT
Breast carcinoma
7 (16)
52/F
MA
Yes
wrist
4
months
Demineralization Osteoblastic
lesions
SBx
Bronchogenic
carcinoma
(presumed)
8 (17)
67/M
Gout
Yes
Ankle
6
weeks
Soft tissue
swelling
Extensive demineralization
with fracture
BBx
Transitional cell
carcinoma,
urinary bladder
9 (18)
48/M
Gout
Yes
IP joint,
great toe
Not
reported
Lytic lesion
Unchanged
X-ray
Squamous cell
carcinoma, lung
IO(19)
89/M
MA
Yes
Hip
10
weeks
Not reported
Blastic lesions
in pelvis
X-ray, BSc
Prostatic
carcinoma
11 (19)
63/F
RA
Yes
Hip
16
months
Not reported
Abnormal (details
not given)
X-ray, BSc
Breast carcinoma
12(19)
51/F
TbA
No
Hip
3
months
Normal
Normal
SBx
Lung carcinoma
13(19)
34/M
INB
No
Hip
2
weeks
Mottling of
femoral head
Abnormal (details
not given)
BBx
Carcinoma,
primary
unknown
Present
case
69/M
TbA
No
Sternoclavicular joint
3
weeks
Normal
Normal
Unchanged
ARCT, BBx
Bronchogenic
carcinoma
(presumed)
* RA = rheumatoid arthritis; MA = monarthritis; TA = traumatic arthritis; TbA = tuberculous arthritis; OA = osteoarthritis; INB = ischemic
necrosis of bone.
t BBx = bone biopsy; AUT = autopsy; ARCT = arthrocentesis; SBx = synovial biopsy; BSc = bone scan.
gier (16) described a patient in which an open synovial
biopsy initially demonstrated non-specific inflammation
consisting of mild synovial hyperplasia, capillary congestion, and plasma cell and lymphocyte infiltrates.
Deeper sectioning revealed undifferentiated epidermoid
carcinoma in underlying connective tissue. Similar find-
ings were reported in synovial tissue obtained from a
patient with metastatic bronchogenic carcinoma (1 1).
No neoplastic cells were detected however, radiographs
revealed extensive osteolytic changes in adjacent bone.
These observations suggest that malignant metastatic
deposits in tissues adjacent to a joint may cause non-
CASE REPORTS
specific synovial inflammation without directly involving the synovial membrane itself. The mechanism
by which this occurs is unknown.
In the majority of cases the pre-existence of a
malignancy was known and provided an important clue
to the etiology of the joint complaint. Nevertheless, an
underlying malignancy was not usually suspected as the
cause of arthritis. This was reflected by the original
diagnoses which included rheumatoid and infectious arthritis in 3, gout in 2, and ischemic necrosis of bone,
osteoarthritis, and traumatic arthritis in 1 patient each.
As a consequence, delays were incurred in making the
appropriate diagnosis. The duration of joint symptoms
from onset to final diagnosis ranged from 2 weeks to 24
months. The median duration was 2 months.
Two additional factors appear to have contributed to this difficulty with early diagnosis. Physical findings often did not suggest the presence of an initial or
recurrent malignancy, and laboratory data were usually
not helpful. Furthermore, the initial radiographic studies of the involved joints were frequently normal or revealed only minimal non-specific changes, such as mild
demineralization or soft tissue swelling (Table 2). The
paucity of radiographic abnormalities associated with
metastatic invasion in these patients can be explained
on the basis of the site of initial metastasis. Since 0sseous metastases begin their proliferation in the marrow
cavity, they can reach macroscopic size without altering
bony architecture or becoming radiographically apparent (24). The exact physiologic mechanisms of bone resorption remain unclear; however, neoplastic activation
of osteoclasts or production of osteolytic substances,
such as prostaglandins, are probably important (26).
Osteolytic changes appear to occur only after the marrow space has been extensively infiltrated by tumor
cells.
The mechanism by which carcinoma metastasizes to synovial tissue remains unclear. Direct hematogenous dissemination of tumor cells to synovium probably occurs, but it appears to be extremely rare.
Goldenberg (14) and Meals (19) have each reported a
case of biopsy-documented synovial membrane involvement by carcinoma in which this mode of metastasis may have occurred. However, in neither case was a
postmortem dissection of the involved joint performed.
It appears more likely that metastasis to juxtaarticular
bone occurs first, with synovial involvement following
secondarily. This could occur by subsequent direct tumor invasion of synovial tissue or by secondary hematogenous metastasis through intercommunicating vascular
channels (27,28) analogous to the way suggested for the
99
development of joint infection following juxtaarticular
osteomyelitis in the adult (29,30). Secondary lymphatic
spread from bone to joint probably does not occur since
the presence of lymphatic vessels in bone marrow where
osseous metastases occur has not been conclusively
demonstrated (3 1). Furthermore, once established in
bone, subsequent tumor spread occurs via established
anatomic channels, namely the medullary cavity and
the haversian and Volkmann’s canals (31). Of the 14
cases reviewed, all but 2 (cases 5 and 12) had evidence
of juxtaarticular osseous involvement.
Why synovial tissue with its large total surface
area and generous blood supply is not involved more
frequently by metastatic neoplasms remains to be answered. That this type of involvement can and does occur, albeit rarely, needs to be more fully appreciated
and considered as a potential cause of monarticular arthritis.
REFERENCES
1. Cohen AS: Tumors of synovial joints, bursae, and tendon
sheaths, Arthritis and Allied Conditions. Eighth edition.
Edited by JL Hollander, DJ McCarty. Philadelphia, Lea
and Febiger, 1972, p 1385
2. Barnes CG: Miscellaneous and uncommon rheumatic
conditions, Copeman’s Textbook of the Rheumatic Diseases. Fifth edition. Edited by JT Scott. Edinburgh,
Churchill Livingstone, 1978, pp 859-860
3. Hammarsten JF, OLeary 3: The features and significance
of hypertropic osteoarthropathy. Arch Intern Med
99:43141, 1957
4. Yu T, Weinreb N, Wittman R, Wasserman LR: Secondary gout associated with chronic myeloproliferative disorders. Semin Arthritis Rheum 5:247-256, 1976
5. Barnes BE: Dermatomyositis and malignancy: a review of
the literature. Ann Intern Med 84:68-76, 1976
6. Tala1 N, Sokoloff L, Barth WF: Extrasalivary lymphoid
abnormalities in Sjogren’s syndrome (reticulum cell sarcoma, “pseudolymphoma,” macroglobulinemia). Am J
Med 43:5O-65, 1967
7. MacKenzie AH, Scherbel AL: Connective tissue syndromes associated with carcinoma. Geriatrics 18:745-753,
1963
8. Spilberg I, Meyer GJ: The arthritis of leukemia. Arthritis
Rheum 15:63O-635, 1972
9. Davis JS, Weber FC, Bartfeld H: Conditions involving
the hemopoietic system resulting in a pseudorheumatoid
arthritis: similarity of multiple myeloma and rheumatoid
arthritis. Ann Intern Med 47:1O-17, 1957
10. Jacox RF, Tristan TA: Carcinoma of the breast metastatic
to the bones of the foot: a case report. Arthritis Rheum
3:170-177, 1960
11. Karten I, Bartfeld H: Bronchogenic carcinoma simulating
100
CASE REPORTS
early rheumatoid arthritis: metastasis to the fingers.
JAMA 179~162-164,1962
12. Benedek TG: Lysis of the patella due to metastatic carcinoma. Arthritis Rheum 8560-566, 1965
13. Gall EP, Didizian NA, Park Y: Acute monarticular arthritis following patellar metastasis: a manifestation of
carcinoma of the lung. JAMA 229:188-189, 1974
14. Goldenberg DL, Kelley W, Gibbons RB: Metastatic
adenocarcinoma of synovium presenting as an acute arthritis: diagnosis by closed synovial biopsy. Arthritis
Rheum 18:107-110, 1975
15. Moutsopoulos HM, Fye KH, Pugay PI, Shearn MA:
Monarthric arthritis caused by metastatic breast carcinoma: value of cytologic study of synovial fluid. JAMA
234:75-76, 1975
16. Lagier R: Synovial reaction caused by adjacent malignant
tumors: anatomicopathologic study of three cases. J
Rheumatol4:65-72, 1977
17. Bevan DA, Ehrlich GE, Gupta VP: Metastatic carcinoma
simulating gout. JAMA 237:2746-2747, 1977
18. Vaezy A, Budson DC: Phalangeal metastases from
bronchogenic carcinoma. JAMA 239:226-227, 1978
19. Meals RA, Hungerford DS, Stevens MB: Malignant disease mimicking arthritis of the hip. JAMA 239:1070-107 1,
1978
20. Mulvey RB: Peripheral bone metastases. J Roentgen01
Radium Ther Nucl Med 91:155-160, 1964
2 1. Wirth CR: Metastatic bone tumors, Clinical Oncology.
Edited by J Horton, GJ Hill. Philadelphia, WB Saunders
Company, 1977, pp 636-644
22. Silverberg E: Cancer statistics, 1979. CA 29:6-21, 1979
23. K e r b R: Metastatic tumors of the hand. J Bone Joint
Surg 40A:263-277, 1958
24. Shackman R, Harrison CV: Occult bone metastases. Br J
Surg 35:385-389, 1948
25. Naib ZM: Cytology of synovial fluids. Acta Cytol 17:299309, 1973
26. Editorial: Osteolytic metastases. Lancet 2: 1063-1064, 1976
27. Gardner E: Blood and nerve supply of joints. Stanford
Med Bull 11:203-209, 1953
28. Trueta J, Harrison MHM: The normal vascular anatomy
of the femoral head in adult man. J Bone Joint Surg
35B:442461, 1953
29. Trueta J: The three types of acute haematogenous osteomyelitis: a clinical and vascular study. J Bone Joint Surg
41B1671-680, 1959
30. Atcheson SG, Ward JR: Acute hematogenous osteomyelitis progressing to septic synovitis and eventual
pyarthrosis: the vascular pathway. Arthritis Rheum
2 11968-971, 1978
31. Milch RA, Changus GW: Response of bone to tumor invasion. Cancer 9:340-351, 1956
Tissue Grafts in Reconstructive Surgery
An international conference will be held in Athens, Greece, May 25-30, 1980, t o commemorate
the tenth anniversary of the Greek Human Tissue Bank. Symposia will deal with problems of tissue banking and tissue transplantation, and poster sessions will be included.
The official languages of the conference will be Greek and English; proceedings of the conference
will be published in both languages.
For further information, contact Dr. Paul Karatzas, General Secretary t o the Conference, N.R.C.
Democritos, Human Tissue Bank, Aghia Paraskevi, Athens, Greece.
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