DOI:10.2214/AJR.08.1352
AJR 2009; 193:61-69
© American Roentgen Ray Society
Features of Nephrogenic Systemic Fibrosis on Radiology Examinations
Michael F. Morris1,
Yang Zhang1,
Honglei Zhang1,
Joan C. Prowda1,
David N. Silvers1,
Rashid A. Fawwaz1 and
Martin R. Prince1
1 Department of Radiology and Department of Dermatology and Dermatopathology at
Columbia and Cornell Universities, 416 E 55th St., New York, NY 10022.
Received June 5, 2008;
accepted after revision December 25, 2008.
M. R. Prince has patent agreements with the following companies, which
manufacture gadolinium-based contrast agents: GE Healthcare, Bayer HealthCare,
Mallinckrodt Imaging, Bracco Laboratories, and Epix.
Address correspondence to M. R. Prince
(map2008{at}med.cornell.edu).
Abstract
OBJECTIVE. The objective of this article is to illustrate the
spectrum of imaging findings with photographic and histopathologic correlation
in patients with biopsy-proven nephrogenic systemic fibrosis (NSF).
CONCLUSION. Features of NSF may be evident on the patient's skin as
well as on routine imaging studies, although these imaging findings are
nonspecific and are more likely to occur with other diseases.
Keywords: CT • gadolinium • mammography • MRI • nephrogenic systemic fibrosis • PET • scintigraphy • ultrasound
Introduction
Nephrogenic systemic fibrosis (NSF) is a rare disease seen in
patients with severe renal impairment that has garnered increased interest
among radiologists because of reports of its association with gadolinium-based
contrast agents (GBCAs)
[1-20].
Many case series have reported that high doses of GBCA and possibly of linear
nonionic GBCA contribute to an increased risk of NSF
[16,
17,
21-25].
These findings have led to recommendations for radiologists to avoid the use
of GBCA or reduce the dose of GBCA in patients with an estimated glomerular
filtration rate (GFR) of less than 30 mL/min
[26]. It is also recommended
that dialysis patients undergo dialysis immediately after GBCA injection to
further minimize the risk of NSF when GBCA is essential
[27].
NSF was originally reported by Cowper et al.
[28] to have first occurred in
1997. NSF affects male and female patients equally and has been reported to
occur in patients of all ages including children as young as 8 years old
[29]. Although the cause of
NSF remains unknown, most patients have a history of gadolinium exposure and
gadolinium has been detected in NSF skin lesions, as reported by several
authors [9,
30].
Cowper [31] has established
the following diagnostic criteria for NSF:
...large areas of hardened skin with slightly raised plaques, papules, or
confluent papules; with or without pigmentary alteration and/or with biopsies
showing increased numbers of fibroblasts, alteration of the normal pattern of
collagen bundles seen in the dermis, and often increased dermal deposits of
mucin.
These criteria have been expanded in a recent review
[32].
Because NSF primarily involves the skin, little attention has been paid to
its imaging characteristics
[33]. We have seen the imaging
studies of 26 biopsy-confirmed cases of NSF at our institution. This article
illustrates the spectrum of imaging findings in these NSF patients with
photographic and histopathologic correlation.
Histopathology
Deep punch biopsy specimens of NSF lesions show, in varying proportions,
spindle cell proliferation, thickened collagen bundles, and mucin deposition
(Figs. 1A, and
1B) in a process believed to be
mediated by circulating fibrocytes inappropriately stimulated by gadolinium
[34]. Although NSF primarily
affects the skin, involvement of skeletal muscle, heart, and lungs has also
been reported [23,
32,
35]. The histologic features
of NSF can be very similar in appearance to other dermatologic conditions,
including scleromyxedema, scleroderma and deep morphea, lipodermatosclerosis,
eosinophilic fasciitis (Shulman syndrome), and chronic graft-versus-host
disease [32]. Thus, diagnosing
NSF requires a combination of characteristic histologic and clinical
findings.
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Fig. 1A —Photomicrographs of H and E-stained skin punch biopsy in
56-year-old woman show interstitial spindle cell proliferation at all levels
of dermis typical of nephrogenic systemic fibrosis. Low power (A,
4x) and higher power (B, 20x).
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Fig. 1B —Photomicrographs of H and E-stained skin punch biopsy in
56-year-old woman show interstitial spindle cell proliferation at all levels
of dermis typical of nephrogenic systemic fibrosis. Low power (A,
4x) and higher power (B, 20x).
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Clinical Manifestations
All NSF patients have significant renal impairment, with an estimated GFR
of < 30 mL/min (stage IV or V kidney disease), dialysis-dependent end-stage
renal disease, or acute renal failure. Patients often initially present with
nonspecific complaints—including joint pain, extremity swelling, and
stiffness—that in turn may lead to multiple imaging procedures. On
physical examination, the cutaneous manifestations of NSF commonly involve the
extremities and trunk beginning distally and spreading proximally while
sparing the face. Patients with mild disease can present with a variety of
nonspecific findings ranging from erythema, papules, and plaques
(Fig. 2) to skin dimpling and
peau d'orange (Figs. 3A, and
3B). Patients may develop
contractures that reduce mobility (Figs.
4A, and
4B). Although most cases of NSF
are self-limiting and some regress spontaneously, an estimated 5% have a
rapidly progressive fulminate course
[23].
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Fig. 3A —56-year-old woman with nephrogenic systemic fibrosis (NSF).
Note skin dimpling in lower extremities (A) and peau d'orange
appearance of woody and indurated skin in upper extremities (B). Biopsy
of right thigh showed proliferation of spindle cells with abundant
interstitial dermal mucin consistent with NSF.
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Fig. 3B —56-year-old woman with nephrogenic systemic fibrosis (NSF).
Note skin dimpling in lower extremities (A) and peau d'orange
appearance of woody and indurated skin in upper extremities (B). Biopsy
of right thigh showed proliferation of spindle cells with abundant
interstitial dermal mucin consistent with NSF.
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Fig. 4A —36-year-old woman with nephrogenic systemic fibrosis (NSF)
involving chest, back, and both lower extremities. Left leg biopsy showed
proliferation of spindle cells and thick collagen bundles consistent with NSF.
Lateral ankle radiographs show flexion contractures with moderately severe
osteopenia bilaterally, likely from disuse. These radiographic findings are
not specific for NSF.
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Fig. 4B —36-year-old woman with nephrogenic systemic fibrosis (NSF)
involving chest, back, and both lower extremities. Left leg biopsy showed
proliferation of spindle cells and thick collagen bundles consistent with NSF.
Lateral ankle radiographs show flexion contractures with moderately severe
osteopenia bilaterally, likely from disuse. These radiographic findings are
not specific for NSF.
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Unlike allergic reactions that happen within minutes of injection and are
independent of contrast agent dose, the skin changes of NSF typically are
delayed, occurring from 2 weeks to 2 months after high-dose GBCA injection.
NSF is rare with standard 0.1 mmol/kg doses of gadolinium
[27]. There may be an initial
prodrome of muscle pain, fever, weakness, swelling, redness, pruritus, or pain
in the limbs sometimes with muscle weakness, edema, or erythema and
occasionally with palpable warmth of the involved extremities; there may be
florid scleral telangiectasia resembling conjunctivitis
[36]. Clinical severity is
related to both the extent of the fibrosing dermopathy and the degree of
systemic involvement. Muscle involvement tends to be underlying the cutaneous
lesions with fibrotic bands in the subcutaneous tissues tethering the skin to
the underlying fascia. In some patients the NSF lesions resolve with
restoration of normal renal function after renal transplantation or resolution
of acute renal failure. In many cases the lesions persist, although a recent
report shows promising results for treating patients with NSF using imatinib
mesylate [37].
Radiography
The conventional radiographic findings of NSF are nonspecific, and
abnormalities on radiographs are rare and usually are secondary to the
sequelae of joint contracture and immobility. Flexion deformities and disuse
osteopenia from contractures occur most commonly in the feet (Figs.
4A, and
4B), knees, hands, and elbows.
In 140 NSF patients described in detail in case reports, limited range of
motion or joint contractions were noted clinically in 106 (58%)
[38]. We saw joint
contractures on radiographs in two of our 26 patients, but the contractures in
one patient were due to juvenile rheumatoid arthritis and had been present
before NSF developed. Note that the differential diagnosis for joint
contractures includes arthritides and immobilization (e.g., due to trauma,
burns, nerve injury, or stroke); the likelihood that a joint contracture
signifies NSF is negligible.
Although microscopic dermal calcifications are common in NSF specimens and
Cowper and colleagues have described skin calcifications on radiographs, these
calcifications are rare in NSF cases
[39]. We found cutaneous
calcifications on an imaging study in only one of our 26 biopsy-positive NSF
patients. In that patient, skin calcifications on abdominopelvic CT were
thought to be more likely related to the patient's other diseases including
juvenile rheumatoid arthritis, dialysis-dependent end-stage renal failure, and
systemic lupus erythematosus. Vascular calcifications visible on radiographs
are usually related to diabetes or renal failure.
Mammography
Three of the six female NSF patients who underwent mammography at our
hospital had skin thickening and increased subcutaneous linear markings (Figs.
5A, and
5B) corresponding to NSF
lesions. Although the breast skin thickening in these patients was readily
identified as part of the NSF process occurring over the legs, arms, and
chest, skin thickening on mammography is much more likely to be related to
inflammatory breast cancer, cellulitis, scarring, or venous or lymphatic
obstruction.
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Fig. 5A —51-year-old woman with nephrogenic systemic fibrosis (NSF) on
chest, back, arms, and buttocks. Chest skin biopsy showed slight dermal
fibrosis consistent with spectrum of histologic findings in NSF. Mammogram
shows skin thickening (arrows), increased breast density, and
infiltration of subcutaneous tissues.
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Fig. 5B —51-year-old woman with nephrogenic systemic fibrosis (NSF) on
chest, back, arms, and buttocks. Chest skin biopsy showed slight dermal
fibrosis consistent with spectrum of histologic findings in NSF. Breast
ultrasound image shows skin thickening, edema (white arrows), and
increased tissue echogenicity with large collateral vessels (black
arrow). These findings are not specific for NSF.
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Ultrasound
Duplex ultrasound may be performed to assess for extremity deep venous
thrombosis (DVT) in patients with NSF because of the common complaints of
extremity pain and swelling. Breast ultrasound may be performed in female
patients with NSF who have mammographic abnormalities, and it may show skin
thickening and subcutaneous edemalike inflammatory changes. Note that these
findings are nonspecific; are much more likely to result from DVT,
inflammation, or cellulitis; and would not be expected to elicit the diagnosis
of NSF.
CT
The most common CT study performed in patients with NSF is of the abdomen
and pelvis; however, occasionally CT of an extremity is performed during a
workup for extremity pain. Depending on the severity of disease, CT may show
varying degrees of skin thickening and infiltration of the subcutaneous and
soft tissues (Figs. 6A,
6B,
6C,
6D,
6E, and
7). Reformations in coronal
and sagittal planes and along the axis of the bones may facilitate assessment
of dermal infiltration. In particular, bands of collagen in the subcutaneous
fat tether the skin to underlying soft tissues
[40]. Systemic involvement of
the internal organs is difficult to identify on CT and thus has been reported
only at autopsy or on surgical and biopsy specimens. The differential
diagnosis for skin thickening and infiltration of the subcutaneous fat on CT
includes edema, cellulitis, fascitis and panniculitis, scleroderma and
sclerodermalike conditions (e.g., morphea), cutaneous T-cell lymphoma, and
Merkel cell carcinoma.
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Fig. 6A —57-year-old woman with nephrogenic systemic fibrosis (NSF)
involving bilateral thighs. Skin biopsy of right thigh showed thickening of
dermal collagen and fibrous septa between fat lobules. Coronal (A) and
axial (B) reformatted lower extremity CT images show nonspecific
findings for NSF including diffuse infiltration of subcutaneous tissues of
thighs with variable degrees of skin thickening (arrowheads,
A).
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Fig. 6B —57-year-old woman with nephrogenic systemic fibrosis (NSF)
involving bilateral thighs. Skin biopsy of right thigh showed thickening of
dermal collagen and fibrous septa between fat lobules. Coronal (A) and
axial (B) reformatted lower extremity CT images show nonspecific
findings for NSF including diffuse infiltration of subcutaneous tissues of
thighs with variable degrees of skin thickening (arrowheads,
A).
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Fig. 6C —57-year-old woman with nephrogenic systemic fibrosis (NSF)
involving bilateral thighs. Skin biopsy of right thigh showed thickening of
dermal collagen and fibrous septa between fat lobules. T1-weighted (C)
and STIR (D) images show dermal thickening (arrowhead,
C) and bands within subcutaneous fat (arrow, D); these
MRI findings are similar to those seen on CT.
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Fig. 6D —57-year-old woman with nephrogenic systemic fibrosis (NSF)
involving bilateral thighs. Skin biopsy of right thigh showed thickening of
dermal collagen and fibrous septa between fat lobules. T1-weighted (C)
and STIR (D) images show dermal thickening (arrowhead,
C) and bands within subcutaneous fat (arrow, D); these
MRI findings are similar to those seen on CT.
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Fig. 6E —57-year-old woman with nephrogenic systemic fibrosis (NSF)
involving bilateral thighs. Skin biopsy of right thigh showed thickening of
dermal collagen and fibrous septa between fat lobules. On conventional
radiograph, skin thickening is difficult to see and changes in subcutaneous
fat are subtle.
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Fig. 7 —71-year-old woman with nephrogenic systemic fibrosis (NSF)
involving left arm and forearm. Left forearm biopsy showed sun-damaged skin
with edema and dermal mucin typical of NSF. Oblique reformatted upper
extremity CT scan shows diffuse infiltration of subcutaneous tissues
(arrows) and variable degrees of skin thickening. These CT findings
are not specific for NSF.
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MRI
The spectrum of abnormal MRI findings in patients with NSF can be similar
to that seen on CT. Subtle areas of edema are seen on STIR or T2-weighted
fat-saturated images in patients with mild clinical manifestations of NSF,
whereas patients with more severe involvement show skin thickening and diffuse
inflammatory changes throughout the soft tissues (Figs.
8A,
8B,
9A,
9B, and
10). Although gadolinium is
contraindicated in patients with severe renal impairment, enhancement of the
subcutaneous tissues and skeletal muscle may be seen on T1-weighted
fat-saturated images when GBCA is administered
[24]. These nonspecific
findings are seen in many inflammatory, neoplastic, and traumatic conditions
and should not raise suspicion for NSF.
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Fig. 8A —56-year-old woman with nephrogenic systemic fibrosis (NSF)
involving thighs and calves bilaterally. Biopsies of right thigh and calf
showed proliferation of spindle cells, thick collagen bundles, and abundant
interstitial mucin in dermis typical of NSF. Unenhanced sagittal STIR images
of right calf show skin thickening (arrows), predominantly
anteriorly, in patient with only mild NSF. These findings are not specific for
NSF.
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Fig. 8B —56-year-old woman with nephrogenic systemic fibrosis (NSF)
involving thighs and calves bilaterally. Biopsies of right thigh and calf
showed proliferation of spindle cells, thick collagen bundles, and abundant
interstitial mucin in dermis typical of NSF. Unenhanced sagittal STIR images
of right calf show skin thickening (arrows), predominantly
anteriorly, in patient with only mild NSF. These findings are not specific for
NSF.
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Fig. 9A —54-year-old woman with nephrogenic systemic fibrosis (NSF)
involving both lower extremities and left upper extremity. Biopsy of right
thigh showed granulomatous septa in panniculus that was not thought to
represent NSF, but Shawn E. Cowper
[31] reviewed histologic
sections and interpreted changes as consistent with NSF. Coronal STIR images
of thigh (A) and calf (B) show increased signal throughout
subcutaneous tissues and muscles of legs bilaterally. These findings are not
specific for NSF.
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Fig. 9B —54-year-old woman with nephrogenic systemic fibrosis (NSF)
involving both lower extremities and left upper extremity. Biopsy of right
thigh showed granulomatous septa in panniculus that was not thought to
represent NSF, but Shawn E. Cowper
[31] reviewed histologic
sections and interpreted changes as consistent with NSF. Coronal STIR images
of thigh (A) and calf (B) show increased signal throughout
subcutaneous tissues and muscles of legs bilaterally. These findings are not
specific for NSF.
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Fig. 10 —60-year-old man with nephrogenic systemic fibrosis (NSF)
involving legs and back and neck. Biopsies of right leg and upper back showed
dermal fibrosis with small amount of mucin consistent with NSF. Axial
T2-weighted MR image with fat saturation shows dermal thickening
(arrowheads) with changes in subcutaneous fat resembling edema and
inflammatory changes in underlying skeletal muscles of anterior thighs
(arrows). These MR findings are not specific for NSF.
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Nuclear Medicine
Extraosseous accumulation of 99mTc-hydroxydiphosphonate (HDP)
can be seen in NSF patients undergoing bone scintigraphy (Figs.
11A, and
11B) and was previously
reported [32,
41,
42]. The differential
diagnosis for diffuse extremity soft-tissue uptake on bone scans includes
myositis ossificans and heterotopic calcifications; dermatomyositis;
rhabdomyolysis; polymyositis; metastatic calcifications; and technical
factors, including contamination and tourniquet effects. There is a case
report describing FDG uptake in NSF
[41]. We found only one NSF
patient with FDG uptake on PET and that patient had cutaneous T-cell lymphoma,
which was more likely to be the reason for FDG activity in the skin.
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Fig. 11A —50-year-old man with nephrogenic systemic fibrosis (NSF)
primarily involving legs and left forearm. Biopsies of right thigh and left
arm show spindle cell proliferation consistent with NSF. Bone scintigraphy
images show diffuse increased 99mTc-hydroxydiphosphonate activity
in skin and subcutaneous tissues on bone scan that corresponds to distribution
of skin rash. These findings are not specific for NSF.
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Fig. 11B —50-year-old man with nephrogenic systemic fibrosis (NSF)
primarily involving legs and left forearm. Biopsies of right thigh and left
arm show spindle cell proliferation consistent with NSF. Bone scintigraphy
images show diffuse increased 99mTc-hydroxydiphosphonate activity
in skin and subcutaneous tissues on bone scan that corresponds to distribution
of skin rash. These findings are not specific for NSF.
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Conclusion
NSF has a variable appearance on routine imaging studies. Often there are
no abnormal imaging findings. However, conventional radiographs can show joint
contractures, skin thickening, and possibly cutaneous calcinosis; ultrasound
may show thickening and edema of the cutis, particularly in the breast; CT may
show skin thickening and infiltration of subcutaneous tissues; MRI may show
increased signal on fluid-sensitive sequences in the skin, subcutaneous
tissues, and extremity musculature; and bone scintigraphy may show diffuse
soft-tissue uptake in the extremities. Studies of the head and anterior neck
fail to show changes related to NSF because the disease spares that region.
All these imaging findings are nonspecific and cannot be used to diagnose NSF
using the currently accepted diagnostic criteria.
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Abstract
Introduction
