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Original Research |
1 Department of Radiology, University of Michigan Hospitals, 1500 E Medical
Center Dr., Room-B1D502G, Ann Arbor, MI 48109-0030.
2 Department of Dermatology, University of Michigan Hospitals, Ann Arbor,
MI.
3 Department of Internal Medicine, Division of Nephrology, University of
Michigan Hospitals, Ann Arbor, MI.
Received September 6, 2007;
accepted after revision September 26, 2007.
R. H. Cohan and J. H. Ellis received a one-time honorarium in 2006 for
providing a lecture CD to the International Center for Postgraduate Medical
Education. This activity was supported by Berlex Laboratories, which had no
control over the lecture content.
Abstract
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MATERIALS AND METHODS. A dermatopathology database was searched to identify patients in whom nephrogenic systemic fibrosis was diagnosed. The medical records of these patients were reviewed. Renal function concurrent with any administration of gadolinium-based contrast material was assessed, as was patient outcome. A database of patients undergoing long-term dialysis was reviewed separately to determine how many had received gadolinium and the frequency of nephrogenic systemic fibrosis among these patients.
RESULTS. Twenty-nine patients were found to have had nephrogenic systemic fibrosis between November 15, 1999, and December 31, 2006. It was known that gadolinium-based contrast material had been administered to 25 of these patients before diagnosis. All 29 patients had compromised renal function (27 had chronic renal failure, and two had acute renal failure). Determination of the temporal relation between gadolinium-based contrast administration and symptom onset often was difficult. Only eight patients had severe morbidity. Nephrogenic systemic fibrosis developed in 12 (2.9%) of 414 patients undergoing long-term dialysis who received gadolinium-based contrast material.
CONCLUSION. We confirm the strong association between nephrogenic systemic fibrosis and gadolinium-based contrast administration. Although the use of high doses of gadolinium and the occurrence of chronic renal failure have been implicated in other reports, several of our patients received standard doses of gadolinium, and two had transient acute renal failure before diagnosis. Most patients had mild or moderate symptoms. Nephrogenic systemic fibrosis developed in 2.9% of patients undergoing long-term dialysis who received gadolinium-based contrast material but in none of the long-term dialysis patients who did not receive gadolinium-based contrast material.
Keywords: contrast material • gadolinium • MRI • nephrogenic systemic fibrosis
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The exact cause of nephrogenic systemic fibrosis remains unknown. In 2006, two groups [6, 7] reported a strong association between nephrogenic systemic fibrosis and administration of gadolinium-based contrast material for MRI. Since then, several reports [8–10] have described the same association. In all, these five series have included 43 patients, all of whom had severely compromised renal function at the time of gadolinium-based contrast injection. All 43 patients had received gadodiamide before symptom onset, although one also had undergone an MRI examination for which gadobenate dimeglumine was injected [10].
As a result of the aforementioned studies and other reports from Europe [11] and the United States, in June 2006 the U.S. Food and Drug Administration issued a warning that MRI contrast agents should be used with caution in patients with renal failure. The American College of Radiology [12] subsequently published a white paper discussing in great detail the risks of gadolinium-based contrast material in renal failure patients. As of this writing, several hundred cases have been reported in the United States and Europe.
We encountered a number of patients at our institution in whom nephrogenic systemic fibrosis had been diagnosed, an initial group having been described in 2003 [3]. We decided to review our experience with nephrogenic systemic fibrosis in more detail, particularly with respect to previous exposure to gadolinium-based contrast material. We had become aware of one case each of nephrogenic systemic fibrosis developing in a patient receiving a standard dose of gadolinium-based contrast material and of nephrogenic systemic fibrosis associated with transient renal dysfunction. We wanted to determine whether these cases were isolated. We also wanted to determine the prevalence of this disease in a subset of patients receiving long-term dialysis who were exposed to gadolinium-based contrast material and to determine the frequency in patients undergoing long-term dialysis who were exposed to multiple doses of gadolinium.
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The dermatopathology database was reviewed retrospectively to determine the number of biopsy-proven cases of nephrogenic systemic fibrosis or nephrogenic fibrosing dermopathy (a previously used term for this entity) that have been encountered at our institution. The medical records of these patients with nephrogenic systemic fibrosis then were reviewed in detail. The following information was obtained: sex, date of any gadolinium-based contrast material exposure, presence and degree of renal dysfunction at the time of gadolinium-based contrast material exposure (by correlating with serum blood urea nitrogen and creatinine levels, history of dialysis, or both), presence of comorbid condition at the time of gadolinium-based contrast injection, date of onset of symptoms related to nephrogenic systemic fibrosis and the relation between symptom onset and any previous gadolinium-based contrast exposure, date of diagnosis of nephrogenic systemic fibrosis, distribution and severity of symptoms, and duration of and condition at follow-up with particular attention to symptoms related to nephrogenic systemic fibrosis. Imaging reports were reviewed to determine the type of MRI or other imaging examination performed, whether gadolinium-based contrast material was administered, and, when available, the volume and type of contrast material administered.
Three gadolinium-based MRI contrast agents were used during the study period. Gadopentetate dimeglumine (Magnevist, Bayer HealthCare) accounted for most (> 90%) of the MRI contrast injections. Gadobenate dimeglumine (MultiHance, Bracco) was used rarely, for fewer than 1% of injections during the study period. Gadodiamide (Omniscan, GE Healthcare) was used less than 10% of the time. It was chosen by the vascular and interventional radiology service during the brief time when gado linium-based contrast material rather than an iodinated contrast agent was being injected for conventional angiography of selected patients owing to the then widely held belief that MRI contrast agents were less nephrotoxic than iodinated contrast material, even at high doses. Gadodiamide was chosen over the other MRI contrast agents because it was a low-osmolality nonionic MRI agent and, at the time, it was believed that, as is the case for iodinated contrast media, such agents would be the least nephrotoxic of the then available MRI contrast agents. Gado diamide also was used preferentially in patients undergoing MR angiographic examinations.
For the second part of this study, we identified from a nephrology department database all patients who underwent regular long-term hemodialysis between January 1, 1999, and April 1, 2007. We determined the number of these patients who had received gadolinium-based contrast injections for imaging studies. We counted the gadolinium-based contrast-enhanced examinations of each of these patients and determined the number who subsequently had nephrogenic systemic fibrosis. In this way, we determined the percentage of long-term hemodialysis patients exposed to gadolinium-based contrast material at our institution in whom nephrogenic systemic fibrosis developed.
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Administration of gadolinium-based contrast material—A history of gadolinium-based contrast administration before diagnosis was identified for 25 of the 29 patients (22 at our institution and three at another institution). No such history was recorded for the other four patients. It is possible that one or more of the four might have received gadolinium-based contrast material at another institution without our knowledge.
The records of the 25 patients who received gadolinium-based contrast injections showed that there had been one such injection in nine patients, two in nine patients, three in five patients, four in one patient, and six in one patient before the onset of nephrogenic systemic fibrosis. The mean time between the first and the last gadolinium exposure of the 16 patients who had received multiple gadolinium injections was 13.6 months (range, 1 day–45 months). The gadolinium-based agents were injected for MRI (nine patients), conventional vascular and interventional studies (six patients), or for both (10 patients). The gadolinium-based contrast-enhanced study closest temporally to the time of diagnosis was MRI or MR angiography for 16 patients, an interventional procedure for eight (four arteriograms, three venograms, and one dialysis vascular access fistulogram), and both for one patient (who underwent MRI and venography within a single 24-hour period).
At our institution, we used a standard gadolinium-based contrast material dose of 0.1 mmol/kg up to a maximum volume of 20 mL for patients undergoing conventional MRI examinations. Higher doses were injected for MR angiography and interventional examinations. For the most recent imaging examination before the diagnosis of nephrogenic systemic fibrosis, the exact volume of gadolinium-based contrast material administered was known for eight (32%) of the 25 patients. Three patients received 100 mL of gadolinium-based contrast material for a conventional angiographic procedure, and four others received 40–60 mL (one was given 60 mL for conventional angiography, and three were given 40 mL each for MR angiography). One patient received 20 mL of gadolinium-based contrast material for a standard MRI examination. Thus the volume of gadolinium-based contrast material administered exceeded 20 mL in seven of eight cases in which the volume was known.
Many of the 17 patients for whom the exact dose of gadolinium-based contrast material administered was unknown likely received doses exceeding 20 mL. Seven studies in which the dose was not recorded were MR angiography, in which double-dose studies are frequently performed, and five other studies were conventional angiograms (the patient undergoing MRI and venography within 24 hours did not have the dose for either study recorded). Thus it is likely that 19 of the 25 patients received doses of gadolinium-based contrast material that exceeded 20 mL. Of the other six patients, one was known to have received a 20-mL dose. Four other patients who underwent abdominal MRI examinations (two at other institutions) and one who underwent lumbar spinal MRI might have received doses of 20 mL or less.
The exact type of gadolinium-based contrast material administered for the imaging studies performed closest to the diagnosis of nephrogenic systemic fibrosis was not recorded for most (22, or 88%) of the 25 patients, including the patient who had undergone conventional and MR angiography within a 24-hour period. Two patients received gadodi-amide, and one received gadopentetate dime-glumine. Of the 16 patients who had received an injection of gadolinium-based contrast material for earlier imaging studies, the specific agent was documented for only one patient. This patient was one of the two known to have received gadodiamide for the imaging study performed closest in time to diagnosis. This patient had received gadopentetate dimeglu-mine for MRI performed 3 months before and gadodiamide for MRI performed 10 months before the temporally closest study.
Renal function at the time of gadolinium administration—All 29 patients had some degree of renal dysfunction (27 had chronic renal failure, and two had acute renal failure). Of the four patients with no known gadolinium-based contrast exposure, two were receiving hemodialysis and one long-term ambulatory peritoneal dialysis at other institutions. The fourth patient presented with symptoms of nephrogenic systemic fibrosis 1 month after an episode of transient acute renal failure, which resulted from an overdose of nonsteroidal antiinflammatory medication. Because she also was treated primarily at another hospital, we were not able to determine whether she had undergone imaging studies or whether she had needed temporary dialysis.
Nineteen (76%) of the 25 patients who received gadolinium-based contrast material were known to be undergoing dialysis. Seventeen of the 19 were undergoing hemodialysis (16 for chronic renal failure and one for acute renal failure) and two were undergoing chronic ambulatory peritoneal dialysis at the time of the gadolinium-based contrast-enhanced study performed closest to the diagnosis of nephrogenic systemic fibrosis. Each of the other six patients who received gadolinium-based contrast material had some degree of chronic kidney disease. Three had stage 4 or 5 chronic kidney disease (serum creatinine level at the time of gadolinium-based contrast injection, 3.4–6.1 mg/100 mL) and started hemodialysis within 2 months of the gadolinium-based contrast-enhanced study. Dialysis was not needed by two patients. There was insufficient follow-up of the other patient, so it could not be determined whether he eventually needed dialysis.
Comorbid conditions—The medical records of three patients were insufficient to determine whether they had comorbid conditions. All 26 of the patients for whom there was medical information on comorbid conditions had multiple medical problems other than renal failure. The 52 comorbid conditions are listed in Table 2. Eleven patients had one comorbid condition, eight patients had two, four had three, two had four, and one patient had five conditions. Eight (31%) of the patients had chronic liver disease necessitating liver transplantation. Because the development of nephrogenic systemic fibrosis has been linked to a proinflammatory condition or vascular injury [10], we assessed patient records for the existence of concomitant processes of this type. Clear coexisting proinflammatory or vascular diseases were found in 17 (65%) of 26 patients for whom sufficient medical records were available (Table 2).
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Interval between gadolinium-based contrast administration and symptom
onset—The interval between the most recent gadolinium-based
contrast injection and symptom onset was unknown for four patients, 1 month or
less for eight (38%) of the other 21 patients, and 1–2 months for seven
patients. In five other patients, symptoms developed 2–12 months after
gadolinium-based contrast injection (
3, 4, 6, 7, and 8 months after
injection). In one patient, symptoms developed 53 months after the closest
known gadolinium-based contrast injection.
Four patients had symptoms of extremity rash (two patients), firmness (one patient), or skin changes (one patient) that preceded gadolinium-based contrast administration. In each of these patients, however, the extremity skin problems (skin discoloration and rash) worsened after gadolinium-based contrast administration. In three other patients, the temporal relation between gadolinium-based contrast administration and symptom onset was difficult to determine with great accuracy. These patients had had mild symptoms of nephrogenic systemic fibrosis for 2 years or more before the pathologic diagnosis was made.
Distribution and manifestations of skin disease—Skin disease distribution was known for all 29 patients. In 14 patients, only the lower extremities were involved with occasional extension into the buttocks. In four patients, only the upper extremities were involved, and in 10 patients, both upper and lower extremities were affected. One patient had manifestations only on his back, groin, and buttocks. Description of disease manifestations included thickened or sclerotic, indu-rated, or discolored skin (16 patients), plaques or nodules (nine patients), rash or erythema (eight patients), and edema (one patient). Five patients had two of these manifestations.
Disease severity and condition at follow-up—For two patients, including one who had had an episode of acute renal failure, there was no follow-up information. For the other 27 patients, the mean follow-up period after diagnosis was 25 months (range, 1–74 months). The presence of the disease was not mentioned in follow-up notes on 11 patients. Of the other 16 patients, three died 1, 4, and 25 months after diagnosis. Deaths were described as being due to acute sepsis or infection in two patients and to cardiac disease in a third. It is impossible to exclude the possibility that nephrogenic systemic fibrosis might have played a role.
Eight patients had disease manifestations severe enough to warrant the mention of chronic debility in follow-up notes: persistent limited range of motion (five patients, two of whom needed a motorized wheel-chair, one of whom needed a cane, and one of whom had flexion contractures of the hands), ongoing pain or neuropathy, ongoing physical therapy sessions, and disfigurement (one patient each). In three other patients, the disease was merely mentioned as being stable (two of whom were noted to have residual skin plaques).
Two patients had documented relief of symptoms, including one of the two patients who had had an episode of transient acute renal failure. In this patient, hyperpigmentation and firmness of the lower extremities resolved completely. The patient did, however, have residual plaques on her lower extremities. In another patient who had end-stage renal disease and was undergoing hemodialysis, sclerotic changes and erythema of the distal shins receded partially. The patient had been treated only with topical application of steroid cream to the affected areas.
Review of Patients Undergoing Long-Term Hemodialysis
Review of the nephrology database revealed that 1,113 patients with
end-stage renal disease underwent ongoing regular hemodialysis between January
1, 1999, and April 1, 2007. Of these, 414 (37%) patients received
gadolinium-based contrast material for an imaging study performed while they
were undergoing dialysis or within 6 months before the start of dialysis.
Three hundred thirty patients received gadolinium-based contrast material for
one or two imaging studies, 65 received gadolinium-based contrast material for
three or four studies, 14 for five or six studies, and four for seven studies.
One patient received contrast material on 10 different occasions.
Nephrogenic systemic fibrosis developed in 12 (2.9%) of the 414 patients who received gadolinium-based contrast material. This number included nine (2.7%) of the 330 patients who had received only one or two injections and three (4.6%) of the 65 patients who had received three or four injections but none of the patients who had received five or more injections of gadolinium-based contrast material. For example, nephrogenic systemic fibrosis did not develop in a 55-year-old woman with chronic renal failure who had been undergoing hemodialysis for 5 years and who received gadolinium-based contrast material for 10 different MRI examinations performed over a 2-year period. Specifically, she had no reports of skin lesions during a follow-up evaluation 6 months after her latest MRI examination. No nephrogenic systemic fibrosis developed in the 699 patients in this database undergoing long-term dialysis who did not receive gadolinium-based contrast material.
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Broome and colleagues [8] described 12 patients, all with renal insufficiency and eight of whom were undergoing chronic dialysis, in whom nephrogenic systemic fibrosis developed 2–11 weeks after gadodiamide exposure. In that series, nephrogenic systemic fibrosis developed in 10 dialysis patients within 2 days of gadolinium-based contrast administration. Three of these patients underwent dialysis on three consecutive days beginning the day of MRI contrast administration. Three of the 12 patients had long-term sequelae due to contractures and myopathy. Sadowski et al. [10] described 13 patients in whom nephrogenic systemic fibrosis developed within 6 months after gadodiamide injection, although one patient also had received gadobenate dimeglumine. All 13 patients had compromised renal function, and four died.
The findings in our review of our experience with nephrogenic systemic fibrosis were similar to the findings of earlier studies. Development of this condition was strongly correlated with renal failure and a history of gadolinium-based contrast administration. Our experience adds an additional 25 patients in whom gadolinium-based contrast exposure was known to have preceded the onset of nephrogenic systemic fibrosis. Unfortunately, the specific implicated contrast agent was unknown for all but three patients in our study (two received gadodiamide, and one received only gadopentetate dimeglumine).
In our study the temporal relation between gadolinium-based contrast administration and symptom onset was occasionally difficult to establish. All of the patients in our series were very ill, and most had coexisting diseases, some of which were dermatologic. An example of this problem is that four of our patients had extremity skin disorders before the earliest known episode of gadolinium-based contrast administration. In each of these patients, however, the symptoms worsened or changed (development of nodules and firmness and a rash in each) after administration of gadolinium-based contrast material. We cannot be absolutely certain whether this worsening represented superimposition of nephrogenic systemic fibrosis on another dermatologic process or whether these patients had mild symptoms of nephrogenic systemic fibrosis before exposure to gadolinium-based contrast material.
In our series, three patients had only mild dermatologic manifestations of nephrogenic systemic fibrosis (extremity rash or firmness) that lasted 2 years or longer before diagnosis. The precise temporal relation between symptom onset and contrast injection for these patients was difficult to determine retrospectively with any precision. Nineteen of our patients had symptoms that were not severely debilitating, an observation that leads us to suspect that nephrogenic systemic fibrosis may be under-diagnosed at our and other centers in a group of patients who have many other medical problems, some of which are dermatologic.
The risk of development of nephrogenic systemic fibrosis among patients with renal failure who receive gadolinium-based contrast material has been estimated previously. In the study by Broome et al. [8], at an institution where gadodiamide was used exclusively, nephrogenic systemic fibrosis developed in 4% of dialysis patients who received a gadolinium-based contrast injection. Kanal and associates [12] estimated the incidence of nephrogenic systemic fibrosis among end-stage renal disease patients after receiving gadodiamide as being approximately 3–5%. In our study, a lower percentage of our patients (2.9%) undergoing long-term dialysis had nephrogenic systemic fibrosis after gadolinium-based contrast exposure. This slight difference may be due to statistical variation, or it may reflect the fact that many of our patients received gadopentetate dimeglumine rather than gadodiamide. If one assumes that there is a lower risk of nephrogenic systemic fibrosis among patients given gadopentetate dimeglu-mine [13], the overall incidence of nephrogenic systemic fibrosis is expected to be lower. We do not know which contrast agent was used in most of our cases, so we cannot calculate separate risk levels for the various agents we used. In any event, it can be seen that the risk of development of nephrogenic systemic fibrosis is relatively low, even among patients at highest risk.
The cause of nephrogenic systemic fibrosis remains to be defined. Some investigators [14] have found that although gadolinium can be detected in the skin and soft tissues of all persons, including healthy volunteers, after injection of gadolinium-based contrast material, on average it is present in higher concentrations in patients in whom nephrogenic systemic fibrosis develops. It has been speculated that this gadolinium, possibly in conjunction with another, as of yet unidentified, comorbid condition in renal failure patients, activates a specific newly identified type of WBC called a circulating fibrocyte, which then triggers a wound-healing response primarily in the skin and subcutaneous tissues and results in fibrosis [15, 16]. If it exists, this mechanism may explain why nephrogenic systemic fibrosis occurred in two of our patients who had acute renal failure at the time of gadolinium-based contrast administration. Nephrogenic systemic fibrosis may occur whether or not gadolinium persists as an active inciting agent or because circulating fibrocyte activation persists, even if renal function is recovered and free gadolinium is eventually cleared.
A number of comorbid conditions that may place a renal failure patient at increased risk have been suggested, including increasing cumulative gadolinium-based contrast exposure [17]; metabolic acidosis [6]; vasculopathy [3]; increased iron, calcium, and phosphate levels, which may promote displacement of free gadolinium from the rest of the MRI contrast molecule [14, 17]; acute proinflammatory events (major surgery, infection, or a vascular event) at the time of contrast-material injection [10]; high-dose erythropoietin-β treatment [17]; and immunosuppression [18]. None of these mechanisms, however, has been proved with any degree of certainty to be responsible for promoting nephrogenic systemic fibrosis.
As our study showed, most patients in whom nephrogenic systemic fibrosis develops are chronically ill owing to renal disease but also have a variety of coexisting conditions. This phenomenon makes it difficult to identify one or two specific additional risk factors for nephrogenic systemic fibrosis in these patients. Our series and others [8] show that a large proportion of patients with nephrogenic systemic fibrosis have renal disease and have chronic liver disease leading to liver transplantation. In the series reported by Broome and associates [8], four (33%) of 12 patients in whom nephrogenic systemic fibrosis developed also had severe liver disease that led to transplantation within 17 days of the MRI examination. In our series, eight (31%) of 26 patients for whom sufficient medical information was available had a history of chronic liver disease.
Our review illustrates several important issues related to the development of nephrogenic systemic fibrosis. We found that nephrogenic systemic fibrosis developed in at least one patient after a single standard dose of gadolinium-based contrast material. Not surprising, however, is that this observation indicates that the minimum administered volume of gadolinium-based contrast material required to induce nephrogenic systemic fibrosis is no more than 20 mL. There would be little reason to assume that nephrogenic systemic fibrosis would be limited to patients receiving a double dose of gadolinium-based contrast material or more, given the wide range of renal function, sensitivity, and co-morbid conditions. It is possible that a dose–response curve exists, but it is probably shifted in either direction by patient-level factors. This patient-level variation also was seen among our chronic dialysis patients. Nephrogenic systemic fibrosis did not develop in most of the patients who received multiple injections of gadolinium-based contrast material. Our findings also show that, although unusual, manifestations may improve in some patients, especially, but not exclusively, in patients in whom renal failure is acute and transient. Symptomatic improvement was seen in two patients in our series.
The most important limitation of our study relates to the fact that it was a retrospective review. We were provided with only limited information concerning the type and amount of gadolinium-based contrast material administered to our patients and with incomplete follow-up notes in the patients' medical records. (As a result, we have instituted measures to ensure that the type and amount of gadolinium-based contrast material used is recorded for all MRI examinations.) In addition, the long period between symptom onset and diagnosis, in part because of the insidious nature of symptoms in a few patients, limited our ability to determine a precise time course in some instances. Almost all patients were extremely ill and had many different medical problems. The number of these problems and their dates of onset were difficult to tabulate.
In summary, our series provides additional evidence of the association between nephrogenic systemic fibrosis and exposure to gadolinium-based contrast material. It shows that nephrogenic systemic fibrosis can develop after exposure to more than one type of gadolinium-based MRI contrast agent. Nephrogenic systemic fibrosis can occur in patients who have acute and transient renal failure. A wide spectrum of severity of nephrogenic systemic fibrosis was found. Although nephrogenic systemic fibrosis can be a severely debilitating disease in some patients, in others it is merely one of a myriad of medical problems and does not appear to contribute substantially to patient disability. In some patients, symptoms are so mild that they are tolerated for long periods before definitive evaluation is performed. Our findings also illustrate the great difficulty encountered in a retrospective review of very ill patients with many medical problems. Identification of the temporal relations among gadolinium-based contrast administration, symptom onset, diagnosis, and recognition of additional risk factors is extremely difficult in many cases.
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