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10.1245/ASO.2006.03.042
Annals of Surgical Oncology 13:96-102 (2006)
© 2006 Society of Surgical Oncology
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Original Article

Long-Term Outcomes in Patients With Calciphylaxis From Hyperparathyroidism

Allison Duffy, MD, Michael Schurr, MD, FACS, Thomas Warner, MD and Herbert Chen, MD, FACS

Section of Endocrine Surgery, Department of Surgery and Department of Pathology, University of Wisconsin-Madison, H4/750 Clinical Science Center, 600 Highland Avenue, Madison, Wisconsin 53792-7375

Correspondence: Address correspondence and reprint requests to: Herbert Chen, MD, FACS; E-mail: chen{at}surgery.wisc.edu.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Background: Calciphylaxis is a rare condition associated with chronic renal failure and entails a very poor prognosis. Pathogenesis is poorly understood but involves abnormalities in calcium and phosphorus metabolism that lead to vascular and extravascular calcification. Patients present with painful ulcerating plaques that progress to gangrenous wounds. Parathyroidectomy has been advanced as a life-saving intervention in these patients, but long-term results with wound healing and survival after parathyroidectomy are not well described.

Methods: Between January 1987 and October 2003, 15 patients with biopsy-confirmed calciphylaxis were treated at the University of Wisconsin. Of these 15 patients, 9 were treated with medical therapy (bisphosphonates and phosphate binders), whereas 6 underwent parathyroidectomy. The medical records were reviewed, and patients or relatives were interviewed. Survival was determined by Kaplan-Meier analysis.

Results: Four patients underwent subtotal parathyroidectomy, and two patients underwent total parathyroidectomy. All had reductions in the intact parathyroid hormone level (mean ± SD, 25.2 ± 4.5 pg/mL). Whereas all six patients treated with parathyroidectomy had partial/complete wound healing, only two of nine in the medical group had any improvements in the skin lesions (P = .006). With up to 80 months of follow-up, patients who underwent parathyroidectomy had a longer median survival compared with those who did not have surgery (39 vs. 3 months; P = .017).

Conclusions: On the basis of our long-term follow-up of this patient population, subtotal or total parathyroidectomy was associated with long-term survival and was more likely to promote healing if performed earlier in the course of disease. Therefore, patients with calciphylaxis from secondary hyperparathyroidism should be referred promptly for potential parathyroidectomy.

Key Words: Calciphylaxis • Secondary hyperparathyroidism • Calcific uremic arteriolopathy • Parathyroidectomy • Wound care


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Calciphylaxis, also now known as calcific uremic arteriolopathy, is a rare but serious condition that is associated with secondary hyperparathyroidism and chronic renal failure. Estimates report that calciphylaxis occurs in up to 4% of patients who receive hemodialysis;1,2 however, it has also been infrequently reported in other patient groups.3–5 Calciphylaxis usually presents with intensely painful areas of superficial, violaceous mottling and resembles purpura or livedo reticularis. The superficial lesions often present suddenly and progress rapidly to cutaneous necrosis and dry gangrene.6 Lesions most commonly develop on the extremities or trunk, but involvement of the penis, breast, digits, muscle, and bowel has been reported.7 Significant mortality—as high as 87% in some studies8—often results from wound expansion and barrier breakdown leading to sepsis. Pathologic criteria for biopsy diagnosis include epidermal ulceration, endovascular fibroblastic proliferation, dermal necrosis, mural vascular calcification, necrosis of dermal collagen, frank luminal vascular thrombosis, and acute and chronic calcifying septal panniculitis9 (Fig. 1Go).


Figure 1
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  		FIG. 1. Histopathologic changes in calciphylaxis. A medium-sized vessel in the subcutis shows extensive calcification of media (C) with thrombus in the lumen (arrow) and necrosis of fat (stain, hematoxylin and eosin; original magnification, x100; University of Wisconsin, Madison).

 
Bryant and White first reported vascular calcification with cutaneous necrosis in association with uremia in 1898; it was known that vascular calcification was prevalent in uremia, but the significance of this syndrome remained unknown. In 1962, Selye et al.10 first used the term calciphylaxis after a series of experiments in nephrectomized rats. Over the years, many other names have been suggested to characterize the pathogenic process, but the most recent term is calcemic uremic arteriolopathy.

The clinical importance of this syndrome was not recognized until the 1976 report by Gipstein et al.11 It is currently thought that an abnormal calcium and phosphorus metabolism, so often associated with renal failure and secondary hyperparathyroidism, leads to an increased serum calcium and phosphorus product, which sets up the metabolic milieu necessary for calciphylaxis.12 Recent studies have suggested that vascular calcification may be due to complex biochemical processes. Calciphylaxis may be due to a direct effect of increased serum calcium and phosphorus levels in vascular smooth muscle that cause bonelike differentiation.12,13 Risk factors that have been well described in the literature include female sex (male-female ratio of 1:3), morbid obesity, white race, diabetes mellitus, warfarin, glucocorticoids, protein C or S deficiency, recent weight loss, or malnutrition.8,14

Traditional medical therapy consists of controlling calcium and phosphate abnormalities with non–calcium-containing phosphate binders such as aluminum hydroxide or sevelamer and providing supportive wound care. Small case series have been reported in the literature,15–19 and total or subtotal parathyroidectomy has been associated with improvements in wound healing and long-term survival. At our institution we identified a retrospective cohort of patients and compared parathyroidectomy with medical management in the treatment of calciphylaxis for long-term survival.


   METHODS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Between January 1987 and October 2003, 15 patients presenting with biopsy-confirmed calciphylaxis were treated at the University of Wisconsin. All had secondary hyperparathyroidism due to renal disease (n = 13) or malabsorption (n = 2). All 15 patients required significant wound care for extensive skin necrosis. Of these 15 patients with calciphylaxis, 9 were treated with medical therapy (bisphosphonates and phosphate binders), and 6 underwent parathyroidectomy in addition to medical management. The medical records were reviewed, and patients or relatives were interviewed to assess symptomatic improvement after parathyroidectomy. Survival was determined by Kaplan-Meier analysis. Statistical analysis was performed with SPSS software (SPSS Inc., Chicago, IL). Significance was defined as P < .05. All values are represented as mean ± standard deviation.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
DISCUSSION
 CONCLUSIONS
 REFERENCES
 
Of the 15 patients with calciphylaxis, 9 were treated with medical therapy (bisphosphonates and phosphate binders) and wound care/supportive measures, and 5 were referred for parathyroidectomy. One patient had a subtotal parathyroidectomy 42 months before presentation. There were no significant differences between the medical and surgical groups with respect to pretreatment calcium levels (9.7 ± .4 mg/dL vs. 10.1 ± .4 mg/dL, respectively) or phosphate levels (4.2 ± .7 mg/dL vs. 4.7 ± 1.3 mg/dL, respectively). The calcium and phosphorus product was not statistically different between the surgical and medical groups (46.7 ± 5.0 vs. 40.7 ± 4.2, respectively), and the average age also was not statistically different (48 ± 5 years vs. 60 ± 3 years). The lack of difference in these factors could be due to low numbers in each group. Comorbidities seemed similar between groups (Table 1Go). All six of the patients in the surgical group had proximal lesions (trunk, abdomen, thighs, and buttocks). Four of the nine patients in the medical group had distal lesions (arms or lower extremities), and five had proximal lesions.


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  		TABLE 1. Individual patient data
 
Of the six patients who underwent surgical treatment, four had subtotal (3.5 gland) parathyroidectomies, and two had total parathyroidectomies. All six had significant reductions in parathyroid hormone (PTH) levels after surgery (mean decrease, 557 ± 278 pg/mL to 22 ± 5.5 pg/mL; mean decrease of 96%; Table 2Go). In addition, all patients experienced reductions in mean calcium and phosphate levels and in the mean calcium and phosphorus product. The mean calcium level changed from 9.7 ± .4 mg/dL to 9.2 ± .7 mg/dL, and the phosphate level decreased from 4.2 ± .7 mg/dL before surgery to 4.0 ± .3 mg/dL after surgery. In the nine patients who had medical management, there were no significant changes in the average serum calcium, phosphorus, or calcium and phosphorus product over time, and mean PTH levels remained increased.


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  		TABLE 2. Study groups and mean laboratory values
 
All of the patients who underwent parathyroidectomy reported resolution of pain and healing of their cutaneous wounds (Fig. 2Go), compared with only two of nine patients in the medical management group (P = .006; Table 3Go). The median survivals of patients in both the surgical and the nonsurgical groups were determined by Kaplan-Meier analysis. Patients who underwent parathyroidectomy had a significantly longer median survival than those who did not have surgery (39 vs. 3 months; P = .017; Fig. 3Go).


Figure 2
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  		FIG. 2. A patient who presented with calciphylaxis to the University of Wisconsin (A and B) and subsequently underwent total parathyroidectomy and split-thickness skin grafting (C). After surgery, the calci-phylaxis wounds healed, the calcium and phosphorus abnormalities normalized, and the patient continues to do well, without recurrences.

 

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  		TABLE 3. Outcomes of patients with calciphylaxis with surgical or nonsurgical management
 

Figure 3
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  		FIG. 3. Actuarial survival comparison of patients with secondary hyperparathyroidism and calciphylaxis treated by parathyroidectomy versus nonsurgical treatment alone.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
CONCLUSIONS
 REFERENCES
 
Although the prevalence of calciphylaxis has been estimated to be as high as 4% in the renal dialysis population,1,2 a low total number of cases have been reported, and prospective trials of treatment have yet to be published. Gipstein et al.11 were the first to describe a patient whose wounds resolved after parathyroidectomy. This was followed by other case reports in which early parathyroidectomy produced dramatic relief of symptoms, improved wound healing, and longer median survival times.15–20 Our series of 15 patients at our institution confirms this trend suggested by prior case series. All patients treated surgically had significant reductions in PTH levels after surgery (mean decrease, 96%) but had only modest reductions in calcium and phosphorus levels (6% and 5%, respectively) and the calcium and phosphorus product (mean decrease, 9%). All patients in the surgical group reported resolution of pain and healing of cutaneous wounds at a statistically significantly higher rate than non–surgically treated patients. Patients who underwent parathyroidectomy had a significantly longer median survival than those who did not have surgery (36 vs. 3 months, P = .017; Fig. 3Go).

The lesion location (proximal vs. distal) is also important to consider. In our case series and other reports in the literature, patients with proximally located lesions had a poorer prognosis, even with proper management.7,8 The patients included in this study had a predominance of proximal locations (trunk, buttocks, thigh, and abdomen). None had distal locations in the surgical group (Table 1Go), and only four patients in the nonsurgical group had distal locations (arms and legs). Mortality was 100% for proximal lesions in the medically treated group and 60% for proximal lesions in the surgical group. For distal lesions in the medically treated group, mortality was 60%, and there were no distal lesions in the surgical group. Thus, the lesion location did not affect the increased survival seen in the surgical group.

Parathyroidectomy is the only curative therapy for hyperparathyroidism.21 It is associated with high cure rates with low complication rates.22–25 We did not see any complications of parathyroidectomy in any of our patients; the most common reported complications were laryngeal nerve paralysis, recurrent hyperparathyroidism, and infection. One patient in our series developed recurrent calciphylaxis 42 months after subtotal parathyroidectomy. His PTH level remained at appropriate levels after surgery, but systemic calcification occurred as a result of increased calcium and phosphorus levels due to noncompliance with therapy (renal diet and calcium-containing phosphate binders).

In our series, although the number of comorbidities between the medical and surgical groups seemed similar, it is likely that there were more severe comorbidities in the medical group. This may have contributed to the decision of their physicians to recommend surgical intervention. Many of the medically treated patients with secondary hyperparathyroidism were not referred for surgery because the diagnosis of calciphylaxis had gone unrecognized for a significant period of time, and, therefore, the patients had become severely ill. In the patients who were medically treated and who had secondary hyperparathyroidism, all died within 20 days of diagnosis. This shortened survival emphasizes the likelihood of the difference in comorbidities. Of the two patients who are currently alive in the surgical group, calciphylaxis was recognized early, before the lesions expanded, and they were offered parathyroidectomy as a treatment modality. The single survivor in the medically treated group had calciphylactic lesions located very distally (right foot) and minimal metabolic abnormalities. The lesions were nonprogressive over the course of 3 years, and once diagnosed with calciphylaxis, the patient was aggressively treated by reduction of increased phosphorus levels and four subsequent skin-grafting procedures. Several authors17 have concluded that the primary factors associated with success are the amount of time that has elapsed between presentation and diagnosis, the time between diagnosis and surgical intervention, the patient’s general health status, and the location, number, and severity of the skin lesions. This is also true in our experience, although the degree of metabolic abnormalities of serum calcium and phosphorus may also serve as a predictor of success in treating patients with calciphylaxis.

There are emerging data to suggest that total parathyroidectomy could be more effective than subtotal parathyroidectomy.26 In the situation of secondary hyperparathyroidism and calciphylaxis, we had favored subtotal parathyroidectomy as the treatment of choice at our institution because of the 5% risk for permanent hypoparathyroidism associated with total parathyroidectomy and autotransplantation. However, we have moved toward total parathyroidectomy. In our study, two patients underwent total parathyroidectomy, and four underwent subtotal parathyroidectomy. Eliminating PTH secretion and removing all parathyroid tissue is being emphasized as the most important goal in the treatment of this disease, and although it will result in permanent hypoparathyroidism, this condition is relatively easy to treat in this patient population. More patients are needed to draw a substantial conclusion of subtotal versus total parathyroidectomy in this patient population. We have recently reported that the gamma probe may facilitate localization of the parathyroid glands and reduce operative time.27,28

The cause of calciphylaxis remains elusive, most likely because it is the common end point of a heterogeneous group of disorders.12 Some nephrologists do not believe that parathyroidectomy is particularly effective in treating patients with calciphylaxis; however, there is a strong consensus that parathyroid resection is associated with pain resolution, better healing of ulcerations, and prolonged survival. Parathyroidectomy offers the only treatment that removes the possible tissue "sensitizer" that perpetuates the disease and hypercalcemia. It seems that serial events, most consistently involving renal failure–induced abnormalities in calcium homeostasis, are required to occur over a period of time for calciphylaxis to develop. PTH may be a key component of the complex biochemical events that occur and result in bonelike differentiation of vascular smooth muscle.13 It is controversial whether parathyroidectomy is indicated in patients whose serum calcium and PTH levels are normal. Kang et al.20 suggested that parathyroidectomy is beneficial only for those with severe hyperparathyroidism, because it would result in low-turnover bone disease, which would eventually increase calcium and phosphorus levels and promote further calciphylaxis. In our study, six of nine patients in the medically treated group did not have extremely high PTH levels. One died within 1 week, three died within 3 months, one died within 1 year, and only one of the six currently remains alive. This demonstrates much shorter survival times on average than those for the patients treated surgically. On the basis of our experience and that of others who have reported a rapid regression of calciphylactic skin lesions after parathyroidectomy,15–19 we suggest that perhaps parathyroidectomy is an important modality for the treatment of this life-threatening condition, and we recommend that it be considered for every calciphylaxis patient, even those without abnormal elevations of their PTH. Further studies and prospective trials are greatly needed to elucidate the pathogenesis of the disorder and identify the optimal treatment modality; however, parathyroidectomy seems to be the most promising treatment modality at this point in time.

Because there seems to be no completely clear reason why these lesions develop, a high level of suspicion is necessary to make the diagnosis. Calciphylaxis is a commonly missed diagnosis: a retrospective chart review at our institution revealed only 15 cases of calciphylaxis, and this is significantly below the expected number if the incidence is truly 4% of the dialysis population.1 It is likely that many cases of calciphylaxis go completely unrecognized at most institutions, and major contributing factors to the high mortality are the significant delay in diagnosis and nonaggressive management.29 With early clinical detection and appropriate intervention, there should be an opportunity to improve the high mortality rate and to relieve the severe pain associated with these lesions. For the surgeon, to whom patients are often referred with necrotic wounds, it is important to include calciphylaxis in the differential diagnosis when evaluating a patient, especially one with malabsorption, hyperparathyroidism, or end-stage renal disease.


   CONCLUSIONS
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
REFERENCES
 
Calciphylaxis is a frequently underrecognized and underdiagnosed condition. Current standards of practice emphasize a multidisciplinary approach with timely communication among surgeons, nephrologists, endocrinologists, and dermatologists.30 Early identification of calciphylaxis, proper medical management of comorbidities, management of calcium and phosphorus levels with non–calcium-containing phosphate binders such as aluminum hydroxide or sevelamer,31 and meticulous wound care32,33 are essential for the proper care of patients with calciphylaxis. On the basis of our long-term follow-up of this patient population, subtotal or total parathyroidectomy was associated with long-term survival and was more likely to promote healing if performed earlier in the course of disease. Therefore, patients with calciphylaxis from secondary hyperparathyroidism should be referred promptly for parathyroidectomy to possibly promote short-term wound healing and long-term survival.

Received for publication March 4, 2005. Accepted for publication September 8, 2005.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 METHODS
 RESULTS
 DISCUSSION
 CONCLUSIONS
 REFERENCES
 

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