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Original Article |

Cost Savings of Patients With a MACIS Score Lower Than 6 When Radioactive Iodine Is Not Given FREE

Pia Z. Pace-Asciak, MD; Richard J. Payne, MD, FRCSC; Spiro J. Eski, MD; Paul Walfish, MD, FRCPC; Manzur Damani, BSc, MRT(N), CNMT; Jeremy L. Freeman, MD, FRCSC
[+] Author Affiliations

Author Affiliations: Department of Otolaryngology, Mount Sinai Hospital, Toronto, Ontario, Canada. Dr Pace-Asciak is now with the Department of Medicine, University of Ottawa, Ottawa, Ontario, Canada.


Arch Otolaryngol Head Neck Surg. 2007;133(9):870-873. doi:10.1001/archotol.133.9.870.
Text Size: A A A
Published online

Objective  To assess the cost savings if the current policy of treating patients with a MACIS (metastases, age, completeness of resection, invasion, and size) score lower than 6 using radioactive iodine (RAI) was changed to reflect the findings of recent studies.

Design  Retrospective medical record review.

Setting  Mount Sinai Hospital, Toronto, Ontario.

Patients  Between January 1, 2002, and July 1, 2005, 199 consecutive patients with a MACIS score lower than 6 who received RAI treatment after total thyroidectomy.

Main Outcome Measures  Patient demographics were analyzed. Costs for the dose of RAI, hospital stay, and health insurance claims were included in the calculations.

Results  For 199 consecutive patients, the cost for sodium iodide 131 treatment totaled Can$161 588, and the required 2-day stay in isolation totaled Can$764 558. The overall cost to the health care system was Can$934 106, which translates into approximately Can$4694 per patient.

Conclusions  By following the recommendations of recent evidence-based studies and by ceasing to treat patients with a MACIS score lower than 6 after total thyroidectomy using RAI, cost savings can be accrued for health care systems involved in the treatment of thyroid cancer. Alternate strategies, such as treating patients who need RAI therapy on an outpatient basis and reducing the dose of RAI, can lower costs as well.

Previous studies1,2 have concluded that radioactive iodine (RAI) treatment in patients with well-differentiated thyroid carcinoma (WDTC) and a MACIS (metastases, age, completeness of resection, invasion, and size) score lower than 6 is unnecessary because it does not decrease the rate of recurrence or affect survival. Well-differentiated thyroid carcinoma accounts for approximately 90% of all thyroid malignant neoplasms.3 This type of thyroid cancer tends to grow slowly and takes a long time to become clinically significant. Papillary and follicular carcinoma fall under the umbrella of WDTC, which often manifests as asymptomatic nodules. The current accepted treatment of WDTC is surgery. Controversy arises about the necessity and extent of surgery, including central compartment and lateral neck dissections, and the indications for adjuvant RAI treatment.

There are several reasons for administering RAI treatment in the postoperative setting. First, it destroys residual thyroid tissue so that subsequent sodium iodide I 131 (131I) scanning can detect persistent disease.4 Radioactive iodine treatment also destroys occult microscopic carcinoma, decreasing disease recurrence.59 Second, RAI therapy enables follow-up using the serum thyroglobulin level as a sensitive tool for detecting recurrent disease.5,10 Testing the serum thyroglobulin level in patients with residual thyroid tissue could be problematic. Third, RAI treatment in the postoperative setting facilitates the use of a high therapeutic dose of RAI that may be necessary for ablation of subsequent persistent carcinoma.5,11,12

The effect on survival rates of the postsurgical management of WDTC using RAI treatment has been debated for decades. Recent studies1,2,9 demonstrate that postoperative 131I treatment should be reserved for high-risk patients to decrease recurrence and death rates. It has also been reported that the long-term prognosis in low-risk patients after total thyroidectomy alone is favorable and that RAI treatment does not confer an added benefit.1,2,5,9 Hay et al1,2 showed that RAI treatment in low-risk patients with a MACIS score lower than 6 does not decrease the recurrence rate or improve survival.

Health care institutions are constantly dealing with the reality of resource accountability. Therefore, we sought to assess the financial burden of ablation therapy at our institution (Mount Sinai Hospital, Toronto, Ontario) in treating patients with a MACIS score lower than 6 after total thyroidectomy using RAI. The objective of our study was to provide insight into the possible cost savings that could be realized by following the recommendations of current evidence-based studies and by ceasing postthyroidectomy RAI treatment in this patient group. In addition, by accounting for the costs involved in treating patients using RAI, we explored potential ways for institutions to save money when RAI treatment is indicated.

A retrospective medical record review of the thyroid cancer database at Mount Sinai Hospital between January 1, 2002, and July 1, 2005, was performed. To be included in the study, patients with WDTC had to have a MACIS score lower than 6 and treatment with total thyroidectomy followed by RAI. Data from 241 consecutive patients with WDTC were collected, but only 199 patients were included in the study. Forty-two patients were excluded because they had MACIS scores of 6 or higher.

Relevant patient demographics (age, sex, and date of surgery), tumor data (type, size, histologic findings, multifocal tumors, and extrathyroidal spread), treatment modalities (total thyroidectomy, adjuvant 131I therapy, and dose in megacuries), and outcomes (survival) were collected primarily from the pathology and surgical reports. The MACIS score was calculated as follows: 3.1 (if age ≤39 years or 0.08 × age if age ≥40 years) + 0.3 × tumor size (in centimeters) + 1 (if completely resected) + 1 (if locally invasive) + 3 (if distant metastases present).1,2

The costs of each specific dose of RAI, as well as the Provincial Health Care system claims totals, were then calculated. The accounting department was consulted for the costs of a 2-day hospital stay, and the Department of Medical Imaging was consulted for the 2005 costs per dose of RAI treatment. The study was approved by the Mount Sinai Hospital research ethics board before collecting data from patient files.

Patients (n = 99) with a MACIS score lower than 6 following total thyroidectomy for WDTC were included in the study. There were 161 women and 38 men in the study. The mean age was 42 years (age range, 17-73 years). The mean MACIS score was 4.51 (range, 3.25-5.90).

The breakdown of costs for hospital stay and RAI treatment is given in Table 1. The mean length of stay in the hospital for patients receiving RAI treatment after total thyroidectomy was 2 days. The treatment required isolation plus registered nurse care for a minimum of 3 h/d. This resulted in a cost of Can$3842 per patient and Can$764 558 for 199 patients for hospital costs alone. Included in the costs are Ontario Health Insurance Plan (government health insurance) claims of Can$350 per patient for 2 days, shipping costs of RAI (Can$30 per patient), and the mean cost of 100 mCi (to convert to becquerels, multiply by 3.7) of RAI treatment (Can$822 per patient).

Table Graphic Jump LocationTable 1. Breakdown of Hospital Costs for 199 Patients

The breakdown of the costs of RAI treatment is given in Table 2. Overall, the mean RAI dose given was 100 mCi at a cost of Can$822 per patient. In total, the cost of RAI treatment per patient, including shipping costs of RAI (Can$30 per patient), amounted to Can$852 per patient and Can$169 548 for 199 patients. Table 3 gives the difference in cost of RAI treatment when a mean dose of RAI (100 mCi) is used vs the actual dose of RAI (Can$169 548 vs Can$167 558), a negligible difference. Therefore, the overall cost to our institution for the 43-month period amounted to Can$934 106, which translates into Can$4694 per patient.

Table Graphic Jump LocationTable 2. Breakdown of Radioactive Iodine (RAI) Treatment Costs for 199 Patients
Table Graphic Jump LocationTable 3. Total Hospital and Radioactive Iodine (RAI) Treatment Costs for 199 Patients

Table 4 gives the cost per dose (in megacuries) of 131I capsules (in 2005) and the number of patients with a MACIS score lower than 6 receiving 131I treatment. One hundred twenty-eight of 199 patients with a MACIS score lower than 6 received 3700 MBq, amounting to Can$105 280. Thirty-five patients received less than 3700 MBq, whereas 36 patients receive greater than 3700 MBq. The total cost for 199 patients to receive RAI treatment amounted to Can$161 588. Furthermore, the mean dose of 131I was 3700 MBq (range, 3644-3755 MBq) among 199 patients with a MACIS score lower than 6 and 3885 MBq (range, 3777-3992 MBq) among 42 patients with a MACIS score of 6 or higher during 43 consecutive months.

Table Graphic Jump LocationTable 4. Cost Per Dose of Sodium Iodide 131 (131I) Capsules (in 2005) and Number of Patients Receiving 131I With a MACIS (Metastases, Age, Completeness of Resection, Invasion, and Size) Score Less Than 6

Most patients with WDTC such as papillary thyroid cancer and follicular thyroid cancer have a good prognosis.1,5 Papillary thyroid carcinoma accounts for 80% of cases and spreads via the lymphatic system, whereas follicular carcinoma accounts for 11% of cases and tends to spread through the blood.5 According to the US National Cancer Database, the 10-year survival rates are 93% for patients with papillary thyroid carcinoma and 85% for patients with follicular thyroid carcinoma.5

The current accepted approach for treating most WDTC is surgery, with the possibility of adjuvant RAI therapy. Following surgery, the MACIS score allows one to identify whether patients are at high risk or low risk for recurrent disease.1,2,13 Other scoring systems exist as guides to help clinicians establish prognosis,4,14 including the EORTC (the earliest classification, developed by the European Organization for Research and Treatment of Cancer center), TNM stage (updated in 2003), AGES (age, grade, extension, and size, developed in 1987 by the Mayo Clinic), AMES (age, metastases, extent, and size, developed in 1988 by Cady and Rossi15), and the system by Mazzaferri and Jhiang.7 Although all of the schemes have been reported to be effective at identifying patients at low risk of death, the EORTC and MACIS systems identify a broader spectrum of risk groups.2 Furthermore, the MACIS system is considered an accurate prognosis scoring system because it accounts for surgical removal of all tumor tissue, which seems most important for a favorable outcome.16

At our institution, RAI treatment is indicated for papillary carcinoma greater than 1.5 cm or for multifocal disease regardless of the size. Radioactive iodine treatment is usually given 6 to 8 weeks after surgery to ablate any persistent thyroid tissue to facilitate long-term monitoring for recurrence.5,710 These reasons for administering RAI treatment are important for treating and then monitoring patients who are at high risk for disease recurrence. However, for low-risk disease, it has been shown that RAI treatment is less likely to confer notable advantage and that the risks of the RAI therapy may outweigh the perceived benefits.2,11

In support of recent evidence-based medicine, an approach for reducing the economic burden to our health care system is to discontinue administering RAI treatment after total thyroidectomy in patients with a MACIS score lower than 6. In the United States, the incidences of death due to thyroid cancer in men and women are 0.17% and 0.26%, respectively.17 Hay et al2 found at 10 years after surgery that the cause-specific survival in the low-risk group is 100% whether or not ablation is performed. Furthermore, they reported that 84% (1917 of 2286) of patients analyzed during 5 decades (1950-1999) had a MACIS score lower than 6 and a 10-year rate of cause-specific survival approaching 100% whether or not RAI treatment was given.2 Tumor recurrence was estimated at 7% to 8%.2 Similarly, in a retrospective study5 of the French population, an overall survival rate among middle-aged adults with thyroid carcinomas was reported to be 80% to 95%. With this in mind, the evidence suggests that patients with a MACIS score lower than 6 do not reap added benefits from a more aggressive treatment approach using adjuvant RAI therapy.

An additional strategy to minimize the costs is the administration of RAI treatment as an outpatient procedure. Outpatient therapies using high doses of 131I have been shown to be safe provided that patients comply with precautions, understand the risks involved, and have a suitable home environment.18 As of May 1997, the US Nuclear Regulatory Commission amended its regulations so that patients could receive RAI therapy on an outpatient basis provided that the total effective dose equivalent to any other individual resulting from exposure to the treated individual does not exceed the 5.0-mSv (to convert millisieverts to millirems, multiply by 100) limit.19,20

Minimizing the dose of RAI given to patients with low-risk disease is another strategy to reduce the financial burden to the health care system.5,21 Although the dose of RAI used at our institution is similar to doses reported in the literature, there is little evidence to demonstrate that 3700 MBq has superior benefit over lower doses of RAI in patients with a MACIS score lower than 6. However, Mazzaferri and Jhiang7 found that low doses of 131I (29-50 mCi [to convert to mega becquerels multiply by 37]) were as effective as high doses (51-200 mCi) in controlling tumor recurrence (7% vs 9%) in patients with stage 2 or stage 3 tumors.

In addition to the monetary costs associated with postsurgical RAI treatment, the cost to the patient includes the adverse effects of the treatment. The concern is that patients may be unnecessarily exposed to irradiation and to its inherent complications. A portion of patients experience adverse effects from RAI treatment. The incidence of local adverse effects increases as the dose of RAI increases. These adverse effects include nausea (67% of patients), taste dysfunction (approximately 50%), radiation thyroiditis and neck pain (≤20%), sialadenitis that may produce chronic xerostomia (12%), and skin changes.11 Less common adverse effects include leukemia and decreased sperm count due to testicular damage after RAI therapy.

Rubino et al22 found a statistically significant relationship between the long-term effects of 131I administration and colorectal cancer, salivary gland cancer, and second primary malignancy of bone and soft tissue. In a European cohort of 6841 patients with thyroid cancer, they concluded that absolute risks of 14.4 for solid cancer and 0.8 for leukemia exist per gigabecquerel of 131I and 105 person-years of follow-up. These results demonstrate the need for careful evaluation of the extent of thyroid disease when deciding the dose of 131I treatment after surgery.

As previously suggested by others,1,2 the management of WDTC should be based on risk group analysis rather than on individual physician or institutional protocols. Based on the surrounding evidence, we are of the opinion that patients with a MACIS score lower than 6 should not receive postsurgical RAI treatment because the prognosis after surgery is close to 100%. Moreover, if RAI therapy is warranted, then treating patients on an outpatient basis would lower the costs, and so would reducing the dose of RAI administered. At our institution, we accrued close to Can$1 million in health care costs associated with hospitalization and RAI treatment during 43 months. By adopting evidence-based practices, a substantial amount of resources could be saved by health care systems on a national level.

Correspondence: Pia Z. Pace-Asciak, MD, Department of Otolaryngology, Mount Sinai Hospital, 600 University Ave, Toronto, ON M5G 1X5, Canada (ppaceasc@hotmail.com or piap@interchange.ubc.ca).

Submitted for Publication: July 28, 2006; final revision received October 19, 2006; accepted April 3, 2007.

Author Contributions: Drs Pace-Asciak and Payne had full access to all the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis. Study concept and design: Pace-Asciak, Payne, Walfish, and Freeman. Acquisition of data: Pace-Asciak, Payne, Eski, Walfish, Damani, and Freeman. Analysis and interpretation of data: Pace-Asciak, Payne, Eski, and Freeman. Drafting of the manuscript: Pace-Asciak, Payne, Walfish, and Freeman. Critical revision of the manuscript for important intellectual content: Pace-Asciak, Payne, Walfish, Damani, and Freeman. Statistical analysis: Payne. Obtained funding: Freeman. Administrative, technical, and material support: Pace-Asciak, Eski, and Freeman. Study supervision: Payne, Walfish, and Freeman.

Financial Disclosure: None reported.

Previous Presentation: This study was presented as a poster at the American Head and Neck Society 2006 Annual Meeting and Research Workshop on the Biology, Prevention, and Treatment of Head & Neck Cancer; August 18, 2006; Chicago, Illinois.

Hay  IDThompson  GBGrant  CS  et al Papillary thyroid carcinoma managed at the Mayo Clinic during six decades (1940-1999). World J Surg2002268879885 [published online ahead of print May 21, 2002]. doi:10.1007/s200268-002-6612-1
PubMed
Hay  IDBergstralh  EJGoellner  JREbersold  JRGrant  CS Predicting outcome in papillary thyroid carcinoma. Surgery 1993;114 (6) 1050- 1057
PubMed
Hundahl  SAFleming  IDFremgen  AMMenck  HR A National Cancer Data Base report on 53,856 cases of thyroid carcinoma treated in the U.S., 1985-1995. Cancer 1998;83 (12) 2638- 2648
PubMed
DeGroot  LJKaplan  ELStraus  FHShukla  MS Does the method of management of papillary thyroid carcinoma make a difference in outcome? World J Surg 1994;18 (1) 123- 130
PubMed
Schlumberger  MJ Papillary and follicular thyroid carcinoma. N Engl J Med 1998;338 (5) 297- 306
PubMed
Grebe  SKHay  ID Thyroid cancer nodal metastases: biological significance and therapeutic considerations. Surg Oncol Clin N Am 1996;5 (1) 43- 63
PubMed
Mazzaferri  ELJhiang  SM Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med1994975418428 [published correction appears in Am J Med. 1995;98(2):215].
PubMed
Samaan  NASchultz  PNHickey  RC  et al.  The results of various modalities of treatment on well differentiated thyroid carcinoma: a retrospective review of 1599 patients. J Clin Endocrinol Metab 1992;75 (3) 714- 720
PubMed
Simpson  WJPanzarella  TCarruthers  JSGospodarowicz  MKSutcliffe  SB Papillary and follicular thyroid cancer: impact of treatment in 1578 patients. Int J Radiat Oncol Biol Phys 1988;14 (6) 1063- 1075
PubMed
Tenenbaum  FCorone  CSchlumberger  MParmentier  C Thyroglobulin measurement and postablative iodine-131 total body scan after total thyroidectomy for differentiated thyroid carcinoma in patients with no evidence of disease [letter]. Eur J Cancer 1996;32A (7) 1262
PubMed
Woodrum  DTGauger  PG Role of 131I in the treatment of well differentiated thyroid cancer. J Surg Oncol 2005;89 (3) 114- 121
PubMed
Sawka  AMThephamongkhol  KBrouwers  MThabane  LBrowman  GGerstein  HC A systematic review and metaanalysis of the effectiveness of radioactive iodine remnant ablation for well-differentiated thyroid cancer. J Clin Endocrinol Metab 2004;89 (8) 3668- 3676
PubMed
Cushing  SLPalme  CEAudet  NEski  SWalfish  PGFreeman  JL Prognostic factors in well-differentiated thyroid carcinoma. Laryngoscope 2004;114 (12) 2110- 2115
PubMed
DeGroot  LJKaplan  ELMcCormick  MStraus  FH Natural history, treatment, and course of papillary thyroid carcinoma. J Clin Endocrinol Metab 1990;71 (2) 414- 424
PubMed
Cady  BRossi  R An expanded view of risk-group definition in differentiated thyroid carcinoma. Surgery 1988;104 (6) 947- 953
PubMed
Kjellman  PZedenius  JLundell  G  et al.  Predictors of outcome in patients with papillary thyroid carcinoma [published online ahead of print February 3, 2006]. Eur J Surg Oncol 2006;32 (3) 345- 352
PubMed
PubMed
Landis  SHMurray  TBolden  S  et al.  Cancer statistics. CA Cancer J Clin 1999;49 (1) 8- 31
PubMed
Caldwell  CBEhrlich  E Outpatient treatment of thyroid cancer using high doses of iodine 131. Can Assoc Radiol J 1999;50 (5) 331- 336
PubMed
Rutar  FJAugustine  SCColcher  D  et al.  Outpatient treatment with 131I-anti-B1 antibody: radiation exposure to family members. J Nucl Med 2001;42 (6) 907- 915
PubMed
Grigsby  PWSiegel  BABaker  SEichling  JO Radiation exposure from outpatient radioactive iodine (131I) therapy for thyroid carcinoma. JAMA 2000;283 (17) 2272- 2274
PubMed
Maxon  HR  IIISmith  HS Radioiodine-131 in the diagnosis and treatment of metastatic well differentiated thyroid cancer. Endocrinol Metab Clin North Am 1990;19 (3) 685- 718
PubMed
Rubino  Cde Vathaire  FDottorini  ME  et al.  Second primary malignancy in thyroid cancer patients. Br J Cancer 2003;89 (9) 1638- 1644
PubMed

Figures

Tables

Table Graphic Jump LocationTable 1. Breakdown of Hospital Costs for 199 Patients
Table Graphic Jump LocationTable 2. Breakdown of Radioactive Iodine (RAI) Treatment Costs for 199 Patients
Table Graphic Jump LocationTable 3. Total Hospital and Radioactive Iodine (RAI) Treatment Costs for 199 Patients
Table Graphic Jump LocationTable 4. Cost Per Dose of Sodium Iodide 131 (131I) Capsules (in 2005) and Number of Patients Receiving 131I With a MACIS (Metastases, Age, Completeness of Resection, Invasion, and Size) Score Less Than 6

References

Hay  IDThompson  GBGrant  CS  et al Papillary thyroid carcinoma managed at the Mayo Clinic during six decades (1940-1999). World J Surg2002268879885 [published online ahead of print May 21, 2002]. doi:10.1007/s200268-002-6612-1
PubMed
Hay  IDBergstralh  EJGoellner  JREbersold  JRGrant  CS Predicting outcome in papillary thyroid carcinoma. Surgery 1993;114 (6) 1050- 1057
PubMed
Hundahl  SAFleming  IDFremgen  AMMenck  HR A National Cancer Data Base report on 53,856 cases of thyroid carcinoma treated in the U.S., 1985-1995. Cancer 1998;83 (12) 2638- 2648
PubMed
DeGroot  LJKaplan  ELStraus  FHShukla  MS Does the method of management of papillary thyroid carcinoma make a difference in outcome? World J Surg 1994;18 (1) 123- 130
PubMed
Schlumberger  MJ Papillary and follicular thyroid carcinoma. N Engl J Med 1998;338 (5) 297- 306
PubMed
Grebe  SKHay  ID Thyroid cancer nodal metastases: biological significance and therapeutic considerations. Surg Oncol Clin N Am 1996;5 (1) 43- 63
PubMed
Mazzaferri  ELJhiang  SM Long-term impact of initial surgical and medical therapy on papillary and follicular thyroid cancer. Am J Med1994975418428 [published correction appears in Am J Med. 1995;98(2):215].
PubMed
Samaan  NASchultz  PNHickey  RC  et al.  The results of various modalities of treatment on well differentiated thyroid carcinoma: a retrospective review of 1599 patients. J Clin Endocrinol Metab 1992;75 (3) 714- 720
PubMed
Simpson  WJPanzarella  TCarruthers  JSGospodarowicz  MKSutcliffe  SB Papillary and follicular thyroid cancer: impact of treatment in 1578 patients. Int J Radiat Oncol Biol Phys 1988;14 (6) 1063- 1075
PubMed
Tenenbaum  FCorone  CSchlumberger  MParmentier  C Thyroglobulin measurement and postablative iodine-131 total body scan after total thyroidectomy for differentiated thyroid carcinoma in patients with no evidence of disease [letter]. Eur J Cancer 1996;32A (7) 1262
PubMed
Woodrum  DTGauger  PG Role of 131I in the treatment of well differentiated thyroid cancer. J Surg Oncol 2005;89 (3) 114- 121
PubMed
Sawka  AMThephamongkhol  KBrouwers  MThabane  LBrowman  GGerstein  HC A systematic review and metaanalysis of the effectiveness of radioactive iodine remnant ablation for well-differentiated thyroid cancer. J Clin Endocrinol Metab 2004;89 (8) 3668- 3676
PubMed
Cushing  SLPalme  CEAudet  NEski  SWalfish  PGFreeman  JL Prognostic factors in well-differentiated thyroid carcinoma. Laryngoscope 2004;114 (12) 2110- 2115
PubMed
DeGroot  LJKaplan  ELMcCormick  MStraus  FH Natural history, treatment, and course of papillary thyroid carcinoma. J Clin Endocrinol Metab 1990;71 (2) 414- 424
PubMed
Cady  BRossi  R An expanded view of risk-group definition in differentiated thyroid carcinoma. Surgery 1988;104 (6) 947- 953
PubMed
Kjellman  PZedenius  JLundell  G  et al.  Predictors of outcome in patients with papillary thyroid carcinoma [published online ahead of print February 3, 2006]. Eur J Surg Oncol 2006;32 (3) 345- 352
PubMed
PubMed
Landis  SHMurray  TBolden  S  et al.  Cancer statistics. CA Cancer J Clin 1999;49 (1) 8- 31
PubMed
Caldwell  CBEhrlich  E Outpatient treatment of thyroid cancer using high doses of iodine 131. Can Assoc Radiol J 1999;50 (5) 331- 336
PubMed
Rutar  FJAugustine  SCColcher  D  et al.  Outpatient treatment with 131I-anti-B1 antibody: radiation exposure to family members. J Nucl Med 2001;42 (6) 907- 915
PubMed
Grigsby  PWSiegel  BABaker  SEichling  JO Radiation exposure from outpatient radioactive iodine (131I) therapy for thyroid carcinoma. JAMA 2000;283 (17) 2272- 2274
PubMed
Maxon  HR  IIISmith  HS Radioiodine-131 in the diagnosis and treatment of metastatic well differentiated thyroid cancer. Endocrinol Metab Clin North Am 1990;19 (3) 685- 718
PubMed
Rubino  Cde Vathaire  FDottorini  ME  et al.  Second primary malignancy in thyroid cancer patients. Br J Cancer 2003;89 (9) 1638- 1644
PubMed

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