Saudi Journal of Kidney Diseases and Transplantation

ORIGINAL ARTICLE
Year
: 2016  |  Volume : 27  |  Issue : 5  |  Page : 950--957

Total parathyroidectomy in patients with chronic kidney disease: Avoiding repeat surgery


Thomas Hanna, Jacob A Akoh 
 Department of Surgery, Plymouth Hospitals NHS Trust, Derriford Hospital, Plymouth PL6 8DH, United Kingdom

Correspondence Address:
Jacob A Akoh
Department of Surgery, Plymouth Hospitals NHS Trust, Derriford Hospital, Plymouth PL6 8DH
United Kingdom

Abstract

Renal hyperparathyroidism (RHPT) is a common complication of renal failure and it is associated with significant morbidity and mortality. The aim of this study was to determine the patient characteristics which might predict persistent or recurrent hyperparathyroidism after surgery and to assess the long-term effect of unsuccessful surgery. This is a retrospective study of all chronic kidney disease patients who required a total parathyroidectomy (TP) because of failed medical management from January 1999 to December 2014. Patient characteristics, preoperative imaging, operative findings, and patient outcome were all studied. Differences between groups (dialysis-dependent and nondialysis-dependent; preoperative imaging and no imaging) were tested by the Chi-square statistic test and P <0.05 was regarded statistically significant. Eighty-eight patients underwent TP during this period and were followed up for a median of 35.5 months (range 1-119 months). Seventy (80%) had removal of all parathyroid glands with associated fall in parathyroid hormone level. There were no statistically significant differences in surgical success rates in neither the dialysis-dependent versus nondialysis-dependent groups nor the preoperative imaging versus no imaging groups. Two patients underwent repeat parathyroid surgery for persistent hyperparathyroidism and 16 were followed up without surgery. Preoperative imaging did not direct surgical management nor reduce surgical failure rate in this series. The long-term effects of pharmaceutical developments in this area are unknown but are likely to change indications for initial parathyroidectomy and reoperation. An agreed protocol is essential for the management of patients with RHPT.



How to cite this article:
Hanna T, Akoh JA. Total parathyroidectomy in patients with chronic kidney disease: Avoiding repeat surgery.Saudi J Kidney Dis Transpl 2016;27:950-957


How to cite this URL:
Hanna T, Akoh JA. Total parathyroidectomy in patients with chronic kidney disease: Avoiding repeat surgery. Saudi J Kidney Dis Transpl [serial online] 2016 [cited 2019 Aug 25 ];27:950-957
Available from: http://www.sjkdt.org/text.asp?2016/27/5/950/190858


Full Text

 Introduction



Chronic kidney disease (CKD) leads to a decrease in the renal conversion of 25-hydroxycholecalciferol to 1,25-dihydroxycholecalcierol resulting in reduced absorption of calcium from the intestinal tract and decreased phosphate excretion. Both mechanisms lead to hypocalcemia which stimulates parathyroid hormone (PTH) secretion and parathyroid gland hyperplasia. Renal hyperparathyroidism (RHPT) is a common complication of CKD [1] can be associated with significant morbidity and mortality. [2],[3]

Most cases can be treated medically with phosphorous chelating agents, Vitamin D, and calcium supplementation. The introduction of the calcimimetic agent, cinacalcet hydrochloride, has been shown in randomized controlled trials to lower PTH levels and improve calcium-phosphorus homeostasis. [4],[5] There is some evidence that the use of cinacalcet can reduce the need for parathyroidectomy. [6],[7] However, direct comparisons of parathyroidectomy rates before and after the introduction of cinacalcet are not available. Despite continuous and intensive interventions to control RHPT, eventually, approximately 5% of these patients will require a parathyroidectomy. [8] Successful parathyroidectomy has been shown to achieve a dramatic drop in PTH levels, improve patient's symptoms, and reduce mortality by prevention of cardiovascular complications. [9] However, it is widely recognized that 20-30% of patients who undergo a total parathyroidectomy (TP) for RHPT develop the persistent or recurrent disease. [10],[11] Due to the extensive adhesions formed and scarring of tissue planes, reoperation for missing glands is associated with increased risks and complications [11] and is also more likely to be unsuccessful. [12] Persistent disease occurs when not all glands can be localized, either due to inadequate exploration, ectopic or supernumerary glands, or incomplete removal of a gland. The use of preoperative imaging to increase the likelihood of locating all glands at surgery has been advocated by some authors. [13],[14] However, preoperative imaging remains controversial, and its use has not been proven to reduce surgical failure rates. The British Association of Endocrine and Thyroid Surgeons (BAETS) does not recommend routine imaging of the parathyroid glands before a first operation. [15] The aims of this study were to determine patient characteristics which might predict persistent or recurrent HPT after surgery, assess the ability of preoperative imaging in locating the parathyroid glands during initial surgery, and to assess the long-term effect of failed surgery.

 Methods



A retrospective study of all patients who required a TP for RHPT because of failed medical management from January 1, 1999, to December 31, 2014, was carried out. For each patient, the etiology of CKD, duration of dialysis, and time from or to renal transplantation were recorded. Preoperative imaging was not routinely used for RHPT in our institution; however, as there was no standardized protocol for the management of these patients at the time of the study, imaging was requested by some treating nephrologists. The outcome of surgery was compared between those that did and those that did not have preoperative imaging. Preoperative vocal cord examination was routinely performed in all patients. Frozen section histology was used in all cases to confirm parathyroid tissue intraoperatively, and this was followed by formal conventional histology by a consultant histopathologist. The glands were labeled right upper, left upper, right lower, and left lower. When <4 glands were found at the original operation, extensive search was made in the relevant paratracheal, paraesophageal, and carotid sheath before ending the operation. Thyroid lobectomy and/ or thymectomy were not performed during the initial operation in this series. At repeat surgery, a transcervical thymectomy was performed if the relevant missing glands were not identified or confirmed on frozen section.

All patients were given a loading dose of alfacalcidol and calcium (Ca) supplementation preoperatively and postoperatively according to the serum Ca level. Patients were discharged when serum Ca level had stabilized. Patients were followed up by their referring nephrologists. Cinacalcet was introduced during the latter period in our study. Four patients (5.3%) were treated with cinacalcet preoperatively for a median duration of six months (range 1-14 months). Before this, alfacalcidol was routinely used for all patients. Records were incomplete in terms of the preoperative loading dose used for patients.

PTH and serum Ca were measured preoperatively and on day 1 postoperatively. A fasting sample of blood, separated in the laboratory within 2-4 h of collection, was used in measuring the PTH level by the Roche Diagnostics PTH assay (West Sussex, UK) an electrochemiluminescence assay which uses a sandwich test principle (biotinylated monoclonal antibody reacts with the N-terminal fragment (1-37) and a monoclonal antibody labeled with a ruthenium complex reacts with the C-terminal fragment). All patients had elevated PTH level preoperatively. Five patients with secondary hyperparathyroidism became hypercalcemic and were considered to have developed tertiary hyperparathyroidism before undergoing TP. Three of these were postrenal transplantation, one after transplant nephrectomy, and one after failed medical therapy. Successful surgery was defined as a PTH level returning to within normal limits on the 1 st postoperative day. Brief case summaries of two patients undergoing re-exploration for missing parathyroid glands are given. Differences between groups (dialysis dependent and nondialysisdependent; and with or without preoperative imaging) were tested by the Chi-square statistic test and P <0.05 was regarded statistically significant.

 Results



During the period, 96 patients were operated on for RHPT. Seven patients who were misdiagnosed as primary HPT and had removal of parathyroid "adenomas" were excluded from analysis. Another patient who had hemithyroidectomy and parathyroidectomy with central node dissection for parathyroid carcinoma was also excluded leaving 88 for analysis. There were 49 (56%) males and 39 (44%) females and an overall median age 56 (range 20-82). Patients were followed up with biochemical measurements for a median of 35.5 months (range 1-119 months). Eighteen (20.5%) of the patients demonstrated persistent HPT two due to supernumerary glands as four glands were confirmed on frozen section during surgery; and the remaining due to one missing gland in 13 and two missing glands in three.

Of the 88 patients, 15 (17%) had preoperative imaging - two had an ultrasound scan (USS), 10 had technetium methoxyisobutylisonitrile (Tc MIBI), and three had both USS and Tc MIBI. The remaining 73 patients (83%) did not receive any preoperative imaging. The failure rate in the group receiving preoperative imaging was 4/15 (26.7%) compared to 14/73 (19.2%) for the group that did not receive preoperative imaging. The difference in failure rates did not reach statistical significance (χ2 = 0.4289; P = 0.5125) Twenty-eight (32%) of 88 patients were not dialysis dependent at the time of surgery. Of these, seven patients had functioning renal transplants and the remaining 21 were in the pre-dialysis phase (two were CKD Stage 3, 14 CKD Stage 4, and five CKD Stage 5). Sixty (68%) patients were receiving chronic dialysis at the time of surgery for an average of 29.3 months (range 1-220 months). The failure rate at initial surgery in this group was 25% (15/60) compared to 10.7% (3/28) for those not on dialysis. The difference in failure rate between the groups did not reach statistical significance (χ2 = 2.3946; P = 0.1218). Of the 18 patients with unsuccessful surgery, 16 did not undergo any further surgery. The reasons for this included four patients who died within 10 months of the original operation. Five patients had modestly elevated PTH levels and normally corrected Ca + levels and one patient's PTH level fell spontaneously while considering redo surgery and two patients had subnormal (low) PTH levels despite having only three glands excised at surgery. The remaining four patients did not have further surgery but had stable serum Ca levels and did not develop any symptoms of HPT and died between 27 and 35 months after surgery of unrelated conditions.

Two patients had four glands removed at the first operation but this failed to correct the HPT.

Complications were seen in 11 of the 88 patients in this series. These include 10 (11.4%) with symptomatic hypocalcemia requiring intravenous Ca gluconate. Apart from the 1 st postoperative day, PTH levels were not routinely performed, so the hypoparathyroidism rates are not known. One patient with a normal preoperative vocal cord check sustained a recurrent laryngeal nerve injury and had a hoarse voice postoperatively. This resolved spontaneously within two years. There were no complications of wound infection or bleeding in this series.

The mean ± standard error of mean (SEM) hospital length of stay was 5.3 ± 0.37 days (range 2-14). The mean ± SEM length of operation was 109 ± 5.63 min (range 39-185). Thirty patients have subsequently died from causes unrelated to secondary HPT [Figure 1]. The mean ± SEM interval between surgery and death was 43 ± 3.83 months (range 0-93) with the mean age at death 58 ± 3.22 years (range 29-84 years).{Figure 1}

 Discussion



Classic indications for surgery for RHPT include failure of medical treatment to normalize hypercalcemia and hyperphosphatemia in the presence of elevated PTH level greater than eight times the normal range with evidence of biomechanical abnormalities and calciphylaxis. [15],[16] Although Elder [17] recommends a trial of cinacalcet in all patients not meeting K/DOQI targets, [18] the cost implications (ͳ1646-ͳ9110 per patient per year) [19] are prohibitive. The National Institute for Health and Clinical Excellence guidelines recommend the use of cinacalcet only in patients with uncontrolled PTH (>900 pg/mL) refractory to standard therapy and in whom surgical parathyroidectomy is contraindicated. [19] In this study, four patients were treated with cinacalcet before surgery.

The optimal surgical management of patients in CKD with RHPT is controversial. TP with autotransplantation (AT) of parathyroid tissue and sub-TP are considered by some as standard surgical procedures in the treatment of RHPT with recurrences between 10% and 12%. [20] A single-surgeon retrospective series of 888 patients undergoing total parathyroidectomy with forearm AT for RHPT, intramuscular parathyroid AT was associated with a higher need for autograftectomy and repeated autograftectomy than subcutaneous AT. [21] Jia et al [22] performed a meta-analysis of seven cohort studies (931 patients comparing total parathyroidectomy with total parathyroidectomy plus AT for RHPT with respect to long-term outcomes. They reported that total parathyroidectomy is associated with a lower incidence of recurrence or persistent hyperparathyroidism, severe hypocalcemia, or adynamic bone disease. The operation of choice for RHPT in our institution is total parathyroidectomy without AT and thymectomy - one of the operative strategies recommended by the BAETS. [15] This avoids many of the problems of AT hyperplasia leading to recurrence of HPT and is not associated with significant hypocalcemia. Furthermore, surgery to remove parathyroid autotransplants is often associated with significant bleeding. In our series of 88 patients, 11.4% required intravenous Ca gluconate to correct hypocalcaemia postoperatively, the rest being adequately controlled with oral supplementation. Overall, our recurrence/persistence rate was 20.5% (18/88). The rate of recurrence/persistence after total parathyroidectomy reported in the literature varies from 2.5% to 35%. [23],[24],[25],[26],[27],[28],[29],[30],[31] Whether the addition of thymectomy improves the yield rate of surgery is debatable. Coulston et al [30] applied the pragmatic approach of thymectomy on the side of the missing gland, but none of the resected thymus glands contained the missing gland.

The role of preoperative imaging is well defined in primary hyperparathyroidism with both Tc MIBI and USS acknowledged to accurately locate the hyperfunctioning adenoma. [32],[33] However, the role of USS and Tc MIBI in imaging RHPT preoperatively is controversial. The sensitivity of Tc MIBI in identifying all glands preoperatively varies from 35% to 66%. [34],[35],[36],[37],[38] Despite this, many authors cite the high recurrence rate and risks of repeat surgery as justification of Tc MIBI in this setting. [39],[40],[41] The BAETS guidelines however do not recommend routine imaging of the parathyroid glands before the first operation. [15] In this study, although not reaching statistical significance, the group receiving preoperative imaging had a higher surgical failure rate than the group that did not. This may be due to selection bias, and no conclusions can be made on this observation. Surgeons would tend to perform preoperative imaging in patients where difficultly localizing the parathyroid glands was anticipated. A prospective randomized controlled trial comparing preoperative imaging with no imaging would be required to overcome this bias. The use of intraoperative gamma probe examination has been reported to increase the resection rate of parathyroid glands. [38] For reoperations, the BAETS guidelines recommend "detailed attempts" at imaging to establish the source of excessive PTH. [15] Tc MIBI has been shown to be the most accurate noninvasive localizing technique. The sensitivity of this method of investigation has been shown in case series to vary from 71% to 93%. [11],[12],[42],[43] As suggested by Hindie et al, [44] the observation that Tc MIBI is significantly more accurate when used for repeat surgery may be due to the fact that residual glands responsible for recurrence of RHPT are regarded as uniformly autonomous and highly hyperactive.

The fate of patients who do not have repeat surgery after their initial failed surgery is not widely reported in the literature. In a similar case series, [45] reoperations were only performed on a proportion of patients who remained hyperparathyroid after their initial surgery. In our experience, this was more likely to be those who presented with distressing symptoms of calciphylaxis and pruritus. Jofre et al [45] reported persistence or recurrence of RHPT in 33 of 148 patients (22.3%) yet performed a reoperation in just over half of these (17/33). In this study, reoperation was carried out in 11% (2/18) who demonstrated persistence or recurrence. Several of those that were not operated on had multiple comorbidities and a short life expectancy; however, a large proportion was followed up for a long period of time without significant problems. Although this subgroup of the series is relatively few in number, their uneventful longterm follow-up demands a fresh look at the indications of redo parathyroid surgery. Reoperation should be approached with caution as it is associated with a higher risk of complications. Partially successful surgery (one or two missing glands) may make medical treatment more amenable to control the effects of RHPT. By employing a critical look at the indications for repeat surgery and using rigorous criteria for determining cases likely to benefit from surgery, the reoperation rate is likely to be reduced further. This is especially so with improving medical management and new more powerful pharmaceuticals such as cinacalcet becoming more widely available.

In this series, the failure rate in patients, receiving chronic dialysis at the time of surgery of 60%, was higher than those who did not (10/7%) (χ2 = 2.3946; P = 0.1218). Although this did not reach statistical significance, it is an interesting trend. Saunders et al [29] observed the same finding in 54 patients undergoing TP for secondary hyperparathyroidism with a rate of undetectable PTH postoperatively of 6/12 (50%) in those with a functional transplant compared to 7/42 (17%) in those on dialysis (P = 0.02). The explanation given by the authors is that, "the stimulus to secrete PTH and develop parathyroid hyperplasia is considerably reduced after successful transplantation when renal function is improved" may be used to explain our data as well.

The limitations of this study are its retrospective nature and relatively small number of patients. Despite this, it serves to highlight several important points in the management of these complex patients. The duration of renal failure or dependency on dialysis did not appear to be a predicting factor of surgical success. The use of preoperative imaging did not direct surgical management nor reduce surgical failure rate in this series. Several patients with a long follow-up after a failed surgery did not appear to come to any harm without redo surgery for failed total parathyroidectomy. The indications for repeat surgery need to be critically looked at, taking special consideration for the role of changing medical management.

Finally, some patients in our institution did not appear to be managed according to best practice guidelines. In light of these findings, an agreed care pathway has now been introduced in our institution and should be considered essential for the appropriate care of all CKD patients undergoing total parathyroidectomy.

 Acknowledgments



We thank to Drs. Jo Edwards and Helen Grimsmo, for their help with data collection.

Conflict of interests: None declared.

References

1Slatopolsky E, Brown A, Dusso A. Pathogenesis of secondary hyperparathyroidism. Kidney Int Suppl 1999;73:S14-9.
2Kestenbaum B, Sampson JN, Rudser KD, et al. Serum phosphate levels and mortality risk among people with chronic kidney disease. J Am Soc Nephrol 2005;16:520-8.
3Stevens LA, Djurdjev O, Cardew S, Cameron EC, Levin A. Calcium, phosphate, and parathyroid hormone levels in combination and as a function of dialysis duration predict mortality: Evidence for the complexity of the association between mineral metabolism and outcomes. J Am Soc Nephrol 2004;15:770-9.
4Block GA, Martin KJ, de Francisco AL, et al. Cinacalcet for secondary hyperparathyroidism in patients receiving hemodialysis. N Engl J Med 2004;350:1516-25.
5Lindberg JS, Culleton B, Wong G, et al. Cinacalcet HCl, an oral calcimimetic agent for the treatment of secondary hyperparathyroidism in hemodialysis and peritoneal dialysis: A randomized, double-blind, multicenter study. J Am Soc Nephrol 2005;16:800-7.
6Cunningham J, Danese M, Olson K, Klassen P, Chertow GM. Effects of the calcimimetic cinacalcet HCl on cardiovascular disease, fracture, and health-related quality of life in secondary hyperparathyroidism. Kidney Int 2005;68:1793-800.
7Lafrance JP, Cardinal H, Leblanc M, et al. Effect of cinacalcet availability and formulary listing on parathyroidectomy rate trends. BMC Nephrol 2013;14:100.
8Decker PA, Cohen EP, Doffek KM, et al. Subtotal parathyroidectomy in renal failure: Still needed after all these years. World J Surg 2001;25:708-12.
9Tominaga Y, Matsuoka S, Uno N. Surgical and medical treatment of secondary hyperparathyroidism in patients on continuous dialysis. World J Surg 2009;33:2335-42.
10Gasparri G, Camandona M, Abbona GC, et al. Secondary and tertiary hyperparathyroidism: Causes of recurrent disease after 446 parathyroidectomies. Ann Surg 2001;233:65-9.
11Seehofer D, Steinmüller T, Rayes N, et al. Parathyroid hormone venous sampling before reoperative surgery in renal hyperparathyroidism: Comparison with noninvasive localization procedures and review of the literature. Arch Surg 2004;139:1331-8.
12Dotzenrath C, Cupisti K, Goretzki E, et al. Operative treatment of renal autonomous hyperparathyroidism: Cause of persistent or recurrent disease in 304 patients. Langenbecks Arch Surg 2003;387:348-54.
13Pahlavan PS, Severin MC. Parathyroid carcinoma: A rare case with mandibular brown tumor. Wien Klin Wochenschr 2006;118:1759.
14Masson EA, MacFarlane IA, Bodmer CW, Vaughan ED. Parathyroid carcinoma presenting with a brown tumour of the mandible in a young man. Br J Oral Maxillofac Surg 1993; 31:117-9.
15The Association of Endocrine Surgeons. Guidelines for the Surgical Management of Endocrine and Training Requirements for Endocrine Surgery; 2003. Available from: http://www.baets.org.uk/Pages/BAETS%20Gu idelines.pdf. Last accessed 25 June 2015.
16Schömig M, Ritz E. Management of disturbed calcium metabolism in uraemic patients: 2. Indications for parathyroidectomy. Nephrol Dial Transplant 2000;15 Suppl 5:25-9.
17Elder GJ. Parathyroidectomy in the calcimimetic era. Nephrology (Carlton) 2005;10:5115.
18National Kidney Foundation. K/DOQI clinical practice guidelines for bone metabolism and disease in chronic kidney disease. Am J Kidney Dis 2003;42 4 Suppl 3:S1-201.
19National Institute for Health and Clinical Excellence. Cinacalcet for the treatment of secondary hyperparathyroidism in patients with end-stage renal disease on maintenance dialysis therapy; 2007. Available from: http://www.guidance.nice.org.uk/TA117. Last accessed 25 June 2015.
20Schlosser K, Veit JA, Witte S, et al. Comparison of total parathyroidectomy without autotransplantation and without thymectomy versus total parathyroidectomy with autotransplantation and with thymectomy for secondary hyperparathyroidism: TOPAR PILOT-Trial. Trials 2007;8:22.
21Hsu YC, Hung CJ. Intramuscular and subcutaneous forearm parathyroid autograft hyperplasia in renal dialysis patients: A retrospective cohort study. Surgery 2015;158:1331-8.
22Jia X, Wang R, Zhang C, Cui M, Xu D. Longterm outcomes of total parathyroidectomy with or without autoimplantation for hyperparathyroidism in chronic kidney disease: A metaanalysis. Ther Apher Dial 2015;19:477-85.
23Gagné ER, Ureña P, Leite-Silva S, et al. Shortand long-term efficacy of total parathyroidectomy with immediate autografting compared with subtotal parathyroidectomy in hemodialysis patients. J Am Soc Nephrol 1992;3:1008-17.
24Debruyne F, Geuens G, Vander Poorten V, Delaere P. Re-operation for secondary hyperparathyroidism. J Laryngol Otol 2008;122: 942-7.
25Tominaga Y, Tanaka Y, Sato K, et al. Recurrent renal hyperparathyroidism and DNA analysis of autografted parathyroid tissue. World J Surg 1992;16:595-602.
26Henry JF, Denizot A, Audiffret J, France G. Results of reoperations for persistent or recurrent secondary hyperparathyroidism in hemodialysis patients. World J Surg 1990;14:303-6.
27Tanaka Y, Seo H, Tominaga Y, Funahashi H, Matsui N, Takagi H. Factors related to the recurrent hyperfunction of autografts after total parathyroidectomy in patients with severe secondary hyperparathyroidism. Surg Today 1993;23:220-7.
28Walgenbach S, Hommel G, Junginger T. Prospective evaluation of parathyroid graft function after total parathyroidectomy and heterotopic autotransplantation in renal hyperparathyroidism by bilateral determination of intact parathormone in cubital venous blood. World J Surg 1998;22:93-7.
29Saunders RN, Karoo R, Metcalfe MS, Nicholson ML. Four gland parathyroidectomy without reimplantation in patients with chronic renal failure. Postgrad Med J 2005;81:255-8.
30Coulston JE, Egan R, Willis E, Morgan JD. Total parathyroidectomy without autotransplantation for renal hyperparathyroidism. Br J Surg 2010;97:1674-9.
31Stracke S, Jehle PM, Sturm D, Schoenberg MH, Widmaier U, Beger HG, et al. Clinical course after total parathyroidectomy without autotransplantation in patients with end-stage renal failure. Am J Kidney Dis 1999;33:304-11.
32Proye CA, Carnaille B, Bizard JP, Quievreux JL, Lecomte-Houcke M. Multiglandular disease in seemingly sporadic primary hyperparathyroidism revisited: Where are we in the early 1990s? A plea against unilateral parathyroid exploration. Surgery 1992;112:1118-22.
33Gofrit ON, Lebensart PD, Pikarsky A, Lackstein D, Gross DJ, Shiloni E. High-resolution ultrasonography: Highly sensitive, specific technique for preoperative localization of parathyroid adenoma in the absence of multinodular thyroid disease. World J Surg 1997; 21:287-90.
34de la Rosa A, Jimeno J, Membrilla E, Sancho JJ, Pereira JA, Sitges-Serra A. Usefulness of preoperative Tc-mibi parathyroid scintigraphy in secondary hyperparathyroidism. Langenbecks Arch Surg 2008;393:21-4.
35Piga M, Bolasco P, Satta L, et al. Double phase parathyroid technetium-99m-MIBI scintigraphy to identify functional autonomy in secondary hyperparathyroidism. J Nucl Med 1996; 37:565-9.
36Périé S, Fessi H, Tassart M, et al. Usefulness of combination of high-resolution ultrasonography and dual-phase dual-isotope iodine 123/technetium Tc 99m sestamibi scintigraphy for the preoperative localization of hyperplastic parathyroid glands in renal hyperparathyroidism. Am J Kidney Dis 2005;45: 344-52.
37Custódio MR, Montenegro F, Costa AF, et al. MIBI scintigraphy, indicators of cell proliferation and histology of parathyroid glands in uraemic patients. Nephrol Dial Transplant 2005;20:1898-903.
38Yuan F, Yu W, Waqas A, et al. Radio-guided parathyroidectomy for secondary hyperparathyroidism. Chin Med J (Engl) 2014;127:24138.
39Fuster D, Ybarra J, Ortin J, et al. Role of preoperative imaging using 99mTc-MIBI and neck ultrasound in patients with secondary hyperparathyroidism who are candidates for subtotal parathyroidectomy. Eur J Nucl Med Mol Imaging 2006;33:467-73.
40Giordano A, Rubello D, Casara D. New trends in parathyroid scintigraphy. Eur J Nucl Med Mol Imaging 2001;28:1409-20.
41Hindié E, Urenã P, Jeanguillaume C, et al. Preoperative imaging of parathyroid glands with technetium-99m-labelled sestamibi and iodine-123 subtraction scanning in secondary hyperparathyroidism. Lancet 1999;353:2200-4.
42Chou FF, Lee CH, Chen HY, Chen JB, Hsu KT, Sheen-Chen SM. Persistent and recurrent hyperparathyroidism after total parathyroidectomy with autotransplantation. Ann Surg 2002;235:99-104.
43Neumann DR, Esselstyn CB Jr., Madera AM. Sestamibi/iodine subtraction single photon emission computed tomography in reoperative secondary hyperparathyroidism. Surgery 2000; 128:22-8.
44Hindié E, Zanotti-Fregonara P, Just PA, et al. Parathyroid scintigraphy findings in chronic kidney disease patients with recurrent hyperparathyroidism. Eur J Nucl Med Mol Imaging 2010;37:623-34.
45Jofré R, López Gómez JM, Menárguez J, et al. Parathyroidectomy: Whom and when? Kidney Int Suppl 2003;85:S97-100.