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ORIGINAL ARTICLE
Year : 2020  |  Volume : 8  |  Issue : 4  |  Page : 192-198

Parathyroidectomy in dialysis patients with secondary hyperparathyroidism, laboratory and clinical assessment


Department of General Surgery, Faculty of Medicine, Minia University, Minya, Egypt

Date of Submission16-Mar-2021
Date of Acceptance22-Jun-2021
Date of Web Publication30-Dec-2021

Correspondence Address:
Hosam M Hamza
Department of General Surgery, Faculty of Medicine, Minia University, Minya
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ssj.ssj_66_21

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  Abstract 


Purpose: Patients on dialysis are at high risk for developing secondary hyperparathyroidism. This study explores the effect of parathyroidectomy (PTx) in dialysis patients having secondary hyperparathyroidism with the assessment of the clinical and laboratory outcome.
Patients and Methods: A combined retrospective and prospective study of twenty patients with chronic kidney disease (CKD) and secondary hyperparathyroidism who underwent total PTx and autotransplantation in the period from January 2017 to January 2019 after approval from the institutional board of ethics.
Results: Of the twenty patients, 17 patients (85%) were symptomatic preoperatively. The most common presentation was generalized bone pain (35%). An early postoperative decrease in the mean serum levels of parathyroid hormone (PTH) and calcium (Ca) level – within 12 h after surgery – was observed. By comparison of the pre- and post-operative laboratory investigations, we found a statistically significant decrease in the value of serum PTH, but there was no statistically significant difference in serum Ca level.
Conclusion: Most of our patients improved clinically post-PTx. We recommend PTx for CKD patients with secondary hyperparathyroidism suffering from bone pain, generalized weakness, pathological fractures, and psychological disturbance.

Keywords: Chronic kidney disease, dialysis, hypocalcemia, parathyroidectomy, secondary hyperparathyroidism


How to cite this article:
Farahat MS, Zaghloul NM, Shemi HE, Hamza HM. Parathyroidectomy in dialysis patients with secondary hyperparathyroidism, laboratory and clinical assessment. Saudi Surg J 2020;8:192-8

How to cite this URL:
Farahat MS, Zaghloul NM, Shemi HE, Hamza HM. Parathyroidectomy in dialysis patients with secondary hyperparathyroidism, laboratory and clinical assessment. Saudi Surg J [serial online] 2020 [cited 2022 Aug 18];8:192-8. Available from: https://www.saudisurgj.org/text.asp?2020/8/4/192/334510




  Introduction Top


Secondary hyperparathyroidism is a major complication of chronic kidney disease (CKD), resulting from the failure of one or more components of the calcium (Ca) homeostatic mechanism.[1]

Ultimately, these patients develop persistently elevated serum level of parathyroid hormone (PTH), Ca, and phosphate, with clinical manifestations ranging from asymptomatic to debilitated by fractures as a result of decreased bone density.[2] Symptoms such as severe pruritus, concentration difficulties, and calciphylaxis are also commonly reported, though it remains unclear whether these are a direct consequence of secondary hyperparathyroidism.[3]

Parathyroidectomy (PTx) should be considered if medical therapy is ineffective in controlling PTH. Nowadays, with the introduction of new alternatives for medical treatment, mainly calcimimetics oral and IV, the indications could be reduced.[4]

This study explores the effect of PTx in dialysis patients having with secondary hyperparathyroidism with the assessment of the clinical and laboratory outcome.


  Patients and Methods Top


Patients

A total number of twenty CKD patients from Minia Nephrology and Urology University Hospital suffering from secondary hyperparathyroidism were scheduled for PTx and enrolled in this study. Surgery was done in the General Surgery Department, Minia University Hospital, Egypt, in the period from January 2017 to January 2019 after approval from the institutional board of ethics. None of our patients was scheduled for kidney transplant. Study is a combined retrospective and prospective study.

All patients signed an informed written consent, accepted, and were aware about the procedure in treatment they will receive according the ethical committee of Minia University hospitals.

Inclusion criteria

  1. Age: >18 years old and <75 years old
  2. Patients diagnosed as CKD on dialysis
  3. Serum PTH level more than 800 pg/mL on two or more occasions (normal range 10–65 pg/mL) with hyperphosphatemia (normal range: 2.5–4.5 mg/dL)
  4. Failure of medical treatment for hyperparathyroidism over a period of 6 month
  5. Patients with symptomatic secondary hyperparathyroidism: musculoskeletal pain, pathologic fractures, and severe pruritus.


Exclusion criteria

  1. Serum PTH level <800 pg/mL on two or more occasions
  2. Patients taking drugs such as bisphosphonates or anticonvulsants that might affect bone density
  3. Patients with conditions such as thyroid cancer or multiple endocrine neoplasia – Type 1 syndrome that might unduly influence the type of surgery or the outcome
  4. Patient unfit for anesthesia and operation as congestive heart failure (these will continue on medical treatment)
  5. Patient refusing surgery at all.


Methods

A complete history was obtained from all patients with a focus on presenting symptoms. We used the “numerical pain rating scale” for the assessment of bone pain, in which the patient is asked to indicate the intensity of current, best, and worst pain levels on a scale of 0 (no pain) to 10 (worst pain imaginable). Physical examination included vital signs assessment, neck examination for any palpable mass or lymph nodes, and assessment of the patients' general medical fitness. Routine laboratory studies were done in addition to serum level of PTH and serum Ca level. Radiological studies comprise high-resolution ultrasonography (HRUS) of the neck for all patients [Figure 1]. Since all parathyroid glands will be affected in secondary hyperparathyroidism, localizing studies are not necessary. We used the Short Form-36 general health survey – for the assessment of psychological disturbances and quality of life (QoL). It determines the degree to which the disease affects physical, psychological, and social functioning.
Figure 1: High resolution ultrasonography of the neck showing enlarged right inferior parathyroid gland in one of our patients

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During dialysis, none of our patients require high-Ca dialysis solutions or Ca supplementations. All patients were planned for total PTx with autotransplantation. Preoperative preparation includes vocal fold assessment by indirect laryngoscopy and heparin-free dialysis session 12 h before surgery.

We adopt slow intravenous (IV) administration of 10 ml of 10% Ca gluconate on 100 cc sodium chloride 0.9% solution over a period of about 20 min immediately after the removal of the first parathyroid – Ca gluconate is preferred over Ca chloride as it is less irritating and less likely to cause tissue necrosis on extravasation. Total PTx was done by removing all the four glands, with the most morphologically normal gland sliced into multiple pieces each of which has the thickness of about 1 mm and autotransplanted into the brachioradialis muscle in the right forearm or into the right sternocleidomastoid muscle and implantation site is marked with a metallic clip or a long limb proline stitch.

Meticulous dissection is adopted to avoid bleeding or tissue injury. Proper hemostasis is secured using bipolar diathermy and ligation of vessels that are too large to be controlled by diathermy alone. A closed system drain is placed through a separate stab incision then passes under the strap muscles to reach the thyroid fossa. During extubation, anesthetist was asked to visualize the movements of vocal cords to confirm that there was no recurrent laryngeal nerve injury and was documented both by anesthetist and surgeon in the case sheet. All specimens are sent for histopathological examination.

As rapid fall in serum Ca level after surgery can cause considerable morbidity and even mortality, 10% Ca gluconate infusion is started immediately after surgery using an infusion pump at a rate between 20 and 40 mL/h which is adjusted according to 6 hourly Ca level to keep it between 8 and 12 mg/dL. Patients were observed for the development of circumoral paresthesia/numbness, change in mental status, carpopedal spasm, or tetany. Serum Ca and PTH levels are assessed in all the patients in the same day of surgery. Drain is usually removed on day 1 postoperatively.

Oral Ca carbonate and Vitamin D supplementation are given for 2–6 months after surgery with the former being stopped when serum Ca is within normal range with no manifestations of hypocalcemia. Regimen adopted for oral Ca supplementation is shown in [Figure 2]. Hypocalcemia is defined as a total serum Ca concentration <8.5 mg/dL “<2.12 mmol/L”).
Figure 2: Regimen of oral calcium given to the patients after parathyroidectomy

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Statistical analysis

The collected data were coded, tabulated, and statistically analyzed using SPSS program (Statistical Package for the Social Sciences) software version 25.(IBM SPSS statistics for windows, Version 25.0, Armonk, NY: IBM Corp.). Descriptive statistics were done for categorical data by number and percentage. For quantitative data, analysis was done using independent samples t-test. Analysis was done for qualitative data using Fisher's exact test. Level of significance was taken at (P < 0.05).


  Results Top


Of the patients enrolled in our study (n = 20), 12 patients (60%) were males and eight (40%) were females. The mean age was 47.25 ± 9.2 years. Demographic data for our patients are presented in [Table 1]. For our patients, the preoperative mean levels of PTH and serum Ca are presented in [Table 1].
Table 1: Patients' characteristics, preoperative laboratory data and sonographic findings of the study group

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Eighty-five percent of our patients were symptomatic preoperatively. Common clinical presentations were generalized bone pain (7 patients), bilateral knee pain and generalized muscle weakness (3 patients for each), and pathological fractures and low back pain [Table 2].
Table 2: The clinical presentation of the study group

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HRUS of the neck was done for all patients. As presented in [Table 1], all parathyroid glands were affected in 70% of patients. If not all glands were involved, the right side was more affected than the left (30% and 20%, respectively) and inferior glands more than superior glands (25% and 5%, respectively). Hyperplasia detected by US was more common (70% of patients) than adenomas.

We observed an early postoperative decrease – within 12 h after surgery – in the mean PTH level to reach 93.10 ± 130.17 pg/mL. Mean serum Ca level also decreased to 8.35 ± 0.365 mg/dL [Table 3].
Table 3: Laboratory data in the early postoperative period and in the period of follow up after operation

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As shown in [Table 3], 2-week postoperative mean serum PTH level decreased to 58 ± 48.9 pg/mL, while the mean serum Ca level was 7.76 ± 0.32 mg/dL in the same period. After 3 months from the date of surgery, mean serum PTH level was 48.9 ± 30.2 pg/mL and mean serum Ca level reached 8.3 ± 0.60 mg/dL. One year after surgery, mean serum PTH level was 58.10 ± 55.33 pg/mL while mean serum Ca level was 8.8 ± 0.51 mg/dL.

By comparison of the pre- and post-operative laboratory investigations, we found a statistically significant decrease in the value of serum PTH giving a “P value of 0.02”. However, there was no statistically significant difference in serum Ca [Table 4].
Table 4: Pre/postoperative laboratory data of the study group

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In the range acceptable probability of postoperative complications, three patients develop hypocalcemia – which was the most common postoperative complication (15%) – ranging from asymptomatic to manifesting by paresthesia and/or numbness in the perioral region and fingertips. A clinical algorithm for treating hypocalcemia is shown in [Figure 3].
Figure 3: Clinical algorithm for treatment of hypocalcemia

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For severely symptomatic hypocalcemia or those with serum Ca below 3.2 mg/dL, IV Ca gluconate is administered and Ca is rechecked after the administration with a check on the serum magnesium level and correction if needed.

Two patients (10%) developed wound seroma not requiring aspiration (managed conservatively by repeated dressing and good coverage of antibiotics). Two patients (10%) had transient voice changes that can be attributed to transient recurrent laryngeal nerve compression but with dyspnea, this was troubleshooted by neurotonic medications and follow-up direct laryngoscopy that revealed no vocal fold paralysis. One patient (5%) developed a subcutaneous wound hematoma which needs to be evacuated under local anesthesia and ultrasonographic guidance [Table 5].
Table 5: Postoperative complications that occurred in the study group

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[Table 6] presents the clinical improvement noticed in our patients after surgery; relief of generalized bone pain was achieved in eight (40%) patients, psychological disturbances improved in three (15%) patients, improvement of the QoL was observed in seven (35%) patients, and no improvement achieved in two (10%) patients. The mean hospital stay is our study was 4 ± 0.67 days.
Table 6: The postoperative clinical improvement of the study group

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  Discussion Top


Secondary hyperparathyroidism is a complex pathology that develops as CKD. The retention of phosphorus and the reductions in Ca and Vitamin D levels stimulate the synthesis and secretion of PTH as well as the proliferation rate of parathyroid cells.[5]

PTx should be considered in patients with severe hyperparathyroidism in dialysis without response to medical treatment.[5] Our study is in an attempt to explore the clinical and laboratory effects of PTx in these patients.

The mean age of our patients was 47.25 years and the majority were males (60%); this is similar to the results recently published by Tan et al., 2020, whose study included 68 patients of secondary hyperparathyroidism with an average age of 42.9 years and 47 (69.1%) out of total patients were males,[6] and similar to the results of Zhang et al. who studied 182 patients having on overage age of 48.5 with 100 male patients.[7]

The most common clinical presentations in our patients were generalized bone pain (35%), followed by generalized muscle weakness (15%) and pathological fractures in (10%); these results resemble those of Lim et al., 2018 that showed indication for PTx to be symptomatic bone pain and fractures in 95.6% and 3.3% of patients, respectively,[8] and the results of Tan et al., 2020, who found 73.5% of their patients presenting with bone pain and 20.6% had muscle weakness.[6] However, in the study of Tsai et al., 2015, the most common presentations of the patients included in the study were bone pain (39%), pruritus (6%), fatigue (3.1%), and then pathological fracture (1.2%).[9]

Parathyroid ultrasound represents a widely available modality with great sensitivity for the detection of parathyroid pathology.[10] Normal parathyroids are generally too small to be seen on ultrasound; therefore, visualization of this gland should raise suspicion for a pathologic process. If an adenoma identifiable on ultrasound, it should appear as homogeneously hypoechoic extrathyroidal oval mass with a fat plane separating it from normal thyroid tissue. A feeding artery may also be visualized entering the superior or inferior pole of the adenoma.[11]

Neck ultrasound was done for all our patients, this was the same for all patients in the work of Ivanova et al., 2020,[12] whereas in the study of Hanna and Akoh, 2016 only 2.2% of patients underwent neck ultrasound,[13] and in the study of Tan et al., 2020 no data are available whether patients received preoperative imaging or not.[6]

Neck HRUS showed that all the four parathyroid glands were affected in 70%, 2 glands in 20%, and 1 gland in 10% of our patients. Ivanova et al. visualized 2–4 enlarged glands by ultrasound.[12]

Parathyroid hyperplasia was observed in 70% of our patients, and the remaining 30% showed adenomas; this can be explained by hyperphosphatemia which caused the stimulation of the nodular hyperplasia of the parathyroid gland and leading to highly elevated PTH.[14] Fülöp et al. reported a similar result with their patients having parathyroid hyperplasia being more commonly (94.6%) than those having adenomas (5.4%),[15] results of Lim et al., 2018 also found 92.2% of their patients to have hyperplasia,[8] and in the study of Kang et al., 47.87% of patients had hyperplasia, and 3.19% had adenoma.[16]

In the current study, the most common complications were hypocalcemia (15%), wound seroma (10%), voice changes (10%), and wound hematoma (5%). We recorded no cases of recurrent or persistent hyperparathyroidism, intraoperative bleeding, postoperative wound infection, or hypoparathyroidism.

However, the findings of some other studies do not agree with ours; Zhang et al., 2019, reported two cases of transitory hoarseness of voice, one case incision hemorrhage, three cases of hypoparathyroidism after surgery, and eight cases of combined infection.[7] Chen et al., 2017, reported recurrence to be the most common complication (1.9% of cases) then hypocalcaemia (0.73%) and hematoma (0.15%).[17] In the study of Schlosser et al., 2016, the most common complications were recurrent laryngeal nerve palsy (10.5%), postoperative bleeding (4%), and persistence of hyperparathyroidism (3%).[18]

The mean early postoperative serum PTH level in our patients was 93.1 ± 130.17 pg/dL, which showed a statistically significant difference from mean preoperative serum PTH, this is similar to the results of Zhang et al., 2019, Fülöp et al., 2018, and Casella et al., 2018; all showed a postoperative dramatic drop in the level of serum PTH indicating the success of surgery.[7],[15],[19]

Postoperative clinical improvement was remarkable in our study compared with the clinical symptoms before operation; generalized bone pain was relieved in eight (40%) patients, improved QoL in seven (35%) patients, improvement of the psychological disturbances in three (15%) patients, whereas no clinical improvement was observed in two (10%) patients. These results are similar to results of Zhang et al., who reported significant improvement in bone pain after operation,[7] and the results of Albuquerque et al. reported control of bone pain in 100% of their patients submitted to PTx.[20]

The mean hospital stay is our study was 4 ± 0.67 days. Similarly, Zmijewski et al., 2019, reported a mean hospital stay of 4.4 ± 3.5 days,[21] whereas Lim et al., 2018, reported a mean hospital stay of 14.4 ± 18.6 days.[8]

Limitations

We present a relatively small number of patients in our study; further clinical studies with a larger population are still needed.


  Conclusion Top


Despite the limitation of this study, most of our patients improved clinically post-PTx, regarding the bone pain, QoL, daily activities, and generalized weakness. We recommend PTx for CKD patients with secondary hyperparathyroidism suffering from bone pain, generalized weakness, pathological fractures, and psychological disturbance.

Further research should consider including a larger number of patients and a more extended follow-up to correlate between different results and observations to improve the long-term outcome in CKD patients with secondary hyperparathyroidism subjected to PTx.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
  References Top

1.
Cozzolino M, Shilov E, Li Z, Fukagawa M, Al-Ghamdi SM, Pisoni R, et al. Pattern of laboratory parameters and management of secondary hyperparathyroidism in countries of Europe, Asia, the Middle East, and North America. Adv Ther 2020;37:2748-62.  Back to cited text no. 1
    
2.
van der Plas WY, Noltes ME, van Ginhoven TM, Kruijff S. Secondary and tertiary hyperparathyroidism: A narrative review. Scand J Surg 2020;109:271-8.  Back to cited text no. 2
    
3.
Steinl GK, Kuo JH. Surgical management of secondary hyperparathyroidism. Kidney Int Rep 2021;6:254-64.  Back to cited text no. 3
    
4.
Rodríguez-Ortiz ME, Pendón-Ruiz de Mier MV, Rodríguez M. Parathyroidectomy in dialysis patients: Indications, methods, and consequences. Semin Dial 2019;32:444-51.  Back to cited text no. 4
    
5.
Rodríguez-Ortiz ME, Rodríguez M. Recent advances in understanding and managing secondary hyperparathyroidism in chronic kidney disease. F1000Res. 2020;9:F1000 Faculty Rev-1077. Published 2020 Sep 1.  Back to cited text no. 5
    
6.
Tan PG, Ab Hadi IS, Zahari Z, Yahya MM, Wan Zain WZ, Wong MP, et al. Predictors of early postoperative hypocalcemia after total parathyroidectomy in renal hyperparathyroidism. Ann Surg Treat Res 2020;98:1-6.  Back to cited text no. 6
    
7.
Zhang Y, Lu Y, Feng S, Zhan Z, Shen H. Evaluation of laboratory parameters and symptoms after parathyroidectomy in dialysis patients with secondary hyperparathyroidism. Ren Fail 2019;41:921-9.  Back to cited text no. 7
    
8.
Lim CT, Kalaiselvam T, Kitan N, Goh BL. Clinical course after parathyroidectomy in adults with end-stage renal disease on maintenance dialysis. Clin Kidney J 2018;11:265-9.  Back to cited text no. 8
    
9.
Tsai WC, Peng YS, Chiu YL, Wu HY, Pai MF, Hsu SP, et al. Risk factors for severe hypocalcemia after parathyroidectomy in prevalent dialysis patients with secondary hyperparathyroidism. Int Urol Nephrol 2015;47:1203-7.  Back to cited text no. 9
    
10.
Mourad V, Barragan C, Rivera H. Ultrasound evaluation of the parathyroid glands. Rev Colomb Radiol 2018;29:4861-6.  Back to cited text no. 10
    
11.
Wolfe S, Sharma S. Parathyroid Adenoma. In: StatPearls. Treasure Island (FL): StatPearls Publishing; 2020. Available from: https://www.ncbi.nlm.nih.gov/booksNBK507870/. [Last updated on 2020 Jun 24].  Back to cited text no. 11
    
12.
Ivanova M, Vetchinnikova O, Zakharova N. P0910 clinical laboratory and cytomorphological characteristics of hyperparathyroidism in patients with cronic kidney disease. Nephrol Dial Trans 2020;35 :gfaa142.P0910.  Back to cited text no. 12
    
13.
Hanna T, Akoh JA. Total parathyroidectomy in patients with chronic kidney disease: Avoiding repeat surgery. Saudi J Kidney Dis Transpl 2016;27:950-7.  Back to cited text no. 13
[PUBMED]  [Full text]  
14.
Goldenstein PT, Elias RM, Pires de Freitas do Carmo L, Coelho FO, Magalhães LP, Antunes GL, et al. Parathyroidectomy improves survival in patients with severe hyperparathyroidism: A comparative study. PLoS One 2013;8:e68870.  Back to cited text no. 14
    
15.
Fülöp T, Koch C, Farah Musa A, Clark CM, Gharaibeh KA, Lengvársky Z, et al. Targeted surgical parathyroidectomy in end-stage renal disease patients and long-term metabolic control: A single-center experience in the current era. Hemodial Int 2018;22:394-404.  Back to cited text no. 15
    
16.
Kang BH, Hwang SY, Kim JY, Hong YA, Jung MY, Lee EA, et al. Predicting postoperative total calcium requirements after parathyroidectomy in secondary hyperparathyroidism. Korean J Intern Med 2015;30:856-64.  Back to cited text no. 16
    
17.
Chen J, Jia X, Kong X, Wang Z, Cui M, Xu D. Total parathyroidectomy with autotransplantation versus subtotal parathyroidectomy for renal hyperparathyroidism: A systematic review and meta-analysis. Nephrology (Carlton) 2017;22:388-96.  Back to cited text no. 17
    
18.
Schlosser K, Bartsch DK, Diener MK, Seiler CM, Bruckner T, Nies C, et al. Total parathyroidectomy with routine thymectomy and autotransplantation versus total parathyroidectomy alone for secondary hyperparathyroidism: Results of a nonconfirmatory multicenter prospective randomized controlled pilot trial. Ann Surg 2016;264:745-53.  Back to cited text no. 18
    
19.
Casella C, Galani A, Totaro L, Ministrini S, Lai S, Dimko M, et al. Total Parathyroidectomy with subcutaneous parathyroid forearm autotransplantation in the treatment of secondary hyperparathyroidism: A single-center experience. Int J Endocrinol 2018;2018:6065720. Published 2018 Jul 9.  Back to cited text no. 19
    
20.
Albuquerque RF, Carbonara CE, Martin RC, Dos Reis LM, do Nascimento CP Júnior, Arap SS, et al. Parathyroidectomy in patients with chronic kidney disease: Impacts of different techniques on the biochemical and clinical evolution of secondary hyperparathyroidism. Surgery 2018;163:381-7.  Back to cited text no. 20
    
21.
Zmijewski PV, Staloff JA, Wozniak MJ, Mazzaglia PJ. Subtotal parathyroidectomy vs total parathyroidectomy with autotransplantation for secondary hyperparathyroidism in dialysis patients: Short- and long-term outcomes. J Am Coll Surg 2019;228:831-8.  Back to cited text no. 21
    


    Figures

  [Figure 1], [Figure 2], [Figure 3]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]



 

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