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Saudi Journal of Kidney Diseases and Transplantation
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ORIGINAL ARTICLE  
Year : 2016  |  Volume : 27  |  Issue : 2  |  Page : 263-269
The relationship between total mass and blood supply of parathyroid glands and their secretion of parathyroid hormone in hemodialysis patients with secondary hyperparathyroidism


1 Nephrology Research Center, Tehran University of Medical Sciences, Tehran, Iran
2 Department of Radiology and Imaging, Imam Khomeini Hospital, Tehran University of Medical Sciences, Tehran, Iran
3 Department of Nephrology, Amir Alam Hospital, Tehran University of Medical Sciences, Tehran, Iran

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Date of Web Publication11-Mar-2016
 

   Abstract 

Characteristics of parathyroid glands usually determined by ultrasonography such as its total weight or volume might be a good indicator for the induction or suppression of parathyroid hormone (PTH) secretion from these glands. In the present study, we investigated the relationship between the volume and blood supply grade of the parathyroid glands, and its PTH secretion. Study subjects included 52 consecutive patients with the secondary hyperparathyroidism undergoing maintenance hemodialysis therapy referred to dialysis wards of the Imam Khomeini and Amiralam University Hospitals in Tehran. Serum intact PTH (i-PTH) was measured by an ELISA assay. The parathyroid glands characteristics were identified by ultrasonography that was performed simultaneously with blood collection. Parathyroid blood flows were evaluated by power-Doppler color imaging. There was no significant correlation between the total mass of the glands and serum concentration of i-PTH. No significant correlations were also observed between both total central and peripheral parathyroid glands blood flow and serum i-PTH level. Dialysis duration and serum alkaline phosphatase were significantly correlated in a positive manner with i-PTH level. Furthermore, serum level of i-PTH was not correlated with the total signals of glands blood flow in a multivariable linear regression analysis. Serum secreted i-PTH level might not be predictable by a total mass of parathyroid glands as well as their blood supply.

How to cite this article:
Ahmadi F, Aghajanzadeh P, Yazdi HR, Maziar S, Gatmiri SM. The relationship between total mass and blood supply of parathyroid glands and their secretion of parathyroid hormone in hemodialysis patients with secondary hyperparathyroidism. Saudi J Kidney Dis Transpl 2016;27:263-9

How to cite this URL:
Ahmadi F, Aghajanzadeh P, Yazdi HR, Maziar S, Gatmiri SM. The relationship between total mass and blood supply of parathyroid glands and their secretion of parathyroid hormone in hemodialysis patients with secondary hyperparathyroidism. Saudi J Kidney Dis Transpl [serial online] 2016 [cited 2019 Nov 22];27:263-9. Available from: http://www.sjkdt.org/text.asp?2016/27/2/263/178257

   Introduction Top


Secondary hyperparathyroidism (SHPT) is one of the most important abnormalities of metabolism in patients with chronic renal dysfunction requiring chronic dialysis. [1] In these patients, parathyroid hormone (PTH) is often elevated in response to the reduced serum calcium levels, deficiency of 1,25-dihydroxyvitamin D3, as well as the diminished expression of Vitamin D receptors and calcium sensing receptors in the parathyroid cell. [2],[3] Thus, measurement of PTH level is the most important indicator for assessing changes in parathyroid glands activity. In patients with chronic kidney disease, persistent hyperparathyroidism often leads to parathyroid hyperplasia, especially in dialysis patients that the severity of hyperplasia is positively correlated with a long dialysis period. [4],[5] Therefore, besides measuring PTH level, characteristics of parathyroid glands usually determined by ultrasonography such as their total weight or volume might be a good indicator for the induction or suppression of PTH secretion from these glands. [6] In fact, these characteristics are suggested as a relevant measure to easily detect parathyroid activity. Previously, it was hypothesized that inducing PTH secretion might be related to the total parathyroid gland size and weight. [1] It can be more important in patients with renal dysfunction because hyperparathyroidism secondary to hemodialysis in patients with severe chronic kidney disease can usually be manifested by parathyroid glands nodular hyperplasia.

Moreover, beside volume of gland, its blood supply measured by power-Doppler images might provide evidences for assessing gland secretion and activity. [7],[8] However, we were able to find only a few reports examining the relationship between the size and volume of the parathyroid glands as well as their blood flow status and serum PTH level secreted by those glands. In the present study, we investigated the relationship between the volume and blood supply grade of the parathyroid glands, and their PTH secretion by high resolution ultrasonography with color Doppler imaging because ultrasonography is the only technique that measures volumetric variations of parathyroid glands and semiquantitative parameters for gland perfusion simultaneously. Hence, the aim of this study is to help evolve diagnostic accuracy ultrasonography for the secondary hyperparathyroidism in hemodialysis patients.


   Materials and Methods Top


In a cross-sectional study performed from June to August 2009, 52 patients with SHPT [intact PTH (i-PTH) ≥500 pg/mL] undergoing maintenance hemodialysis therapy were referred to dialysis wards of the Imam Khomeini and Amiralam University Hospitals (Tehran, Iran). The patients' age ranged from 21 to 79 years and they had undergone maintenance hemodialysis therapy for 6-332 months. None of the patients had a past history of parathyroidectomy, steroid therapy, or pulse calcitriol therapy. All patients were free of significant acute illness or malnutrition.

The study protocol was approved by the Ethics Committee of the Tehran University of Medical Sciences and all patients gave their consent to participate this study.

Baseline data were collected by face to face interviewing or from the hospital recorded files, including demographics, medical and drug history, clinical manifestations and baseline laboratory parameters.

Blood samples were treated with Ethylene-diaminetetraacetic acid (EDTA), and the plasma was stored at −20°C until the measurements were done. EDTA-plasma samples were sent to the hospital laboratory for i-PTH assay. Serum i-PTH was measured by an ELISA assay (Roche elecsys PTH kit 1-84).

In all patients, the parathyroid glands were identified by ultrasonography that was performed simultaneously with blood collection by two radiologists for each patient. The radiologists were unaware of clinical data and used a 5.7-10 MHz ultrasonography probe (Siemens G 40, Germany). Parathyroid blood flow was evaluated by power-Doppler color imaging. Power-Doppler criteria [Figure 1] shows the power-Doppler images used to assess peripheral (P) and central (C) blood flow signals from each gland. Based on the signal pattern, four groups were defined. Group A represents cases with no blood flow signal, Group B those with only a peripheral signal, Group C those with some signals inside the gland, and Group D those with many signals in the gland. The peripheral signals had no bearing on the definitions of Groups C and D.
Figure 1: Power-Doppler finding and group definietion. There degrees were classified for peripheral (P) and central (C) blood flow signals. After applying this classification, four Groups (A-D) were defined.

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The correlations between total weight of the glands as well as the signals of glands blood flow and i-PTH level were investigated by Pearson's correlation coefficient test. Parametric tests such as ANOVA and t-test, and nonparametric Kruskal-Wallis, Mann-Whitney, and Spearman's tests were used for bivariate analysis. Multivariable linear regression models were used to determine variables correlated with i-PTH level. P <0.05 were considered significant.

Statistical analysis was done with SPSS version 16.0 for Windows (SPSS, Chicago, IL, USA) to observe any significant difference.


   Results Top


Baseline characteristics and clinical data of the study subjects are summarized in [Table 1]. Mean age of the patients was 51 years with the male:female ratio of 1.8. The most common underlying cause of kidney disease was diabetes mellitus (21.2%). More than one-third of patients were asymptomatic. In 52 patients, 37 glands were detected by ultrasonography that only one of them was categorized in four-gland group. The ultrasonography exam showed that the patients varied from having one to four parathyroid glands with different vascular patterns of A, B, C, or D in power-Doppler sonography. Biochemical profiles of the patients are shown in [Table 2]. Mean levels of serum i-PTH was 939.37 ± 565.61 pg/mL (ranged 507-3065 pg/mL).
Table 1: Baseline characteristics of the study subjects (n = 52).

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Table 2: Baseline laboratory parameters in the study subjects (n=52).

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As shown in [Table 3], in patients with one parathyroid gland, 31.8% were categorized in Group C and 68.2% were categorized in Group D (the groups with any magnitude of blood flow in the gland). In the two-gland group, 70.0% of patients were graded as Group D. All patients with three parathyroid glands were categorized in Group D.
Table 3: Power-Doppler findings and group definition.

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There was no significant correlation between the total mass of the glands and serum concentration of i-PTH (r = 0.191, P = 0.408) [Figure 2]. Moreover, no significant correlation was observed between both total central and peripheral parathyroid glands blood flow and serum i-PTH level [Figure 3].
Figure 2: Correlation between total weight of parathyroid glands and concentration of intact parathyroid hormone (Pearson's r = 0.191, P = 0.408).

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Figure 3: Correlation between total grade of central (A) and peripheral (B) blood flow signals of parathyroid gland and concentration of intact parathyroid hormone.

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[Table 4] shows the linear regression analysis of parathyroid gland weight with various clinical variables in study patients. Dialysis duration and serum alkaline phosphatase (ALKp) were significantly correlated in a positive manner with i-PTH level. However, the serum level of i-PTH was not correlated with the total weight of parathyroid glands.
Table 4: Relationship between total weight of parathyroid glands and intact parathyroid hormone Level I a multivariable linear regression model.

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Furthermore, serum level of i-PTH was not correlated with the total signals of glands blood flow in a multivariable linear regression analysis [Table 5].
Table 5: Relationship between total signals of parathyroid glands blood flood flow and intact parathyroid hormone level in a multivariable linear regression model.

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   Discussion Top


SHPT is a common complication among patients with chronic kidney disease. [1],[9] Diagnosis of SHPT usually depends on i-PTH and other mineral metabolism parameters. [10] However, ultrasonography has primary role for the screening and follow-up of patients with secondary SHPT and sensitivity of this method is 45-70%. [11] The increase in volume of gland may be associated with increased PTH secretion and progression of SHPT, but Matsuoka et al showed that the correlation between gland volume and i-PTH is weak. [12]

Our result indicates two important clinical points. The first is that secretion of i-PTH is not dependant on the total weight and also blood supply of the parathyroid glands. In addition, in patients with one parathyroid gland, 31.8% were categorized in Group C and 68.2% were categorized in Group D (the groups with any magnitude of blood flow in the gland). In the two-gland group, 70% of patients were graded as Group D. All patients with three parathyroid glands were categorized in Group D. Onoda et al's study shows that in Groups A and B, seven out of 10 glands (70%) showed diffuse or nodular type of hyperplasia, whereas of the glands in Groups C and D, nine of 10 (90.0%), showed only nodular hyperplasia. These observations showed that the parathyroid histopathology was predicted by preoperative power-Doppler imaging but not by glandular weight. [13]

In fact, these two indices might not to be indications for determining types of treatment in these patients. In a similar study by McCarron et al. total parathyroid size was not predicted by basal C-terminal PTH levels. [5] Moreover, Onoda et al reported that the serum total-PTH did not correlate significantly in a positive manner with the maximal diameter of the gland as determined by ultrasonography. [13] Contrarily, Kakuta et al [1] showed a positive correlation between the mass of each individual gland and whole PTH level; however, massive parathyroid gland did not secrete more whole PTH per unit mass. Furthermore, status of blood supply could not be correlated with the serum level of i-PTH. On the other hand, it seems that the level of secreted i-PTH is not related to the structural characteristics of gland such as its size, weight, or volume as well as its blood supply condition.

Opposite results are reported by Ozcan and Oktay. In this study, the total volume of the visualized enlarged glands had positive correlation with i-PTH. [14] In addition, Anari et al showed that there is a significant correlation between iPTH and enlargement of parathyroid gland. [15] Inaba et al compared bio-i-PTH (1-84) with iPTH for its correlation with parathyroid gland size. He concluded that serum bio-PTH assay provide better assay than i-PTH to estimate parathyroid function in hemodialysis patients. [16] Although novel assay of PTH has better correlation with parathyroid gland size, we need additional studies with large sample size to confirm this result. Serum ALKp is used for evaluating hyperplasia of parathyroid gland and normal level of alkaline phosphates is associated with undetectable parathyroid gland in sonography. [15]

Another finding of our study is that two parameters of dialysis duration and serum concentration of ALKp can be effectively correlated to the serum concentration of i-PTH. Regarding the relationship between i-PTH and ALKp, Saravani et al [17] showed that this correlation was different between two genders. In this study, no correlation was observed between PTH and ALKp in men, however, the women showed correlation between PTH and ALKp. In fact, based on the findings of this study, SHPT and its effects on bone tissue were more severe in women than men undergoing hemodialysis. Moreover, in the study of Rahman et al [18] serum i-PTH level was positively correlated with inorganic phosphate and serum ALKp. Besides, with respect to the role of dialysis duration to predict i-PTH level, Nasri and Kheiri [19] revealed a positive correlation between serum i-PTH with the duration as well as with doses of dialysis treatment. Similar result was found in Heaf and Løkkegård [20] study. It seems that the role of these two parameters for predicting iPTH level is stronger than other indices shown in previous similar studies such as advanced age, diabetes mellitus, or calcium-phosphorus product.

Although it is potulated that power-Doppler sonography might provide evidences for assessing parathyroid gland secretion and activity, our study did not show correlation between the serum level of i-PTH and the total mass and blood supply of parathyroid glands. Hence, serum i-PTH level might not be predictable by total mass of parathyroid glands as well as their blood supply.

However, because of our small sample size, further studies are recommended for demonstrating the predictive role of these parameters.

Conflict of interest : None declared.

 
   References Top

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Kakuta T, Tanaka R, Kanai G, et al. Relationship between the weight of parathyroid glands and their secretion of parathyroid hormone in hemodialysis patients with secondary hyperparathyroidism. Ther Apher Dial 2008;12:385-90.  Back to cited text no. 1
    
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US Renal Data System. USRDS 2000 Annual Report. Bethesda: National Institutes of Health. National Institute of Diabetes and Digestive and Kidney Diseases; 2000.  Back to cited text no. 2
    
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Patient Registration Committee, Japanese Society for Dialysis Therapy. An overview of regular dialysis treatment in Japan (as of 31 December 2002). Ther Apher Dial 2004;8:358-82.  Back to cited text no. 3
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Tominaga Y, Kohara S, Namii Y, et al. Clonal analysis of nodular parathyroid hyperplasia in renal hyperparathyroidism. World J Surg 1996; 20:744-50.  Back to cited text no. 4
    
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McCarron DA, Muther RS, Lenfesty B, Bennett WM. Parathyroid function in persistent hyperparathyroidism: Relationship to gland size. Kidney Int 1982;22:662-70.  Back to cited text no. 5
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Okuno S, Ishimura E, Kitatani K, et al. Relationship between parathyroid gland size and responsiveness to maxacalcitol therapy in patients with secondary hyperparathyroidism. Nephrol Dial Transplant 2003;18:2613-21.  Back to cited text no. 6
    
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Mazzeo S, Caramella D, Lencioni R, et al. Usefulness of echo-color Doppler in differentiating parathyroid lesions from other cervical masses. Eur Radiol 1997;7:90-5.  Back to cited text no. 7
    
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Lane MJ, Desser TS, Weigel RJ, Jeffrey RB Jr. Use of color and power Doppler sonography to identify feeding arteries associated with para-thyroid adenomas. AJR Am J Roentgenol 1998; 171:819-23.  Back to cited text no. 8
    
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Obregón LM, Taylor MF, Mir G, et al. Parathyroidectomy for parathyroid carcinoma in renal transplantation. Transplant Proc 2005;37: 973-6.  Back to cited text no. 9
    
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Souberbielle JC, Boutten A, Carlier MC, et al. Inter-method variability in PTH measurement: Implication for the care of CKD patients. Kidney Int 2006;70:345-50.  Back to cited text no. 10
    
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Defechereux T, Meurisse M. Renal hyperparathyroidism: Current therapeutic approaches and future directions. Oper Tech Otolaryngol Head Neck Surg 2009;20:71-8.  Back to cited text no. 11
    
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Matsuoka S, Tominaga Y, Sato T, et al. Relationship between the dimension of parathyroid glands estimated by ultrasonography and the hyperplastic pattern in patients with renal hyperparathyroidism. Ther Apher Dial 2008;12: 391-5.  Back to cited text no. 12
    
13.
Onoda N, Kurihara S, Sakurai Y, et al. Evaluation of blood supply to the parathyroid glands in secondary hyperparathyroidism compared with histopathology. Nephrol Dial Transplant 2003;18 Suppl 3:iii34-7.  Back to cited text no. 13
    
14.
Ozcan UA, Oktay I. Assessment of parathyroid glands in hemodialysis patients by using color Doppler sonography. Eur Radiol 2009;19:2750-5.  Back to cited text no. 14
    
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Anari H, Bashardoust B, Pourissa M, Refahi S. The diagnostic accuracy of high resolution ultrasound imaging for detection of secondary hyperparathyroidism in patients with chronic renal failure. Acta Med Iran 2011;49:527-30.  Back to cited text no. 15
    
16.
Inaba M, Okuno S, Chou H, et al. Positive correlation of serum bio-intact PTH(1-84) but not intact PTH with parathyroid gland size in hemodialysis patients. Biomed Pharmacother 2006;60:62-5.  Back to cited text no. 16
    
17.
Saravani R, Qureshi MI, Jafari MM. Correlation between serum level parathormone, alkaline phosphatase, calcium and phosphorus of patients hemodialysis in Zahedan. J Med Sci 2007;7:154-7.  Back to cited text no. 17
    
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Rahman MH, Hossain MM, Sultana S, Jamal CY, Karim MA. Correlation of serum parathormone level with biochemical parameters in chronic renal failure. Indian Pediatr 2005;42: 250-4.  Back to cited text no. 18
    
19.
Nasri H, Kheiri S. Effects of diabetes mellitus, age, and duration of dialysis on parathormone in chronic hemodialysis patients. Saudi J Kidney Dis Transpl 2008;19:608-13.  Back to cited text no. 19
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Heaf JG, Løkkegård H. Parathyroid hormone during maintenance dialysis: Influence of low calcium dialysate, plasma albumin and age. J Nephrol 1998;11:203-10.  Back to cited text no. 20
    

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Correspondence Address:
Farrokhlagha Ahmadi
Nephrology Research Center, Tehran University of Medical Sciences, Tehran
Iran
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DOI: 10.4103/1319-2442.178257

PMID: 26997379

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