World J Surg DOI 10.1007/s00268-015-3070-0

ORIGINAL SCIENTIFIC REPORT

Parathyroid Reimplantation in Forearm Subcutaneous Tissue During Thyroidectomy: A Simple and Effective Way to Avoid Hypoparathyroidism Giuseppe Cavallaro1 • Olga Iorio1 • Marco Centanni1 • Natale Porta1 • Angelo Iossa1 • Lucilla Gargano1 • Susanna Del Duca1 • Angela Gurrado2 Mario Testini2 • Vincenzo Petrozza1 • Gianfranco Silecchia1



Ó Socie´te´ Internationale de Chirurgie 2015

Abstract Introduction Parathyroid autotransplantation plays an important role in preventing hypoparathyroidism following thyroidectomy. The preferred reimplantation site is still the sternocleidomastoid muscle, but this approach does not permit to check graft vitality postoperatively. The authors report the first prospective evaluation of normal parathyroid gland reimplantation in forearm subcutaneous tissue (using the same technique proposed during parathyroidectomy for hyperplasia) in case of devascularized or inadvertently removed glands during thyroid surgery. Materials and methods From January 2013 to August 2014, we performed 348 consecutive thyroidectomies for various disease, both benign and malignant. In 25 cases, due to inadvertent parathyroid removal or evidence of insufficient blood supply, we removed and fragmented the gland into 0.5–1 mm slices (one for frozen section) and reimplanted it into two subcutaneous pockets on the non-dominant forearm. After surgery we checked grafted gland function by evaluation of serum parathormone gradient between reimplanted versus non-reimplanted arm (considering significant a ratio of 1.5 or more), at 1 week, 1 and 3 months after surgery. Results We observed recovery of reimplanted graft function in 48, 88 and 96 % of patients respectively at 1 week, 1 and 3 months after surgery. All patients showed normal parathormone levels in peripheral blood (non-reimplanted arm). In one case we observed post-operative wound hematoma on graft-site. This patient showed no graft functionality in post-operative period (even at 3 months follow-up). Conclusions Parathyroid gland reimplantation in forearm subcutaneous tissue during thyroid surgery is a safe, easy and effective procedure; furthermore, it allows a good control of graft functionality and would allow an easy grafted gland removal if needed.

Introduction & Giuseppe Cavallaro [email protected] 1

Department of Medico-Surgical Sciences and Biotechnologies, Sapienza University of Rome, Corso della Repubblica 79, 04100 Latina, LT, Italy

2

Department of Biomedical Sciences and Human Oncology, University of Bari, Bari, Italy

Parathyroid autotransplantation, first described in 1908 in animal models [1], has not been widely considered of clinical utility until the last decades [2, 3], when it has been proposed to preserve parathyroid function after parathyroidectomy for secondary hyperparathyroidism, primary parathyroid hyperplasia, recurrent or persistent hyperparathyroidism. Today this technique plays an important

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role even in the prevention of hypoparathyroidism following thyroid surgery [4]. Functionality of reimplanted parathyroid gland has been widely described, both in animal studies [1, 5] and in case of surgery for hyperparathyroidism; high success rates of reimplantation should be attributed to angiogenesis induced by parathyroid cells, as seen in in vitro studies [6, 7]. Nevertheless, the check of reimplanted parathyroid gland function is impossible after thyroid surgery, since glands are usually reimplanted within the sternocleidomastoid muscle [8], and there aren’t non-invasive methods to check functional parathyroid tissue within this muscle [9]. So, the determination of parathyroid function by peripheral blood sampling by serum intact parathormone (PTH) measurement, that is routinely used to predict the risk of permanent hypocalcemia, cannot be specific for reimplanted graft functionality. In literature there is just one study dealing with this matter [9]; the authors reimplanted the inadvertently removed or devascularized parathyroid into multiple pockets within the brachioradialis muscle in seven patients, documenting good graft function in six cases. On the basis of this study, we investigated the effectiveness of parathyroid gland reimplantation into the forearm subcutaneous tissue using the same technique yet described in previous studies on parathyroidectomy for hyperplasia [9–12], in order to establish a less invasive method of reimplantation of normal glands and to check graft vitality and function.

examination, based on frozen sections stained with rapid hematoxylin-eosin. After confirming the presence of parathyroid tissue, the gland was sliced into 0.5–1 mm pieces. Slices were implanted into two or three small pockets fashioned in the subcutaneous tissue of the nondominant forearm through 2–3 mm skin incisions (Fig. 1). Hemostasis was then achieved, and each pocket was closed by 4–0 non-absorbable suture [10]. The entire reimplantation procedure took about 5 min in all cases. Postoperative controls included both clinical evaluation and blood sampling, in order to check any possible symptom or sign of hypoparathyroidism, and compare, as yet described, the functionality of reimplanted parathyroid by the ratio between serum PTH levels of the two arms. A ratio of at least 1.5 folds for reimplanted gland functionality was considered significant for graft function recovery, as demonstrated by previous studies [4, 9]. Postoperative controls comprended as follows: –

– –

Total serum calcium (Ca), magnesium (Mg) and phosphorus (P) measurement on the 1st and 2nd postoperative day. Ca, Mg, P, and serum intact parathormone (PTH) from left and righ arm measurement 7 days after surgery. Ca and PTH measurement from left and right arm 1 and 3 months after surgery.

We decided not to check serum PTH levels on 1st and 2nd postoperative days considering:

Materials and methods From January 2013 to August 2014, 348 consecutive thyroidectomies (223 women and 125 men, mean age 49.8, range 18–84) were performed (and prospectively evaluated) for the treatment of various thyroid diseases. All patients underwent preoperative workup including: serum thyroid hormone, serum total calcium (Ca), inorganic phosphorus (P) and intact parathormone (PTH) measurement, and determination of thyroid antibodies. Neck ultrasounds, plain chest scan and laryngoscopy to determine vocal cord motility were carried out in all patients. Thyroid scintigraphy, fine-needle aspiration cytology and neck CTscan were restricted to patients having hyperthyroidism, thyroid nodules suspected of carcinoma or cervico-mediastinal goiter, respectively. All surgical procedures were performed by skilled surgeons. Accurate dissection and identification of parathyroid glands and their blood supply were obtained by 2.59 loop magnification [8] to leave functioning glands in situ. Nevertheless, in 25 cases, due to intraoperative findings of insufficient blood supply or signs of sufferance (like intracapsular hematoma), or inadvertent excision, one (or more) parathyroid gland was carefully removed and placed in saline solution. A small specimen of the tissue was sent to intraoperative histological

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– –

The presence of peripheral vein catheter and fluid infusions on the non-reimplanted arm (that could modify blood sampling results). The possibility of complications (like phlebitis) on the reimplanted arm, potentially affecting graft vitality. The unreliability of PTH sampling from blood taken from the implanted arm. In fact, PTH normal range is referred to ‘‘peripheral’’ blood samples, and the PTH values from blood close to a reimplanted gland should not be considered a reliable value.

All patients received and signed specific informed consent regarding thyroid surgery and the possibility of parathyroid gland reimplantation in non-dominant forearm subcutaneous tissue, specifying the possible advantages of this procedure in controlling graft functionality with respect to the usual site of reimplantation, that is the sternocleidomastoid muscle.

Results Patients demographics, thyroid diseases, surgical procedures and post-operative results of patients having reimplanted parathyroid are summarized on Table 1. Only two

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Fig. 1 a The parathyroid gland fragmented in 1–2 mm pieces. b intraoperative frozen section with rapid hematoxylin-eosin. Medium-power microphotograph showing normal parathyroid tissue

(209). c skin incisions on the forearm. d parathyroid reimplantation in subcutaneous pocket. e skin incisions after closure by nonabsorbable suture. f skin incisions: 1 month after surgery

patients developed post-operative transient symptomatic hypocalcemia requiring replacement therapy for a maximum of 6 days, then the serum calcium levels returned to normal values, and symptoms disappeared. One patient developed postoperative wound hematoma on reimplantation site that solved spontaneously in 8 days. There were no other post-operative complications, except one case of transient laryngeal recurrent nerve palsy documented by laryngoscopy. All patients were discharged on the second postoperative day after drain removal. Parathyroid graft functionality, described as the ratio of serum PTH levels from reimplanted versus non-reimplanted forearm blood, was significant in 48 % (12 on 25) of patients 1 week after surgery, in 88 % (22 on 25) 1 month after surgery, and in 96 % (24 on 25) of patients 3 months after surgery (Table 1) (Figs. 2, 3). Interestingly, the only patient having no evidence of graft functionality even after 3 months was the one with post-operative wound hematoma on reimplantation site. All patients showed normal PTH values verified by serum PTH levels from non-reimplanted forearm blood samples within 1 month after surgery, meaning normal overall parathyroid gland functionality.

Discussion Parathyroid damage or inadvertent removal still affect thyroid surgery, even in case of careful dissection, and can lead to transient or definitive hypoparathyroidism; its occurrence varies widely among centers and among surgeons, depending on the regional and individual experience, ranging from 0 to 43 % [13–15]. Literature data show a rate of 11 % of inadvertent parathyroid removal during thyroidectomy [16], and the presence of parathyroid gland in up to 19 % of histological examination made on removed thyroid glands [17, 18]; even during our prospective evaluation, 16 parathyroid glands were found in 348 thyroid specimens (4.6 %). During the last decades, reimplantation of devascularized or accidentally removed parathyroid glands during thyroid surgery has been advocated to reduce or minimize the risk of post-operative permanent hypoparathyroidism [4–8], mainly during re-do surgery or extended lymph-node dissection. Several authors show excellent results, with a reported incidence of definitive hypoparathyroidism of \1 % [19], advocating routine parathyroid reimplantation during thyroid surgery

123

Age

70

46

72

61

68

67

72

40

51

61

48

52

37

62

51

38

47

57

70

45

Sex

F

F

F

F

F

M

M

M

F

F

M

F

M

F

F

M

F

M

F

F

NO

1

123

2

3

4

5

6

7

8

9

10

11

12

13

14

15

16

17

18

19

20

Graves disease

substernal goiter

substernal goiter

substernal goiter

Graves disease

papillary carcinoma

substernal goiter

substernal goiter

substernal goiter

substernal goiter

multi nodular goiter

multi nodular goiter

multi nodular goiter

Graves disease

substernal goiter

substernal goiter

multi nodular goiter

multi nodular goiter

multi nodular goiter

multi nodular goiter

Preop. Diagnosis

TT

TT

TT

TT

TT

TT, central neck dissection

TT

TT

TT

TT

TT

TT

TT

TT

TT

TT

TT

TT

TT

TT

Surgical Procedure

Papillary carcinoma pT1

benign disease

benign disease

benign disease

benign disease

papillary carcinoma pT1-pN0

benign disease

benign disease

benign disease

benign disease

benign disease

benign disease

benign disease

benign disease

benign disease

benign disease

benign disease

benign disease

benign disease

benign disease

Histology

left

left

left

left

left

left

left

left

left

left

left

left

left

left

left

left

left

left

left

left

Reimpl. Side

9.1

8.8

8.8

8.3

9.0

7.5

9.0

8.4

8.2

7.9

8.8

7.1

8.8

8.3

9.0

8.3

9.1

8.0

8.5

9.4

3.2

4.4

3.0

3.1

3.8

3.3

2.5

2.5

2.8

2.7

2.9

3.1

2.8

4.0

4.2

3.1

3.0

2.8

2.4

2.7

2.0

1.8

1.9

1.7

1.9

2.1

1.4

1.7

1.6

1.8

2.3

1.5

2.0

2.2

2.1

1.9

2.1

1.9

2.0

1.8

8.8

8.4

8.6

8.5

8.4

7.4

8.1

8.0

8.3

8.1

8.0

7.3

8.1

9.0

8.8

8.4

9.7

8.4

8.1

9.7

3.5

3.6

3.2

3.6

4.2

3.9

4.5

3.3

3.2

2.9

3.8

2.5

2.5

2.8

2.7

3.1

2.9

2.8

3.1

2.8

P

2.1

1.7

1.7

1.8

1.8

2.1

1.7

1.6

1.9

2.1

2.2

1.4

2.1

1.7

1.9

1.8

2.6

1.6

2.5

2.2

Mg

Ca

Mg

Ca

P

2nd P.O.day

1st P.O.day

9.2

8.6

8.2

9.4

8.7

7.7

8.2

8.1

8.0

8.2

8.6

8.9

9.2

9.9

9.4

9.8

9.4

10.0

9.6

9.4

Ca

15.6

54.1

33.0

54.1

28.5

4.6

32.1

33.4

19.0

27.8

31.3

1.6

10.0

53.10

30.6

22.1

38.0

15.2

20.3

20.0

PTH NRA

1 Week

18.2

63.9

50.1

63.9

45.2

13.1

35.6

42.1

28.6

35.0

50.6

6.3

35.2

83.9

35.9

19.9

45.2

14.2

32.9

30.1

PTH RA

4.1

3.3

3.2

3.9

4.0

4.5

3.9

4.2

3.0

3.1

4.1

3.2

3.9

4.3

3.1

3.4

2.7

4.2

3.4

2.6

P

Table 1 Patients characteristics, diagnosis, surgical procedures, reimplantation site, post-operative controls and results

1.8

2.4

2.1

1.9

1.6

2.2

2.1

1.8

2.2

1.5

1.6

1.8

2.0

2.1

1.5

1.4

1.7

1.8

2.2

1.4

Mg

1.2

1.2

1.5

1.2

1.6

2.8

1.1

1.3

1.5

1.2

1.6

3.9

3.5

1.6

1.2

0.9

1.2

0.9

1.6

1.5

Pth Ratio

8.3

8.8

8.4

8.7

8.4

8.8

9.1

9.3

8.7

8.7

9.1

9.0

9.3

9.4

9.9

9.6

9.5

9.9

9.7

9.8

Ca

24.6

48.3

34.2

48.2

35.7

16.2

33.4

30.2

22.1

26.4

38.1

21.5

18.5

42.5

41.0

57.5

58.5

41.0

33.6

60.1

PTH NRA

1 Month

42.1

83.1

60.0

97.2

72.0

28.6

49.7

65.1

38.3

41.0

62.4

178.0

42.1

155.0

43.0

119.0

90.5

39.9

75.9

90.0

PTHRA

1.7

1.7

1.7

2.0

2.0

1.7

1.5

2.1

1.7

1.5

1.6

8.3

2.3

3.6

1.1

2.1

1.5

0.9

2.2

1.5

PTH Ratio

8.3

8.8

8.6

8.9

9.3

8.4

9.9

8.7

9.1

9.2

9.2

9.9

8.8

8.9

9.7

9.3

8.8

9.1

9.8

9.6

Ca

34.1

45.5

28.6

33.1

27.6

15.6

29.8

19.6

24.6

30.1

25.1

28.5

22.3

61.3

30.0

44.5

40.6

26.5

27.7

45.0

PTH NRA

3 months

98.3

86.2

54.2

75.9

50.1

26.1

52.0

35.1

42.3

52.6

60.2

152.4

43.2

166.2

46.5

108.4

62.1

25.4

69.8

92.1

PthRA

2.9

1.9

1.9

2.3

1.8

1.7

1.7

1.8

1.7

1.7

2.4

5.3

1.9

2.7

1.5

2.4

1.5

0.9

2.5

2.1

PTH Ratio

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29

46

45

74

73

F

M

F

F

F

21

22

23

24

25

multinodular goiter

Substernal goiter

papillary carcinoma

Multi nodular goiter

Papillary carcinoma

Preop. Diagnosis

TT

TT

TT, central neck dissection

TT

TT, central neck dissection

Surgical Procedure

benign disease

benign disease

papillary carcinoma pT1-pN0

benign disease

papillary carcinoma pT1-pN0

Histology

right

right

right

left

left

Reimpl. Side

8.4

8.0

7.2

8.1

7.8

2.1

1.4

2.1

1.5

1.6

7.9

8.2

7.6

8.0

7.9

3.1

3.0

3.3

2.8

3.2

2.0

1.6

2.1

1.6

1.9

2nd P.O.day Ca P Mg

TT total thyroidectomy, PTH NRA PTH from non-reimplanted arm, PTH RA PTH from reimplanted arm

PTH ratio means the gradient of PTH value of grafted/nongrafted forearm

3.1

2.5

2.8

2.9

3.1

1st P.O.day Ca P Mg

PTH value is expressed as pg/ml of serum intact parathormone (normal value: 10–60)

Mg value is expressed as mg/dll of serum magnesium (normal value: 1.7–2.5)

P value is expressed as mg/dl ofserum phosphate (normal value: 2.5–4.5)

Ca value is expressed as mg/dl of serum total calcium (normal value: 8.5–10.5)

Age

Sex

NO

Table 1 continued

8.8

8.4

8.2

8.3

8.5

22.6

10.8

1.2

6.3

5.1

1 Week Ca PTH NRA

30.7

11.6

1.0

15.5

17.2

PTH RA

2.8

3.6

3.6

3.5

4.2

P

2.5

2.5

2.3

1.9

2.3

Mg

1.3

1.1

0.8

2.5

3.4

Pth Ratio

8.9

8.8

8.6

8.4

9.1

23.0

18.4

4.5

22.1

18.2

1 Month Ca PTH NRA

41.7

23.1

8.2

79.0

112.5

PTHRA

1.8

1.2

1.8

3.6

6.1

PTH Ratio

9.0

8.5

10.0

8.6

8.2

23.2

25.2

20.4

28.4

35.2

3 months Ca PTH NRA

40.0

43.1

32.1

83.1

102.1

PthRA

1.7

1.7

1.6

2.9

2.9

PTH Ratio

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Fig. 2 Mean value of serum PTH levels (pg/ml) from nonreimplanted arm (NRA) versus reimplanted arm (RA), at 1 week, 1 month, and 3 months

Fig. 3 Graphic showing the percentage of patients having PTH ratio [1.5 at 1 week, 1 and 3 months

[20, 21]. Various reimplantation techniques have been described, both during thyroid surgery as well as during surgery for hyperparathyroidism. During thyroid surgery, the preferred site for reimplantation is the sternocleidomastoid muscle (or even the neck strap muscles) [8, 19– 22]. The advantage of this method is the possibility to create the intramuscular pocket and reimplant the parathyroid with no need of further skin incisions. Unfortunately, it is not possible to verify whereas post-operative serum calcium and PTH levels depend on grafted gland function recovery or on preserved in situ glands. Furthermore, even if uncommon, in case of need to remove the grafted gland, a re-do cervical surgery could lead to augmented risk of post-operative complications, would require general anesthesia and cervical muscles resections.

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Another described site for reimplantation (used in case of thyroidectomy and lymph-node dissection for thyroid malignancies) is the pectoralis major muscle [22, 23], but this method shows unclear advantages with respect to sternocleidomastoid muscle. In case of surgery for parathyroid hyperplasia (both in primary and in secondary hyperparathyroidism), the brachioradialis muscle is the preferred site for reimplantation [24, 25]; this in order to easily check graft vitality and/or dysfunction (by the PTH ratio) and to avoid complications and difficulties of neck re-do surgery in case of need to remove the grafted gland; this occurrence may affect up to 12 % of these patients [26]. Other authors report similar results using forearm subcutaneous pocket as reimplantation site [9–12], with fewer complication rates than in case of reimplantation in brachioradialis muscle [11] or even direct injection of minced gland into the forearm subcutaneous space [27]. So, why do not use the forearm as reimplantation site of normal parathyroid glands accidentally removed or devascularized during thyroid surgery? This method could achieve post-operative control of graft functionality (PTH ratio) and even easy graft removal if needed. In literature, there is just one study dealing with this matter [9]; the authors reimplanted the inadvertently removed or devascularized parathyroid into multiple pockets within the brachioradialis muscle in seven patients, documenting (by PTH gradient between reimplanted vs not-reimplanted arm) good graft function in six cases. On the basis of this experience, we tried to investigate the possibility to use the forearm subcutaneous tissue as reimplantation site, as yet described for parathyroid hyperplasia. We prospectively evaluated 25 unselected patients (out of 348 consecutive thyroidectomies performed in 1 year) submitted to parathyroid reimplantation in forearm subcutaneous tissue for intraoperative findings of inadvertent gland removal. We chose this site for reimplantation for the aforementioned matters and for the less invasiveness of this technique when compared to intramuscular reimplantation. Furthermore, this procedure is very quick, requires very small skin incisions of about 2 mm in length, and the postoperative cosmetic results are excellent. We decided not to apply any patient selection, since thyroid surgery may include many different pathologies and many different patients with different ages and even comorbidities, and reimplantation may be potentially applied to all patients. Our results show a 96 % rate of success (24 on 25 patients) in terms of graft function recovery, by the PTH ratio. In fact, a positive gradient of serum PTH reveals the presence of functioning parathyroid tissue in reimplanted forearm. We observed one local complication after reimplantation, a subcutaneous wound hematoma. The occurrence of this complication just in the only case of unsuccessful grafting let us suppose (but not demonstrate) that this may be the

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cause of graft failure. In conclusion, reimplantation of inadvertently removed or devascularized normal parathyroid glands in forearm subcutaneous tissue during thyroid surgery can be considered a safe, easy and effective procedure that can help avoid or minmize the risk for postoperative hypoparathyroidism; furthermore, this procedure allows a good and not-invasive control of graft functionality (by the ratio between serum PTH levels of reimplanted vs not-reimplanted arm blood samples) and would permit an easy grafted gland removal if needed. This technique may be considered an effective alternative to the usual reimplantation into the sternocleidomastoid muscle even during surgery for thyroid cancer. Further studies with larger series and longer follow-up will help us confirm the results of this prospective evaluation.

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Parathyroid Reimplantation in Forearm Subcutaneous Tissue During Thyroidectomy: A Simple and Effective Way to Avoid Hypoparathyroidism.

Parathyroid autotransplantation plays an important role in preventing hypoparathyroidism following thyroidectomy. The preferred reimplantation site is...
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