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Abstract

Background

Hypocalcaemia is a common complication after thyroidectomy. Bariatric surgery is associated with significant changes in calcium metabolism. Some studies have identified bariatric surgery as a risk factor for hypocalcaemia after thyroidectomy. This systematic review and meta-analysis assessed whether a history of bariatric surgery was associated with an increased risk of hypocalcaemia after thyroidectomy.

Methods

This prospectively registered systematic review (PROSPERO; CRD42021295423) was performed in accordance with PRISMA guidelines. Meta-analysis was undertaken using the Mantel–Haenszel method, with outcomes reported as ORs with 95 per cent confidence intervals.

Results

Twenty studies were included in the qualitative synthesis. Five studies incorporating 19 547 patients met the inclusion criteria for meta-analysis, of whom 196 (1.0 per cent) had a history of bariatric surgery. Patients with a history of bariatric surgery were more likely to develop hypocalcaemia after thyroidectomy (30.6 versus 13.0 per cent; OR 3.90, 95 per cent c.i. 1.50 to 10.12; P = 0.005). Among those with a history of bariatric surgery, patients who underwent a bypass procedure were more likely to develop hypocalcaemia after thyroidectomy than those who had a restrictive procedure (38 versus 23 per cent; OR 2.12, 1.14 to 3.97; P = 0.020).

Conclusion

Patients with a history of bariatric surgery have a significantly greater risk of hypocalcaemia after thyroidectomy, with a heightened risk among those who have had a bypass procedure. Surgeons performing thyroid surgery should be aware of the increased risk of hypocalcaemia after thyroidectomy among these patients.

Lay Summary

Low calcium levels are a common complication after surgical removal of the thyroid gland. Patients who have had weight loss surgery (bariatric surgery) have altered calcium metabolism and are prone to low calcium levels. This study assessed whether previous weight loss surgery increased the risk of low calcium levels after thyroid surgery. A search was made of previously published studies assessing the relationship between previous weight loss surgery and low calcium levels after thyroid surgery. Studies have shown that previous weight loss surgery makes patients more than three times more likely to have low calcium levels after thyroid surgery. Management of low calcium in these patients is more challenging than in patients who have not had weight loss surgery. Surgeons performing thyroid surgery need to be aware of whether a patient has previously had weight loss surgery as they have an increased risk of low calcium after thyroid surgery.

Introduction

Thyroidectomy involves excision of the thyroid gland, and is a well established treatment for both malignant and benign thyroid diseases1. It is associated with a 30-day complication rate of 7.7 per cent2. Hypocalcaemia is a common complication after thyroidectomy and may be transient or permanent. It can lead to serious complications, such as cardiac arrhythmias, tetany, seizures, and laryngospasm3. Thus, the early identification of postoperative hypocalcaemia in these patients is imperative to ensure timely treatment, and to avoid unnecessary anxiety, morbidity, and potential death.

Obesity is becoming more common in the Western world, and poses a number of inherent physiological and metabolic risks to patients4,5. The increasing prevalence of obesity, in combination with the large proportion of non-responders to medical weight reduction strategies, has led to the emergence of bariatric surgery (BS) in managing the obesity epidemic6. BS is an efficacious treatment for obesity7, often facilitating the reversal of pre-existing co-morbidities such as diabetes mellitus, hypertension, and hyperlipidaemia8. A number of different procedures exist, and these can be broadly categorized as bypass procedures (such as Roux-en-Y gastric bypass or biliopancreatic diversion) and restrictive procedures (sleeve gastrectomy or gastric banding). As the prevalence of obesity and number of BS procedures being performed in the Western world increases9, clinicians must be cognisant of the implications of anatomical and physiological disruption of the upper gastrointestinal system for prospective medical and surgical care10. In particular, BS is associated with significant biochemical alterations, including calcium and vitamin D metabolism11. Potential reasons for this include an overall reduction in stomach acidity, as well as bypass-type procedures delegating the mechanical responsibility of calcium reabsorption to the less effective distal small bowel, with a negative impact on calcium absorption12,13. Therefore, clinicians have hypothesized that patients who have undergone BS may be at an increased risk of hypocalcaemia after thyroidectomy.

The primary aim of this systematic review and meta-analysis was to determine whether patients who have undergone BS are at increased risk of hypocalcaemia after thyroidectomy. Additionally, the review sought to establish whether the management of post-thyroidectomy hypocalcaemia in patients who have undergone BS differs from that of patients with no history of BS.

Methods

A systematic review was performed in accordance with the PRISMA guidelines14. As this was a review of previously published studies, ethical approval was not required. This systematic review was prospectively registered in PROSPERO (CRD42021295423).

Search strategy

An electronic search of the PubMed, EMBASE, Cochrane Central, and Scopus databases was undertaken on 3 September 2021 for relevant studies using the search terms (thyroidectomy ‘OR’ thyroid surgery) and (bariatric surgery ‘OR’ gastric bypass ‘OR’ gastric banding) and (calcium ‘OR’ hypocalcaemia), which were linked using the Boolean operator ‘AND’. Included studies were limited to those published in the English language; there was no restriction based on year of publication. All duplicate studies were removed manually, before screening of titles. The abstracts of studies deemed appropriate were reviewed, and the full text of the remaining studies was then reviewed for eligibility. References in studies considered for inclusion were also reviewed to assess for potentially eligible studies.

Eligibility criteria

Studies meeting the following inclusion criteria were included in the qualitative synthesis: reporting outcomes on patients undergoing total thyroidectomy or near-total thyroidectomy, with no restriction based on the indication for surgery; including a proportion of patients who had previously undergone BS; and reporting data on new-onset hypocalcaemia after thyroidectomy. Studies meeting any of the following exclusion criteria were excluded: reporting outcomes of patients undergoing Dunhill’s operation, subtotal thyroidectomy, hemithyroidectomy or thyroid lobectomy; not reporting on hypocalcaemia rates after thyroidectomy; including patients with premorbid hypocalcaemia or hypoparathyroidism diagnosed before operation; not published in the English language; review articles; and editorials. Case series with fewer than five patients and case reports were included in the qualitative analysis. Case series with five patients or fewer were excluded from the quantitative synthesis.

Definitions

The following definitions of hypocalcaemia were considered acceptable: symptomatic hypocalcaemia (such as paraesthesia, muscles cramps, tetany); requirement for intravenous calcium replacement; or biochemical evidence of hypocalcaemia after thyroidectomy.

In the present study, thyroidectomy included both total thyroidectomy and near-total thyroidectomy. Total thyroidectomy was defined as complete surgical removal of the thyroid gland with no residual thyroid tissue remaining. Near-total thyroidectomy comprised excision of all thyroid tissue bilaterally except for residual thyroid tissue with a volume less than 1.0 ml15.

Review process and risk-of-bias assessment

This literature search was performed by two independent reviewers using the search strategy described. Where discrepancies in opinion occurred between the reviewers, a third reviewer was asked to arbitrate. All retrieved manuscripts were reviewed by both reviewers to ensure that all inclusion criteria were met, before extracting the following data: first author name, year of publication, study design, country, level of evidence, study title, number of patients, indication for thyroidectomy, central neck dissection performed, number of patients who had undergone BS, number of patients who had not undergone BS, type of BS performed (Roux-en-Y gastric bypass, gastric bypass, sleeve gastrectomy or gastric banding), incidence of hypocalcaemia after thyroidectomy, and management strategy for patients with postoperative hypocalcaemia.

The risk-of-bias quality assessment of included articles was undertaken independently by two reviewers using the Newcastle–Ottawa Scale for observational studies16. The quality score rating was determined for each publication; 8 or more stars represented observational studies of higher quality.

Quantitative synthesis and statistical analysis

Statistical analysis was done according to the Cochrane guidelines17. Results of comparisons of dichotomous variables were displayed as ORs with 95 per cent confidence intervals estimated using the Mantel–Haenszel method. Statistical heterogeneity was determined using I2 statistics and visual inspection of forest plots, and random-effects models were used as there was significant heterogeneity between included studies. Subgroup analysis based on bariatric procedure performed—bypass (Roux-en-Y gastric bypass or biliopancreatic diversion) versus restrictive (sleeve gastrectomy or gastric banding)—was undertaken for those who had undergone BS. Intergroup characteristics were compared using Student’s t and χ2 tests, as appropriate. P < 0.050 was considered statistically significant. Statistical analysis was performed using Review Manager (RevMan), version 5.4 (Nordic Cochrane Centre, Copenhagen, Denmark).

Results

Literature search

The initial search of PubMed, EMBASE, Cochrane Central, and Scopus resulted in identification of a total of 133 studies. After removal of 35 duplicates, titles of 97 studies were reviewed for relevance. Following review, the full text of 25 studies was assessed for eligibility. Finally, 20 studies remained for inclusion in the qualitative synthesis, including 15 case reports or case series with fewer than five patients. After qualitative analysis, five observational studies were included in the meta-analysis (Fig. 1).

PRISMA flow chart showing selection of studies for review
Fig. 1

PRISMA flow chart showing selection of studies for review

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Qualitative synthesis

The 20 studies identified for inclusion in the qualitative synthesis included two retrospective cohort studies18,19, three case–control studies20–22, three case series23–25, and 12 case reports26–37 (Table 1). They included 113 patients who had undergone Roux-en-Y gastric bypass, five biliopancreatic diversion, 57 gastric banding, 41 sleeve gastrectomy, and one patient who had undergone stomach intestinal pylorus-sparing surgery (Table 1). All included studies found a risk of hypocalcaemia after thyroidectomy in patients who had undergone BS previously, irrespective of the bariatric procedure performed.

Table 1
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Summary of studies in qualitative synthesis

ReferenceCountryLOEBariatric surgery typeNo undergoing bariatric surgeryTime between thyroidectomy and bariatric surgeryHypocalcaemia treatment
Cali et al.18France335 GB
29 SG
26 RYGB		904 (2–15) years*i.v., oral calcium, vitamin D
Chereau et al.20France322 GB
11 SG
15 RYGB		483.3 (0.2–15.3) years†i.v., oral calcium, vitamin D
Droeser et al.19Sweden3RYGB25All < 7 yearsi.v., oral calcium and vitamin D
Dequanter et al.21France3RYGB14n.r.i.v., oral calcium, vitamin D
McKenzie et al.22USA3RYGB1952.6 (4–109) months†i.v., oral calcium, vitamin D, magnesium if required
Durr et al.25USA4RYGB26, 3 yearsi.v., oral calcium, vitamin D, magnesium
Manco et al.23‡Italy4BPD4Between 1 and 5 yearsDifferent for each patient§
Gooi et al.24USA4RYGB3n.r.Staged total thyroidectomy
Corbeels et al.26Belgium5RYGB13 yearsi.v. calcium, vitamin D, teriparatide, reversal of RYGB
Jensen et al.27USA5SIPS12 yearsi.v. calcium, vitamin D, conversion of SIPS to RYGB
Baldane et al.28Turkey5RYGB12 yearsi.v. calcium, i.v. magnesium, vitamin D, pancrelipase
Allo Miguel et al.29Spain5RYGB18 yearsi.v., oral calcium, vitamin D, teriparatide revision/partial reversal of RYGB
Alfonso et al.34USA5RYGB1n.r.i.v., oral calcium, vitamin D
Panazzolo et al.30Brazil5RYGB16 monthsi.v., oral calcium, vitamin D, magnesium, pancrelipase
Gross et al.35USA5RYGB16 monthsi.v., oral calcium, vitamin D, i.v. magnesium, thiazide diuretic
Salinger and Moore36‡USA5RYGB15 yearsi.v., oral calcium, vitamin D
Pietras and Holick31‡USA5RYGB18 monthsPerithyroidectomy high-dose oral calcium, still required i.v. calcium and magnesium, vitamin D after operation
Rojas-Marcos et al.32Spain5BPD13 yearsi.v., oral calcium, vitamin D, magnesium
Zaarour et al.33France5RYGB11 yeari.v., oral calcium, vitamin D, teriparatide, reversal of RYGB
Vemuri et al.37‡USA5SG1n.r.i.v., oral calcium, vitamin D
ReferenceCountryLOEBariatric surgery typeNo undergoing bariatric surgeryTime between thyroidectomy and bariatric surgeryHypocalcaemia treatment
Cali et al.18France335 GB
29 SG
26 RYGB		904 (2–15) years*i.v., oral calcium, vitamin D
Chereau et al.20France322 GB
11 SG
15 RYGB		483.3 (0.2–15.3) years†i.v., oral calcium, vitamin D
Droeser et al.19Sweden3RYGB25All < 7 yearsi.v., oral calcium and vitamin D
Dequanter et al.21France3RYGB14n.r.i.v., oral calcium, vitamin D
McKenzie et al.22USA3RYGB1952.6 (4–109) months†i.v., oral calcium, vitamin D, magnesium if required
Durr et al.25USA4RYGB26, 3 yearsi.v., oral calcium, vitamin D, magnesium
Manco et al.23‡Italy4BPD4Between 1 and 5 yearsDifferent for each patient§
Gooi et al.24USA4RYGB3n.r.Staged total thyroidectomy
Corbeels et al.26Belgium5RYGB13 yearsi.v. calcium, vitamin D, teriparatide, reversal of RYGB
Jensen et al.27USA5SIPS12 yearsi.v. calcium, vitamin D, conversion of SIPS to RYGB
Baldane et al.28Turkey5RYGB12 yearsi.v. calcium, i.v. magnesium, vitamin D, pancrelipase
Allo Miguel et al.29Spain5RYGB18 yearsi.v., oral calcium, vitamin D, teriparatide revision/partial reversal of RYGB
Alfonso et al.34USA5RYGB1n.r.i.v., oral calcium, vitamin D
Panazzolo et al.30Brazil5RYGB16 monthsi.v., oral calcium, vitamin D, magnesium, pancrelipase
Gross et al.35USA5RYGB16 monthsi.v., oral calcium, vitamin D, i.v. magnesium, thiazide diuretic
Salinger and Moore36‡USA5RYGB15 yearsi.v., oral calcium, vitamin D
Pietras and Holick31‡USA5RYGB18 monthsPerithyroidectomy high-dose oral calcium, still required i.v. calcium and magnesium, vitamin D after operation
Rojas-Marcos et al.32Spain5BPD13 yearsi.v., oral calcium, vitamin D, magnesium
Zaarour et al.33France5RYGB11 yeari.v., oral calcium, vitamin D, teriparatide, reversal of RYGB
Vemuri et al.37‡USA5SG1n.r.i.v., oral calcium, vitamin D

Values are *median (range) and †mean (range). ‡Patients underwent near-total thyroidectomy. §Two patients were treated with prolonged high dose oral calcium and vitamin D; one patient had lengthening of the common limb after biliopancreatic diversion (BPD); the final patient had prophylactic intravenous (i.v.) calcium immediately after near-total thyroidectomy and did not develop hypocalcaemia. LOE, level of evidence; GB, gastric banding; SG, sleeve gastrectomy; RYGB, Roux-en-Y gastric bypass; n.r., not reported; SIPS, stomach intestinal pylorus-sparing surgery.

Table 1
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Summary of studies in qualitative synthesis

ReferenceCountryLOEBariatric surgery typeNo undergoing bariatric surgeryTime between thyroidectomy and bariatric surgeryHypocalcaemia treatment
Cali et al.18France335 GB
29 SG
26 RYGB		904 (2–15) years*i.v., oral calcium, vitamin D
Chereau et al.20France322 GB
11 SG
15 RYGB		483.3 (0.2–15.3) years†i.v., oral calcium, vitamin D
Droeser et al.19Sweden3RYGB25All < 7 yearsi.v., oral calcium and vitamin D
Dequanter et al.21France3RYGB14n.r.i.v., oral calcium, vitamin D
McKenzie et al.22USA3RYGB1952.6 (4–109) months†i.v., oral calcium, vitamin D, magnesium if required
Durr et al.25USA4RYGB26, 3 yearsi.v., oral calcium, vitamin D, magnesium
Manco et al.23‡Italy4BPD4Between 1 and 5 yearsDifferent for each patient§
Gooi et al.24USA4RYGB3n.r.Staged total thyroidectomy
Corbeels et al.26Belgium5RYGB13 yearsi.v. calcium, vitamin D, teriparatide, reversal of RYGB
Jensen et al.27USA5SIPS12 yearsi.v. calcium, vitamin D, conversion of SIPS to RYGB
Baldane et al.28Turkey5RYGB12 yearsi.v. calcium, i.v. magnesium, vitamin D, pancrelipase
Allo Miguel et al.29Spain5RYGB18 yearsi.v., oral calcium, vitamin D, teriparatide revision/partial reversal of RYGB
Alfonso et al.34USA5RYGB1n.r.i.v., oral calcium, vitamin D
Panazzolo et al.30Brazil5RYGB16 monthsi.v., oral calcium, vitamin D, magnesium, pancrelipase
Gross et al.35USA5RYGB16 monthsi.v., oral calcium, vitamin D, i.v. magnesium, thiazide diuretic
Salinger and Moore36‡USA5RYGB15 yearsi.v., oral calcium, vitamin D
Pietras and Holick31‡USA5RYGB18 monthsPerithyroidectomy high-dose oral calcium, still required i.v. calcium and magnesium, vitamin D after operation
Rojas-Marcos et al.32Spain5BPD13 yearsi.v., oral calcium, vitamin D, magnesium
Zaarour et al.33France5RYGB11 yeari.v., oral calcium, vitamin D, teriparatide, reversal of RYGB
Vemuri et al.37‡USA5SG1n.r.i.v., oral calcium, vitamin D
ReferenceCountryLOEBariatric surgery typeNo undergoing bariatric surgeryTime between thyroidectomy and bariatric surgeryHypocalcaemia treatment
Cali et al.18France335 GB
29 SG
26 RYGB		904 (2–15) years*i.v., oral calcium, vitamin D
Chereau et al.20France322 GB
11 SG
15 RYGB		483.3 (0.2–15.3) years†i.v., oral calcium, vitamin D
Droeser et al.19Sweden3RYGB25All < 7 yearsi.v., oral calcium and vitamin D
Dequanter et al.21France3RYGB14n.r.i.v., oral calcium, vitamin D
McKenzie et al.22USA3RYGB1952.6 (4–109) months†i.v., oral calcium, vitamin D, magnesium if required
Durr et al.25USA4RYGB26, 3 yearsi.v., oral calcium, vitamin D, magnesium
Manco et al.23‡Italy4BPD4Between 1 and 5 yearsDifferent for each patient§
Gooi et al.24USA4RYGB3n.r.Staged total thyroidectomy
Corbeels et al.26Belgium5RYGB13 yearsi.v. calcium, vitamin D, teriparatide, reversal of RYGB
Jensen et al.27USA5SIPS12 yearsi.v. calcium, vitamin D, conversion of SIPS to RYGB
Baldane et al.28Turkey5RYGB12 yearsi.v. calcium, i.v. magnesium, vitamin D, pancrelipase
Allo Miguel et al.29Spain5RYGB18 yearsi.v., oral calcium, vitamin D, teriparatide revision/partial reversal of RYGB
Alfonso et al.34USA5RYGB1n.r.i.v., oral calcium, vitamin D
Panazzolo et al.30Brazil5RYGB16 monthsi.v., oral calcium, vitamin D, magnesium, pancrelipase
Gross et al.35USA5RYGB16 monthsi.v., oral calcium, vitamin D, i.v. magnesium, thiazide diuretic
Salinger and Moore36‡USA5RYGB15 yearsi.v., oral calcium, vitamin D
Pietras and Holick31‡USA5RYGB18 monthsPerithyroidectomy high-dose oral calcium, still required i.v. calcium and magnesium, vitamin D after operation
Rojas-Marcos et al.32Spain5BPD13 yearsi.v., oral calcium, vitamin D, magnesium
Zaarour et al.33France5RYGB11 yeari.v., oral calcium, vitamin D, teriparatide, reversal of RYGB
Vemuri et al.37‡USA5SG1n.r.i.v., oral calcium, vitamin D

Values are *median (range) and †mean (range). ‡Patients underwent near-total thyroidectomy. §Two patients were treated with prolonged high dose oral calcium and vitamin D; one patient had lengthening of the common limb after biliopancreatic diversion (BPD); the final patient had prophylactic intravenous (i.v.) calcium immediately after near-total thyroidectomy and did not develop hypocalcaemia. LOE, level of evidence; GB, gastric banding; SG, sleeve gastrectomy; RYGB, Roux-en-Y gastric bypass; n.r., not reported; SIPS, stomach intestinal pylorus-sparing surgery.

There was no apparent association reported between preoperative calcium, vitamin D or parathyroid (PTH) levels and post-thyroidectomy hypocalcaemia among patients who had previously undergone BS. Two studies23,31 outlined a trial prescription of calcium supplementation at time of thyroidectomy in an attempt to prevent hypocalcaemia after surgery. Manco et al.23 prescribed intravenous calcium gluconate prophylactically immediately after thyroidectomy followed by lifelong oral calcium and vitamin D supplementation in a patient who had previously undergone Roux-en-Y gastric bypass. This patient did not develop symptomatic hypocalcaemia after thyroidectomy. In contrast, Pietras and Holick31 trialled high-dose prophylactic oral calcium and vitamin D after thyroidectomy, which subsequently resulted in the patient developing symptomatic hypocalcaemia requiring intravenous calcium and magnesium replacement. Interestingly, Gooi et al.24 described a case series of 3 patients being managed with a staged thyroidectomy to encourage revascularization of the ipsilateral parathyroid glands before completion thyroidectomy. None of the patients in this series developed post-thyroidectomy hypocalcaemia and all had previously undergone Roux-en-Y gastric bypass.

In all studies included in the qualitative analysis, postoperative hypocalcaemia significantly prolonged hospital stay. In total, 19 of 20 studies reported managing acute hypocalcaemia using intravenous calcium gluconate and high-dose oral vitamin D (Table 1). Seven of the 20 studies reported using magnesium replacement when indicated. Nineteen studies documented at least 1 patient with a history of BS requiring lifelong calcium and vitamin D replacement. Despite this, 6 of 20 series described patients with refractory hypocalcaemia frequently requiring repeated hospital admissions and intravenous calcium replacement to treat symptomatic hypocalcaemia.

Three case reports26,29,33 trialled recombinant PTH therapy (teriparatide, a synthetic PTH analogue) for persistent hypocalcaemia that was resistant to high-dose oral supplementation with calcium and vitamin D. All patients had undergone Roux-en-Y gastric bypass. Teriparatide therapy did not achieve normocalcaemia in these patients, and all 3 subsequently underwent revision of the Roux-en-Y gastric bypass without significant improvement in calcium levels. In contrast, Jensen et al.27 reported a patient in whom revision of a previous bariatric procedure did improve postoperative hypocalcaemia after thyroidectomy. This patient had previous stomach intestinal pylorus-sparing surgery converted to Roux-en-Y gastric bypass. Two case reports28,30 described trialling pancrelipase (a combination of synthetic amylase, lipase, and protease) for recalcitrant hypocalcaemia in patients who had undergone Roux-en-Y gastric bypass, both of which noted a biochemical improvement in serum calcium levels after treatment.

Quantitative synthesis

In total, 5 studies18–22 including 19 547 patients were included in the quantitative synthesis. Overall, 19 351 (99.0 per cent) patients had not undergone BS, whereas patients 196 (1.0 per cent) had (Table 2). Patients with a history of BS before thyroidectomy were significantly more likely to be women (91.2 versus 79.7 per cent; P < 0.001). The mean age at the time of thyroidectomy was 50.0 (range 46.0–51.9) years and patients with a history of BS were significantly younger at the time of thyroidectomy (48.8 versus 50.1 years; P < 0.001). Mean BMI was 32.9 kg/m2 among those who had undergone BS and 24.1 kg/m2 among those who had not (P < 0.001). All patients in the quantitative synthesis apart from 4 in the study by McKenzie et al.22 (19 543 of 19 547, 99.9 per cent) underwent total thyroidectomy (two patients each in the BS and no BS groups underwent near-total thyroidectomy). Four studies18–20,22 reported indications for thyroidectomy; 24.7 per cent of patients had surgery for a thyroid malignancy, with no significant difference between those who had a history of BS and those who did not (31.8 versus 27.4 per cent; P = 0.182). Two studies19,20 reported on whether or not central neck lymph node dissection was performed; 17.5 per cent of patients underwent central neck dissection at the time of thyroidectomy (20.5 per cent with a history of BS versus 17.4 per cent with no history of BS; P = 0.480) (Table 2). In total, four of five included studies were of high quality measured using the Newcastle–Ottawa Scale. Risk-of-bias assessment and individual study characteristics are shown in Table 3.

Table 2
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Characteristics of patients who had undergone previous bariatric surgery and those who had not

Bariatric surgery (n = 196)No bariatric surgery (n = 19 351)P†
Age (years), mean (range)*48.8 (48.0–49.7)50.1 (46.0–52.0)<0.001‡
BMI (kg/m2), meam (range)*32.9 (30.9–45.3)24.1 (24.0–44.5)<0.001‡
Sex*<0.001
 M16 of 182 (8.8)3919 of 19 328 (20.3)
 F166 of 182 (91.2)15 409 of 19 328 (79.7)
CLND0.480
 Yes15 of 73 (21)1071 of 6138 (17.4)
 No58 of 73 (805067 of 6138 (82.6)
Indication for surgery*0.182
 Thyroid neoplasm58 of 182 (31.8)5302 of 19 328 (27.4)
 Benign indication124 of 182 (68.2)14 026 of 19 328 (72.6)
Bariatric surgery (n = 196)No bariatric surgery (n = 19 351)P†
Age (years), mean (range)*48.8 (48.0–49.7)50.1 (46.0–52.0)<0.001‡
BMI (kg/m2), meam (range)*32.9 (30.9–45.3)24.1 (24.0–44.5)<0.001‡
Sex*<0.001
 M16 of 182 (8.8)3919 of 19 328 (20.3)
 F166 of 182 (91.2)15 409 of 19 328 (79.7)
CLND0.480
 Yes15 of 73 (21)1071 of 6138 (17.4)
 No58 of 73 (805067 of 6138 (82.6)
Indication for surgery*0.182
 Thyroid neoplasm58 of 182 (31.8)5302 of 19 328 (27.4)
 Benign indication124 of 182 (68.2)14 026 of 19 328 (72.6)

Values are n (%) unless otherwise indicated. *Not reported by all studies. †χ2 test, except ‡Student’s t test.

CLND = central neck lymph node dissection

Table 2
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Characteristics of patients who had undergone previous bariatric surgery and those who had not

Bariatric surgery (n = 196)No bariatric surgery (n = 19 351)P†
Age (years), mean (range)*48.8 (48.0–49.7)50.1 (46.0–52.0)<0.001‡
BMI (kg/m2), meam (range)*32.9 (30.9–45.3)24.1 (24.0–44.5)<0.001‡
Sex*<0.001
 M16 of 182 (8.8)3919 of 19 328 (20.3)
 F166 of 182 (91.2)15 409 of 19 328 (79.7)
CLND0.480
 Yes15 of 73 (21)1071 of 6138 (17.4)
 No58 of 73 (805067 of 6138 (82.6)
Indication for surgery*0.182
 Thyroid neoplasm58 of 182 (31.8)5302 of 19 328 (27.4)
 Benign indication124 of 182 (68.2)14 026 of 19 328 (72.6)
Bariatric surgery (n = 196)No bariatric surgery (n = 19 351)P†
Age (years), mean (range)*48.8 (48.0–49.7)50.1 (46.0–52.0)<0.001‡
BMI (kg/m2), meam (range)*32.9 (30.9–45.3)24.1 (24.0–44.5)<0.001‡
Sex*<0.001
 M16 of 182 (8.8)3919 of 19 328 (20.3)
 F166 of 182 (91.2)15 409 of 19 328 (79.7)
CLND0.480
 Yes15 of 73 (21)1071 of 6138 (17.4)
 No58 of 73 (805067 of 6138 (82.6)
Indication for surgery*0.182
 Thyroid neoplasm58 of 182 (31.8)5302 of 19 328 (27.4)
 Benign indication124 of 182 (68.2)14 026 of 19 328 (72.6)

Values are n (%) unless otherwise indicated. *Not reported by all studies. †χ2 test, except ‡Student’s t test.

CLND = central neck lymph node dissection

Table 3
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Characteristics of studies in quantitative synthesis

Cali et al.18Chereau et al.20Droeser et al.19Dequanter et al.21McKenzie et al.22Overall
No. of patients13 242966115375719 547
Mean age (years)51.948.046.0–49.750.0
Bariatric surgery
 Yes90 (0.7)48 (50)25 (0.5)14 (37.8)19 (33.3)196 (1.0)
 No13 152 (99.3)48 (50)6090 (99.5)23 (62.2)38 (67.7)19 351 (99.0)
Mean BMI (kg/m2)
 Bariatric surgery30.931.9––45.332.9
 No bariatric surgery24.031.0––44.524.1
Central neck dissection
 Bariatric surgery–8 (17)7 (28.0)––15 (1.4)
 No bariatric surgery–10 (21)1061 (17.4)––1071 (98.6)
Thyroid cancer
 Bariatric surgery28 (31.1)13 (27.1)7 (28.0)–10 (52.6)58 (1.1)
 No bariatric surgery4317 (32.8)15 (31.3)949 (15.6)–21 (55.3)5302 (98.9)
Newcastle–Ottawa Scale score88878–
Cali et al.18Chereau et al.20Droeser et al.19Dequanter et al.21McKenzie et al.22Overall
No. of patients13 242966115375719 547
Mean age (years)51.948.046.0–49.750.0
Bariatric surgery
 Yes90 (0.7)48 (50)25 (0.5)14 (37.8)19 (33.3)196 (1.0)
 No13 152 (99.3)48 (50)6090 (99.5)23 (62.2)38 (67.7)19 351 (99.0)
Mean BMI (kg/m2)
 Bariatric surgery30.931.9––45.332.9
 No bariatric surgery24.031.0––44.524.1
Central neck dissection
 Bariatric surgery–8 (17)7 (28.0)––15 (1.4)
 No bariatric surgery–10 (21)1061 (17.4)––1071 (98.6)
Thyroid cancer
 Bariatric surgery28 (31.1)13 (27.1)7 (28.0)–10 (52.6)58 (1.1)
 No bariatric surgery4317 (32.8)15 (31.3)949 (15.6)–21 (55.3)5302 (98.9)
Newcastle–Ottawa Scale score88878–

Values are n (%) unless otherwise indicated.

Table 3
Open in new tab

Characteristics of studies in quantitative synthesis

Cali et al.18Chereau et al.20Droeser et al.19Dequanter et al.21McKenzie et al.22Overall
No. of patients13 242966115375719 547
Mean age (years)51.948.046.0–49.750.0
Bariatric surgery
 Yes90 (0.7)48 (50)25 (0.5)14 (37.8)19 (33.3)196 (1.0)
 No13 152 (99.3)48 (50)6090 (99.5)23 (62.2)38 (67.7)19 351 (99.0)
Mean BMI (kg/m2)
 Bariatric surgery30.931.9––45.332.9
 No bariatric surgery24.031.0––44.524.1
Central neck dissection
 Bariatric surgery–8 (17)7 (28.0)––15 (1.4)
 No bariatric surgery–10 (21)1061 (17.4)––1071 (98.6)
Thyroid cancer
 Bariatric surgery28 (31.1)13 (27.1)7 (28.0)–10 (52.6)58 (1.1)
 No bariatric surgery4317 (32.8)15 (31.3)949 (15.6)–21 (55.3)5302 (98.9)
Newcastle–Ottawa Scale score88878–
Cali et al.18Chereau et al.20Droeser et al.19Dequanter et al.21McKenzie et al.22Overall
No. of patients13 242966115375719 547
Mean age (years)51.948.046.0–49.750.0
Bariatric surgery
 Yes90 (0.7)48 (50)25 (0.5)14 (37.8)19 (33.3)196 (1.0)
 No13 152 (99.3)48 (50)6090 (99.5)23 (62.2)38 (67.7)19 351 (99.0)
Mean BMI (kg/m2)
 Bariatric surgery30.931.9––45.332.9
 No bariatric surgery24.031.0––44.524.1
Central neck dissection
 Bariatric surgery–8 (17)7 (28.0)––15 (1.4)
 No bariatric surgery–10 (21)1061 (17.4)––1071 (98.6)
Thyroid cancer
 Bariatric surgery28 (31.1)13 (27.1)7 (28.0)–10 (52.6)58 (1.1)
 No bariatric surgery4317 (32.8)15 (31.3)949 (15.6)–21 (55.3)5302 (98.9)
Newcastle–Ottawa Scale score88878–

Values are n (%) unless otherwise indicated.

Incidence of hypocalcaemia

Overall, 13.2 per cent of patients had hypocalcaemia after thyroidectomy (2583 of 19 547). Previous BS was significantly associated with having hypocalcaemia after thyroidectomy (30.6 versus 13.0 per cent; OR 3.90, 95 per cent c.i. 1.50 to 10.12; P = 0.005) (Fig. 2). Although this association was seen across all studies, there was interstudy heterogeneity regarding the strength of the effect (I2 = 62 per cent). Among those with a history of BS, patients who had undergone a bypass procedure were significantly more likely to have hypocalcaemia after thyroidectomy than those who had undergone a restrictive procedure (38 versus 23 per cent; OR 2.12, 1.14 to 3.97; P = 0.020) (Fig. 3).

Forest plot illustrating rates of hypocalcaemia after thyroidectomy for patients who had previously undergone bariatric surgery versus those who had not
Fig. 2

Forest plot illustrating rates of hypocalcaemia after thyroidectomy for patients who had previously undergone bariatric surgery versus those who had not

A Mantel–Haenszel random-effects model was used for meta-analysis. ORs are shown with 95% confidence intervals. BS, bariatric surgery.

Open in new tabDownload slide
Risk of hypocalcaemia after thyroidectomy by type of previous bariatric surgery
Fig. 3

Risk of hypocalcaemia after thyroidectomy by type of previous bariatric surgery

A Mantel–Haenszel random-effects model was used for meta-analysis. ORs are shown with 95% confidence intervals.

Open in new tabDownload slide

Discussion

This is the first systematic review and meta-analysis to evaluate the risk of hypocalcaemia after thyroidectomy in patients who had undergone BS previously. The most important finding is that almost one-third of patients (30.6 per cent) with a history of BS had hypocalcaemia after thyroidectomy. These patients were 3.9 times more likely to have hypocalcaemia than those without a history of BS (30.6 versus 13.0 per cent; OR 3.90, 95 per cent c.i. 1.50 to 10.12; P = 0.005). This finding is important given the increasing volume of BS being undertaken worldwide9,38. Should thyroidectomy be required for such patients, the present findings suggest that they require close monitoring of serum calcium levels and that perioperative endocrinology input is vital. There has been a vogue in recent times to permit thyroidectomy as a day-case procedure39. Given the high risk of hypocalcaemia after thyroidectomy in these patients, and the need for close monitoring of perioperative calcium levels, it would appear that day-case thyroidectomy is not suitable for patients with a history of BS.

In total, 196 patients with a history of BS were included in the meta-analysis. Patients who had undergone bypass procedures were significantly more likely to have hypocalcaemia after thyroidectomy than those with a history of a restrictive procedures (38 versus 23 per cent; OR 2.12, 1.14 to 3.97; P = 0.020). These data suggest a stepwise increase in hypocalcaemia rates for those with no history of BS (13.0 per cent) versus restrictive BS (23 per cent) versus bypass BS (38 per cent) (P < 0.001).

Following BS, patients are predisposed to developing hypocalcaemia owing to significant alterations in metabolism of calcium and fat-soluble vitamins, including vitamin D12,13. Patients have reduced gastric acid secretion after BS, which affects the disintegration and solubility of nutrients40. The aim of BS is to reduce dietary intake and, as a result, patients may have decreased oral intake of vitamin D and calcium. BS reduces the time that food is in contact with the intestinal mucosa and reduces absorption of nutrients41. These physiological changes may explain why all patients with a history of BS are at increased risk of hypocalcaemia after thyroidectomy. Several mechanisms that predispose patients who have undergone a bypass procedure to hypocalcaemia do not occur in those who have had a restrictive procedure. The vast majority of dietary calcium is absorbed via active transporters in the duodenum and proximal jejunum, anatomical locations that food is diverted from after a bypass procedure30. Following bypass procedures, food does not mix with bile and pancreatic digestive enzymes until it reaches the common alimentary channel. Vitamin D is a fat-soluble vitamin, and requires bile and digestive enzymes to be absorbed properly. Thus, patients who have undergone BS may develop a deficiency of vitamin D and secondary hypocalcaemia. Such patients are frequently prescribed lifelong supplementation after BS42. Unfortunately, it was not possible to assess the effect of patient adherence to such supplements on the incidence of hypocalcaemia after thyroidectomy in the present study. These additional mechanisms may establish a rationale for the incremental (or stepwise) increase in hypocalcaemia risk based on the degree of disruption to the gastrointestinal tract. As patients with a history of a bypass procedure, such as Roux-en-Y gastric bypass or biliopancreatic diversion, have the highest risk of hypocalcaemia after thyroidectomy, knowledge and details of the BS procedure are important in understanding the likely risk of hypocalcaemia associated with thyroidectomy.

Overall, 13.2 per cent of patients developed postoperative hypocalcaemia after thyroidectomy. Hypocalcaemia following thyroidectomy is usually transient, resulting from parathyroid handling during surgery. The parathyroid glands may, however, be removed inadvertently or devascularized during the procedure, resulting in permanent hypocalcaemia43. The present systematic review has demonstrated that correction of hypocalcaemia after thyroidectomy in patients with a history of BS is challenging. Patients who had undergone BS and developed hypocalcaemia after thyroidectomy required at minimum lifelong high-dose oral calcium and vitamin D replacement. Recombinant PTH therapy did not appear to be successful in the management of hypocalcaemia. This suggests that postoperative hypocalcaemia among patients who have undergone BS is potentially due to malabsorption; however, validation of this hypothesis is required. Moreover, qualitative analysis suggests that reversal of BS was of trivial value in correcting hypocalcaemia after thyroidectomy, although the data supporting this are limited to level IV evidence. Interestingly, case reports28,30 describing trialling pancrelipase therapy documented a significant improvement in calcium levels. It is evident from the qualitative analysis that the management of post- thyroidectomy hypocalcaemia in the BS population should be more aggressive than in patients without a history of BS. It is also evident that there is currently no coherent consensus regarding the optimal management strategy for post-thyroidectomy hypocalcaemia in the BS population. Thus, translational research efforts focused around the understanding and manipulation of calcium metabolism in this population at time of thyroidectomy are warranted to guide future management of patients with a history of BS undergoing thyroidectomy.

This study has a number of limitations. No prospective studies were included. This implies that the included studies had low-to-intermediate levels of evidence, suggesting inherent bias, including selection, confounding, and ascertainment biases. For example, qualitative synthesis included a high proportion of case reports and case series (15 of 20) indicating low levels of evidence. The majority of included studies did not report the impact of associated central neck dissection, failure to identify/handling of the parathyroid glands during surgery, and of inflammatory thyroid diseases on post-thyroidectomy rates of hypocalcaemia, all of which are renowned risk factors for postoperative hypocalcaemia after thyroidectomy44. Additionally, the length of time between BS and thyroidectomy may influence an individual patient’s risk of hypocalcaemia after thyroidectomy. From the available literature, it was not possible to evaluate the impact of the interval between thyroidectomy and BS on the incidence of post-thyroidectomy hypocalcaemia. There was also limited availability of data facilitating evaluation of the incidence of transient versus permanent hypocalcaemia.

The management paradigm for treating post-thyroidectomy hypocalcaemia in patients with a history of BS poses a clinical challenge, with a paucity of data available from which to form consensus. In essence, prospective controlled trials are required to fully establish the risk, and the most appropriate management, of hypocalcaemia after thyroidectomy in patients who have previously undergone BS.

Funding

The authors have no funding to declare.

Disclosure

The authors declare no conflict of interest.

References

1

Haugen
BR
,
Alexander
EK
,
Bible
KC
,
Doherty
GM
,
Mandel
SJ
,
Nikiforov
YE
et al.
2015 American Thyroid Association management guidelines for adult patients with thyroid nodules and differentiated thyroid cancer: The American Thyroid Association Guidelines Task Force on Thyroid Nodules and Differentiated Thyroid Cancer
.
Thyroid
2016
;
26
:
1
–
133

Google Scholar

Crossref
Search ADS
PubMed

 
2

Caulley
L
,
Johnson-Obaseki
S
,
Luo
L
,
Javidnia
H
.
Risk factors for postoperative complications in total thyroidectomy: a retrospective, risk-adjusted analysis from the National Surgical Quality Improvement Program
.
Medicine (Baltimore)
2017
;
96
:
e5752

Google Scholar

Crossref
Search ADS
PubMed

 
3

Carroll
R
,
Matfin
G
.
Endocrine and metabolic emergencies: hypocalcaemia
.
Ther Adv Endocrinol Metab
2010
;
1
:
29
–
33

Google Scholar

Crossref
Search ADS
PubMed

 
4

Sturm
R
,
Hattori
A
.
Morbid obesity rates continue to rise rapidly in the United States
.
Int J Obes (Lond)
2013
;
37
:
889
–
891

Google Scholar

Crossref
Search ADS
PubMed

 
5

Pi-Sunyer
X
.
The medical risks of obesity
.
Postgrad Med
2009
;
121
:
21
–
33

Google Scholar

Crossref
Search ADS
PubMed

 
6

le Roux
CW
,
Heneghan
HM
.
Bariatric surgery for obesity
.
Med Clin North Am
2018
;
102
:
165
–
182

Google Scholar

Crossref
Search ADS
PubMed

 
7

Heymsfield
SB
,
Wadden
TA
.
Mechanisms, pathophysiology, and management of obesity
.
N Engl J Med
2017
;
376
:
254
–
266

Google Scholar

Crossref
Search ADS
PubMed

 
8

Schauer
PR
,
Mingrone
G
,
Ikramuddin
S
,
Wolfe
B
.
Clinical outcomes of metabolic surgery: efficacy of glycemic control, weight loss, and remission of diabetes
.
Diabetes Care
2016
;
39
:
902
–
911

Google Scholar

Crossref
Search ADS
PubMed

 
9

Nguyen
NT
,
Vu
S
,
Kim
E
,
Bodunova
N
,
Phelan
MJ
.
Trends in utilization of bariatric surgery, 2009–2012
.
Surg Endosc
2016
;
30
:
2723
–
2727

Google Scholar

Crossref
Search ADS
PubMed

 
10

Longitudinal Assessment of Bariatric Surgery (LABS) Consortium
;
Flum
DR
,
Belle
SH
,
King
WC
,
Wahed
AS
,
Berk
P
et al.
Perioperative safety in the longitudinal assessment of bariatric surgery
.
N Engl J Med
2009
;
361
:
445
–
454

Google Scholar

PubMed
OpenURL Placeholder Text

 
11

Mechanick
JI
,
Apovian
C
,
Brethauer
S
,
Garvey
WT
,
Joffe
AM
,
Kim
J
et al.
Clinical practice guidelines for the perioperative nutrition, metabolic, and nonsurgical support of patients undergoing bariatric procedures—2019 update: cosponsored by American Association of Clinical Endocrinologists/American College of Endocrinology, the Obesity Society, American Society for Metabolic & Bariatric Surgery, Obesity Medicine Association, and American Society of Anesthesiologists—executive summary
.
Endocr Pract
2019
;
25
:
1346
–
1359

Google Scholar

PubMed
OpenURL Placeholder Text

 
12

Carrasco
F
,
Basfi-Fer
K
,
Rojas
P
,
Csendes
A
,
Papapietro
K
,
Codoceo
J
et al.
Calcium absorption may be affected after either sleeve gastrectomy or Roux-en-Y gastric bypass in premenopausal women: a 2-y prospective study
.
Am J Clin Nutr
2018
;
108
:
24
–
32

Google Scholar

Crossref
Search ADS
PubMed

 
13

Schafer
AL
,
Weaver
CM
,
Black
DM
,
Wheeler
AL
,
Chang
H
,
Szefc
GV
et al.
Intestinal calcium absorption decreases dramatically after gastric bypass surgery despite optimization of vitamin D status
.
J Bone Miner Res
2015
;
30
:
1377
–
1385

Google Scholar

Crossref
Search ADS
PubMed

 
14

Moher
D
,
Liberati
A
,
Tetzlaff
J
,
Altman
DG
,
PRISMA Group
.
Preferred reporting items for systematic reviews and meta-analyses: the PRISMA statement
.
BMJ
2009
;
339
:
b2535

Google Scholar

Crossref
Search ADS
PubMed

 
15

Cirocchi
R
,
Trastulli
S
,
Randolph
J
,
Guarino
S
,
Di Rocco
G
,
Arezzo
A
et al.
Total or near-total thyroidectomy versus subtotal thyroidectomy for multinodular non-toxic goitre in adults
.
Cochrane Database Syst Rev
2015
; (8)
CD010370

Google Scholar

OpenURL Placeholder Text

 
16

Stang
A
.
Critical evaluation of the Newcastle–Ottawa scale for the assessment of the quality of nonrandomized studies in meta-analyses
.
Eur J Epidemiol
2010
;
25
:
603
–
605

Google Scholar

Crossref
Search ADS
PubMed

 
17

Higgins
JPT
,
Thomas
J
,
Chandler
J
,
Cumpston
M
,
Li
T
,
Page
MJ
et al. (eds). Cochrane Handbook for Systematic Reviews of Interventions version 6.3 (updated February 2022). Cochrane, 2022. Available from www.training.cochrane.org/handbook (accessed 4 March 2022).

18

Cali
B
,
Hasani
A
,
Buffet
C
,
Menegaux
F
,
Chereau
N
.
Is there a relationship between different types of prior bariatric surgery and post-thyroidectomy hypocalcemia?
Gland Surg
2021
;
10
:
2088
–
2094

Google Scholar

Crossref
Search ADS
PubMed

 
19

Droeser
RA
,
Ottosson
J
,
Muth
A
,
Hultin
H
,
Lindwall-Ahlander
K
,
Bergenfelz
A
et al.
Hypoparathyroidism after total thyroidectomy in patients with previous gastric bypass
.
Langenbecks Arch Surg
2017
;
402
:
273
–
280

Google Scholar

Crossref
Search ADS
PubMed

 
20

Chereau
N
,
Vuillermet
C
,
Tilly
C
,
Buffet
C
,
Tresallet
C
,
du Montcel
ST
et al.
Hypocalcemia after thyroidectomy in patients with a history of bariatric surgery
.
Surg Obes Relat Dis
2017
;
13
:
484
–
490

Google Scholar

Crossref
Search ADS
PubMed

 
21

Dequanter
D
,
Shahla
M
,
Deniz
Y
,
Aubert
C
,
Lothaire
P
.
Recalcitrant hypocalcemia after total thyroidectomy and bariatric surgery
.
B-ENT
2016
;
12
:
207
–
209

Google Scholar

PubMed
OpenURL Placeholder Text

 
22

McKenzie
TJ
,
Chen
Y
,
Hodin
RA
,
Shikora
SA
,
Hutter
MM
,
Gaz
RD
et al.
Recalcitrant hypocalcemia after thyroidectomy in patients with previous Roux-en-Y gastric bypass
.
Surgery
2013
;
154
:
1300
–
1306

Google Scholar

Crossref
Search ADS
PubMed

 
23

Manco
M
,
Nanni
G
,
Tondolo
V
,
Iaconelli
A
,
Greco
AV
,
Castagneto
M
et al.
Hypocalcemia complicating near-total thyroidectomy in patients with coexisting lipid malabsorption due to biliopancreatic diversion
.
Obes Surg
2004
;
14
:
1429
–
1434

Google Scholar

Crossref
Search ADS
PubMed

 
24

Gooi
Z
,
Ward
BK
,
Mener
DJ
,
Ozgursoy
OB
,
Pai
SI
.
A staged thyroidectomy approach for gastric bypass patients
.
Laryngoscope
2015
;
125
:
1028
–
1030

Google Scholar

Crossref
Search ADS
PubMed

 
25

Durr
ML
,
Saunders
JR
,
Califano
JA
,
Tufano
RP
,
Koch
WM
,
Ha
PK
.
Severe hypocalcemia complicating thyroid surgery after Roux-en-Y gastric bypass procedure
.
Arch Otolaryngol Head Neck Surg
2009
;
135
:
507
–
510

Google Scholar

Crossref
Search ADS
PubMed

 
26

Corbeels
K
,
Steenackers
N
,
Lannoo
M
,
Mertens
A
,
Deleus
E
,
Cunha
N
et al.
Reversal of Roux-en-Y gastric bypass fails to facilitate the management of recalcitrant hypocalcaemia caused by primary hypoparathyroidism
.
Obes Surg
2020
;
30
:
5150
–
5152

Google Scholar

Crossref
Search ADS
PubMed

 
27

Jensen
SM
,
Thompson
RE
,
Machineni
S
,
Overby
DW
,
Farrell
TM
.
Refractory hypocalcemia following stomach intestinal pylorus-sparing bariatric surgery and thyroidectomy: successful management with creation of a proximal Roux-en-Y gastric bypass
.
Am Surg
2021
;
87
:
576
–
580

Google Scholar

Crossref
Search ADS
PubMed

 
28

Baldane
S
,
Ipekci
SH
,
Kebapcilar
L
.
Pancrelipase treatment in a patient with the history of Roux-en-Y gastric bypass operation that developed resistant hypocalcemia secondary to total thyroidectomy
.
Endocr Regul
2016
;
50
:
27
–
31

Google Scholar

Crossref
Search ADS
PubMed

 
29

Allo Miguel
G
,
García Fernández
E
,
Martínez Díaz-Guerra
G
,
Valero Zanuy
MÁ
,
Pérez Zapata
A
,
de la Cruz Vigo
F
et al.
Recalcitrant hypocalcaemia in a patient with post-thyroidectomy hypoparathyroidism and Roux-en-Y gastric bypass
.
Obes Res Clin Pract
2016
;
10
:
344
–
347

Google Scholar

Crossref
Search ADS
PubMed

 
30

Panazzolo
DG
,
Braga
TG
,
Bergamim
A
,
Pires
B
,
Almeida
H
,
Kraemer-Aguiar
LG
.
Hypoparathyroidism after Roux-en-Y gastric bypass—a challenge for clinical management: a case report
.
J Med Case Rep
2014
;
8
:
357

Google Scholar

Crossref
Search ADS
PubMed

 
31

Pietras
SM
,
Holick
MF
.
Refractory hypocalcemia following near-total thyroidectomy in a patient with a prior Roux-en-Y gastric bypass
.
Obes Surg
2009
;
19
:
524
–
526

Google Scholar

Crossref
Search ADS
PubMed

 
32

Rojas-Marcos
PM
,
Rubio
MA
,
Kreskshi
WI
,
Cabrerizo
L
,
Sanchez-Pernaute
A
.
Severe hypocalcemia following total thyroidectomy after biliopancreatic diversion
.
Obes Surg
2005
;
15
:
431
–
434

Google Scholar

Crossref
Search ADS
PubMed

 
33

Zaarour
M
,
Zaharia
R
,
Bretault
M
,
Jublanc
C
,
De Marcellus
C
,
Bouillot
JL
et al.
Laparoscopic revision of bariatric surgeries in two patients with severe resistant hypocalcemia after endocrine cervical surgery
.
Obes Surg
2020
;
30
:
1616
–
1620

Google Scholar

Crossref
Search ADS
PubMed

 
34

Alfonso
B
,
Jacobson
AS
,
Alon
EE
,
Via
MA
.
Previous gastric bypass surgery complicating total thyroidectomy
.
Ear Nose Throat J
2015
;
94
:
E12
–
E16

Google Scholar

PubMed
OpenURL Placeholder Text

 
35

Gross
JA
,
Olsen
SM
,
Koch
CA
,
Moore
EJ
.
Severe symptomatic hypocalcemia following total thyroidectomy in a patient with a history of Roux-en-Y gastric bypass surgery
.
Ear Nose Throat J
2014
;
93
:
E6
–
E11

Google Scholar

PubMed
OpenURL Placeholder Text

 
36

Salinger
EM
,
Moore
JT
.
Profound hypocalcemia after near-total thyroidectomy in a Roux-en-Y gastric bypass patient
.
Am Surg
2010
;
76
:
E7
–
E8

Google Scholar

Crossref
Search ADS
PubMed

 
37

Vemuri
SR
,
Koganti
SB
,
Mukerji
A
,
Razi
S
,
Shah
A
,
Gilchrist
BF
.
Recalcitrant hypocalcemia after thyroidectomy in patients post sleeve gastrectomy—challenges in management
.
Am Surg
2015
;
81
:
E426
–
E427

Google Scholar

Crossref
Search ADS
PubMed

 
38

Desogus
D
,
Menon
V
,
Singhal
R
,
Oyebode
O
.
An examination of who is eligible and who is receiving bariatric surgery in England: secondary analysis of the health survey for England dataset
.
Obes Surg
2019
;
29
:
3246
–
3251

Google Scholar

Crossref
Search ADS
PubMed

 
39

Noel
CW
,
Griffiths
R
,
Siu
J
,
Forner
D
,
Urbach
D
,
Freeman
J
et al.
A population-based analysis of outpatient thyroidectomy: safe and under-utilized
.
Laryngoscope
2021
;
131
:
2625
–
2633

Google Scholar

Crossref
Search ADS
PubMed

 
40

Corbeels
K
,
Verlinden
L
,
Lannoo
M
,
Simoens
C
,
Matthys
C
,
Verstuyf
A
et al.
Thin bones: vitamin D and calcium handling after bariatric surgery
.
Bone Rep
2018
;
8
:
57
–
63

Google Scholar

Crossref
Search ADS
PubMed

 
41

Shah
M
,
Simha
V
,
Garg
A
.
Review: long-term impact of bariatric surgery on body weight, comorbidities, and nutritional status
.
J Clin Endocrinol Metab
2006
;
91
:
4223
–
4231

Google Scholar

Crossref
Search ADS
PubMed

 
42

Slater
GH
,
Ren
CJ
,
Siegel
N
,
Williams
T
,
Barr
D
,
Wolfe
B
et al.
Serum fat-soluble vitamin deficiency and abnormal calcium metabolism after malabsorptive bariatric surgery
.
J Gastrointest Surg
2004
;
8
:
48
–
55

Google Scholar

Crossref
Search ADS
PubMed

 
43

Orloff
LA
,
Wiseman
SM
,
Bernet
VJ
,
Fahey
TJ
III,
Shaha
AR
,
Shindo
ML
et al.
American Thyroid Association Statement on postoperative hypoparathyroidism: diagnosis, prevention, and management in adults
.
Thyroid
2018
;
28
:
830
–
841

Google Scholar

Crossref
Search ADS
PubMed

 
44

Edafe
O
,
Antakia
R
,
Laskar
N
,
Uttley
L
,
Balasubramanian
SP
.
Systematic review and meta-analysis of predictors of post-thyroidectomy hypocalcaemia
.
Br J Surg
2014
;
101
:
307
–
320

Google Scholar

Crossref
Search ADS
PubMed

 
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Topic:
Subject
General Surgery
Issue Section:
Systematic review
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