ORIGINAL RESEARCH |
https://doi.org/10.5005/jp-journals-10002-1454 |
Exploring the Presence of Risk Factors for Developing Hypocalcemia after Thyroid Surgery: A Descriptive Cross-sectional Study in Jordan
1–6Department of General Surgery, Faculty of Medicine, The University of Jordan, Amman, Jordan
Corresponding Author: Ayman A Mismar, Department of General Surgery, Faculty of Medicine, The University of Jordan, Amman, Jordan, Phone: +962799060822, e-mail: aymanmismar@yahoo.com
Received on: 25 December 2022; Accepted on: 28 August 2023; Published on: 30 October 2023
ABSTRACT
Aim: In our study, we aim to identify the presence of certain risk factors for developing hypocalcemia among patients who underwent thyroid surgery at Jordan University Hospital (JUH) to help endocrine surgeons improve the clinical outcomes of their patients.
Materials and methods: We conducted a cross-sectional, descriptive study at JUH located in Amman, Jordan. Our sample included 200 patients who underwent thyroid surgery at JUH over 2 years (2017–2018). We collected data retrospectively from the medical electronic files of patients. The studied factors included age, gender, comorbidities, surgery type, thyroid pathological results, cervical lymph node dissection, incidental removal of parathyroid glands, and preoperative and postoperative calcium and phosphorus levels. Hypocalcemia was defined as serum calcium level <8 mg/dL or the presence of its signs and symptoms. It was categorized into transient hypocalcemia (early and late) and permanent hypocalcemia. We applied descriptive statistics including charts, frequencies, and percentages.
Results: Hypocalcemia was detected in 19 (9.5%) patients out of 200 postoperatively, from which 16 presented with transient hypocalcemia and three presented with permanent hypocalcemia. Around 16 patients out of 19 were females and only three were males. Total thyroidectomy constituted 68.4% of their surgical operations. Papillary carcinoma was the most common thyroid pathology followed by multinodular goiter. Three out of 12 patients who had central lymph node dissection experienced hypocalcemia.
Conclusion: Important risk factors were present among patients who developed hypocalcemia after thyroid surgery at JUH. Our study helps in determining the high-risk groups of patients and constitutes the basis for further studies in our region.
Clinical significance: Our study draws the attention of endocrine surgeons in our region to take more precautions among patients presenting with risk factors for developing hypocalcemia to help them avoid this complication after thyroidectomy.
How to cite this article: Baki JO, Haimour HN, Al-omoush EA, et al. Exploring the Presence of Risk Factors for Developing Hypocalcemia after Thyroid Surgery: A Descriptive Cross-sectional Study in Jordan. World J Endoc Surg 2023;15(2):34–39.
Source of support: Nil
Conflict of interest: None
Keywords: Hypocalcemia, Risk factors, Thyroidectomy
INTRODUCTION
Thyroidectomy is a commonly performed procedure in surgical units worldwide. It is indicated when thyroid goiter starts causing obstructive symptoms or cosmetic problems.1 Patients with suspected thyroid tumors undergo thyroidectomy to rule out the presence of an ongoing neoplastic process. Furthermore, patients presenting with hyperthyroidism occasionally need thyroid gland removal.1 It has been reported in the literature that decreased serum calcium and recurrent laryngeal nerve injury are the most common complications of thyroid surgeries.2
Postoperative hypocalcemia is most likely caused by injury, devascularization, venous drainage obstruction, or unintentional removal of a single parathyroid gland or more during surgery resulting in hypoparathyroidism.3,4 Depending on the severity of the parathyroid glands’ injury, hypocalcemia can manifest as either transient hypocalcemia lasting for several months or permanent hypocalcemia which persists much longer imposing a greater burden on patients regarding treatment with calcium and vitamin D.5 Other factors including acute elevation in calcitonin, hungry bone syndrome, and vitamin D deficiency can further contribute to the decline of serum calcium postthyroidectomy.6,7
Studies reported different ranges of hypocalcemia following thyroid surgery; 6–30% of patients usually present with transient hypocalcemia,8,9 whereas the rate of permanent hypocalcemia among them usually does not exceed 2%.10,11 The presence of signs and symptoms characteristic of hypocalcemia besides the prolongation of hospitalization time due to the need for frequent laboratory testing and observation indicates how negatively hypocalcemia affects the patient’s quality of life as well as the healthcare system.12,13
Different studies14-16 have been conducted all over the world to define possible risk factors for developing hypocalcemia after thyroid surgery. Our aim in this study is to identify the presence of these risk factors among patients who underwent thyroidectomy at Jordan University Hospital (JUH). Our study highlights the importance of determining the high-risk groups of patients in order to help endocrine surgeons and other healthcare providers take more precautions to avoid this complication and reduce the load on the healthcare system.
MATERIALS AND METHODS
We conducted a cross-sectional, descriptive study on a 200-patient sample in JUH which is a teaching hospital located in Amman, Jordan. The approval of our study was obtained from the Deanship of Scientific Research at the University of Jordan and from the review board in JUH. Inclusion criteria included patients of all age-groups who were admitted to JUH to undergo thyroid surgery during the period starting from January 2017 to December 2018 and followed up in the endocrine surgery clinic for >6 months postoperatively. Exclusion criteria included patients who were diagnosed with primary parathyroid disorders.
We collected the required data retrospectively from the electronic medical files of patients in the hospital database. The data included age, gender, type of surgery, thyroid pathological result, and comorbidities of the patients. Regarding laboratory results, we recorded preoperative measurements of serum calcium (mg/dL) as well as the levels of postoperative serum calcium measured at 24, 48, and 48 hours to 6 months and after 6 months of surgery. We also recorded preoperative levels of serum phosphorus (mg/dL) and postoperative serum phosphorus measured at 24- and 48-hours following surgery. We registered the type of cervical lymph node dissection including central, lateral or both types of dissection. We further searched for the presence of parathyroid tissue in the histopathology of resected specimens. We lastly collected the prescriptions for calcium and vitamin D given to patients after the operation. We maintained the confidentiality of patients as we labeled the record of each patient with a certain number to refer to in data revision.
Hypocalcemia was defined based on our institution as serum calcium level below 8 mg/dL or the presence of characteristic signs and symptoms of hypocalcemia including paresthesia in distal extremities, perioral numbness, tetany, and Chvostek’s sign. Hypocalcemia which occurred within 24 hours following thyroidectomy was defined as early transient hypocalcemia,15 whereas hypocalcemia which presented from 48 hours to 6 months after thyroid surgery was labeled as late transient hypocalcemia. When hypocalcemia persisted beyond 6 months of surgery, it was considered to be permanent hypocalcemia.17,18 Data was recorded in a Microsoft Excel Worksheet using descriptive statistics illustrated as charts, percentages, and frequencies.
RESULTS
The sample included a total of 200 patients of whom 48 (24%) were males and 152 (76%) were females. The age of patients in the sample ranged from 17 to 80 years with a mean age of 45.4 years (Fig. 1). Regarding the type of surgery, total thyroidectomy was conducted in 77 (38.5%) patients, hemithyroidectomy in 76 (38%) patients, near total and completion thyroidectomies in 17 (8.5%), and 16 (8%) patients, respectively. Around 10 patients underwent subtotal thyroidectomy, three had a redo surgical operation, and only one patient underwent isthmectomy. Among the recorded comorbidities in our sample, hypertension and diabetes mellitus had the highest frequencies followed by rheumatoid arthritis.
Fig. 1: The distribution of all studied patients according to age-group
Regarding pathological reports, thyroid pathological results of the whole sample are illustrated in Table 1. The pathological sections of 28 (14%) patients out of 200 patients revealed parathyroid tissue. We found that central lymph node dissection was conducted in 12 (6%) patients, lateral dissection in two (1%) patients, and both types of dissection in 10 (5%) patients according to their primary pathology. There was also a total of 44 patients whose specimens contained one to five lymph nodes dissected for sampling purposes.
| Pathological result | Number | Percentage (%) |
|---|---|---|
| Papillary carcinoma | 74 | 37 |
| Multinodular goiter | 62 | 31 |
| Follicular adenoma | 13 | 6.5 |
| Goitrous nodule | 10 | 5 |
| Adenomatoid hyperplasia | 8 | 4 |
| Hashimoto thyroiditis | 5 | 2.5 |
| Lymphocytic thyroiditis | 4 | 2 |
| Hyperplastic nodule | 4 | 2 |
| Follicular carcinoma | 3 | 1.5 |
| Thyroiditis | 3 | 1.5 |
| Grave’s thyroiditis | 3 | 1.5 |
| Hürthle cell adenoma | 3 | 1.5 |
| Diffuse goiter | 2 | 1 |
| Cyst | 2 | 1 |
| B-cell lymphoma | 1 | 0.5 |
| Benign colloid nodule | 1 | 0.5 |
| Medullary carcinoma | 1 | 0.5 |
| NIFTP* | 1 | 0.5 |
*NIFTP, noninvasive follicular neoplasm with papillary-like nuclear features
A total of 19 patients out of 200 patients presented with hypocalcemia after thyroidectomy; 16 patients had transient hypocalcemia including six patients with early transient hypocalcemia, three patients with late transient hypocalcemia, and seven patients manifested as both early and late transient hypocalcemia. The remaining three patients presented with permanent hypocalcemia. Figure 2 demonstrates calcium levels among patients who experienced postoperative hypocalcemia. Calcium was measured preoperatively and postoperatively at 24, 48, and 48 hours to 6 months and after 6 months of surgery (Fig. 2).
Fig. 2: Calcium laboratory levels (mg/dL) in patients who developed hypocalcemia
Out of the 19 patients who had hypocalcemia, 16 patients were females, and only three were males. Figure 3 demonstrates the type of surgery among these patients in which total thyroidectomy recorded the highest percentage followed by completion thyroidectomy. Regarding thyroid pathological results, papillary carcinoma was found in 10 patients followed by multinodular goiter found in five patients (Fig. 4).
Fig. 3: Type of surgery in patients who developed hypocalcemia
Fig. 4: Thyroid pathological results in patients who developed hypocalcemia
Serum phosphorus levels were measured preoperatively and at 24 and 48 hours postsurgery. Five female patients had increased phosphorus levels during the first 48 hours postthyroidectomy. Calcium and vitamin D supplements were prescribed to patients postoperatively. To sum up our findings, Table 2 illustrates the changes in postoperative calcium levels according to the presence of the studied factors.
| Variable | Number | Early TH* (n = 6) no. (%) | Late TH* (n = 3) no. (%) | Early + late TH* (n = 7) no. (%) | PH* (n = 3) no. (%) |
|---|---|---|---|---|---|
| Age | |||||
| ≥40 | 139 | 4 (2.8) | 3 (2.1) | 5 (3.5) | 2 (1.4) |
| <40 | 61 | 2 (3.2) | 0 (0) | 2 (3.2) | 1 (1.6) |
| Gender | |||||
| Male | 48 | 1 (2.08) | 2 (4.1) | 0 (0) | 0 (0) |
| Female | 152 | 5 (3.2) | 1 (0.65) | 7 (4.6) | 3 (1.9) |
| Type of surgery | |||||
| Total thyroidectomy | 77 | 3 (3.8) | 2 (2.5) | 6 (7.7) | 2 (2.5) |
| Completion | 16 | 1 (6.25) | 0 (0) | 1 (6.25) | 1 (6.25) |
| Hemithyroidectomy | 76 | 2 (2.6) | 0 (0) | 0 (0) | 0 (0) |
| Redo | 3 | 0 (0) | 1(33.33) | 0 (0) | 0 (0) |
| Thyroid pathology | |||||
| Papillary CA** | 74 | 3 (4.05) | 1 (1.3) | 4 (5.4) | 2 (2.7) |
| Multinodular goiter | 62 | 1 (1.6) | 1 (1.6) | 3 (4.8) | 0 (0) |
| Follicular CA** | 3 | 00 | 1 (3.33) | 00 | 00 |
| Other | 61 | 2 (3.2) | 0 (0) | 0 (0) | 1 (1.6) |
| Comorbidity | |||||
| DM*** | 44 | 1 (2.27) | 0 (0) | 2 (4.54) | 1 (2.27) |
| HTN*** | 58 | 1 (1.7) | 1 (1.7) | 2 (3.4) | 1 (1.7) |
| Grave’s | 10 | 0 (0) | 0 (0) | 2 (20) | 1 (10) |
| Hashimoto | 4 | 1 (25) | 0 (0) | 0 (0) | 0 (0) |
| Parathyroid in histopathology | |||||
| Yes | 28 | 2 (7.14) | 1 (3.57) | 0 (0) | 0 (0) |
| No | 172 | 4 (2.32) | 2 (1.16) | 7 (4.06) | 3 (1.7) |
| Lymph nodes dissection | |||||
| Central | 12 | 1 (8.3) | 0 (0) | 2 (16.6) | 0 (0) |
| Central and lateral | 10 | 1 (10) | 0 (0) | 0 (0) | 0 (0) |
| One sampling lymph node | 32 | 0 (0) | 0 (0) | 2 (6.25) | 1 (3.12) |
*TH, transient hypocalcemia; **CA, carcinoma; ***DM, diabetes mellitus; HTN, hypertension; PH, permanent hypocalcemia
DISCUSSION
Our results indicated that most patients who developed postoperative hypocalcemia underwent total thyroidectomy. Thyroid surgical procedures vary according to their indications; subtotal thyroidectomy is sometimes preferred to total thyroidectomy as it provides more protection to the parathyroid glands, recurrent laryngeal nerve, and other surrounding structures.19,20 A study by Lale et al.21 emphasized that the more extended the surgery area is, the higher the risk of developing hypocalcemia is postoperatively. According to Caglià et al.,22 another risk factor of hypocalcemia is the redo thyroid operation which was indeed found to be present in one patient in our results.
Most patients who experienced postoperative hypocalcemia in our study were females. Several studies in the literature15,21,23 confirmed that being a female is considered a significant risk factor for hypocalcemia after thyroidectomy. Many causes contribute to this gender disparity including the higher parathyroid weight in men compared to that in women,23 the effect of sex hormones on the secretion of parathyroid hormone (PTH), and the narrow operative field in women raising the probability of trauma to the parathyroid glands.24 However, we should take into consideration the high number of female patients in our sample, probably resulting in the increased risk of developing hypocalcemia in this gender. According to a study done by Docimo et al.,25 female gender was found to be a significant risk factor in univariate analyzes, whereas it had no significance in multivariate analyzes.
A wide range of ages was noted among them starting from 27 to 80 with a mean age estimated as 47.6 years. There is a debate in the literature about its association with hypocalcemia. Thomusch et al.26 concluded that advanced age triggers permanent hypocalcemia; other studies14,27 stated that younger age is associated with this complication. However, no association was found between age and decreased serum calcium postthyroidectomy according to a prospective study done by Khazaeni and Mousavi.28
Our pathological reports indicated a dominance of malignant histological findings followed by multinodular goiter. Regarding thyroid histopathology, different studies14,21,29 demonstrated the increased risk of hypocalcemia when malignancy is diagnosed. This is mostly attributed to the usual aggressive approach applied by surgeons to resect malignant tumors which invade the thyroid’s capsule, resulting in ischemic injuries or unwanted parathyroidectomies.21,30 According to another retrospective study in Jordan,31 most patients who experienced hypocalcemia after thyroidectomy had benign thyroid diseases. Regarding cervical lymph node dissection, it was concluded by Wang et al.32 that transient and permanent hypocalcemia’s are increased by 2.36 and 5.22-folds, respectively when central lymph node dissection is performed. On the contrary, our results indicated that three patients who had central lymph node dissection developed only transient hypocalcemia without persisting to the permanent type. A retrospective study which was conducted on a sample of the Chinese population17 confirmed the increased incidence of hypoparathyroidism when lateral lymph node dissection is performed, attributing the cause to the fragility of parathyroids’ blood vessels. In the study of Cho et al.,14 parathyroid glands were detected in the permanent histopathological sections in 23.6% of patients who developed hypocalcemia after total thyroidectomy. However, 10% of patients who had normal calcium levels after surgery in the same study had parathyroid tissue in their pathological sections.14 This phenomenon could be probably explained by compensation of the other remaining parathyroid glands depending on their vascular condition.14 This is consistent with our findings in which normal postoperative calcium levels were recorded in 25 patients out of 28 patients who had incidental removal of parathyroid glands during surgery.
Regarding comorbidities, we detected decreased postoperative serum calcium levels in four cases of diabetes mellitus, three cases of Grave’s disease, and one case of Hashimoto thyroiditis. Similar studies in literature highlighted the effect of comorbidities on developing hypocalcemia after thyroidectomy. For instance, diabetes mellitus was considered a risk factor due to the increased susceptibility of parathyroid hypoxia as a result of small vessel disease.33,34 Grave’s disease and Hashimoto thyroiditis similarly increase the risk of hypocalcemia because of the autoimmune etiology of both diseases, leading to thrombosis of parathyroid arteries followed by the occurrence of intraoperative ischemic injury.35,36 In addition, active thyroid eye disease manifesting in Grave’s increases the chance of hypocalcemia postsurgery.35,36
Regarding the increase in postoperative serum phosphorus levels recorded in our results, it was found to be an important predictive factor of developing hypocalcemia as illustrated by Pattou et al.37
We eventually discovered the presence of signs and symptoms of hypocalcemia in eight patients out of 19, six of them had transient hypocalcemia, and two patients had permanent hypocalcemia. Perioral numbness and paresthesia in the distal extremities recorded the highest frequencies followed by tetany and Chvostek’s sign with lower frequencies. To understand the cause of the occurrence of decreased serum calcium level and its associated signs and symptoms postthyroidectomy, the study of Thomusch et al.26 stated that the technique of inferior thyroid artery ligation was found to be a strong determinant of the development of hypocalcemia. The presence of characteristic signs and symptoms of this complication depends on how rapid the decline of PTH levels is following excision or trauma to the parathyroid glands.38,39 Calcium and vitamin D supplements were prescribed to patients postoperatively to reduce the occurrence of hypocalcemia after thyroid surgery corresponding to the results of a study conducted by Bellantone et al.40
Our study was limited by the small sample size which may not be representative of all patients who underwent thyroidectomy in Jordan. Since the number of patients who developed hypocalcemia was small, no statistical significance of the studied factors could be elicited, necessitating the application of descriptive statistics.
CONCLUSION
Our findings identified the presence of certain risk factors that contribute to developing hypocalcemia after undergoing thyroidectomy in JUH. This study helps in identifying the high-risk groups of patients and constitutes the basis for further analytical studies in the future.
Clinical Significance
Since there is a lack of similar research in our region, our study highlights commonly presenting risk factors for developing hypocalcemia after undergoing thyroidectomy in our institution. Identifying the high-risk groups of patients helps endocrine surgeons and healthcare providers take more intraoperative precautions to identify and protect parathyroid glands in addition to prescribing postoperative prophylactic calcium and vitamin D to avoid this complication in these patients.
ORCID
Joud O Baki https://orcid.org/0000-0001-9794-6879
Hana N Haimour https://orcid.org/0000-0002-3625-2264
Eman A Al-omoush https://orcid.org/0000-0001-8770-9538
Mohammad E Salameh https://orcid.org/0000-0001-8240-3994
Khaled S Jabaiti https://orcid.org/0000-0002-4520-2912
Ayman A Mismar https://orcid.org/0000-0002-2949-7597
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