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Address reprint requests and correspondence: Mira Milas, MD, Department of Endocrine Surgery, Cleveland Clinic, 9500 Euclid Ave/A80, Cleveland, OH 44195
In recent years, there has been considerable interest in unilateral parathyroid surgery with the goals of achieving high cure rates of hyperparathyroidism but accomplishing this with perhaps shorter operative times, fewer complications, and better cosmesis than associated with traditional bilateral exploration. Although limited parathyroid exploration has had demonstrated success in selected patients, clear indications still exist for evaluating all 4 parathyroids by bilateral neck exploration. This article describes our technique and the pre- and intraoperative contexts warranting bilateral parathyroid exploration.
Bilateral parathyroid exploration (BE) with identification of all 4 glands and excision of abnormally enlarged glands has been the standard treatment for primary hyperparathyroidism (PHPT), with a 95% long-term cure rates. BE is also the surgical treatment for hyperparathyroidism associated with renal failure or renal transplantation (secondary and tertiary hyperparathyroidism; SHPT and THPT, respectively). The knowledge gained from exploration of all 4 parathyroid glands has contributed to the understanding of disease patterns (single- versus multiple-gland hyperplasia), the appreciation of abnormal parathyroid morphology, and the finesse of surgical approaches required to address challenging and ectopic parathyroid abnormalities. As recently as 10 years ago, BE was the preferred surgical approach by 90% of parathyroid surgeons, whereas currently 10% of surgeons practice BE exclusively and another 22% practice BE in combination with more limited explorations (LE).
The advent of new technologies such as 99-technetium-sestamibi scans (MIBI), radioguided, laparoscopic and videoscopic surgery, and intraoperative parathyroid hormone (PTH) monitoring have allowed the transition to an era in which LE is the preferred initial choice of surgery for hyperparathyroidism (HPT). Whether focal (examining only 1 parathyroid gland) or unilateral (examining both glands on the same side), with LE surgeons seek to identify solitary adenomas and end the operation with confirmation of a biochemical cure based on a decrease in the intraoperative PTH level. It is important to understand, however, that the success of LE is contingent on the following factors: underlying incidence of multiple gland disease, accuracy of imaging studies to predict single gland disease, ability of intraoperative PTH measurement to determine that all pathologic parathyroids have been removed, thoroughness of long-term patient follow-up to detect recurrences, and balance between proposed benefits of LE measured against reasonably acceptable failure rates. With careful selection criteria based on preoperative imaging, several studies have reported the success of LE with short- and long-term results similar to the conventional bilateral approach.
However, even in these studies, patients initially scheduled for LE require conversion to BE based on intraoperative findings and others have unhelpful preoperative localization of disease. Overall, most studies report that only 70% of patients with PHPT are found to be candidates for LE.
Predicting the success of limited exploration for primary hyperparathyroidism using ultrasound, sestamibi, and intraoperative parathyroid hormone: Analysis of 1158 cases.
Thus, the need for familiarity and proficiency with BE will continue to be essential for surgical management of HPT.
Indications
Based on the disease process
Because multigland hyperplasia is the underlying biology of disease in patients with familial PHPT (for example, MEN1 and MEN 2 syndromes) and SHPT and THPT, BE is the advised approach for first-time parathyroid surgery in these cases. BE should also be strongly considered for patients with history of head and neck radiation and lithium-induced hyperparathyroidism and for those with coexisting thyroid pathology. Awareness and preoperative diagnosis of thyroid diseases, which can be found in up to 40% of patients with PHPT and include a 4% thyroid cancer incidence, may affect the choice of parathyroid operation.
Accuracy of preoperative localization studies and intraoperative parathyroid hormone assay in patients with primary hyperparathyroidism and double adenoma.
MIBI scans are widely appreciated to poorly predict multigland disease and often are entirely negative even in the presence of large parathyroid glands in patients with multigland hyperplasia.
Surgeon-performed ultrasound (US) is becoming an increasingly useful tool in the surgical evaluation of HPT. It is our practice to perform US in the office on every patient with HPT at the time of their first evaluation. In addition to the central neck and thyroid region, US is used to scan the lateral neck to exclude ectopic parathyroids along the carotid/jugular chain. US is not without its own limitations. Ectopic glands in other locations, especially those located in retroesophageal, intrathymic, and mediastinal spaces, are harder to image. For PHPT more than for SHPT patients, multigland hyperplasia again poses difficulty for the surgeon in identifying all abnormal glands because they tend to be smaller than single adenomas. However, US is the best preoperative imaging modality to allow clear evaluation of the thyroid and diagnose disease that may also require thyroid surgery. An ectopic or intrathyroidal parathyroid suspected on US can be biopsied and the aspirate sent for both cytology and PTH measurement.
Negative, discordant, or unclear localizations by MIBI or US during preoperative evaluation are indications for BE. Even if focal exploration is initially planned, these are the patients most likely to prompt conversion to BE intraoperatively.
Based on intraoperative findings
Certain findings during an operation should bring consideration for BE. One of the most significant contributions to parathyroid surgery has been the introduction of intraoperative PTH measurement. Although a number of guidelines exist, the one most frequently used advocates conversion to BE if intraoperative PTH levels measured 10 minutes after excision of the suspected adenoma fail to decrease by 50% from pre-excision levels.
Although it is most feasible to proceed with identification of the ipsilateral gland initially, approximately 75% of second adenomas will be contralateral (Figure 1).
Figure 1Distribution of double parathyroid adenomas reveals a nonrandom pattern where the majority of parathyroid abnormalities are bilateral, and the largest single pattern involves enlargement of both upper parathyroid glands.
Unusually small adenoma size should also raise suspicion for multigland disease. Some studies have suggested a correlation of preoperative calcium and PTH values with weight and/or volume of single parathyroid adenomas.
Although these are not uniformly reliable predictors, a very small abnormal parathyroid, especially in the face of more severe HPT disease manifestation, must at least prompt caution to evaluate again all information (including PTH decrease), and consider the possibility of additional abnormal glands before concluding any LE.
Technique
Anatomy
To perform a safe and effective BE, a thorough understanding of both normal and ectopic parathyroid anatomy is essential. The upper and lower parathyroid glands develop embryologically from the fourth and the third branchial pouches, respectively. They migrate caudally along with the development of the thyroid (superior gland) and the thymus (inferior gland). Four glands are present in the majority of people; however, in autopsy reports, up to 13% of people have more than 4 and 3% have fewer than 4 parathyroids.
The upper parathyroid glands are fairly reliably positioned in the posterior perithyroidal fat, behind the superior pole of the thyroid and near the path of the recurrent laryngeal nerve as it enters the cricothyroid muscle. The lower parathyroid glands cluster around the inferior pole vessels of the thyroid close to the thymic tissue. Both glands usually obtain their blood supply from branches of the inferior thyroid artery. In relation to this artery, the lower parathyroids are more inferior (caudal), anterior, and medial, whereas the upper parathyroids are positioned superior (cranial) and deep to its axis. An unusual branching pattern of the inferior thyroid artery or extra branches visible along its main trunk can also alert to possible ectopic parathyroids located at the end of those branches, often at distances away from the thyroid. There is considerable symmetry between the locations on the right and left and sides, which helps to guide the BE.
Ectopic glands occur from disrupted migration during embryological development. The distribution of ectopic or supernumerary glands is shown in Figure 2.
As the upper parathyroid gland migrates with the thyroid, it can become embedded within the ipsilateral lobe of the thyroid. Additionally, the upper parathyroid can arrest migration along a path in retropharyngeal, retrolaryngeal, retroesophageal, and posterior mediastinal positions. The retroesophageal position is perhaps most frequently missed during surgery as the parathyroid sinks deeply below the usual plane of exploration and can be located along the anterior cervical spine.
Figure 2Ectopic parathyroid glands can be located along a broad spectrum of cervical and mediastinal regions. Awareness of these patterns and their frequency of occurrence at each site may help guide bilateral neck exploration in challenging cases of hyperparathyroidism.
The lower parathyroid glands have a longer, less fixed migratory path and have slightly more variable positions. Ectopic locations occur most commonly within the thymus, but also anywhere in high cervical locations, along the carotid sheath, and in the anterior mediastinum.
Surgery
The patient is brought to the operating room and positioned on the table with a small beanbag in place under the shoulders. Once the patient is intubated with the endotracheal tube taped, both arms are tucked along the patient's side. A hand is then placed behind the beanbag between the scapulae for elevation and the suction is applied to the beanbag for fixation. Alternatively a scapular roll can be used. The head is placed on enough foam to extend the neck gently and avoid the head hanging without support. The bed is then flexed to open up the angle of the neck even further. While the patient was still awake and sitting in the preoperative area, potential cosmetic locations of skin incisions were marked, as these can move and become less visible once the patient is supine.
In preparation for parathyroidectomy, all of our patients have undergone a clinic-based US by the surgeon as discussed previously. After the patient is positioned appropriately in the operating room, the US is repeated to confirm the suspected location of the parathyroid abnormality and to help correlate the position of the incision to the isthmus. Additionally this localizes the abnormal parathyroid gland with the patient in operative position, since the glands, especially lower ones, can move variably with positioning. The laboratory is then alerted to ensure availability and calibration of the PTH machine. No preoperative antibiotics are given because this is a clean case and wound infections are a remote risk. The exception occurs in reoperative cases where antibiotics are administered.
We use chlorhexidine for sterile prep because this avoids potential irritation and staining of the face and neck. We use a 2.5-cm midline incision positioned near the isthmus within a natural crease in the neck for optimal cosmesis. A larger incision, if needed for safe and adequate exposure, should always be made according to surgical judgment. The incision is carried down by electrocautery through the platysma muscle to the plane just above the anterior jugular veins, which are carefully preserved. Subplatysmal flaps are then created superiorly toward the thyroid cartilage and inferiorly toward the sternal notch. These flaps allow for optimal exposure through the small incision by increasing the ease of retraction.
The midline raphe of the strap muscles is then opened vertically along the midline to expose and separate the muscles. The strap muscles are not cut. Dissection is started on the side of the pathology suggested by the preoperative imaging. The sternohyoid muscle is separated from the sternothyroid a short distance, again to aid in mobility for lateral retraction of the incision for exposure. The loose areolar attachments of the sternothyroid muscle to the thyroid are taken down with cautery at low settings or blunt dissection. Very fine instruments are used, a small retractor is inserted, and a peanut gently moves the thyroid medially (Figure 3).
Figure 3Bilateral neck exploration can be performed safely with the use of very few, simple and delicate instruments. (Color version of figure is available online.)
The abnormal gland is then identified, beginning in the area suggested by the preoperative imaging. If imaging is negative, the area of the lower parathyroid is exposed first because it is more accessible and the search is begun at the inferior pole vessels, looking and feeling for an area of fullness. Often the eye is drawn to areas of plump-appearing fatty tissue. Careful blunt dissection is done using a fine curved hemostat to separate this fatty tissue looking for subtle color changes (darker orange to brown) of the parathyroid gland (Figure 4). The exposure of the upper parathyroid usually requires a greater degree of medial rotation of the thyroid lobe to facilitate examination of the posterior surface of the thyroid. The aim is to identify fatty tissue along the posterior, upper edge of the thyroid pole, or between the upper pole and the insertion of the inferior thyroid artery into the thyroid. A normal parathyroid will often have a leaf-like vascular pattern absent in simple fat or thymus (Figure 5).
Figure 4Detecting subtle changes in color alerts to the identification of both normal and abnormal parathyroid glands below areolar tissue, which should be exposed with minimal dissection of surrounding tissue planes. This illustration of a normal parathyroid is taken during a thyroid procedure for better demonstration. (Color version of figure is available online.)
Once the pathologic gland or glands are identified, a pre-excision rapid intact PTH sample is drawn. Our preferred method is from the anterior jugular veins. If these are too small in caliber or difficult to access, they can be augmented with a Valsalva maneuver by the anesthesiologist. The puncture defect is grasped with a forceps and cauterized. Alternatively, the sample can be drawn directly from the internal jugular vein by the surgeon or peripheral vein by the anesthesiologist. This sample, drawn after mobilization but immediately before excision, gives the most accurate baseline as manipulation of the glands can cause PTH hormone release and skew a pre-excision measurement against which the 50% decrease is interpreted. When the gland is ready to be excised, the vascular pedicle is ligated to release the gland and pass it off as a specimen. In BE performed when a single adenoma has been identified or is strongly suspected, the abnormal gland is removed first then dissection continues to view the normal parathyroids while awaiting PTH results. In BE for suspected or known hyperplasia, the dissection continues to identify the remaining abnormal glands before excision of any one of them. A postexcision level can be drawn 10 minutes after excision of the last abnormal parathyroid.
An ipsilateral gland should be located next. The usual positions of the upper parathyroids should be evaluated as described above, with further mobilization of the thyroid guided by the need for better visualization. Again, purposeful observation of what is already visible in the operative field is more effective than blind dissection. Look for the subtle concentrations of fat on or near the thyroid capsule, and in the tracheo-esophageal groove. Identify the inferior thyroid artery to have a frame of reference. Care should be taken to stay close to the thyroid to avoid injury to the recurrent laryngeal nerve (RLN). The nerve does not have to be exposed as part of BE dissection, although its presence in the vicinity should always be considered and careful dissection performed if needed along its anatomical path. If the RLN is visible or exposed, it is not necessary to skeletonize it free of surrounding tissue, only reveal it enough to ensure its safety during further dissection. This will help prevent inadvertent injury during excision of the parathyroid. RLN exposure is more crucial when imaging studies or intraoperative findings reveal glands in the tracheoesophageal groove or retroesophageal spaces, where the nerve can be displaced in any direction surrounding an adenoma.
If a pathological gland (“A”) is found in a more mid-lower location on the thyroid, and an upper gland cannot be found, consideration should be given that gland “A” is actually a descended upper parathyroid and further investigation directed to find a lower gland. If one or both of the glands cannot be identified at this point, the process is repeated on the contralateral side. Keep in mind the symmetry of the parathyroids to help localize the contralateral glands. In addition, if a parathyroid was not found on the first side explored, identification on the contralateral side may help on re-exploration of the first side. Thus, identification of the 4 glands expected at the usual anatomical regions along the thyroid can constitute a “primary parathyroid survey” during BE (Figure 6).
Figure 6Primary parathyroid survey: examination for presence of multigland hyperplasia along the usual anatomical regions of distribution of upper and lower parathyroid glands.
If any of the 4 glands cannot be identified, then further dissection is required, if the missing parathyroid is thought to be abnormal. This “secondary survey” of the dissection is more involved and potentially disrupts more surgical planes, thus should be embarked on logically and strategically, starting on the side of the missing abnormal parathyroid. It is not performed just to locate a normal parathyroid. The thymus should be identified and retracted out of the mediastinum as far as possible without avulsion (Figure 7A). This should be carefully inspected and palpated for an abnormal gland, and removed. Additional mobilization of the thyroid with ligation of the middle thyroid vein if present can provide better exposure, with further medial and anterior rotation. This will aid in inspecting the entire length of the tracheoesophageal groove and if needed, the retroesophageal space (Figure 7B). If an upper gland is still not found, taking down the superior pole vessels of the thyroid can be done without devascularization of the thyroid. This provides increased mobility and occasionally the superior gland (Figure 7C) is found in this manner. The carotid sheath should be opened next and inspected for as long a distance as the skin incision will allow as this is a lower yield ectopic position (Figure 7D). If a preoperative ultrasound indicated a potential intrathyroidal parathyroid, this should be noted and dealt with only after all other areas are explored. If no preoperative US was performed, and a thyroid lobe has a palpable nodule, a thyroid lobectomy (Figure 7E) can be performed on the side of a missing abnormal parathyroid. A lobectomy may be justifiable even when no palpable abnormalities exist on the side of the missing parathyroid, but clearly this circumstance is less desirable and potentially avoidable had a preoperative US described a normal thyroid. The skin incision can be enlarged to permit adequate exploration of any of these regions.
Hopefully, the surgeon achieves the goal of identifying all 4 parathyroid glands. Let us consider the situation of 4-gland hyperplasia so that subtotal parathyroidectomy is needed. Some authors describe total parathyroidectomy with autotransplantation into the forearm. For its greater risks of hypocalcemia, this is not our practice and will not be described here. It is helpful first to decide which parathyroid would constitute the best remnant (see comments below). The remnant is ideally created first, so that its viability can be observed longer while the remaining parathyroids are excised. If only 2 or 3 of the 4 glands are abnormal, the abnormal parathyroids are excised while the normal parathyroids can be left in situ without resection and their general location marked with a clip. If fewer than all 4 parathyroids have been identified in a patient with known or suspected multigland hyperplasia, the extent of resection requires careful surgical judgment, and a portion of some parathyroid tissue should remain to avert permanent hypocalcemia (Figure 8). The failure to find an abnormal parathyroid gland does not justify removing normal-appearing parathyroids.
After all glands are identified, the neck is irrigated with sterile water and hemostasis is achieved. Each gland or remnant should be re-evaluated for viability at this point. There may be some bruising to the glands; however, they should otherwise appear healthy. If there is any concern for viability, a normal gland in question can be re-implanted into the ipsilateral sternocleidomastoid muscle (SCM). The strap muscles then platysma are reapproximated with absorbable suture. Our preferred method of skin closure for these small incisions is approximation with a nonabsorbable 3-0 Prolene subcuticular stitch with long tails left in place and the use of surgical glue. Once the patient is extubated, the suture easily pulls through the skin to be removed, leaving the surgical glue in place.
Special considerations
Principles of tissue handling
Bilateral parathyroid surgery follows the general surgical principles of minimizing tissue damage and protecting surrounding structures. The parathyroid gland is very delicate and the capsule can easily be torn. If disrupted, abnormal parathyroid tissue can seed in the neck causing diffuse parathyromatosis that can be difficult to manage. The normal or abnormal parathyroid glands themselves are rarely grasped. Rather, with gentle grasping of the surrounding fatty tissue and circumferential release of the encompassing adventitia, the parathyroid gland should easily “pop” out of the surrounding tissue. The vascular pedicle should be ligated as the last step as this will allow the gland to be mobilized around a fixed structure, facilitating movement away from sensitive structures. This is particularly helpful when dealing with a superior gland with its close association with the RLN. As mentioned previously, vigilance to the potential locations of the RLN and not skeletonizing it will help to protect the blood supply and to avoid injury. Exposing the other normal parathyroid glands to dissection and potential injury or devascularization is theoretical pitfall of BE and one that is exceedingly rare, especially because routine biopsy of normal parathyroid glands is not as universal as was once practiced. Identification of the glands only to the extent that they can be evaluated for size and texture is the most important goal. It is imperative to confirm that the visible normal appearing gland is not just a normal cap of tissue with a large adenoma extending distally (Figure 9). Once the extent of the gland is assessed to be normal, dissection can stop without complete separation from surrounding fatty tissue or its blood supply.
Certain physical findings are characteristic of an abnormal parathyroid gland in size, shape, and texture, and firmness and these can have a considerable degree of variability in multigland hyperplasia (Figure 10). Regardless of size, abnormal glands have a plumper contour and generally darker brown appearance and are less compressible when gently probed. They may have a more generous vascular supply or plexus at their pedicle. They may have irregular, knobby shape and be firm or hard, even to palpation. Irregular shapes may be a rare but normal variation if the other features are normal: yellow to orange or light tan color, soft and compressible, and normal size. It is instructive to be familiar with original literature describing bilateral parathyroid explorations, as the degree of detailed observation of normal versus abnormal patterns and techniques gives important highlights.
A normal parathyroid usually weighs 20 to 50 mg and is up to 7 to 8 mm long. In attempting to determine whether a gland is larger than expected, one can use in vivo measurements to obtain an approximation of weight. Measurements of length (L), width (W), and height (H) without removing the gland estimate the volume of an ellipsoid which correlates with weight in mg (Weight [mg] ≈ L × W × H × 1/2 [mm3]). Except in patients on dialysis who have SHPT, the size of individual parathyroid glands in multigland hyperplasia is smaller than a typical single adenoma (Figure 11).
Figure 11Normal parathyroid glands can have variable and unusual shapes.
This should not be mistaken for hyperplasia. The size of individual abnormal parathyroid glands tends to be different in single adenomas (700 mg), hyperplastic glands from multigland disease of primary hyperparathyroidism (150 mg), and hyperplasia from secondary hyperparathyroidism (1000 mg).
If a normal parathyroid gland has been devascularized, it can be reimplanted into the ipsilateral SCM. Before doing so, a portion should be sent to pathology for frozen section for histological confirmation that it is, in fact, normal parathyroid tissue. This can be done on a fragment as small as 2 to 3 mm. The remaining gland is placed on sterile ice until the end of the case, before closing the incision. The gland is then cut with a 10-blade scalpel into small pieces approximately 1 mm × 1 mm. The SCM is exposed and small pockets are created 1 to 2 cm apart by bluntly separating the muscle fibers. Two or three pieces are placed in each pocket and the pocket is closed with microclips to facilitate identification in case of future re-operation. This same methodology applies to autotranplantation of hyperplastic parathyroid tissue into the nondominant forearm, or other described sites, such as the sternocleidomastoid or anterior chest wall tissue close to the clavicle.
A subtotal parathyroidectomy procedure may be applicable to the treatment of hyperplasia in PHPT, SHPT, and THPT. Remnants are best fashioned from a lower parathyroid since these are generally easier to approach in their more anterior position. A good vascular stalk is important to ensure viability. The remnant should be made first, before the other glands being removed. Remnant size is based on clinical judgment, but about 25 mg for multigland PHPT, and up to 40 mg for SHPT. During the remainder of the excisions, repeated checks on the viability of the remnant should be made in case a second remnant needs to be created. We leave a large clip on the transected edge of the gland to facilitate identification of the remnant in the case of recurrent hyperparathyroidism.
Cryopreservation
Cryopreservation is the process of freezing parathyroid remnants for future reimplantation in the rare case of permanent hypoparathyroidism. Cryopreservation is not immediately available and has to be developed as a protocol at each hospital (only about 20% of academic centers have parathyroid cryopreservation capabilities). Cryopreservation allows more aggressive subtotal resection and a smaller remnant. In the absence of this capability, the surgeon should use judgment about the extent of surgery for multigland hyperplasia to minimize risks of hypocalcemia. To be cryopreserved, a parathyroid gland is partially submitted to pathology for histological evaluation and partially submitted for cryopreservation. These cryo portions are cut into small pieces, again about 1 mm in size and brought into suspension in sterile saline. These portions are labeled from which parathyroid gland they were derived and are sent to the cryopreservation bank. The need to reimplant cryopreserved fragments usually becomes evident within 6 months of surgery if the remaining partial gland becomes nonfunctional.
Summary
Bilateral neck exploration for 4-gland parathyroid evaluation is the required surgical approach in cases of multigland hyperplasia. Thus, this applies obviously to patients with familial hyperparathyroidism and those with SHPT and THPT. It remains the advised treatment of choice when preoperative parathyroid imaging is equivocal, negative or discordant, and when coexisting thyroid pathology warrants a broader evaluation of the central neck. A diagnosis of hyperplasia may be apparent before surgery, or BE may become necessary when findings during limited or unilateral exploration suggest additional diseased glands. Even in the modern era of limited parathyroid surgery, BE is needed in 30% of patients. Ectopic and bilateral parathyroid disease remains difficult to predict reliably before surgery. It should be emphasized that BE can be performed via small incisions and minimal tissue handling. The same principles of safely proceeding with parathyroid exposure and evaluation, gentle tissue handling techniques and knowledge of anatomy apply to both LE and BE approaches. BE requires, however, a more detailed and unique set of skills: familiarity with strategy to expose parathyroids in ectopic sites, knowledgeable assessment of subtle parathyroid gland abnormalities (both morphological and biochemical), and the experience in accomplishing subtotal parathyroid resection that balances long-term cure and avoidance of hypoparathyroidism. A bilateral parathyroid exploration is a necessary skill to develop or maintain for any surgeon who seeks to specialize in the treatment of parathyroid diseases.
References
Milas M.
Greene A.
Mitchell J.
et al.
National trends in parathyroid surgery from 1997 to 2007: A decade of change.
American College of Surgeons Clinical Congress,
San Francisco, CA2008
Predicting the success of limited exploration for primary hyperparathyroidism using ultrasound, sestamibi, and intraoperative parathyroid hormone: Analysis of 1158 cases.
Accuracy of preoperative localization studies and intraoperative parathyroid hormone assay in patients with primary hyperparathyroidism and double adenoma.
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