- Email: [email protected]
Impact of sonography on surgery for primary hyperparathyroidism
Impact of Sonography on Surgery for Primary Hyperparathyroidism
William H. Brewer, MD, Richmond, Virginia James W. Walsh, MD, Richmond, Virginia Heber H. Newsome, Jr., MD, Richmond, Virginia
Methods for the preoperative localization of abnormal parathyroid glands have recently been of great interest, but clinical reports have focused almost exclusively on the effectiveness of the methods’in locating the parathyroid glands. The actual importance of accurate gland localization in regard to length of operation and the complication rate has not been examined. In the present study, we have used sonography to determine the impact of successful preoperative localization on these two operative considerations. Methods Fifty-three patients underwent initial neck exploration following cervical sonography. Sonographic findings were reported to be either positive, negative, or equivocal for an abnormal parathyroid gland. The findings were all reported before operation, and the report was used in later statistical analyses. A definitive reading was obtained from the sonograms in 44 patients who were subsequently proved to have enlarged parathyroid glands. Of the nine other patients who underwent sonography and neck exploration, the scan reading was indeterminate in three patients and negative in six patients with normal, minimally enlarged, or missing glands. Operative times were analyzed. No effort was made to exclude patients from statistical analysis who were unlikely to have successful sonographic imaging of their parathyroid glands. Therefore, findings in patients with small adenomas, hyperplastic glands, or ectopic adenomas were classified as false-negative. Individual glands were not used as units for statistical analysis. An effort was made in each patient to identify at least four glands by biopsy confirmation at surgery. The same surgeon participated in all of the operations. Sonography was carried out with a commercially available articulated neon /?-scanner (Siemens) using a 5 MHz transducer with either direct skin contact or a water bath. Images of the anterior neck were obtained at 0.5 cm intervals in transversely, longitudinally, and medially angled scanning planes. Real-time scanning was performed when needed to help identify the esophagus when the patient swallowed.
From the Departments of Fiadiologyand Surgery, Medical College of Virginia, Virginia Commonwealth University, Richmond, Virginia. Requests for reprints should be addressed to Heber H. Newsome, Jr., MD. P.O. Box 485, MCV Station, Richmond, Virginia 23298.
270
Results Sonographic accuracy: Of the 44 patients with surgically proved enlarged glands, 25 had definitely positive sonographic findings which coincided with the operative localization of the enlarged glands (22 adenomas, 3 hyperplasias) found at surgery (truepositive). The other 19 patients had sonograms that failed to show enlarged parathyroid glands (17 adenomas, 2 hyperplasias), and these were considered to be false-negative findings. There were an additional six patients who had either four normal glands (three patients), four slightly enlarged hyperplastic glands (two patients), or three normal and one missing gland (one patient). Sonographic findings were negative in all six (true-negative). Two other patients had combined normal and missing glands, and one patient had a very small adenoma. Their scans were suggestive only and the three readings were considered indeterminate. There were no false-positive findings. Length of operation: To eliminate confounding variables such as indeterminate sonographic findings, missing glands, or all normal glands, only those patients with surgically proved enlarged glands and clearly positive or negative sonographic findings were included in a comparison of length of operations. In the 44 patients with proved enlarged glands, the average size of the glands was the same in the patients with positive findings as in patients with false-negative findings. In Table I the distribution of operative times between the patients with positive findings and those with negative findings is shown. There was no significant difference between the patients with positive findings and, those with negative findings when they were tested by the chi-square method. The precise operative times (incision to skin closure) were also averaged for the two groups of patients: 111 minutes for the group with positive findings and 135 minutes for the group with negative findings. Analysis of the logarithmic averages, to minimize scatter around the means, revealed a statistically significant difference in time between the two groups with a p value of less than 0.05 by the Student’s t test. Thus, there appeared to be a modest decrease in operative
The American Journal of Surgery
Sonography
time for patient’s who had successful preoperative localization. Complications: There were four patients with signs of tetany and eight patients with temporary hoarseness. No patients required permanent calcium or vitamin D therapy. The incidence of complications was the same in patients with positive findings as in those with false-negative findings. Of the patients with positive findings, three experienced signs and symptoms of tetany, and three had temporary hoarseness, whereas in the group with false-negative findings, one patient had tetany and three had temporary hoarseness. The other two patients with temporary hoarseness were in the true-negative group. Comments A large body of literature attests to the interest in localization procedures performed before parathyroid exploration. The noninvasive methods include computerized tomography [l-3], sonography [4-111, thermography [12], and radiographic scanning [13-151. The two major invasive methods have been arteriography [16-201 and venous sampling for assay of serum parathyroid hormone levels [21-361. Although emphasis has been appropriately placed on technique and accuracy, little attention has been given to such questions as the impact of accurate localization on operative time and complication rates. Edis et al [34] examined the effect of successful localization and found no difference in the surgical success rates between those patients with positive findings and those with negative findings. The unsuccessful explorations in the present study were in the patients with negative findings, but the impact on the success rate cannot be definitively examined in a nonrandomized study. We could demonstrate a small but significant shortening in the length of operative time in those patients with accurate localization compared with those with false-negative findings. There was no demonstrable difference in the complication rate between the two groups. At least in terms of shortening the operation and lowering the complication rate, improvement in accuracy of localization techniques may have only modest effects on surgical results in patients with clearly enlarged glands. On the other hand, of the nine patients with either truenegative or indeterminate findings, six patients had either a small adenoma (one patient), small-gland hyperplasia (two patients), or four normal glands (three patients). It is conceivable that a neck operation in these particular patients might well be facilitated by improved sensitivity in the method used to detect glands of normal size. Of course, in the three patients with presumed adenomas that were missed at operation, a more sensitive and widely probing method may have led to successful surgical localization.
Volume 145, February 1993
and Primary Hyperparathyroidism
TABLE I Distribution of Patients Among Three Ranges of Operative Time’ Sonographic Finding Positive Negative l
1 to 2 Hours 62.5% 52.9%
Length of Operation 2 to 3 Hours 20.8 % 23.5%
3 to 4 Hours 16.7% 23.5%
Chi-square = 0.10.
Our view of the usefulness of preoperative localization, at least in terms of length of operation and complication rate, may be a more positive one if our current policy of searching for all four glands were changed. For example, if we limited surgery to the removal of one enlarged and one ipsilateral normal gland, accurate preoperative localization would allow unilateral neck exploration. The recent report of Tibblin et al [37] is interesting in this regard. Fifty patients were approached unilaterally, and in 25 of these patients it was necessary to explore the second side because of the contralateral location of the adenoma. Operative time was significantly shorter in the unilateral explorations. In another 50 patients an attempt was made to find all four glands. When one or more missing glands were encountered, the operative time was significantly longer than in the other patients. Provided that operative policy allows completion of surgery after one large and one normal gland are found, it is obvious that accurate preoperative localization of parathyroid glands would eliminate bilateral dissection since the correct side would always be explored first. No postoperative hypercalcemia was reported in those patients in whom all four glands were not identified [37]; however, the occurrence of residual multiple adenomas is a potential risk in such patients. When approaching the neck unilaterally under these circumstances, the surgeon should recognize the possibility of second and even third adenomas being present on the contralateral side. Of course, improved methods to allow accurate localization of multiple adenomas would lower such a risk. Finally, further improvements that allow the detection of normal glands also would shorten operative time, even if a policy of four-gland biopsy were maintained. Summary The impact of preoperative sonographic localization of enlarged parathyroid glands was evaluated from the standpoint of operative time and complication rates. There was a reduction in the average time from 135 minutes when findings were falsenegative to 111 minutes when findings were positive. The rate of complication was not changed by accurate preoperative localization. When the operative goal is to find all parathyroid glands in every patient, the value of preoperative
271
Brewer et al
localization of parathyroid tumors by any current method is slight. Should operative policy favor a search for only one enlarged and one normal gland, or should methods improve to the point that even normal parathyroid glands can be located reliably, noninvasive localization should prove to be useful, safe, and cost-effective, even when it is carried out before initial operation. Acknowledgment: The authors thank Patricia South, RT, RDMS; Ellen Filbert, RT, RDMS; and Susan Brickhead, RT, RDMS for their excellent assistance. Addendum: A related study from the Mayo Clinic on ultrasonography in primary hyperparathyroidism has recently been published [38]. References 1. Wolverson MK, Sundaram M, Eddelston B. Prendergast J. Diagnosis of parathyroid adenoma by computed tomography. J Comput Assist Tomogr 1981;5:818-21. 2. Whitley NO, Bohlman M, Connor TB, McCrea ES, Mason GR, Whitley JE. Computed tomography for localization of parathyroid adenomas. J Comput Assist Tomogr 1981;5:8127. 3. Gouliamos AD, Carter BL. Parathyroid adenomas: identified by CT scan. Comput Tomogr 1981;5:59-83. 4. Welter VG, Schmidt KR, Welter HF, Pfeifer KJ, Spelsberg F. Sonographische diagnostik vergrtiberter nebenschildriisen beim hyperparathyreoidismus. Fortschr RGntgenstr 1981; 134:254-g. 5. Welter G, Welter HF, Spelsberg F. F%operative sonographische lokalisationsdiagnostik vergrbberter nebenschildriisen bei verdacht auf hyperparathyreoidismus. Chirurg 1981;52: 385-8. 8. Egdahl RH. Preoperative parathyroid localization. N Engl J Med 1979;301:548-9. 7. Moreau J-F, Dubost C, Buy J-N, Ferry J. Depistage ultrasonographique pre-operatoire des adenomes parathyroidiens. La Nouvelle Presse Medicale 1981;23:1923-7. 8. Edis AJ, Evens TC Jr. High-resolution, real-time ultrasonography in the preoperative location of parathyroid tumors. N Engl J Med 1979;301:532-4. 9. Sample WF, Mitchell STP, Bledsoe RC. Parathyroid ultrason&raphy. Radiology 1978;127:485-90. 10. Scheible W. Deutsch AL. Leooold GR. Parathvroid ademona: accuracy. of preoper&ve iocalization by high-resolution real-time sonography. J Clin Ultrasound 1981;9:325-30. 11. Simeone JF, Mueller PR, Ferruci JT, et al. High-resolution real-time sonography of the parathyroid. Radiology 1981; 141:745-51. 12. Samuels BI, Dowdy AH, Lechy JW. Localization of parathyroids by thermography. N Engl J Med 1972;288:218. 13. Stock JL, Krudy AG. Doppman JL, et al: Parathyroid imaging after intraarterial injections of [75Se]selenomethionine. J Clin Endocrinol Metab 1981:52:835-g. 14. Potchen EJ, Wilson RE, Deaiy JB Jr. External parathyroid scanning with Se75 selenomethionine. Ann Surg 1965; 162:492-504. 15. DiGiulio W, Morales JO. The value of the selenomethionine Se 75 scan in preoperative localization of parathyroid adenomas. JAMA 1969;209:1873-80. 16. Doppman JL. The localization and treatment of parathyroid adenomas by angiographic techniques. Ann Radio1 1980; 23:253-8. 17. Eisenberg H, Pallotta J, Sherwood LM. Selective arteriography, venography and venous hormone ass&y in diagnosis and localization of parathyroid lesions. Am J Med 1974;56: 810-20.
272
18. Jelenko C Ill, Teeslink CR, Hemdon JR, Morgan DG, Parrish RA, MOretZ WH. Localization of parathyroid adenomata by selective arteriography. Am Surg 1971;37:25-33. 19. Newton TH, Eisenberg E. Angiography of paraihyroid adenomas. Radiology 1966;86:843-50. 20. Seldinger SI. Localization of parathyroid adenomata by arteriography. Acta Radio1 1954;42:353-66. 21. Reitz RE, Pollard JJ, Wang CA, et al. Localization of parathyroid adenomas by selective venous catheterization and radio_ immunoassay. N Engl J Med 1969;281:348-51. 22. Wang CA, Reitz RE, Pollard JJ, et al. Localization of hyperfunctioning parathyroids. Am J Surg 1970; 119:462-4. 23. O’Riordan JLH, Kendall BE, Woodhead JS. Preoperative localisation of parathyroid tumours. Lancet 1971;2:1172-5. 24. Powell D, Shimkin PM, Doppman JL, et al. Primary hyperparathyroidism: preoperative tumor localization and differentiation between adenoma and hyperplasia. N Engl J Med 1972;286:1169-75. 25. Wells SA, Doppman JL, Bilezikian JP, et al. Repeated neck exploration in primary hyperparathyroidism. Localization of abnormal glands by selective thyroid arteriography, selective venous sampling, and radioimmunoassay. Surgery 1973; 74:678-86. 26. Wells SA, Ketcham AS, Marx SJ, et al. Preoperative localization of hyperfunctioning parathyroid tissue. Radioimmunoassay of parathyroid hormone in plasma from selectively catheterized thyroid veins. Ann Surg 1973;177:93-8. 27. Powell D, Murray TM, Pollard JJ, Cope 0, Wang CA, Potts JT. Parathyroid localization using venous catheterization and radioimmunoassay. Arch Intern Med 1973;131:645-8. 28. Bilezikian JP, Doppman JL, Shimkin PM. Preoperative localization of abnormal parathyroid tissue. Cumulative experience with venous sampling and arteriography. Am J Med 1973;55:505-14. 29. Davies DR, Shaw DG, Ives DR, Thomas BM, Watson L. Selective venous catheterisation and radioimmunoassay of parathyroid hormone in the diagnosis and localisation of parathyroid tumours. Lancet 1973;1:1079-82. 30. Samaan NA, Hickey RC, Hill CS Jr, Medellin H, Gates RB. Parathyroid tumors: preoperative localization and association with other tumors. Cancer 1974;33:933-9. 31. Tomlinson S, Clements VR, Smith JG, Kendall BE, O’Riordan JLH. Selective catheterization of the thyroid veins for preoperative localization of parathyroid tumours. Br J Surg 1974;61:633-7. 32. Monchik JM, Doppman JL, Earl1 JM, Aurbach GD. Localization of hyperfunctioning parathyroid tissue: radioimmunoassay of parathyroid hormone on samples from the large veins of the neck and thorax and selectively catheterized thyroid veins. Am J Surg 1975;129:413-20. 33. Hjern B, Almqvist S, Granberg PO, Lindvall N, Wlsthed. Preoperative localization of parathyroid tissue by selective neck vein catheterization and radioimmunoassay of parathyroid hormone. Acta Chir Stand 1975;141:31-9. 34. Edis AJ, Sheedy PF, Beahrs Olj, van Heerden JA. Results of reoperation for hyperparathyroidism, with evaluation of preoperative localization studies. Surgery 1978;84:38493. 35. Monchik JM, Pallotta JA, Sacks B, Shimkin PM. Role of selective venous catheterization of the small thyroid veins as a diagnostic study in hypercalcemic states. Am J Surg 1980; 139:575-80. 36. Dunlop DAB, Papapoulos SE, Lodgs RW, Fulton AJ, Kendall BE, O’Riordan JLH. Parathyroid venous sampling: anatomic considerations and results in 95 patients with primary hyperparathyroidism. Br J Radio1 1980;53: 183-9 1. 37. Tibblin S, Bondeson AG, Ljungberg 0. Unilateral parathyroidectomy in hyperparathyroidism due to single adenoma. Ann Surg 1982;195:245-52. 38. van Herden JA, James EM, Karsell PR, Charboneau JW, Grant CT, Purnell DC. Small-part ultrasonography in primary hyperparathyroidism. Ann Surg 1982;195:774-80.
The American Journal of Surgery
William H. Brewer, MD, Richmond, Virginia James W. Walsh, MD, Richmond, Virginia Heber H. Newsome, Jr., MD, Richmond, Virginia
Methods for the preoperative localization of abnormal parathyroid glands have recently been of great interest, but clinical reports have focused almost exclusively on the effectiveness of the methods’in locating the parathyroid glands. The actual importance of accurate gland localization in regard to length of operation and the complication rate has not been examined. In the present study, we have used sonography to determine the impact of successful preoperative localization on these two operative considerations. Methods Fifty-three patients underwent initial neck exploration following cervical sonography. Sonographic findings were reported to be either positive, negative, or equivocal for an abnormal parathyroid gland. The findings were all reported before operation, and the report was used in later statistical analyses. A definitive reading was obtained from the sonograms in 44 patients who were subsequently proved to have enlarged parathyroid glands. Of the nine other patients who underwent sonography and neck exploration, the scan reading was indeterminate in three patients and negative in six patients with normal, minimally enlarged, or missing glands. Operative times were analyzed. No effort was made to exclude patients from statistical analysis who were unlikely to have successful sonographic imaging of their parathyroid glands. Therefore, findings in patients with small adenomas, hyperplastic glands, or ectopic adenomas were classified as false-negative. Individual glands were not used as units for statistical analysis. An effort was made in each patient to identify at least four glands by biopsy confirmation at surgery. The same surgeon participated in all of the operations. Sonography was carried out with a commercially available articulated neon /?-scanner (Siemens) using a 5 MHz transducer with either direct skin contact or a water bath. Images of the anterior neck were obtained at 0.5 cm intervals in transversely, longitudinally, and medially angled scanning planes. Real-time scanning was performed when needed to help identify the esophagus when the patient swallowed.
From the Departments of Fiadiologyand Surgery, Medical College of Virginia, Virginia Commonwealth University, Richmond, Virginia. Requests for reprints should be addressed to Heber H. Newsome, Jr., MD. P.O. Box 485, MCV Station, Richmond, Virginia 23298.
270
Results Sonographic accuracy: Of the 44 patients with surgically proved enlarged glands, 25 had definitely positive sonographic findings which coincided with the operative localization of the enlarged glands (22 adenomas, 3 hyperplasias) found at surgery (truepositive). The other 19 patients had sonograms that failed to show enlarged parathyroid glands (17 adenomas, 2 hyperplasias), and these were considered to be false-negative findings. There were an additional six patients who had either four normal glands (three patients), four slightly enlarged hyperplastic glands (two patients), or three normal and one missing gland (one patient). Sonographic findings were negative in all six (true-negative). Two other patients had combined normal and missing glands, and one patient had a very small adenoma. Their scans were suggestive only and the three readings were considered indeterminate. There were no false-positive findings. Length of operation: To eliminate confounding variables such as indeterminate sonographic findings, missing glands, or all normal glands, only those patients with surgically proved enlarged glands and clearly positive or negative sonographic findings were included in a comparison of length of operations. In the 44 patients with proved enlarged glands, the average size of the glands was the same in the patients with positive findings as in patients with false-negative findings. In Table I the distribution of operative times between the patients with positive findings and those with negative findings is shown. There was no significant difference between the patients with positive findings and, those with negative findings when they were tested by the chi-square method. The precise operative times (incision to skin closure) were also averaged for the two groups of patients: 111 minutes for the group with positive findings and 135 minutes for the group with negative findings. Analysis of the logarithmic averages, to minimize scatter around the means, revealed a statistically significant difference in time between the two groups with a p value of less than 0.05 by the Student’s t test. Thus, there appeared to be a modest decrease in operative
The American Journal of Surgery
Sonography
time for patient’s who had successful preoperative localization. Complications: There were four patients with signs of tetany and eight patients with temporary hoarseness. No patients required permanent calcium or vitamin D therapy. The incidence of complications was the same in patients with positive findings as in those with false-negative findings. Of the patients with positive findings, three experienced signs and symptoms of tetany, and three had temporary hoarseness, whereas in the group with false-negative findings, one patient had tetany and three had temporary hoarseness. The other two patients with temporary hoarseness were in the true-negative group. Comments A large body of literature attests to the interest in localization procedures performed before parathyroid exploration. The noninvasive methods include computerized tomography [l-3], sonography [4-111, thermography [12], and radiographic scanning [13-151. The two major invasive methods have been arteriography [16-201 and venous sampling for assay of serum parathyroid hormone levels [21-361. Although emphasis has been appropriately placed on technique and accuracy, little attention has been given to such questions as the impact of accurate localization on operative time and complication rates. Edis et al [34] examined the effect of successful localization and found no difference in the surgical success rates between those patients with positive findings and those with negative findings. The unsuccessful explorations in the present study were in the patients with negative findings, but the impact on the success rate cannot be definitively examined in a nonrandomized study. We could demonstrate a small but significant shortening in the length of operative time in those patients with accurate localization compared with those with false-negative findings. There was no demonstrable difference in the complication rate between the two groups. At least in terms of shortening the operation and lowering the complication rate, improvement in accuracy of localization techniques may have only modest effects on surgical results in patients with clearly enlarged glands. On the other hand, of the nine patients with either truenegative or indeterminate findings, six patients had either a small adenoma (one patient), small-gland hyperplasia (two patients), or four normal glands (three patients). It is conceivable that a neck operation in these particular patients might well be facilitated by improved sensitivity in the method used to detect glands of normal size. Of course, in the three patients with presumed adenomas that were missed at operation, a more sensitive and widely probing method may have led to successful surgical localization.
Volume 145, February 1993
and Primary Hyperparathyroidism
TABLE I Distribution of Patients Among Three Ranges of Operative Time’ Sonographic Finding Positive Negative l
1 to 2 Hours 62.5% 52.9%
Length of Operation 2 to 3 Hours 20.8 % 23.5%
3 to 4 Hours 16.7% 23.5%
Chi-square = 0.10.
Our view of the usefulness of preoperative localization, at least in terms of length of operation and complication rate, may be a more positive one if our current policy of searching for all four glands were changed. For example, if we limited surgery to the removal of one enlarged and one ipsilateral normal gland, accurate preoperative localization would allow unilateral neck exploration. The recent report of Tibblin et al [37] is interesting in this regard. Fifty patients were approached unilaterally, and in 25 of these patients it was necessary to explore the second side because of the contralateral location of the adenoma. Operative time was significantly shorter in the unilateral explorations. In another 50 patients an attempt was made to find all four glands. When one or more missing glands were encountered, the operative time was significantly longer than in the other patients. Provided that operative policy allows completion of surgery after one large and one normal gland are found, it is obvious that accurate preoperative localization of parathyroid glands would eliminate bilateral dissection since the correct side would always be explored first. No postoperative hypercalcemia was reported in those patients in whom all four glands were not identified [37]; however, the occurrence of residual multiple adenomas is a potential risk in such patients. When approaching the neck unilaterally under these circumstances, the surgeon should recognize the possibility of second and even third adenomas being present on the contralateral side. Of course, improved methods to allow accurate localization of multiple adenomas would lower such a risk. Finally, further improvements that allow the detection of normal glands also would shorten operative time, even if a policy of four-gland biopsy were maintained. Summary The impact of preoperative sonographic localization of enlarged parathyroid glands was evaluated from the standpoint of operative time and complication rates. There was a reduction in the average time from 135 minutes when findings were falsenegative to 111 minutes when findings were positive. The rate of complication was not changed by accurate preoperative localization. When the operative goal is to find all parathyroid glands in every patient, the value of preoperative
271
Brewer et al
localization of parathyroid tumors by any current method is slight. Should operative policy favor a search for only one enlarged and one normal gland, or should methods improve to the point that even normal parathyroid glands can be located reliably, noninvasive localization should prove to be useful, safe, and cost-effective, even when it is carried out before initial operation. Acknowledgment: The authors thank Patricia South, RT, RDMS; Ellen Filbert, RT, RDMS; and Susan Brickhead, RT, RDMS for their excellent assistance. Addendum: A related study from the Mayo Clinic on ultrasonography in primary hyperparathyroidism has recently been published [38]. References 1. Wolverson MK, Sundaram M, Eddelston B. Prendergast J. Diagnosis of parathyroid adenoma by computed tomography. J Comput Assist Tomogr 1981;5:818-21. 2. Whitley NO, Bohlman M, Connor TB, McCrea ES, Mason GR, Whitley JE. Computed tomography for localization of parathyroid adenomas. J Comput Assist Tomogr 1981;5:8127. 3. Gouliamos AD, Carter BL. Parathyroid adenomas: identified by CT scan. Comput Tomogr 1981;5:59-83. 4. Welter VG, Schmidt KR, Welter HF, Pfeifer KJ, Spelsberg F. Sonographische diagnostik vergrtiberter nebenschildriisen beim hyperparathyreoidismus. Fortschr RGntgenstr 1981; 134:254-g. 5. Welter G, Welter HF, Spelsberg F. F%operative sonographische lokalisationsdiagnostik vergrbberter nebenschildriisen bei verdacht auf hyperparathyreoidismus. Chirurg 1981;52: 385-8. 8. Egdahl RH. Preoperative parathyroid localization. N Engl J Med 1979;301:548-9. 7. Moreau J-F, Dubost C, Buy J-N, Ferry J. Depistage ultrasonographique pre-operatoire des adenomes parathyroidiens. La Nouvelle Presse Medicale 1981;23:1923-7. 8. Edis AJ, Evens TC Jr. High-resolution, real-time ultrasonography in the preoperative location of parathyroid tumors. N Engl J Med 1979;301:532-4. 9. Sample WF, Mitchell STP, Bledsoe RC. Parathyroid ultrason&raphy. Radiology 1978;127:485-90. 10. Scheible W. Deutsch AL. Leooold GR. Parathvroid ademona: accuracy. of preoper&ve iocalization by high-resolution real-time sonography. J Clin Ultrasound 1981;9:325-30. 11. Simeone JF, Mueller PR, Ferruci JT, et al. High-resolution real-time sonography of the parathyroid. Radiology 1981; 141:745-51. 12. Samuels BI, Dowdy AH, Lechy JW. Localization of parathyroids by thermography. N Engl J Med 1972;288:218. 13. Stock JL, Krudy AG. Doppman JL, et al: Parathyroid imaging after intraarterial injections of [75Se]selenomethionine. J Clin Endocrinol Metab 1981:52:835-g. 14. Potchen EJ, Wilson RE, Deaiy JB Jr. External parathyroid scanning with Se75 selenomethionine. Ann Surg 1965; 162:492-504. 15. DiGiulio W, Morales JO. The value of the selenomethionine Se 75 scan in preoperative localization of parathyroid adenomas. JAMA 1969;209:1873-80. 16. Doppman JL. The localization and treatment of parathyroid adenomas by angiographic techniques. Ann Radio1 1980; 23:253-8. 17. Eisenberg H, Pallotta J, Sherwood LM. Selective arteriography, venography and venous hormone ass&y in diagnosis and localization of parathyroid lesions. Am J Med 1974;56: 810-20.
272
18. Jelenko C Ill, Teeslink CR, Hemdon JR, Morgan DG, Parrish RA, MOretZ WH. Localization of parathyroid adenomata by selective arteriography. Am Surg 1971;37:25-33. 19. Newton TH, Eisenberg E. Angiography of paraihyroid adenomas. Radiology 1966;86:843-50. 20. Seldinger SI. Localization of parathyroid adenomata by arteriography. Acta Radio1 1954;42:353-66. 21. Reitz RE, Pollard JJ, Wang CA, et al. Localization of parathyroid adenomas by selective venous catheterization and radio_ immunoassay. N Engl J Med 1969;281:348-51. 22. Wang CA, Reitz RE, Pollard JJ, et al. Localization of hyperfunctioning parathyroids. Am J Surg 1970; 119:462-4. 23. O’Riordan JLH, Kendall BE, Woodhead JS. Preoperative localisation of parathyroid tumours. Lancet 1971;2:1172-5. 24. Powell D, Shimkin PM, Doppman JL, et al. Primary hyperparathyroidism: preoperative tumor localization and differentiation between adenoma and hyperplasia. N Engl J Med 1972;286:1169-75. 25. Wells SA, Doppman JL, Bilezikian JP, et al. Repeated neck exploration in primary hyperparathyroidism. Localization of abnormal glands by selective thyroid arteriography, selective venous sampling, and radioimmunoassay. Surgery 1973; 74:678-86. 26. Wells SA, Ketcham AS, Marx SJ, et al. Preoperative localization of hyperfunctioning parathyroid tissue. Radioimmunoassay of parathyroid hormone in plasma from selectively catheterized thyroid veins. Ann Surg 1973;177:93-8. 27. Powell D, Murray TM, Pollard JJ, Cope 0, Wang CA, Potts JT. Parathyroid localization using venous catheterization and radioimmunoassay. Arch Intern Med 1973;131:645-8. 28. Bilezikian JP, Doppman JL, Shimkin PM. Preoperative localization of abnormal parathyroid tissue. Cumulative experience with venous sampling and arteriography. Am J Med 1973;55:505-14. 29. Davies DR, Shaw DG, Ives DR, Thomas BM, Watson L. Selective venous catheterisation and radioimmunoassay of parathyroid hormone in the diagnosis and localisation of parathyroid tumours. Lancet 1973;1:1079-82. 30. Samaan NA, Hickey RC, Hill CS Jr, Medellin H, Gates RB. Parathyroid tumors: preoperative localization and association with other tumors. Cancer 1974;33:933-9. 31. Tomlinson S, Clements VR, Smith JG, Kendall BE, O’Riordan JLH. Selective catheterization of the thyroid veins for preoperative localization of parathyroid tumours. Br J Surg 1974;61:633-7. 32. Monchik JM, Doppman JL, Earl1 JM, Aurbach GD. Localization of hyperfunctioning parathyroid tissue: radioimmunoassay of parathyroid hormone on samples from the large veins of the neck and thorax and selectively catheterized thyroid veins. Am J Surg 1975;129:413-20. 33. Hjern B, Almqvist S, Granberg PO, Lindvall N, Wlsthed. Preoperative localization of parathyroid tissue by selective neck vein catheterization and radioimmunoassay of parathyroid hormone. Acta Chir Stand 1975;141:31-9. 34. Edis AJ, Sheedy PF, Beahrs Olj, van Heerden JA. Results of reoperation for hyperparathyroidism, with evaluation of preoperative localization studies. Surgery 1978;84:38493. 35. Monchik JM, Pallotta JA, Sacks B, Shimkin PM. Role of selective venous catheterization of the small thyroid veins as a diagnostic study in hypercalcemic states. Am J Surg 1980; 139:575-80. 36. Dunlop DAB, Papapoulos SE, Lodgs RW, Fulton AJ, Kendall BE, O’Riordan JLH. Parathyroid venous sampling: anatomic considerations and results in 95 patients with primary hyperparathyroidism. Br J Radio1 1980;53: 183-9 1. 37. Tibblin S, Bondeson AG, Ljungberg 0. Unilateral parathyroidectomy in hyperparathyroidism due to single adenoma. Ann Surg 1982;195:245-52. 38. van Herden JA, James EM, Karsell PR, Charboneau JW, Grant CT, Purnell DC. Small-part ultrasonography in primary hyperparathyroidism. Ann Surg 1982;195:774-80.
The American Journal of Surgery