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Comparative histologic study of 43 metastasizing and nonmetastasizing adrenocortical tumors
Abstract
A series of 43 adrenocortical tumors was analyzed using nine histologic features. Mitotic activity, especially with atypical forms, and venous invasion correlated best with metastasizing or recurring tumors; however, no single criterion was useful alone. The combination of the following nine criteria was most useful in distinguishing malignant from benign tumors: nuclear grade III or IV; mitotic rate greater than 5/50 high-power fields; atypical mitoses; clear cells comprising 25% or less of the tumor; a diffuse architecture; microscopic necrosis; and invasion of venous, sinusoidal, and capsular structures. None of the 24 tumors with two or less of these criteria metastasized or recurred, while all but one of the 19 tumors with four or more of these criteria either recurred or metastasized.
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In the initial study by Weiss, the features with the strongest association to outcome were mitotic rate >5/50 high powered field, atypical mitoses, and venous invasion; in the second study by Weiss in 1989, the strongest association with patient outcome was the mitotic rate.
“In the initial study by Weiss, the features with the strongest association to outcome were the mitotic rate >5/50 high powered field, atypical mitoses, and venous invasion (111) and in the second study by Weiss in 1989 the strongest association with patient outcome was the mitotic rate (112).”
From Adrenal incidentaloma (2020) · cites this paper as [111]
The most widely used histological scoring system for ACC is the Weiss score, based on 9 histological parameters.
“The most widely used histological scoring system is the Weiss score (Table 4) based on 9 histological parameters (scored as 0 if absent and 1 if present) (110,111).”
From Adrenal incidentaloma (2020) · cites this paper as [111]
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Faßnacht, M., Dekkers, O. M., Else, T., Baudin, É., Berruti, A., de Krijger, R. R., Haak, H. R., Mihai, R., Assié, G., & Terzolo, M. (2018) · European Journal of Endocrinology · doi:10.1530/eje-18-0608 · Cited by 976
Else, T., Kim, A. C., Sabolch, A., Raymond, V. M., Kandathil, A., Caoili, E. M., Jolly, S., Miller, B. S., Giordano, T. J., & Hammer, G. D. (2014) · Endocrine Reviews · doi:10.1210/er.2013-1029 · Cited by 892
Incidentally Discovered Adrenal Masses*
Kloos, R. T., Gross, M. D., Francis, I. R., KOROBKIN, M. T., & Shapiro, B. (1995) · Endocrine Reviews · doi:10.1210/edrv-16-4-460 · Cited by 869
The clinically inapparent adrenal mass: update in diagnosis and management
Mansmann, G., Lau, J., Balk, E., Rothberg, M., Miyachi, Y., & Bornstein, S. R. (2004) · Endocrine Reviews · doi:10.1210/er.2002-0031 · Cited by 781
“For adrenocortical tumors, the histological classification system by Weiss is most commonly used (312, 313).”
MethodAdjuvant Mitotane Treatment for Adrenocortical Carcinoma
Terzolo, M., Angeli, A., Faßnacht, M., Daffara, F., Tauchmanovà, L., Conton, P. A., Rossetto, R., Buci, L., Sperone, P., Grossrubatscher, E. M., et al. (2007) · New England Journal of Medicine · doi:10.1056/nejmoa063360 · Cited by 759
Adrenocortical carcinoma in the United States: Treatment utilization and prognostic factors
Bilimoria, K. Y., Shen, W. T., Elaraj, D., Bentrem, D. J., Winchester, D. J., Kebebew, E., & Sturgeon, C. (2008) · Cancer · doi:10.1002/cncr.23886 · Cited by 493
Tissier, F., Cavard, C., Groussin, L., Perlemoine, K., Fumey, G., Hagneré, A.-M., René-Corail, F., Jullian, E., Gicquel, C., Bertagna, X., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-05-0593 · Cited by 474
“The sections were examined to assess their Weiss score (0 to 9) on the basis of the presence or absence of the following nine histologic features: high mitotic rate, atypical mitoses, high nuclear grade, low percentage of clear cells, necrosis, diffuse tumor architecture, capsular invasion, sinusoidal invasion, and ve…”
BackgroundWajchenberg (2000) · doi:10.1002/(sici)1097-0142(20000215)88:4
Faßnacht, M., Assié, G., Baudin, É., Eisenhofer, G., de la Fouchardière, C., Haak, H. R., de Krijger, R. R., Porpiglia, F., Terzolo, M., & Berruti, A. (2020) · Annals of Oncology · doi:10.1016/j.annonc.2020.08.2099 · Cited by 446
Management of patients with adrenal cancer: recommendations of an international consensus conference
Schteingart, D. E., Doherty, G. M., Gauger, P. G., Giordano, T. J., Hammer, G. D., Korobkin, M., & Worden, F. P. (2005) · Endocrine Related Cancer · doi:10.1677/erc.1.01029 · Cited by 421
“Positive predictive value of histological and molecular markers (Weiss 1984, Cibas et al. 1990, Medeiros & Weiss 1991, Fetsch et al. 1999) Histopathological assessment should follow current guidelines.”
BackgroundAdrenocortical carcinoma: diagnosis, evaluation and treatment
NG, L., & LIBERTINO, J. M. (2003) · Journal of Urology · doi:10.1016/s0022-5347(05)64023-2 · Cited by 423
Molecular classification and prognostication of adrenocortical tumors by transcriptome profiling
Giordano, T. J., Kuick, R., Else, T., Gauger, P. G., Vinco, M., Bauersfeld, J., Sanders, D., Thomas, D. G., Doherty, G., & Hammer, G. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-08-1067 · Cited by 401
Adrenocortical carcinoma: a clinician’s update
Fassnacht, M., Libé, R., Kroiss, M., & Allolio, B. (2011) · Nature Reviews Endocrinology · doi:10.1038/nrendo.2010.235 · Cited by 396
Wooten (1993) · doi:10.1002/1097-0142(19931201)72:11
Distinct transcriptional profiles of adrenocortical tumors uncovered by DNA microarray analysis
Giordano, T. J., Thomas, D. G., Kuick, R., Lizyness, M., Misek, D. E., Smith, A. L., Sanders, D., Aljundi, R. T., Gauger, P. G., Thompson, N. W., et al. (2003) · The American Journal of Pathology · doi:10.1016/s0002-9440(10)63846-1 · Cited by 383
de Reyniès, A., Assié, G., Rickman, D. S., Tissier, F., Groussin, L., René-Corail, F., Dousset, B., Bertagna, X., Clauser, E., & Bertherat, J. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.18.5678 · Cited by 382
Aubert, S., Wacrenier, A., Leroy, X., Devos, P., Carnaille, B. M. L., Proye, C. A. G., Wemeau, J. L., Lecomte-Houcke, M., & Leteurtre, E. (2002) · The American Journal of Surgical Pathology · doi:10.1097/00000478-200212000-00009 · Cited by 378
Adrenal Cortical Neoplasms in the Pediatric Population
Wieneke, J. A., Thompson, L. D. �., & Heffess, C. S. (2003) · The American Journal of Surgical Pathology · doi:10.1097/00000478-200307000-00001 · Cited by 350
“Pathologic criteria for malignancy in the adult population are well established in the literature.(10,37,39,40) In contrast, definitive pathologic criteria for malignancy in adrenal cortical neoplasms in the pediatric age group remain uncertain.”
BackgroundMethodOverview of the 2022 WHO Classification of Adrenal Cortical Tumors
Mete, Ö., Erickson, L. A., Juhlin, C. C., de Krijger, R. R., Sasano, H., Volante, M., & Papotti, M. G. (2022) · Endocrine Pathology · doi:10.1007/s12022-022-09710-8 · Cited by 353
“The classic criteria of Weiss and colleagues described in 1984 and modified (also known as modified Weiss system) in 1989 continue to be used for the classification of conventional adrenal cortical neoplasms in adults [128, 129] (Tables 1 and 2).”
MethodSherlock, M., Scarsbrook, A., Abbas, A., Fraser, S., Limumpornpetch, P., Dineen, R., & Stewart, P. M. (2020) · Endocrine Reviews · doi:10.1210/endrev/bnaa008 · Cited by 347
“The most widely used histological scoring system is the Weiss score (Table 4) based on 9 histological parameters (scored as 0 if absent and 1 if present) (110,111).”
BackgroundMethodAdrenocortical Carcinoma: Diagnosis, Evaluation and Treatment
NG, L., & LIBERTINO, J. M. (2003) · The Journal of Urology · doi:10.1097/00005392-200301000-00003 · Cited by 330
Adrenocortical Oncocytic Tumors: Report of 10 Cases and Review of the Literature
Bisceglia, M., Ludovico, O., Mattia, A. D., Ben‐Dor, D., Sandbank, J., Pasquinelli, G., Lau, S. K., & Weiss, L. M. (2004) · International Journal of Surgical Pathology · doi:10.1177/106689690401200304 · Cited by 317
“In order to assess tumor behavior and clinical prognosis, each case was morphologically evaluated according to the 9 histologic parameters of the Weiss system used for discriminating benign from malignant conventional adrenocortical tumors [4].”
BackgroundMethodSelf-citationAdrenocortical Carcinoma: Clinical, Morphologic, and Molecular Characterization
Stojadinovic, A., Ghossein, R. A., Hoos, A., Nissan, A., Marshall, D., Dudas, M. E., Cordon‐Cardo, C., Jaques, D. P., & Brennan, M. F. (2002) · Journal of Clinical Oncology · doi:10.1200/jco.2002.20.4.941 · Cited by 312
Gicquel, C., BERTAGNA, X. Y., Gaston, V., Coste, J., Louvel, A., Baudin, É., Bertherat, J. Y., Chapuis, Y., Duclos, J. M., Schlumberger, M. J., et al. (2001) · PubMed · Cited by 285
Imai, H., Nakano, Y., Kiyosawa, K., & Tan, E. M. (1993) · Cancer · doi:10.1002/1097-0142(19930101)71:1 · Cited by 76
Adrenocortical cancer: pathophysiology and clinical management
Libé, R., Fratticci, A., & Bertherat, J. Y. (2007) · Endocrine Related Cancer · doi:10.1677/erc.1.01130 · Cited by 271
“Since the initial paper of Weiss (1984), it is assumed that a score above 3 is most likely to be associated with a malignant tumor.”
Backgroundde Fraipont, F., El Atifi, M., Cherradi, N., Le Moigne, G., Defaye, G., Houlgatte, R., Bertherat, J., Bertagna, X., Plouin, P.-F., Baudin, E., et al. (2005) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2004-1075 · Cited by 261
“The analysis of the expression level of this group of 22 genes appeared almost as powerful as the well recognized histological score of Weiss at identifying the true carcinomas.”
MethodInfluentialmiR-195 and miR-483-5p Identified as Predictors of Poor Prognosis in Adrenocortical Cancer
Soon, P. S. H., Tacon, L. J., Gill, A. J., Bambach, C. P., Sywak, M. S., Campbell, P. R., Yeh, M. W., Wong, S. G., Clifton-Bligh, R. J., Robinson, B. G., et al. (2009) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-09-1587 · Cited by 262
BUSAM, K. J., Iversen, K., Coplan, K. A., Old, L. J., Stockert, E., Chen., Y., McGregor, D. K., & Jungbluth, A. A. (1998) · The American Journal of Surgical Pathology · doi:10.1097/00000478-199801000-00007 · Cited by 235
Prognostic parameters of metastatic adrenocortical carcinoma
Assié, G., Antoni, G., Tissier, F., Caillou, B., Abiven, G., Gicquel, C., Leboulleux, S., Travagli, J.-P., Dromain, C., Bertagna, X., et al. (2007) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2006-0706 · Cited by 236
“Atypical mitoses have also been considered as a significant diagnostic parameter in a one-score pathological system (37), associated with a low disease-free survival in a univariate analysis in another study (12), and identified as an important predictor of malignancy in childhood adrenocortical tumors (41).”
BackgroundMethodAdrenocortical carcinoma (ACC): diagnosis, prognosis, and treatment
Libé, R. (2015) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2015.00045 · Cited by 233
“It is established that a Weiss score≥ 3 define an ACC, whereas scores between 0 and 2 defines the adrenal adenoma, even if sometimes aWeiss score of 2 can be suspicious (Weiss, 1984).”
BackgroundGaujoux, S., Mihai, R., Carnaille, B. M. L., Dousset, B. E., Fiori, C., Porpiglia, F., Hellman, P., Iacobone, M., Kraimps, J. L., Donatini, G., et al. (2017) · British journal of surgery · doi:10.1002/bjs.10414 · Cited by 226
The Weiss system for evaluating adrenocortical neoplasms: 25 years later
Lau, S. K., & Weiss, L. M. (2009) · Human Pathology · doi:10.1016/j.humpath.2009.03.010 · Cited by 223
Self-citationChildhood Adrenocortical Tumors1
Sandrini, R., Ribeiro, R. C., & DeLacerda, L. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.7.4057 · Cited by 237
Adrenocortical carcinoma: the range of appearances on CT and MRI
Bharwani, N., Rockall, A. G., Sahdev, A., Gueorguiev, M., Drake, W., Grossman, A. B., & Reznek, R. H. (2011) · American Journal of Roentgenology · doi:10.2214/ajr.10.5540 · Cited by 215
“Pathologic Features Separating benign from malignant adrenal cortical neoplasms is not always possible on the basis of histologic findings alone, particularly from biopsy specimens [2, 14]; however, there are macroscopic and microscopic criteria that favor malignancy [14–17].”
BackgroundGicquel, C., Raffin‐Sanson, M., Gaston, V., BERTAGNA, X. Y., Plouin, P., Schlumberger, M. J., Louvel, A., LUTON, J. P., & Bouc, Y. L. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.8.4170 · Cited by 213
Management of adrenocortical carcinoma
Allolio, B., Hahner, S., Weismann, D., & Fassnacht, M. (2004) · Clinical Endocrinology · doi:10.1046/j.1365-2265.2003.01881.x · Cited by 214
“For diagnosis of ACC, different Management of adrenocortical carcinoma 277 © 2003 Blackwell Publishing Ltd, Clinical Endocrinology, 60, 273–287 diagnostic scores (Hough et al., 1979; Weiss, 1984; van Slooten et al., 1985; Weiss et al., 1989; Table 2) have been developed.”
MethodPorpiglia, F., Fiori, C., Daffara, F., Zaggia, B., Bollito, E., Volante, M., Berruti, A., & Terzolo, M. (2010) · European Urology · doi:10.1016/j.eururo.2010.01.036 · Cited by 188
“histologic diagnoses were confirmed by two experienced pathologists at our centre (EB, MV) according to the Weiss criteria [17,18].”
MethodSerum miR-483-5p and miR-195 are predictive of recurrence risk in adrenocortical cancer patients
Chabre, O., Libé, R., Assié, G., Barreau, O., Bertherat, J. Y., BERTAGNA, X. Y., Feige, J., & Cherradi, N. (2013) · Endocrine Related Cancer · doi:10.1530/erc-13-0051 · Cited by 189
“Malignancy was assessed according to Weiss criteria (Weiss 1984) by a single experienced pathologist, and tumor staging was performed using the European Network for the Study of Adrenal Tumors classification (Fassnacht et al. 2009).”
Latronico, A. C., & Chrousos, G. P. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.5.3921 · Cited by 191
The molecular pathogenesis of hereditary and sporadic adrenocortical and adrenomedullary tumors
Koch, C. A., Pacak, K., & Chrousos, G. P. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2002-021069 · Cited by 177
Almeida, M. Q., Fragoso, M. C. B. V., Lotfi, C. F. P., Santos, M. G., Nishi, M. Y., Costa, M. H. S., Lerario, A. M., Maciel, C. C., Mattos, G. E., Jorge, A. A. L., et al. (2008) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2008-0065 · Cited by 176
“Adult adrenocortical tumors were classified according to Weiss criteria: 20 adrenocortical adenomas (Weiss score 3) and 14 carcinomas (Weiss score 4) (26).”
MethodProspective evaluation of mitotane toxicity in adrenocortical cancer patients treated adjuvantly
Daffara, F., De Francia, S., Reimondo, G., Zaggia, B., Aroasio, E., Porpiglia, F., Volante, M., Termine, A., Di Carlo, F., Dogliotti, L., et al. (2008) · Endocrine Related Cancer · doi:10.1677/erc-08-0103 · Cited by 167
“…diagnoses were re-evaluated according to the Weiss criteria (nuclear atypia, atypical mitoses, frequent mitoses, small percentage of clear cells, diffuse architecture, necrosis, invasion of venous, sinusoidal, or capsular structures; Weiss 1984, Weiss et al. 1989) by an expert pathologist (M.V.).”
MethodSperone, P., Ferrero, A., Daffara, F., Priola, A. M., Zaggia, B., Volante, M., Santini, D., Vincenzi, B., Badalamenti, G., Intrivici, C., et al. (2010) · Endocrine Related Cancer · doi:10.1677/erc-09-0281 · Cited by 167
“These data suggest to explore the efficacy of continuing mitotane in addition to new chemotherapeutic drugs in patients experiencing progression during an (Weiss 1984) initial mitotane-based regimen.”
BackgroundMethodBiology, clinical characteristics, and management of adrenocortical tumors in children
Rodriguez‐Galindo, C., Figueiredo, B. C., Zambetti, G. P., & Ribeiro, R. C. (2005) · Pediatric Blood & Cancer · doi:10.1002/pbc.20318 · Cited by 146
“The histologic criteria for malignant tumors were the mitotic index, the presence of confluent necrosis and atypical mitoses, and the nuclear grade, as previously defined byWeiss [45,47].”
BackgroundGaujoux, S., Grabar, S., Fassnacht, M., Ragazzon, B., Launay, P., Libé, R., Chokri, I., Audebourg, A., Royer, B., Sbiera, S., et al. (2011) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-2006 · Cited by 146
“The Weiss score was established on the basis of 9 Weiss histologic criteria (20, 21).”
MethodAdrenal tumors: How to establish malignancy?
Faßnacht, M., Kenn, W., & Allolio, B. (2004) · Journal of Endocrinological Investigation · doi:10.1007/bf03351068 · Cited by 141
Veytsman, I. G., Nieman, L. K., & Fojo, T. (2009) · Journal of Clinical Oncology · doi:10.1200/jco.2008.17.2775 · Cited by 147
Wong, D., Spagnolo, D. V., Bisceglia, M., Havlat, M. F., McCallum, D., & Platten, M. A. (2011) · Human Pathology · doi:10.1016/j.humpath.2010.08.010 · Cited by 141
“Failing to recognize an OAN may lead one to incorrectly apply the popular Weiss criteria [19], commonly used for conventional adrenocortical tumors to assess biological potential.”
BackgroundMethodMORIMOTO, R., SATOH, F., MURAKAMI, O., SUZUKI, T., ABE, T., TANEMOTO, M., ABE, M., URUNO, A., ISHIDOYA, S., ARAI, Y., et al. (2008) · Endocrine Journal · doi:10.1507/endocrj.k07-079 · Cited by 141
“The diagnosis of ACC has been made according to the criteria of Weiss [6, 7], which is a well-validated and established scoring system for a histopathological diagnosis of ACC [1, 8].”
Methodp53 Mutations in sporadic adrenocortical tumors
Ohgaki, H., Kleihues, P., & Heitz, P. U. (1993) · International Journal of Cancer · doi:10.1002/ijc.2910540310 · Cited by 139
Kendrick, M. L. (2001) · Archives of Surgery · doi:10.1001/archsurg.136.5.543 · Cited by 140
Volante, M., Bollito, E., Sperone, P., Tavaglione, V., Daffara, F., Porpiglia, F., Terzolo, M., Berruti, A., & Papotti, M. G. (2009) · Histopathology · doi:10.1111/j.1365-2559.2009.03423.x · Cited by 138
Adrenocortical carcinoma — towards genomics guided clinical care
Crona, J., & Beuschlein, F. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0221-7 · Cited by 142
Soon, P., Gill, A. J., Benn, D. E., Clarkson, A., Robinson, B. G., McDonald, K. L., & Sidhu, S. B. (2009) · Endocrine Related Cancer · doi:10.1677/erc-08-0237 · Cited by 135
“Britain DOI: 10.1677/ERC-08-0237 Online version via http://www.endocrinology-journals.org When Weiss first published in 1984, ACTs with a score of R4 were considered to be carcinomas (Weiss 1984).”
BackgroundInfluentialTerzolo, M., Baudin, A. E., Ardito, A., Kroiss, M., Leboulleux, S., Daffara, F., Perotti, P., Feelders, R. A., deVries, J. H., Zaggia, B., et al. (2013) · European Journal of Endocrinology · doi:10.1530/eje-13-0242 · Cited by 134
“All diagnoses were confirmed by experienced pathologists according to the Weiss criteria with a score of 3, or more, identifying malignancy (18, 19).”
BackgroundMethodRibeiro, R. C., Pinto, E. M., Zambetti, G. P., & Galindo, C. R. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.10.015 · Cited by 134
Bonnet, S., Gaujoux, S., Launay, P., Baudry, C., Chokri, I., Ragazzon, B., Libé, R., René-Corail, F., Audebourg, A., Vacher-Lavenu, M.-C., et al. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2010-1885 · Cited by 133
Identification of a CpG Island Methylator Phenotype in Adrenocortical Carcinomas
Barreau, O., Assié, G., Wilmot-Roussel, H., Ragazzon, B., Baudry, C., Perlemoine, K., René-Corail, F., Bertagna, X., Dousset, B., Hamzaoui, N., et al. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2012-2993 · Cited by 132
Molecular Markers and the Pathogenesis of Adrenocortical Cancer
Soon, P. S. H., McDonald, K. L., Robinson, B. G., & Sidhu, S. B. (2008) · The Oncologist · doi:10.1634/theoncologist.2007-0243 · Cited by 129
Parathyroid Hyperplasia, Adenomas, and Carcinomas
Erickson, L. A., Jin, L. G., Wollan, P. C., Thompson, G. B., van Heerden, J. A., & Lloyd, R. V. (1999) · The American Journal of Surgical Pathology · doi:10.1097/00000478-199903000-00007 · Cited by 128
Oncocytic Adrenocortical Neoplasms
Lin, B. T.-Y., Bonsib, S. M., Mierau, G. W., Weiss, L. M., & Medeiros, L. J. (1998) · The American Journal of Surgical Pathology · doi:10.1097/00000478-199805000-00012 · Cited by 127
Self-citationThe Weiss Score and Beyond—Histopathology for Adrenocortical Carcinoma
Papotti, M. G., Libé, R., Duregon, E., Volante, M., Bertherat, J. Y., & Tissier, F. (2011) · Hormones and Cancer · doi:10.1007/s12672-011-0088-0 · Cited by 132
“Therefore, in the last decades, variable combinations of such parameters in different scoring systems have been proposed in the literature [21, 43] being the scoring method proposed by Weiss in 1984 [48] with subsequent modifications [49] and revisions [2] by far the most widely employed.”
BackgroundMethodAdrenocortical tumors in children
Ribeiro, R. C., Michalkiewicz, E., de Figueiredo, B. C., DeLacerda, L., Sandrini, F., Pianovski, M. A. D., Sampaio, G., & Sandrini, R. (2000) · Brazilian Journal of Medical and Biological Research · doi:10.1590/s0100-879x2000001000013 · Cited by 134
Gaujoux, S., Pinson, S., Gimenez‐Roqueplo, A., Amar, L., Ragazzon, B., Launay, P., Méatchi, T., Libé, R., BERTAGNA, X. Y., Audebourg, A., et al. (2010) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-10-1497 · Cited by 121
Pathologic Features of Prognostic Significance for Adrenocortical Carcinoma After Curative Resection
Harrison, L. E. (1999) · Archives of Surgery · doi:10.1001/archsurg.134.2.181 · Cited by 117
“The presence of mitotic figures has been used as a major criterion to separate benign from malignant cortical tumors.(7,9,10) In addition, mitotic rate has been reported as a predictor of survival rate in patients with adrenocortical carcinoma.”
MethodHelsinki score—a novel model for prediction of metastases in adrenocortical carcinomas
Pennanen, M., Heiskanen, I., Sane, T., Remes, S. M., Mustonen, H. K., Haglund, C. H., & Arola, J. T. (2014) · Human Pathology · doi:10.1016/j.humpath.2014.11.015 · Cited by 115
Hoang, M. P., Ayala, A. G., & Albores‐Saavedra, J. (2002) · Modern Pathology · doi:10.1038/modpathol.3880638 · Cited by 115
“According to Weiss (19, 20), adrenocortical carcinoma would have four or more of the following findings: high nuclear grade, eosinophilic cytoplasm (more than 75%), diffuse architecture (more than 33%), and presence of necrosis, mitotic figures (more than 5/50HPFs), atypical mitotic figures, capsular invasion, venous…”
Libè, R., Groussin, L., Tissier, F., Elie, C., René-Corail, F., Fratticci, A., Jullian, E., Beck-Peccoz, P., Bertagna, X., Gicquel, C., et al. (2007) · Clinical Cancer Research · doi:10.1158/1078-0432.ccr-06-2085 · Cited by 115
Adrenocortical Adenoma and Carcinoma: Histopathological and Molecular Comparative Analysis
Stojadinovic, A., Brennan, M. F., Hoos, A., Ömeroğlu, A., Leung, D. H. Y., Dudas, M. E., Nissan, A., Cordon‐Cardo, C., & Ghossein, R. A. (2003) · Modern Pathology · doi:10.1097/01.mp.0000081730.72305.81 · Cited by 113
“The pathologic criteria of Weiss et al. (4) were applied in the present histopathological analysis of adrenocortical neoplasms, and carcinomas were defined as tumors demonstrating three or more histologic criteria.”
BackgroundMethodInfluentialAnalysis by cDNA microarrays of gene expression patterns of human adrenocortical tumors
Slater, E. P., Diehl, S. M., Langer, P., Samans, B., Ramaswamy, A., Zielke, A., & Bartsch, D. K. (2006) · European Journal of Endocrinology · doi:10.1530/eje.1.02116 · Cited by 113
“The classification was determined by both conventional histologic methods (14) and Weiss score ( 15 ) where adenomas met fewer than four and carcinomas at least four of the criteria.”
MethodMendonca, B. B., Lucón, A. M., Menezes, C. A. V., Saldanha, L. B., Latronico, A. C., Zerbini, M. C. N., Madureira, G., Domenice, S., Albergaria, M. A. P., Camargo, M. H. A., et al. (1995) · The Journal of Urology · doi:10.1016/s0022-5347(01)66673-4 · Cited by 117
ADRENOCORTICAL CARCINOMA IN CHILDREN
Liou, L. S., & Kay, R. M. (2000) · Urologic Clinics of North America · doi:10.1016/s0094-0143(05)70089-6 · Cited by 111
Satoh, F., Abe, T., Tanemoto, M., Nakamura, M., Abe, M., Uruno, A., Morimoto, R., Akihiro, S. A. T. O., Takase, K., Ishidoya, S., et al. (2007) · Hypertension Research · doi:10.1291/hypres.30.1083 · Cited by 112
“All the lesions were diagnosed as benign adenomas based on the histological criteria of Weiss (28).”
MethodTP53 Germline Mutations in Adult Patients with Adrenocortical Carcinoma
Herrmann, L. J. M., Heinze, B., Fassnacht, M., Willenberg, H. S., Quinkler, M., Reisch, N., Zink, M., Allolio, B., & Hahner, S. (2012) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1982 · Cited by 109
“Histopathological evaluation of adrenal tissue, including assessment of the Weiss score (24), was used to establish the diagnosis of ACC.”
MethodContemporary Management of Adrenocortical Carcinoma
Laurent Zini, A., Porpiglia, F., & Faßnacht, M. (2011) · European Urology · doi:10.1016/j.eururo.2011.07.062 · Cited by 111
“Among these, theWeiss criteria aremostwidely utilised [69,70].”
The role of laparoscopic adrenalectomy for adrenal tumours of 6 cm or greater
Parnaby, C. N., Chong, P. S., Chisholm, L. J., Farrow, J., Connell, J. M. C., & Dwyer, P. J. O. (2007) · Surgical Endoscopy · doi:10.1007/s00464-007-9709-7 · Cited by 107
“Out of 39 LA performed for tumours C6 cm, only three had a histological diagnosis of adrenal cortical carcinoma based on the Weiss criteria [ 19 ,20].”
MethodThe Reticulin Algorithm for Adrenocortical Tumor Diagnosis
Duregon, E., Fassina, A., Volante, M., Nesi, G., Santi, R., Gatti, G., Cappellesso, R., Ciaramella, P. D., Ventura, L., Gambacorta, M., et al. (2013) · The American Journal of Surgical Pathology · doi:10.1097/pas.0b013e31828d387b · Cited by 105
“5 (2-30) Weight, (range) (g) 39 (4-150) 428 (8-3100) 46 (2.”
Rosa, S. L. (2023) · Endocrine Pathology · doi:10.1007/s12022-023-09755-3 · Cited by 102
“Adrenal cortical neoplasms include adenoma and carcinoma that have been traditionally differentiated using specific classification systems based on morphological criteria not including Ki67 evaluation: the Weiss system [111], the reticulin algorithm [112], the Lin-Weiss-Bisceglia system for oncocytic neoplasms [113],…”
MethodDistinguishing Benign from Malignant Euadrenal Masses
Gross, M., Shapiro, B., Bouffard, J. A., Glazer, G. M., Francis, I. R., Wilton, G. P., Khafagi, F. A., & Sonda, L. P. (1988) · Annals of Internal Medicine · doi:10.7326/0003-4819-109-8-613 · Cited by 99
Validation of the prognostic role of the “Helsinki Score” in 225 cases of adrenocortical carcinoma
Duregon, E., Cappellesso, R., Maffeis, V., Zaggia, B., Ventura, L., Berruti, A., Terzolo, M., Fassina, A., Volante, M., & Papotti, M. (2017) · Human Pathology · doi:10.1016/j.humpath.2016.09.035 · Cited by 98
“) having a specific interest in endocrine pathology and classified according to the appropriate diagnostic systems, ie, Weiss Score [1] and Revised Weiss Score [2] for conventional ACC, LinWeiss-Bisceglia System [10] for pure oncocytic adrenocortical tumors and Wienecke classification [11] for pediatric tumors.”
BackgroundMethodInfluentialImmunohistochemical assessment of Ki-67 in the differential diagnosis of adrenocortical tumors
Terzolo, M., Boccuzzi, A., Bovio, S., Cappia, S., Giuli, P. D., Alı̀, A., Paccotti, P., Porpiglia, F., Fontana, D., & Angeli, A. (2001) · Urology · doi:10.1016/s0090-4295(00)00852-9 · Cited by 96
Histopathology of the human adrenal cortex.
Neville, A., & O'Hare, M. (1985) · Clinics in Endocrinology and Metabolism · doi:10.1016/s0300-595x(85)80078-5 · Cited by 88
Adrenocortical Carcinoma: Impact of Surgical Margin Status on Long-Term Outcomes
Margonis, G. A., Kim, Y., Prescott, J. D., Tran, T. B., Postlewait, L. M., Maithel, S. K., Wang, T. S., Evans, D. B., Hatzaras, I. S., Shenoy, R. S., et al. (2015) · Annals of Surgical Oncology · doi:10.1245/s10434-015-4803-x · Cited by 96
“had previously noted that capsular invasion can be characterized by nests or cords of tumor cells extending into or through the capsule with stromal reaction and was a surrogate for an aggressive underlying tumor biology.(34) Collectively, the data strongly suggest that surgical margin status is an important factor as…”
BackgroundSchmitt, A., Saremaslani, P., Schmid, S., Rousson, V, Montani, M., Schmid, D. M., Heitz, P. U., Komminoth, P., & Perren, A. (2006) · Histopathology · doi:10.1111/j.1365-2559.2006.02505.x · Cited by 94
Large Degenerated Adrenal Adenomas: Radiologic-Pathologic Correlation
Newhouse, J. H., Heffess, C. S., Wagner, B. J., Imray, T. J., Adair, C. F., & Davidson, A. J. (1999) · Radiology · doi:10.1148/radiology.210.2.r99fe12385 · Cited by 91
Localization of Steroidogenic Enzymes in Adrenal Cortex and Its Disorders.
Sasano, H. (1994) · Endocrine Journal · doi:10.1507/endocrj.41.471 · Cited by 94
Mir, M. C., Klink, J. C., Guillotreau, J., Long, J., Miocinovic, R., Kaouk, J. H., Simmons, M. N., Klein, E. A., Krishnamurthi, V., Campbell, S. C., et al. (2012) · Annals of Surgical Oncology · doi:10.1245/s10434-012-2760-1 · Cited by 92
Reincke, M., Mora, P., Beuschlein, F., Arlt, W., Chrousos, G. P., & Allolio, B. (1997) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.82.9.4211 · Cited by 93
“The clinical and pathological diagnosis was made according to established criteria (2, 3, 11, 12).”
Risk factors for conversion and complications after unilateral laparoscopic adrenalectomy
Gaujoux, S., Bonnet, S., Leconte, M., Zohar, S., Bertherat, J. Y., BERTAGNA, X. Y., & Dousset, B. E. (2011) · British journal of surgery · doi:10.1002/bjs.7558 · Cited by 89
Duregon, E., Volante, M., Giorcelli, J., Terzolo, M., Lalli, E., & Papotti, M. G. (2012) · Human Pathology · doi:10.1016/j.humpath.2012.07.025 · Cited by 90
“Many diagnostic methods have been proposed, either based on scoring systems including the most frequently used Weiss system [2,3] or using alternative algorithmic approaches [4,5].”
MethodAdrenocortical Neoplasms: Role of Prognostic Markers MIB-1, P53, and RB
Vargas, M. P., Vargas, H. I., Kleiner, D. E., & Merino, M. J. (1997) · The American Journal of Surgical Pathology · doi:10.1097/00000478-199705000-00008 · Cited by 89
Comprehensive DNA methylation analysis of benign and malignant adrenocortical tumors
Fonseca, A. L., Kugelberg, J., Starker, L. F., Scholl, U. I., Choi, M., Hellman, P., Åkerström, G., Westin, G., Lifton, R. P., Björklund, P., et al. (2012) · Genes Chromosomes and Cancer · doi:10.1002/gcc.21978 · Cited by 87
Discerning malignancy in adrenocortical tumors: are molecular markers useful?
Wachenfeld, C., Beuschlein, F., Zwermann, O., Mora, P., Faßnacht, M., Allolio, B., & Reincke, M. (2001) · European Journal of Endocrinology · doi:10.1530/eje.0.1450335 · Cited by 84
“Adrenal adenoma 30 1/28 (2) 1/23 ( 7 ) 0.44^0.29 2.11^1.01 5/26 (4) Adrenal carcinoma 10 3/10 (0) 5/5 (2) 4.57^4.43* 11.94^7.58* 6/8 (2)”
InfluentialGupta, N., Rivera, M., Novotny, P. J., Rodriguez, V., Bancos, I., & Lteif, A. N. (2018) · Hormone Research in Paediatrics · doi:10.1159/000488855 · Cited by 85
Papotti, M. G., Volante, M., Duregon, E., Delsedime, L., Terzolo, M., Berruti, A., & Rosaí, J. (2010) · The American Journal of Surgical Pathology · doi:10.1097/pas.0b013e3181e2b726 · Cited by 81
“The rate of functioning tumors of the present series is in line with the literature data on the 13 currently reported malignant ACC with myxoid features (3-5,12,18,28) and is higher than that generally recorded in conventional ACC, ranging from less than 50% in our experience (27) to 60% in the literature (8).”
Erickson, L. A., Jin, L. G., Goellner, J. R., Lohse, C. M., Pankratz, V. S., Zukerberg, L. R., Thompson, G. B., van Heerden, J. A., Grant, C. S., & Lloyd, R. V. (2000) · Modern Pathology · doi:10.1038/modpathol.3880034 · Cited by 81
Saeger, W., Faßnacht, M., Chita, R., Prager, G., Nies, C., Lorenz, K., Bärlehner, E., Simon, D., Niederle, B., Beuschlein, F., et al. (2003) · Human Pathology · doi:10.1053/hupa.2003.24 · Cited by 79
Differences in the molecular mechanisms of adrenocortical tumorigenesis between children and adults
Faria, A. M., & Almeida, M. Q. (2011) · Molecular and Cellular Endocrinology · doi:10.1016/j.mce.2011.09.040 · Cited by 82
“Differentiation between benign and malignant adrenal lesions is based on macroscopic features (tumor weight, hemorrhage, breached or intact tumor capsule) and microscopic diagnostic criteria with the Weiss score, the most widely used tool (Aubert et al., 2002; Lau and Weiss, 2009; Weiss, 1984).”
Pan, C., Chen, P. C.-H., Tsay, S., et al. (2005) · Applied immunohistochemistry & molecular morphology · doi:10.1097/01.pai.0000146525.72531.19 · Cited by 80
“The diagnosis of ACC was made based on the Weiss system.(18,19) Five hundred nine tumors of other kinds, preferentially epithelial tumors, were randomly selected from the same surgical pathologic archive.”
Method
Metadata
- Authors
- Weiss, L. M.
- Corresponding author
- Weiss, Lawrence M.
- ORCID
- Weiss, Lawrence M.
- Venue
- The American Journal of Surgical Pathology
- Published
- 1984-03
- Volume
- 8
- Issue
- 3
- Pages
- 163-170
- ISSN
- 0147-5185 (ISSN-L)
- OpenAlex
- W2039836243
- Cited by
- 920
- References
- 0
- Citations by year
- 2026: 21 · 2025: 19 · 2024: 24 · 2023: 23 · 2022: 31 · 2021: 38 · 2020: 36 · 2019: 24 · 2018: 32 · 2017: 28 · 2016: 39 · 2015: 44 · 2014: 50 · 2013: 29 · 2012: 26
- FWCI
- 6.86
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- The American Journal of Surgical Pathology (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Health Sciences › Medicine › Surgery › Adrenal and Paraganglionic Tumors
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adrenal Hormones and Disorders
- Health Sciences › Medicine › Oncology › Renal cell carcinoma treatment
- Keywords
- adrenocortical tumors, adrenal metastasis, tumor recurrence, histologic grading, mitotic activity, atypical mitoses, venous invasion, capsular invasion, clear cells, tumor differentiation, adrenocortical carcinoma
- MeSH terms
- Adenoma, Adrenal Cortex Neoplasms, Adult, Aged, Carcinoma, Female, Humans, Male, Middle Aged, Mitosis, Necrosis, Neoplasm Recurrence, Local, Prognosis
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