Pathologic features of prognostic significance in adrenocortical carcinoma
Abstract
There are currently no well-established pathologic prognostic factors helpful in distinguishing low versus high grade adrenocortical carcinomas. The effect of 11 pathologic parameters on survival was investigated in 42 cases of adrenocortical carcinoma. Only one variable, mitotic rate, had a strong statistical association with patient outcome. The 21 patients with carcinomas with greater than 20 mitoses per 50 high power fields (hpf) had a median survival of 14 months, whereas the 21 patients with carcinomas with less than or equal to 20 mitoses had a median survival of 58 months (p less than 0.02). The presence of atypical mitoses, capsular invasion, tumor weight greater than 250 g, and size greater than 10 cm each showed a marginal statistical association with poor survival (p less than 0.06), whereas other features assessed, such as nuclear grade, presence of necrosis or of venous or sinusoidal invasion, character of the tumor cell cytoplasm, or architectural pattern, showed no statistical significance in predicting survival. It is proposed that adrenal cortical carcinomas with greater than 20 mitoses be designated high grade, whereas tumors with less than or equal to 20 mitoses be designated low grade.
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A Weiss score above 3 (also on the modified score) is associated with an increased risk of malignant behavior.
“A threshold above a Weiss score of 3 (also on the modified score) was associated with an increased risk of malignant behavior (112).”
From Adrenal incidentaloma (2020) · cites this paper as [112]
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 [112]
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Lacroix, A., Feelders, R. A., Stratakis, C. A., & Nieman, L. K. (2015) · The Lancet · doi:10.1016/s0140-6736(14)61375-1 · Cited by 1,777 · see citing works
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 · see citing works
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“ACCs can be graded into low- and high-grade carcinoma groups based on their mitotic rates ( 20 mitoses per 50 high-power fields [HPFs] vs 20 mitoses per 50 HPFs), an observation first made by examining the individual components of the Weiss score for prognostic significance (139).”
MethodA Survey on Adrenal Incidentaloma in Italy
Mantero, F. (2000) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.85.2.637 · Cited by 907 · see citing works
The clinically inapparent adrenal mass: update in diagnosis and management
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“For adrenocortical tumors, the histological classification system by Weiss is most commonly used (312, 313).”
BackgroundMethodAdrenocortical Carcinoma: Clinical Update
Allolio, B., & Fassnacht, M. (2006) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2005-2639 · Cited by 775 · see citing works
Adjuvant 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 · see citing works
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Zheng, S., Cherniack, A. D., Dewal, N., Moffitt, R. A., Danilova, L., Murray, B. A., Lerario, A. M., Else, T., Knijnenburg, T. A., Ciriello, G., et al. (2016) · Cancer Cell · doi:10.1016/j.ccell.2016.04.002 · Cited by 657 · see citing works
“Histologic grading of ACC based on proliferation (Giordano, 2011; Weiss et al., 1989) refines treatment decisions for specific patient subgroups, but is not universally accepted (Miller et al., 2010).”
Michalkiewicz, E., Sandrini, R., Figueiredo, B., Miranda, E. C. M., Caran, E., Oliveira-Filho, A. G., Marques, R., Pianovski, M. A. D., Lacerda, L., Cristofani, L. M., et al. (2004) · Journal of Clinical Oncology · doi:10.1200/jco.2004.08.085 · Cited by 519 · see citing works
“These data are consistent with the results of several studies [4,14,26-30] that found tumor size to be associated with prognosis.”
ResultUrine steroid metabolomics as a biomarker tool for detecting malignancy in adrenal tumors
Arlt, W., Biehl, M., Taylor, A. E., Hahner, S., Libé, R., Hughes, B. A., Schneider, P., Smith, D. J., Stiekema, H., Krone, N., et al. (2011) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2011-1565 · Cited by 458 · see citing works
“a The Weiss system scores the presence or absence of nine histopathological features (Weiss score range 0–9); scores under 3 are indicative of a benign adrenal tumor, scores of 3 are borderline, and scores of 4 and above are indicative of malignancy (14).”
BackgroundFaßnacht, 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 · see citing works
Management of patients with adrenal cancer: recommendations of an international consensus conference
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“Recommended criteria for determining prognosis (Weiss et al. 1988)”
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 · see citing works
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“Additionally, based on mitotic activity, it is possible to divide ACCs into prognostically significant low- and high-grade subgroups.(3) There are also undifferentiated tumors of the retroperitoneum that are not readily identified as adrenocortical in origin using routine pathological methods.”
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Adrenal Cortical Neoplasms in the Pediatric Population
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“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.”
BackgroundMethodClinical management of adrenocortical carcinoma
Fassnacht, M., & Allolio, B. (2009) · Best Practice & Research Clinical Endocrinology & Metabolism · doi:10.1016/j.beem.2008.10.008 · Cited by 349 · see citing works
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“The Lin–Weiss–Bisceglia system (Table 4) has been developed to evaluate oncocytic adrenal cortical neoplasms [122, 128, 135].”
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“com/edrv A threshold above a Weiss score of 3 (also on the modified score) was associated with an increased risk of malignant behavior (112).”
BackgroundAdrenal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up
Berruti, A., Baudin, É., Gelderblom, H. A. J., Haak, H. R., Porpiglia, F., Faßnacht, M., & Pentheroudakis, G. (2012) · Annals of Oncology · doi:10.1093/annonc/mds231 · Cited by 330 · see citing works
“[8] and includes the following parameters: mitosis, atypical mitosis, necrosis, venous invasion, sinusal invasion, capsular invasion, nuclear atypia, diffuse architecture, and clear cell.”
BackgroundAdrenocortical Carcinoma: Diagnosis, Evaluation and Treatment
NG, L., & LIBERTINO, J. M. (2003) · The Journal of Urology · doi:10.1097/00005392-200301000-00003 · Cited by 330 · see citing works
Adrenocortical Oncocytic Tumors: Report of 10 Cases and Review of the Literature
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“The presence of 2 of these criteria is considered allowable in benign tumors while the presence of ≥3 criteria is suggestive of malignancy [32,34].”
BackgroundSelf-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 · see citing works
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 · see citing works
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“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 · see citing works
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“From a prognostic point of view, the mitotic index or the Ki-67 staining index has emerged as single parameters correlated with survival in various studies (11, 12, 17, 19, 39, 40).”
BackgroundMethodGatta-Cherifi, B., Chabre, O., Murat, A., Niccoli, P., Cardot-Bauters, C., Rohmer, V, Young, J., Delemer, B., Du Boullay, H., Verger, M. F., et al. (2012) · European Journal of Endocrinology · doi:10.1530/eje-11-0679 · Cited by 230 · see citing works
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Self-citationChildhood Adrenocortical Tumors1
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Management of adrenocortical carcinoma
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“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.”
BackgroundMethodElse, T., Williams, A. R., Sabolch, A. N., Jolly, S., Miller, B. S., & Hammer, G. D. (2013) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2013-2856 · Cited by 199 · see citing works
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“histologic diagnoses were confirmed by two experienced pathologists at our centre (EB, MV) according to the Weiss criteria [17,18].”
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Incidentally Discovered Adrenal Tumors: Endocrine and Scintigraphic Correlates1
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Update on CT and MRI of adrenal nodules
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Prospective evaluation of mitotane toxicity in adrenocortical cancer patients treated adjuvantly
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“…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.).”
MethodKimura, N., Watanabe, T., Noshiro, T., Shizawa, S., & Miura, Y. (2005) · Endocrine Pathology · doi:10.1385/ep:16:1:023 · Cited by 162 · see citing works
Kyles, A. E., Feldman, E. C., Cock, H. E. V. D., Kass, P. H., Mathews, K. G., Hardie, E. M., Nelson, R. W., Ilkiw, J. E., & Gregory, C. R. (2003) · Journal of the American Veterinary Medical Association · doi:10.2460/javma.2003.223.654 · Cited by 164 · see citing works
Saji, H., Koike, M., Yamori, T., Saji, S., Seiki, M., Matsushima, K., & Toi, M. (2001) · Cancer · doi:10.1002/1097-0142(20010901)92:5 · Cited by 283 · see citing works
Biology, 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 · see citing works
“Mitotic rate is consistently reported as the most important determinant of aggressive behavior [32,41,47,48].”
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 · see citing works
“The Weiss score was established on the basis of 9 Weiss histologic criteria (20, 21).”
BackgroundMethodAdrenal tumors: How to establish malignancy?
Faßnacht, M., Kenn, W., & Allolio, B. (2004) · Journal of Endocrinological Investigation · doi:10.1007/bf03351068 · Cited by 141 · see citing works
MORIMOTO, 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 · see citing works
“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].”
MethodComparative Genomic Hybridization Analysis of Adrenocortical Tumors
Sidhu, S. B., Marsh, D. J., Theodosopoulos, G., Philips, J. N., Bambach, C. P., Campbell, P. R., Magarey, C. J., Russell, C. F. J., Schulte, K., Röher, H. D., et al. (2002) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jcem.87.7.8697 · Cited by 144 · see citing works
<i>p53</i> 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 · see citing works
Kendrick, M. L. (2001) · Archives of Surgery · doi:10.1001/archsurg.136.5.543 · Cited by 140 · see citing works
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 · see citing works
“Concerning mitotic index, the most significant prognostic cut-off in our series was 9 ⁄ 50 HPF (representing the median value), at variance with other authors who used a level of 20 ⁄ 50 HPF.12,20 However, irrespective of the cut-off values employed, it is noteworthy that the vast majority of published series agree th…”
ResultChildhood adrenocortical tumours
Ribeiro, R. C., & de Figueiredo, B. C. (2004) · European Journal of Cancer · doi:10.1016/j.ejca.2004.01.031 · Cited by 140 · see citing works
Adrenocortical carcinoma — towards genomics guided clinical care
Crona, J., & Beuschlein, F. (2019) · Nature Reviews Endocrinology · doi:10.1038/s41574-019-0221-7 · Cited by 140 · see citing works
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 · see citing works
“A total score of %2 is typically associated with a benign ACT while a score of R3 is indicative of malignancy (Weiss 1984, Weiss et al. 1989).”
BackgroundMethodInfluentialTerzolo, 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 · see citing works
“All diagnoses were confirmed by experienced pathologists according to the Weiss criteria with a score of 3, or more, identifying malignancy (18, 19).”
BackgroundMethodBonnet, 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 · see citing works
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 130 · see citing works
Seccia, T. M., Fassina, A., Nussdorfer, G. G., Pessina, A. C., & Rossi, G. P. (2005) · Endocrine Related Cancer · doi:10.1677/erc.1.00867 · Cited by 131 · see citing works
“…1984, Stone et al. 1984, Scott et al. 1986, Valentini et al. 1986, Farge et al. 1987, Fraser et al. 1987, Isles et al. 1987, Tenschert et al. 1987, Weiss et al. 1989, Touitou et al. 1992, Barksdale et al. 1993, Boscaro et al. 1995, Weingartner et al. 1995, Sakai et al. 1997, Taylor et al. 1997,…”
BackgroundAldosterone- and cortisol-co-secreting adrenal tumors: the lost subtype of primary aldosteronism
Späth, M. R., Korovkin, S., Antke, C., Anlauf, M., & Willenberg, H. S. (2011) · European Journal of Endocrinology · doi:10.1530/eje-10-1070 · Cited by 130 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
“The prognostic importance of histology has been controversial (51,52, 54).”
BackgroundMethodMcAteer, J. P., Huaco, J. A., & Gow, K. W. (2013) · Journal of Pediatric Surgery · doi:10.1016/j.jpedsurg.2013.02.017 · Cited by 127 · see citing works
“The system developed by Weiss is widely utilized as a criterion to differentiate adrenocortical adenomas from carcinomas, and in adults these criteria tend to be accurate predictors of malignant behavior [4,10].”
MethodSangoi, A. R., Fujiwara, M., West, R. B., Montgomery, K. D., Bonventre, J. V., Higgins, J., Rouse, R. V., Gökden, N., & McKenney, J. K. (2011) · The American Journal of Surgical Pathology · doi:10.1097/pas.0b013e3182152629 · Cited by 121 · see citing works
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 · see citing works
Schmitz, K., Helwig, J., Bertram, S., Sheu, S., Suttorp, A., Seggewiss, J., Willscher, E., Walz, M., Worm, K., & Schmid, K. W. (2011) · Journal of Clinical Pathology · doi:10.1136/jcp.2010.085621 · Cited by 120 · see citing works
“The validation cohort comprised 15 primary adrenocortical lesions and one lung metastasis, all scored according to the criteria of Weiss et al.(15) The tumours for this study were reviewed by KJS.”
MethodMao, B., Zhang, L., Ning, P., Ding, F. H., Wu, F., Lu, G. G., Geng, Y., & Ma, J. (2020) · European Radiology · doi:10.1007/s00330-020-07056-5 · Cited by 120 · see citing works
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 · see citing works
“A variety of histologic indices of adrenal malignancy has been proposed based on the presence of a diffuse growth pattern, nuclear pleomorphism, tumor necrosis, intratumoral fibrous bands, mitotic figures, vascular, capsular, or sinusoidal invasion, and less than 25% of clear cells.(6,7) The distinction of adrenocorti…”
BackgroundHelsinki 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 · see citing works
Hoang, M. P., Ayala, A. G., & Albores‐Saavedra, J. (2002) · Modern Pathology · doi:10.1038/modpathol.3880638 · Cited by 115 · see citing works
“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…”
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 · see citing works
“Both studies identified mitotic activity as the single most important determinant of tumor-related mortality from adrenocortical carcinoma (5, 6).”
BackgroundMethodInfluentialAdrenal oncocytic neoplasm: a systematic review.
Mearini, L., Sordo, R. D., Costantini, E., et al. (2013) · PubMed · doi:10.1159/000345141 · Cited by 113 · see citing works
Mendonca, 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 · see citing works
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 · see citing works
Contemporary 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 · see citing works
“Among these, theWeiss criteria aremostwidely utilised [69,70].”
The 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 · see citing works
“5 (2-30) Weight, (range) (g) 39 (4-150) 428 (8-3100) 46 (2.”
Diagnostic value of urinary steroid profiling in the evaluation of adrenal tumors
Kerkhofs, T. M. A., Kerstens, M. N., Kema, I. P., Willems, T. P., & Haak, H. R. (2015) · Hormones and Cancer · doi:10.1007/s12672-015-0224-3 · Cited by 102 · see citing works
“In patients with ACC, the Weiss score (a set of nine histopathological criteria with prognostic value in adrenocortical tumors) was extracted from the original pathology reports and disease progression was staged according to the European Network for Study of Adrenal Tumors (ENSAT) staging system [16, 17].”
MethodAdrenal cortical carcinoma in Norway, 1970–1984
Søreide, J. A., Brabrand, K., & Thoresen, S. (1992) · World Journal of Surgery · doi:10.1007/bf02067349 · Cited by 101 · see citing works
Operative management for recurrent and metastatic adrenocortical carcinoma
Datrice, N., Langan, R. C., Ripley, R. T., Kemp, C. D., Steinberg, S. M., Wood, B. J., Libutti, S. K., Fojo, T., Schrump, D. S., & Avital, I. (2011) · Journal of Surgical Oncology · doi:10.1002/jso.23015 · Cited by 99 · see citing works
“In our review, the number of patients receiving neoadjuvant therapy was small [5], making it difficult to draw conclusions from this group.”
BackgroundValidation 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 · see citing works
“As a matter of fact, in 1989 Dr Weiss himself proposed a mitotic count–based, two-tier grading system, distinguishing low-grade (<20/50 HPF) from high-grade ACC (>20/50 HPF) [20].”
BackgroundInfluentialAdrenal Cortical Neoplasms in Children: Why So Many Carcinomas and Yet So Many Survivors?
Dehner, L. P., & Hill, D. A. (2009) · Pediatric and Developmental Pathology · doi:10.2350/08-06-0489.1 · Cited by 95 · see citing works
“Histologic criteria for malignancy consisted of 11 features that were adapted from several previously cited systems [30,31,33].”
BackgroundMethodImmunohistochemical 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 · see citing works
Schmitt, 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 · see citing works
Galindo, C. R., Krailo, M., Pinto, E. M., Pashankar, F., Weldon, C. B., Huang, L. T., Caran, E. M. M., Hicks, J. M., McCarville, M. B., Malkin, D. M., et al. (2021) · Journal of Clinical Oncology · doi:10.1200/jco.20.02871 · Cited by 98 · see citing works
“Central pathology review was required for eligibility.(14,15) The trial was approved by the Pediatric Central Institutional Review Board of the National Cancer Institute, and by the institutional review boards of participating institutions.”
Genetic landscape of sporadic unilateral adrenocortical adenomas without PRKACA p.Leu206Arg mutation
Ronchi, C. L., Di Dalmazi, G., Faillot, S., Sbiera, S., Assié, G., Weigand, I., Calebiro, D., Schwarzmayr, T., Appenzeller, S., Rubin, B., et al. (2016) · The Journal of Clinical Endocrinology & Metabolism · doi:10.1210/jc.2016-1586 · Cited by 93 · see citing works
Fragoso, M. C. B. V., Almeida, M. Q., Mazzuco, T. L., Mariani, B. M. P., Brito, L. P., Gonçalves, T. C., Alencar, G. A., Lima, L. D. O., Faria, A. M., Bourdeau, I., et al. (2012) · European Journal of Endocrinology · doi:10.1530/eje-11-0806 · Cited by 93 · see citing works
Ichijo, T., Ueshiba, H., Nawata, H., & Yanase, T. (2019) · Endocrine Journal · doi:10.1507/endocrj.ej18-0486 · Cited by 92 · see citing works
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 · see citing works
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 · see citing works
“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 · see citing works
Value of Molecular Classification for Prognostic Assessment of Adrenocortical Carcinoma
Assié, G., Jouinot, A., Faßnacht, M., Libé, R., Garinet, S., Jacob, L., Hamzaoui, N., Néou, M., Sakat, J., Villéon, B. D. L., et al. (2019) · JAMA Oncology · doi:10.1001/jamaoncol.2019.1558 · Cited by 88 · see citing works
Yang, J. Y., Yang, M. Q., Luo, Z., Ma, Y., Li, J., Deng, Y., & Huang, X. (2008) · BMC Genomics · doi:10.1186/1471-2164-9-s1-s23 · Cited by 88 · see citing works
Diagnostic and Prognostic Biomarkers of Adrenal Cortical Carcinoma
Mete, Ö., Güçer, H., Kefeli, M., & Asa, S. L. (2017) · The American Journal of Surgical Pathology · doi:10.1097/pas.0000000000000943 · Cited by 86 · see citing works
Proposal for modification of the ENSAT staging system for adrenocortical carcinoma using tumor grade
Miller, B. S., Gauger, P. G., Hammer, G. D., Giordano, T. J., & Doherty, G. M. (2010) · Langenbeck s Archives of Surgery · doi:10.1007/s00423-010-0698-y · Cited by 84 · see citing works
Fenske, W., Völker, H., Adam, P., Hahner, S., Johanssen, S., Wortmann, S., Schmidt, M., Morcos, M., Müller–Hermelink, H., Allolio, B., et al. (2009) · Endocrine Related Cancer · doi:10.1677/erc-08-0211 · Cited by 84 · see citing works
“All histological diagnoses were confirmed by the reference pathologist of the German ACC Registry (Wolfgang Saeger, Hamburg, Germany) and malignancy was established by a Weiss score R3 (Weiss et al. 1989).”
Method
- Authors
- Weiss, L. M., Medeiros, L. J., & Vickery, A. L.
- Affiliations
- Stanford University (US)
- Massachusetts General Hospital (US)
- Venue
- The American Journal of Surgical Pathology
- Published
- 1989-03
- Volume
- 13
- Issue
- 3
- Pages
- 202-206
- ISSN
- 0147-5185 (ISSN-L)
- OpenAlex
- W2023370041
- Cited by
- 818
- References
- 0
- Citations by year
- 2026: 13 · 2025: 21 · 2024: 19 · 2023: 20 · 2022: 33 · 2021: 30 · 2020: 34 · 2019: 22 · 2018: 27 · 2017: 30 · 2016: 31 · 2015: 40 · 2014: 38 · 2013: 33 · 2012: 34
- FWCI
- 8.11
- 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 › Pulmonary and Respiratory Medicine › Renal cell carcinoma treatment
- Health Sciences › Medicine › Pulmonary and Respiratory Medicine › Sarcoma Diagnosis and Treatment
- Keywords
- adrenocortical carcinoma, prognostic factors, mitotic activity, tumor grade, survival, capsular invasion, tumor size, tumor weight, atypical mitoses, venous invasion, nuclear grade, necrosis
- MeSH terms
- Adolescent, Adrenal Cortex Neoplasms, Adult, Aged, Carcinoma, Child, Humans, Middle Aged, Mitotic Index, Neoplasm Invasiveness, Prognosis
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