{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2025,12,6]],"date-time":"2025-12-06T04:17:56Z","timestamp":1764994676101,"version":"3.46.0"},"reference-count":35,"publisher":"BMJ","issue":"5","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["J Clin Pathol"],"published-print":{"date-parts":[[1990,5]]},"abstract":"<jats:p>Nucleolar organiser regions (NORs), which are important for regulating protein synthesis, were identified in 20 breast carcinomas by means of a silver (Ag) staining technique. Infiltrating neoplasms with metastases in four or more axillary lymph nodes possessed, on average, a greater number of AgNORs per cell nucleus compared with neoplasms without nodal disease, or with one to three positive lymph nodes. The size, morphology, and distribution of AgNORs within the nucleus were also different in the two study groups. Overall, these findings suggest that breast carcinomas with multiple, irregular, and widely dispersed AgNORs tend to be of high grade malignancy.<\/jats:p>","DOI":"10.1136\/jcp.43.5.390","type":"journal-article","created":{"date-parts":[[2007,6,9]],"date-time":"2007-06-09T00:50:46Z","timestamp":1181350246000},"page":"390-392","source":"Crossref","is-referenced-by-count":44,"title":["Nucleolar organiser regions: new prognostic variable in breast carcinomas."],"prefix":"10.1136","volume":"43","author":[{"given":"E","family":"Sivridis","sequence":"first","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]},{"given":"B","family":"Sims","sequence":"additional","affiliation":[],"role":[{"role":"author","vocabulary":"crossref"}]}],"member":"239","published-online":{"date-parts":[[1990,5,1]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"189","DOI":"10.1111\/j.1768-322X.1986.tb00452.x","article-title":"The nucleolus and the nucleolar organizer regions","volume":"56","author":"Fakan, S.; Hernandez-Verdun, D.","year":"1986","unstructured":"Fakan S, Hernandez-Verdun D. The nucleolus and the nucleolar organizer regions. Biol Cell 1986;56:189-206.","journal-title":"Biol Cell"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"638","DOI":"10.1016\/S0140-6736(61)91655-5","article-title":"Observations on the satellited human chromosomes","volume":"i:","author":"Ferguson-Smith, M.A.; Handmaker, S.D.","year":"1961","unstructured":"Ferguson-Smith MA, Handmaker SD. Observations on the satellited human chromosomes. Lancet 1961;i:638-40.","journal-title":"Lancet"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1002\/path.1711510203","article-title":"Nucleolar organizer regions in lymphomas","volume":"151","author":"Crocker, J.; Nar, P.","year":"1987","unstructured":"Crocker J, Nar P. Nucleolar organizer regions in lymphomas. J Pathol 1987;151:111-8.","journal-title":"J Pathol"},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"113","DOI":"10.1111\/j.1365-2559.1988.tb01923.x","article-title":"Evaluation of nucleolar organizer region-associated proteins in breast malignancy","volume":"12","author":"Smith, R.; Crocker, J.","year":"1988","unstructured":"Smith R, Crocker J. Evaluation of nucleolar organizer region-associated proteins in breast malignancy. Histopathology 1988;12:113-25.","journal-title":"Histopathology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1007\/BF01676192","article-title":"Improvement in the staining and in the visualization of the argyrophilic proteins of the nucleolar organizer region at the optical level","volume":"18","author":"Ploton, D.; Menager, M.; Jeanesson, P.; Himber, G.; Pigeon, F.; Adnet, J.-J.","year":"1986","unstructured":"Ploton D, Menager M, Jeanesson P, Himber G, Pigeon F, Adnet J-J. Improvement in the staining and in the visualization of the argyrophilic proteins of the nucleolar organizer region at the optical level. Histochem J 1986; 18:5-14.","journal-title":"Histochem J"},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"615","DOI":"10.1016\/0309-1651(79)90060-2","article-title":"Identification of a silver binding protein associated with the cytologicaf silver staining of actively transcribing nucleolar regions","volume":"3","author":"Hubbell, H.R.; Rothblum, L.I.; Hsu, T.C.","year":"1979","unstructured":"Hubbell HR, Rothblum LI, Hsu TC. Identification of a silver binding protein associated with the cytologicaf silver staining of actively transcribing nucleolar regions. Cell Biol Int Rep 1979;3:615-22.","journal-title":"Cell Biol Int Rep"},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"701","DOI":"10.1016\/0024-3205(79)90512-5","article-title":"Proteins C23 and B23 are the major nucleolar silver staining proteins","volume":"25","author":"Lischwe, M.A.; Smetana, K.; Olson, M.O.J.; Busch, H.","year":"1979","unstructured":"Lischwe MA, Smetana K, Olson MOJ, Busch H. Proteins C23 and B23 are the major nucleolar silver staining proteins. Life Sci 1979;25:701-8.","journal-title":"Life Sci"},{"key":"ref_8","first-page":"139","article-title":"Localization of nucleolar phosphoproteins B23 and C23 during mitosis. Exp Cell Res 1983; 146","author":"Ochs, R.; Lischwe, M.; O'Leary, P.; Busch, H.","unstructured":"Ochs R, Lischwe M, O'Leary P, Busch H. Localization of nucleolar phosphoproteins B23 and C23 during mitosis. Exp Cell Res 1983;146:139-49."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1016\/0014-4827(82)90035-0","article-title":"Argyrophilic nuclear and nucleolar proteins of Xenopus laevis oocytes identified by gel electrophoresis","volume":"137","author":"Williams, M.A.; Kleinschmidt, J.A.; Krohne, G.; Franke, W.W.","year":"1982","unstructured":"Williams MA, Kleinschmidt JA, Krohne G, Franke WW. Argyrophilic nuclear and nucleolar proteins of Xenopus laevis oocytes identified by gel electrophoresis. Exp Cell Res 1982;137:341-51.","journal-title":"Exp Cell Res"},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1159\/000131585","article-title":"Expression of silver stained nucleolar organizing regions (AgNORs) in human cancer","volume":"30","author":"Trent, J.M.; Carlin, D.A.; Davies, JR","year":"1981","unstructured":"Trent JM, Carlin DA, Davies JR. Expression of silver stained nucleolar organizing regions (AgNORs) in human cancer. Cytogenet Cell Genet 1981;30:31-8.","journal-title":"Cytogenet Cell Genet"},{"key":"ref_11","first-page":"307","article-title":"Silver-binding nucleolar organizer regions (Ag-NORs) in benign and malignant breast lesions: correlations with ploidy and growth phase by DNA flow cytometry","volume":"57","author":"Giri, D.D.; Nottingham, J.F.; Lawry, J.; Dundas, S.A.C.; Underwood, J.C.E.","year":"1986","unstructured":"Giri DD, Nottingham JF, Lawry J, Dundas SAC, Underwood JCE. Silver-binding nucleolar organizer regions (Ag-NORs) in benign and malignant breast lesions: correlations with ploidy and growth phase by DNA flow cytometry. J Pathol 1986;57:307-13.","journal-title":"J Pathol"},{"key":"ref_12","first-page":"925","article-title":"Relationship between interphasic nucleolar organizer regions and growth rate in two neuroblastoma cell lines","volume":"134","author":"Derenzini, M.; Pession, A.; Farabegoli, F.; Trere, D.; Badiali, M.; Dehan, P.","year":"1989","unstructured":"Derenzini M, Pession A, Farabegoli F, Trere D, Badiali M, Dehan P. Relationship between interphasic nucleolar organizer regions and growth rate in two neuroblastoma cell lines. Am J Pathol 1989;134:925-32.","journal-title":"Am J Pathol"},{"key":"ref_13","first-page":"166","article-title":"The relationship between numbers of interphase NORs and NOR-bearing chromosomes in nonHodgkin's lymphoma","volume":"157","author":"Crocker, J.; Janmohamed, R.M.I.; Armstrong, S.J.; Hulten, M.; Leyland, M.J.","year":"1989","unstructured":"Crocker J, Janmohamed RMI, Armstrong SJ, Hulten M, Leyland MJ. The relationship between numbers of interphase NORs and NOR-bearing chromosomes in nonHodgkin's lymphoma. JPathol 1989;157:166A.","journal-title":"JPathol"},{"key":"ref_14","first-page":"885","article-title":"Nucleolar organizer region associated proteins in cutaneous melanotic lesions: a quantitative Sivridis, Sims study.]J Clin Pat\/aol","volume":"40","author":"Croker, J.; Skilbeck, N.","year":"1987","unstructured":"Croker J, Skilbeck N. Nucleolar organizer region associated proteins in cutaneous melanotic lesions: a quantitative Sivridis, Sims study.]J Clin Pat\/aol 1987;40:885-9."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1111\/j.1365-2559.1988.tb02007.x","article-title":"Nucleolar organizer regions in melanocytic dysplasia and melanoma","volume":"13","author":"Fallowfield, M.E.; Dodson, A.R.; Cook, M.G.","year":"1988","unstructured":"Fallowfield ME, Dodson AR, Cook MG. Nucleolar organizer regions in melanocytic dysplasia and melanoma. Histopathology 1988;13:95-9.","journal-title":"Histopathology"},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"227","DOI":"10.1002\/path.1711560307","article-title":"Silverstained nucleoli and nucleolar organizer region counts are of no prognostic value in thick cutaneous malignant melanoma","volume":"156","author":"Howat, A.J.; Giri, D.D.; Wright, A.L.; Underwood, J.C.E.","year":"1988","unstructured":"Howat AJ, Giri DD, Wright AL, Underwood JCE. Silverstained nucleoli and nucleolar organizer region counts are of no prognostic value in thick cutaneous malignant melanoma. J Pathol 1988;156:227-32.","journal-title":"J Pathol"},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"123","DOI":"10.1093\/ajcp\/88.2.123","article-title":"Predictors of recurrence and survival of patients with breast cancer","volume":"88","author":"Russo, J.; Frederick, J.; Ownby, H.E.","year":"1987","unstructured":"Russo J, Frederick J, Ownby HE. Predictors of recurrence and survival of patients with breast cancer. Am J Clin Pathol 1987;88:123-31.","journal-title":"Am J Clin Pathol"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1918","DOI":"10.1002\/1097-0142(19870601)59:11<1918::AID-CNCR2820591113>3.0.CO;2-Y","article-title":"Angioinvasion in breast carcinoma. An immunohistochemical study of factor VIII-related antigen","volume":"59","author":"Martin, S.A.; Perez-Reyes, N.; Mendelsohn, G.","year":"1987","unstructured":"Martin SA, Perez-Reyes N, Mendelsohn G. Angioinvasion in breast carcinoma. An immunohistochemical study of factor VIII-related antigen. Cancer 1987;59:1918-22.","journal-title":"Cancer"},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"1299","DOI":"10.1002\/1097-0142(19870915)60:6<1299::AID-CNCR2820600623>3.0.CO;2-L","article-title":"Histologic malignancy grading of invasive ductal breast carcinoma","volume":"60","author":"Rank, F.; Dombernowsky, P.; Jespersen, N.C.B.","year":"1987","unstructured":"Rank F, Dombernowsky P, Jespersen NCB, et al. Histologic malignancy grading of invasive ductal breast carcinoma. Cancer 1987;60:1299-305.","journal-title":"Cancer"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"758","DOI":"10.1002\/1097-0142(19880215)61:4<758::AID-CNCR2820610421>3.0.CO;2-T","article-title":"The prognostic value and relationships of patient characteristics, estrogen and progestin receptors, and site of relapse in primary breast cancer","volume":"61","author":"Alexieva-Figusch, J.; van Putten, W.L.J.; Blankestein, M.A.","year":"1988","unstructured":"Alexieva-Figusch J, van Putten WLJ, Blankestein MA, et al. The prognostic value and relationships of patient characteristics, estrogen and progestin receptors, and site of relapse in primary breast cancer. Cancer 1988;61:758-68.","journal-title":"Cancer"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"2883","DOI":"10.1002\/1097-0142(197706)39:6<2883::AID-CNCR2820390676>3.0.CO;2-9","article-title":"L-Phenylalanine mustard (L-PAM) in the management of primary breast cancer: An update of earlier findings and a comparison of the utilizing L-PAM plus 5 fluorouracil (5 FU)","volume":"39","author":"Fisher, B.; Glass, A.; Redmond, C.","year":"1977","unstructured":"Fisher B, Glass A, Redmond C, et al. L-Phenylalanine mustard (L-PAM) in the management of primary breast cancer: An update of earlier findings and a comparison of the utilizing L-PAM plus 5 fluorouracil (5 FU). Cancer 1977;39:2883-903.","journal-title":"Cancer"},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"2917","DOI":"10.1002\/1097-0142(19800615)45:12<2917::AID-CNCR2820451203>3.0.CO;2-M","article-title":"Management and survival of female breast cancer: Results of a national survey by the American College of Surgeons","volume":"45","author":"Nemoto, T.; Vana, J.; Bedwani, R.N.","year":"1980","unstructured":"Nemoto T, Vana J, Bedwani RN, et al. Management and survival of female breast cancer: Results of a national survey by the American College of Surgeons. Cancer 1980; 45:2917-24.","journal-title":"Cancer"},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"1551","DOI":"10.1002\/1097-0142(19831101)52:9<1551::AID-CNCR2820520902>3.0.CO;2-3","article-title":"Redmon CK, Fisher ER. Relation of number of positive axillary nodes to prognosis of patients with primary breast cancer","volume":"52","author":"Fisher, B.; Bauer, M.; Wickerham, I.","year":"1980","unstructured":"Fisher B, Bauer M, Wickerham I, Redmon CK, Fisher ER. Relation of number of positive axillary nodes to prognosis of patients with primary breast cancer. Cancer 1980; 52:1551-7.","journal-title":"Cancer"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"21","DOI":"10.1093\/ajcp\/65.1.21","article-title":"Pathologic findings from the National Surgical Adjuvant Breast Project (Protocol N. 4). II. The significance of regional node histology other than sinus histiocytosis in invasive mammary cancer","volume":"65","author":"Fisher, E.R.; Gregorio, R.; Redmond, C.","year":"1976","unstructured":"Fisher ER, Gregorio R, Redmond C. Pathologic findings from the National Surgical Adjuvant Breast Project (Protocol N. 4). II. The significance of regional node histology other than sinus histiocytosis in invasive mammary cancer. Am J Clin Pathol 1976;65:21-30.","journal-title":"Am J Clin Pathol"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"2809","DOI":"10.1002\/1097-0142(197812)42:6<2809::AID-CNCR2820420642>3.0.CO;2-9","article-title":"Primary Therapy ofBreast Cancer Study Group. Identification of breast cancer patients with high risk of early recurrence after radical mastectomy. II. Clinical and pathological correlation","volume":"42","year":"1978","unstructured":"Primary Therapy ofBreast Cancer Study Group. Identification of breast cancer patients with high risk of early recurrence after radical mastectomy. II. Clinical and pathological correlation. Cancer 1978;42:2809-26.","journal-title":"Cancer"},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"181","DOI":"10.1002\/1097-0142(19890101)63:1<181::AID-CNCR2820630129>3.0.CO;2-H","article-title":"Relation of tumour size, lymph node status, and survival in 24,740 breast cancer cases","volume":"63","author":"Carter, C.L.; Allen, C.; Henson, D.E.","year":"1989","unstructured":"Carter CL, Allen C, Henson DE. Relation of tumour size, lymph node status, and survival in 24,740 breast cancer cases. Cancer 1989;63:181-7.","journal-title":"Cancer"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"151","DOI":"10.1002\/path.1711540207","article-title":"Correlation between DNA flow cytometric and nucleolar organizer region data in non-Hodgkin's lymphomas","volume":"154","author":"Crocker, J.; Macartney, J.C.; Smith, P.J.","year":"1988","unstructured":"Crocker J, Macartney JC, Smith PJ. Correlation between DNA flow cytometric and nucleolar organizer region data in non-Hodgkin's lymphomas. J Pathol 1988;154:151-6.","journal-title":"J Pathol"},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"225","DOI":"10.1136\/jcp.42.3.225","article-title":"Statistics on microcomputers: A nonalgebraic guide to the appropriate use of statistical packages in biomedical research and pathology laboratory practice. 6 Statistical methods for diagnostic tests","volume":"42","author":"Brown, R.A.; Beck, J.S.","year":"1989","unstructured":"Brown RA, Beck JS. Statistics on microcomputers: A nonalgebraic guide to the appropriate use of statistical packages in biomedical research and pathology laboratory practice. 6 Statistical methods for diagnostic tests. J Clin Pathol 1989;42:225-30.","journal-title":"J Clin Pathol"},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1136\/jcp.41.5.527","article-title":"Comparative study ofthe degree ofdifferentiation ofneuroblastoma and mean numbers of nucleolar organiser regions","volume":"41","author":"Egan, M.; Raafat, F.; Crocker, J.; Williams, D.","year":"1988","unstructured":"Egan M, Raafat F, Crocker J, Williams D. Comparative study ofthe degree ofdifferentiation ofneuroblastoma and mean numbers of nucleolar organiser regions. J Clin Pathol 1988;41:527-31.","journal-title":"J Clin Pathol"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1136\/jcp.41.1.31","article-title":"Nucleolar organizer regions in fibrous proliferations of childhood and infantile fibrosarcoma","volume":"41","author":"Egan, M.; Raafat, F.; Crocker, J.; Smith, K.","year":"1988","unstructured":"Egan M, Raafat F, Crocker J, Smith K. Nucleolar organizer regions in fibrous proliferations of childhood and infantile fibrosarcoma. J Clin Pathol 1988;41:31-3.","journal-title":"J Clin Pathol"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"247","DOI":"10.1002\/path.1711540307","article-title":"Nucleolar organizer regions in cutaneous tumours","volume":"154","author":"Egan, M.J.; Crocker, J.","year":"1988","unstructured":"Egan MJ, Crocker J. Nucleolar organizer regions in cutaneous tumours. J Pathol 1988;154:247-53.","journal-title":"J Pathol"},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"1136","DOI":"10.1136\/jcp.41.10.1136-a","article-title":"Limited value of AgNOR enumeration in the assessment of thyroid neoplasms","volume":"41","author":"Nairn, E.R.; Crocker, J.; McGovern, J.","year":"1988","unstructured":"Nairn ER, Crocker J, McGovern J. Limited value of AgNOR enumeration in the assessment of thyroid neoplasms. J Clin Pathol 1988;41:1136.","journal-title":"J Clin Pathol"},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1002\/1097-0142(19890201)63:3<474::AID-CNCR2820630314>3.0.CO;2-3","article-title":"Nucleolar organizer regions in Spitz nevi and malignant melanomas","volume":"63","author":"Howat, A.J.; Giri, D.D.; Cotton, D.W.K.; Slater, D.N.","year":"1989","unstructured":"Howat AJ, Giri DD, Cotton DWK, Slater DN. Nucleolar organizer regions in Spitz nevi and malignant melanomas. Cancer 1989;63:474-8.","journal-title":"Cancer"},{"key":"ref_34","first-page":"173","article-title":"Silverbinding nucleoli and nucleolar organizer regions in fine needle aspiration cytology of the breast","volume":"33","author":"Giri, D.D.; Dundas, S.A.C.; Sanderson, P.R.; Howat, A.J.","year":"1989","unstructured":"Giri DD, Dundas SAC, Sanderson PR, Howat AJ. Silverbinding nucleoli and nucleolar organizer regions in fine needle aspiration cytology of the breast. Acta Cytol 1989;33: 173-5.","journal-title":"Acta Cytol"},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"307","DOI":"10.1002\/path.1711570407","article-title":"Silver-binding nucleolar organizer regions (AgNORs) in benign and malignant breast lesions: correlations with ploidy and growth phase by DNA flow cytometry","volume":"157","author":"Giri, D.D.; Nottingham, J.F.; Lawry, J.; Dundas, S.A.C.; Underwood, J.C.E.","year":"1989","unstructured":"Giri DD, Nottingham JF, Lawry J, Dundas SAC, Underwood JCE. Silver-binding nucleolar organizer regions (AgNORs) in benign and malignant breast lesions: correlations with ploidy and growth phase by DNA flow cytometry. J Pathol 1989;157:307-13.","journal-title":"J Pathol"}],"container-title":["Journal of Clinical Pathology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/syndication.highwire.org\/content\/doi\/10.1136\/jcp.43.5.390","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,12,6]],"date-time":"2025-12-06T03:07:03Z","timestamp":1764990423000},"score":1,"resource":{"primary":{"URL":"https:\/\/jcp.bmj.com\/lookup\/doi\/10.1136\/jcp.43.5.390"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[1990,5]]},"references-count":35,"journal-issue":{"issue":"5","published-online":{"date-parts":[[1990,5,1]]},"published-print":{"date-parts":[[1990,5]]}},"alternative-id":["10.1136\/jcp.43.5.390"],"URL":"https:\/\/doi.org\/10.1136\/jcp.43.5.390","relation":{},"ISSN":["0021-9746","1472-4146"],"issn-type":[{"type":"print","value":"0021-9746"},{"type":"electronic","value":"1472-4146"}],"subject":[],"published":{"date-parts":[[1990,5]]}}}