Advertisement
Research Article| Volume 10, ISSUE 1, P77-103, March 1990

The Application of Monoclonal Antibodies in the Cytologic Evaluation of Tumors

DOI:https://doi.org/10.1016/S0272-2712(18)30583-3
The Application of Monoclonal Antibodies in the Cytologic Evaluation of Tumors
Previous ArticleImmunohfstochemistry in Surgical Pathology: The Case of the Undifferentiated Malignant Neoplasm
Next ArticleTumor Markers in Gynecologic Neoplasms
      This paper is only available as a PDF. To read, Please Download here.
      Advances in monoclonal antibody technology have influenced the practice of diagnostic cytopathology from the types of specimens prepared to the use of antibodies as discriminating adjuncts. Because the type of cytologic specimen often dictates the differential diagnosis and the potential applications of these antibodies, this review focuses on the types of cytopathologic specimens received in the laboratory, including serous effusions, peritoneal washings, fine needle aspirates, cerebrospinal fluid, and cervical-vaginal smears, and describes the potential adjunctive application of antibodies in these specimens.
      To read this article in full you will need to make a payment

      Purchase one-time access:

      Academic & Personal: 24 hour online accessCorporate R&D Professionals: 24 hour online access
      One-time access price info
      • For academic or personal research use, select 'Academic and Personal'
      • For corporate R&D use, select 'Corporate R&D Professionals'

      Subscribers receive full online access to your subscription and archive of back issues up to and including 2002.

      Content published before 2002 is available via pay-per-view purchase only.

      Subscribe:

      Subscribe to Clinics in Laboratory Medicine
      Already a print subscriber? Claim online access
      Already an online subscriber? Sign in
      Register: Create an account
      Institutional Access: Sign in to ScienceDirect

      References

        • Aaronson S.A.
        • Tronick S.R.
        The role of oncogenes in human neoplasia.
        in: DeVita V.T. Heilman S. Rosenberg S.A. Important Advances in Oncology 1985. JB Lippincott, Philadelphia1985: 3
        • Allan P.M.
        • Garson J.A.
        • Harper E.L.
        • et al.
        Biological characterization and clinical applications of a monoclonal antibody recognizing an antigen restricted to neuroectodermal tissues.
        Int J Cancer. 1983; 31: 591
        • Angeli S.
        • Koelma I.
        • Fleuren G.J.
        • et al.
        Malignant melanoma in fine needle aspiration biopsies and effusions. An immunocytochemical study using monoclonal antibodies.
        Acta Cytol. 1988; 32: 707
        • Ashall F.
        • Bramwell M.E.
        • Harris H.
        A new marker for human cancer cells. 1. The Ca antigen and the Ca 1 antibody.
        Lancet. 1982; 2: 1
        • Banks P.M.
        • Caron B.L.
        • Morgan T.W.
        Use of imprints for monoclonal antibody studies: Suitability of air-dried preparations from lymphoid tissues with an immunohistochemical method.
        Am J Clin Pathol. 1983; 79: 438
        • Banks P.M.
        Technical aspects of specimen preparation and special studies.
        in: JaflFe E.S. Surgical Pathology of the Lymph Nodes and Related Organs. WB Saunders, Philadelphia1985: 1
        • Banner B.F.
        • Gould V.F.
        • Radosevich J.A.
        • et al.
        Application of monoclonal antibody 44-3A6 in the cytodiagnosis and classification of pulmonary carcinomas.
        Diagn Cytopathol. 1985; 1: 300
        • Battifora H.
        • Kopinski M.I.
        Distinction of mesothelioma from adenocarcinoma: An immunohistochemical approach.
        Cancer. 1985; 55: 1679
        • Berge T.
        • Hetlsten S.
        Cytological diagnosis of cancer cells in pleural and ascitic fluid.
        Acta Cytol. 1966; 10: 138
        • Bergeron C.
        • Shatz P.
        • Margolese R.
        • et al.
        Immunohistochemical studies with monoclonal antibodies B72.3 and MA5 on histologic and cytologic specimens from benign and malignant breast lesions.
        Anal Quantit Cytol Histol. 1989; 11: 33
        • Bigner S.H.
        • Johnston W.W.
        The diagnostic challenge of tumors manifested initially by the shedding of cells into cerebrospinal fluid.
        Acta Cytol. 1984; 28: 29
        • Bishop J.M.
        Cellular onocogenes and retroviruses.
        Annu Rev Biochem. 1983; 52: 301
        • Bollinger D.J.
        • Wick M.R.
        • Dehner L.P.
        • et al.
        Peritoneal malignant mesothelioma versus serous papillary adenocarcinoma. A histochemical and immunohistochemical com-comparison.
        Am J Surg Pathol. 1989; 13: 659
        • Bramwell M.E.
        • Ghosh A.K.
        • Smith W.D.
        • et al.
        Ca2 and Ca3. New monoclonal antibodies evaluated as tumor markers in serious effusions.
        Cancer. 1985; 56: 105
        • Brown D.C.
        • Gatter K.C.
        • Dunnill M.S.
        • et al.
        Immunocytochemical analysis of cytocertifuged fine needle aspiration biopsies. A study based on lung tumors aspirates in vitro.
        Anal Quant Cytol Histol. 1989; 11: 140
        • Burger P.C.
        • Rawlings C.E.
        • Cox E.B.
        • et al.
        Clinicopathologic correlations in the oligo dendroglioma.
        Cancer. 1987; 59: 1345
        • Canevari S.
        • Fossati G.
        • Balsari A.
        • et al.
        Immunochemical analyses of the determinant recognized by a monoclonal antibody (MBrl) which specifically binds to human mammary epithelial cells.
        Cancer Res. 1983; 43: 1301
        • Carey P.J.
        • Malcolm A.J.
        • Pearson A.D.J.
        • et al.
        Immunocytochemical detection of tumors of neuroectodermal origin.
        J Clin Pathol. 1988; 26: 586
        • Ceriani R.L.
        • Thompson K.
        • Peterson J.A.
        • et al.
        Surface differentiation antigens of human mammary epithelial cells carried on the human milk fat globule.
        Proc Natl Acad Sci USA. 1977; 74: 582
        • Cibas E.S.
        • Carson J.M.
        • Pinkus G.S.
        The distinction of adenocarcinoma from malignant mesothelioma in cell blocks in effusions: The role of routine mucin histochemistry and immunohistochemical assessment of carcinoembryonic antigen, keratin proteins, epithelial membrane antigen, and milk fat globule derived antigen.
        Hum Pathol. 1987; 18: 67
        • Coakham H.B.
        • Brownell B.
        Monoclonal antibodies in the diagnosis of cerebral tumors and CSF neoplasia.
        in: Cavanaugh J.B. Recent Advances in Neuropathology. 3. Churchill Livingstone, New York1986: 25
        • Coakham H.B.
        • Harper E.J.
        • Garson J.A.
        • et al.
        Carcinomatous meningitis diagnosed with monoclonal antibodies.
        Br Med J. 1984; 288: 1272
        • Coakham H.
        • Garson J.
        • Allan P.
        • et al.
        Immunohistological diagnosis of central nervous system tumours using a monoclonal antibody panel.
        J Clin Pathol. 1985; 38: 165
        • Coakham H.
        • Garson J.
        • Brownell B.
        • et al.
        Diagnosis of cerebral neoplasms using monoclonal antibodies.
        Prog Exp Tumor Res. 1985; 29: 57
        • Colcher D.
        • Horan Hand P.
        • Nuti M.
        • et al.
        A spectrum of monoclonal antibodies reactive with human mammary tumor cells.
        Proc Natl Acad Sci USA. 1981; 78: 3199
        • Coleman D.V.
        • Ormerod M.B.
        Tumor markers in cytology.
        in: Koss L.G. Coleman D.V. Advances in Clinical Cytology. 2. Masson, New York1984: 33
        • Collins V.P.
        Monoclonal antibodies to glial fibrillary acidic protein in the cytologic diagnosis of brain tumors.
        Acta Cytol. 1984; 28: 401
        • Cordell J.L.
        • Falini B.
        • Erber W.N.
        • et al.
        Immunoenzymatic labelling of monoclonal antibodies using immune complexes of alkaline phosphatase and monoclonal an tialkaline phosphatase (APAAP).
        J Histochem Cytochem. 1984; 32: 219
        • Cosgrove M.
        • Fitzgibbons P.L.
        • Sherrod A.
        • et al.
        Intermediate filament expression in astrocytic neoplasms.
        Am J Surg Pathol. 1989; 13: 141
        • Cowsert L.M.
        • Lake P.
        • Jenson A.B.
        Topographical and confirmational epitopes of bovine papillomavirus type I defined by monoclonal antibodies.
        JNCI. 1987; 79: 1053
        • Crum C.P.
        • Ikenberg H.
        • Richart R.M.
        • et al.
        Human papillamavirus type 16 in early cervical neoplasia.
        N Engl J Med. 1984; 310: 880
        • Cuttita F.
        • Rosen S.
        • Gazdar A.F.
        • et al.
        Monoclonal antibodies that demonstrate specificity for several types of human lung cancer.
        Proc Natl Acad Sci USA. 1981; 78: 4591
        • Czerniak B.
        • Herz F.
        • Koss L.G.
        • et al.
        Ras oncogene p21 as a tumor marker in the cytodiagnosis of gastric and colonic carcinomas.
        Cancer. 1987; 60: 2432
        • Czerniak B.
        • Papenhausen P.R.
        • Herz F.
        • et al.
        Flow cytometric identification of cancer cells in effusions with Cal monoclonal antibody.
        Cancer. 1985; 55: 2783
        • Darbyshire P.J.
        • Bourne S.P.
        • Allan P.M.
        • et al.
        The use of a panel of monoclonal antibodies in pediatric oncology.
        Cancer. 1987; 59: 726
        • DeArmond S.J.
        • Eng L.F.
        Immunohistochemistry: Techniques and application to neurooncology.
        Prog Exp Tumor Res. 1984; 27: 92
        • Debus E.
        • Moll R.
        • Franke W.W.
        • et al.
        Immunohistochemical distinction of human carcinomas by cytokeratin typing with monoclonal antibodies.
        Am J Pathol. 1984; 114: 121
        • Debus E.
        • Weber K.
        • Osborn M.
        Monoclonal antibodies to desmin, the muscle-specific intermediate filament protein.
        EMBO J. 1983; 2: 2305
        • Debus E.
        • Weber K.
        • Osborn M.
        Monoclonal antibodies specific for glial fibrillary acid protein (GFA) and for each of the individual neurofilament triplet proteins.
        Differentiation. 1983; 25: 193
        • Deck J.H.N.
        • Eng L.F.
        • Bigbee J.
        • et al.
        The role of glial fibrillary acidic protein in the diagnosis of central nervous system tumors.
        Acta Neuropathol. 1978; 42: 183
        • Dinges H-P
        • Wirnsberger G.
        • Hofler H.
        Immunocytochemistry in cytology: Comparative evaluation of different techniques.
        Anal Quant Cytol Histol. 1989; 11: 22
        • Domagala W.
        • Lubinski J.
        • Lasota J.
        • et al.
        Decisive role of intermediate filament typing of tumor cells in the differential diagnosis of difficult fine needle aspiration biopsies.
        Acta Cytol. 1987; 31: 253
        • Domagala W.
        • Lubinski J.
        • Lasota J.
        • et al.
        Neuroendocrine (Merkel-cell) carcinoma of the skin. Cytology, intermediate filament typing, and ultrastructure of tumor cells in fine needle aspiration biopsies.
        Acta Cytol. 1987; 31: 267
        • Domagala W.
        • Lubinski J.
        • Weber K.
        • et al.
        Intermediate filament typing of tumor cells in fine needle aspirate biopsies by means of monoclonal antibodies.
        Acta Cytol. 1986; 30: 214
        • Domagala W.
        • Weber K.
        • Osborn M.
        Differential diagnosis of lymph node aspirates by intermediate filament typing of tumor cells.
        Acta Cytol. 1986; 30: 225
        • Domagala W.
        • Weber K.
        • Osborn M.
        Diagnostic significance of coexpression of inter mediate filaments in fine needle aspiration biopsies of human tumors.
        Acta Cytol. 1988; 32: 49
        • Drebin J.A.
        • Link V.C.
        • Weinberg R.A.
        • et al.
        Inhibition of tumor growth by a monoclonal antibody reactive with an oncogene-encoded tumor antigen.
        Proc Natl Acad Sci USA. 1986; 83: 9129
        • Drebin J.A.
        • Link V.C.
        • Greene M.I.
        Monoclonal antibodies specific for the neu oncogene product directly mediate anti-tumor effects in vivo.
        Oncogene. 1988; 2: 273
        • Droese M.
        • Altmansberger M.
        • Kehl A.
        • et al.
        Ultrasound-guided percutaneous fine needle aspiration biopsy of abdominal and retroperitoneal masses. Accuracy of cytology in the diagnosis of malignancy, cytologic tumor typing, and use of antibodies to intermediate filaments in selected cases.
        Acta Cytol. 1984; 28: 368
        • Duffy P.E.
        • Graf L.
        • Huang Y-Y
        • et al.
        Glial fibrillary acidic protein in ependymomas and other brain tumors.
        J Neurol Sci. 1976; 40: 133
        • Duggan M.A.
        • Masters C.B.
        • Alexander F.
        Immunohistochemical differentiation of malignant mesothelioma, mesothelial hyperplasia, and metastatic adenocarcinoma in serous effusions utilizing staining for carcinoembryonic antigen, keratin and vimentin.
        Acta Cytol. 1987; 31: 807
        • Dwarkanath S.
        • Lee A.K.C.
        • DeLellis R.A.
        • et al.
        S-100 protein positivity in breast carcinomas: A potential pitfall in diagnostic immunohistochemistry.
        Hum Pathol. 1987; 18: 1144
        • Eng L.F.
        • DeArmond S.
        Immunochemistry of the glial fibrillary acidic protein.
        in: Zimmerman H.M. Progress in Neuropathology. 15. Raven Press, New York1983: 19
        • Epenetos A.A.
        • Canti G.
        • Taylor-Papadimitriou J.
        • et al.
        Use of two epithelium-specific monoclonal antibodies for diagnosis of malignancy in serous effusions.
        Lancet. 1982; 2: 1004
        • Firzlaff J.M.
        • Kiviat N.B.
        • Beckman A.M.
        • et al.
        Detection of human papillomavirus capsid antigens in various squamous epithelial lesions using antibodies directed against the LI and L2 open reading frames.
        Virology. 1988; 164: 467
        • Flint A.
        • McCoy Jr., J.P.
        • Esch T.R.
        • et al.
        Simultaneous measurement of DNA content and detection of surface antigens of cervico vaginal cells by flow cytometry.
        Anal Quant Cytol Histol. 1987; 9: 419
        • Flowers J.L.
        • Burton G.V.
        • Cox E.B.
        • et al.
        Use of monoclonal antiestrogen receptor antibody to evaluate estrogen receptor content in fine needle aspiration breast biopsies.
        Ann Surg. 1986; 203: 250
        • Garson J.A.
        • Coakham H.B.
        • Kemshead J.T.
        • et al.
        The role of monoclonal antibodies in brain tumor diagnosis and cerebrospinal fluid (CSF) cytology.
        J Neurooncol. 1985; 3: 165
        • Garson J.A.
        • Garson J.A.
        • Brownell B.
        • et al.
        Use of monoclonal antibody panel to identify malignant cells in cerebrospinal fluid.
        Lancet. 1984; 1: 1095
        • Gerdes J.
        • Lemke H.
        • Baisch H.
        • et al.
        Cell cycle analysis of a cell proliferation-associated human nuclear antigen defined by monoclonal antibody Ki 67.
        J Immunol. 1984; 133: 1710
        • Ghosh A.K.
        • Mason D.Y.
        • Spriggs A.I.
        Immunocytochemical staining with monoclonal antibodies in cytologically “negative” serous effusions from patients with malignant disease.
        J Clin Pathol. 1983; 36: 1150
        • Ghosh A.K.
        • Spriggs A.I.
        • Mason D.Y.
        Immunocytochemical staining ofT and B lymphocytes in serous effusions.
        J Clin Pathol. 1985; 38: 608
        • Ghosh A.K.
        • Spriggs A.I.
        • Taylor-Papadimitriou J.
        • et al.
        Immuno-cytochemical stainingof cells in pleural and peritoneal effusions with a panel of monoclonal antibodies.
        J Clin Pathol. 1983; 36: 1154
        • Gissman L.
        • Pfister H.
        • zur Hausen H.
        Human papillomavirus (HPV): Characterization of four different isolates.
        Virology. 1977; 76: 569
        • Gorra J.
        • Lancaster W.
        • Kurman R.
        • et al.
        Bovine papillamovirus type 1 monoclonal antibodies.
        JNCI. 1985; 75: 121
        • Gown A.M.
        • Vogel A.M.
        • Hoak D.
        • et al.
        Monoclonal antibodies specific for melanocytictumors distinguish subpopulations of melanocytes.
        Am J Pathol. 1986; 123: 195
        • Greene G.L.
        • Fitch F.W.
        • Jensen E.V.
        Monoclonal antibodies to estrophilin: Probes for the study of estrogen receptors.
        Proc Natl Acad Sci USA. 1980; 77: 157
        • Greene G.L.
        • Jensen E.V.
        Monoclonal antibodies as probes for estrogen receptor detection and characterization.
        J Steroid Biochem. 1982; 16: 353
        • Greene G.L.
        • Nolan C.
        • Engler J.P.
        • et al.
        Monoclonal antibodies to human estrogen receptor.
        Proc Natl Acad Sci USA. 1980; 77: 5115
        • Gupta J.W.
        • Gupta P.K.
        • Shah K.V.
        • et al.
        Distribution of human papillomavirus antigen in cervicovaginal smears and cervical-tissues.
        Int J Gynecol Pathol. 1983; 2: 160
        • Gupta P.K.
        • Myers J.D.
        • Baylin S.B.
        • et al.
        Improved antigen detection in ethanol-fixed cytologic specimens. A modified avidin-biotin-peroxidase complex method.
        Diagnostic Cytopathol. 1985; 1: 133
        • Guzman J.
        • Hilgarth M.
        • Bross K.G.
        • et al.
        Malignant ascites of serous papillary ovarian adenocarcinoma. An immunocytochemical study of the tumor cells.
        Acta Cytol. 1989; 32: 519
        • Haan E.A.
        • Boss B.D.
        • Cowan W.M.
        Production and characterization of monoclonal antibodies against the “brain-specific” proteins 14-3-2 and S-100.
        Proc Natl Acad Sci USA. 1982; 79: 7585
        • Haines H.G.
        • McCoy J.P.
        • Hofheinz D.E.
        • et al.
        Cervical carcinoma antigens in the diagnosis of human squamous cell carcinoma of the cervix.
        JNCI. 1981; 66: 465
        • Halliday W.C.
        • Yeger H.
        • Duwe G.F.
        • et al.
        Intermediate filaments in meningiomas.
        J Neuropathol Exp Neurol. 1985; 44: 617
        • Highely H.R.
        • McNulty J.A.
        • Rowden G.
        Glial fibrillary acidic protein and S-100 protein in pineal supportive cells: An electron microscopic study.
        Brain Res. 1984; 304: 117
        • Hilborne L.H.
        • Cheng L.
        • Nieberg R.K.
        • et al.
        Evaluation of an antibody to human milk fat globule antigen in the detection of metastatic carcinoma in pleural, pericardial, and peritoneal fluids.
        Acta Cytol. 1986; 30: 245
        • Hines T.R.
        • Ernst C.S.
        • Koprowska I.
        Loss of blood isoantigens in exfoliated cells during the progression of CIN demonstrated by monoclonal antibody staining.
        Acta Cytol. 1986; 30: 461
        • Homans A.C.
        • Forman E.N.
        • Barker B.E.
        Use of monoclonal antibodies to identify cere brospinal fluid lymphoblasts in children with acute lymphoblastic leukemia.
        Blood. 1985; 66: 1321
        • Horan-Hand P.
        • Thor A.
        • Wunderlich D.
        • et al.
        Monoclonal antibodies of predefined specificity detect activated ras gene expression in human mammary and colon carcinomas.
        Proc Natl Acad Sci USA. 1984; 81: 5227
        • Howley P.M.
        The role of papillomoviruses in human cancer.
        in: DeVita Jr., V.T. Heilman S. Rosenberg S.A. Advances in Oncology. JB Lippincott, Philadelphia1987: 55-73
        • Howley P.M.
        • Schlegel R.
        The human papillomaviruses.
        Am J Med. 1988; 85: 155
        • Hsu S.M.
        • Raine L.
        • Fanger H.
        Use of avidin-biotin-peroxidase complex (ABC) in immunoperoxidase techniques: A comparison between ABC and unlabeled antibody (PA) procedures.
        J Histochem Cytochem. 1981; 29: 577
        • Huffman J.L.
        • Garin-Chesa P.
        • Gay H.
        • et al.
        Flow cytometric identification of human bladder cells using a cytokeratin monoclonal antibody.
        in: Andreef M. Clinical Cytometry, Vol. 468. New York Academy of Sciences, New York1986: 302
        • Jenson A.B.
        • Rosenthal J.D.
        • Olson C.
        • et al.
        Immunologic relatedness of papillomaviruses from species.
        JNCI. 1980; 64: 494
        • Johnson V.G.
        • Schlom J.
        • Paterson A.J.
        • et al.
        Analyses of a human tumor-associated glycoprotein (TAG-72) identified by monoclonal antibody B72.3.
        Cancer Res. 1986; 46: 850
        • Johnson W.D.
        The cytologic diagnosis of cancer in serous effusions.
        Acta Cytol. 1996; 10: 161
        • Johnston W.W.
        The malignant pleural effusion.
        Cancer. 1985; 56: 905
        • Johnston W.W.
        • Borowitz M.J.
        • Stuhlmiller G.M.
        • et al.
        Expression of a melanoma-tumor-associated antigen as demonstrated by a monoclonal antibody (D6.1) in cytopathologic preparations of human tumor cells from effusions and fine needle aspirates.
        Anal Quant Cytol Histol. 1985; 7: 72
        • Johnston W.W.
        • Szpak C.A.
        • Thor A.
        • et al.
        Phenotypic characterization of lung cancers in fine needle aspiration biopsies using monoclonal antibody B72.3.
        Cancer Res. 1986; 46: 6462
        • Johnston W.W.
        • Szpak C.A.
        • Lottich S.C.
        • et al.
        Use of a monoclonal antibody (B72.3) as a novel immunocytochemical adjunct for the diagnosis of carcinoma in fine needle aspiration biopsy specimens.
        Hum Pathol. 1986; 17: 501
        • Johnston W.W.
        • Szpak C.A.
        • Lottich S.C.
        • et al.
        An adenocarcinoma associated determinant in human effusions: Use of a monoclonal antibody as an immunocytochemical adjuvant to diagnosis.
        Cancer Res. 1985; 45: 1894
        • Jones G.R.
        • Mason W.H.
        • Fishman L.S.
        • et al.
        Primary central nervous system lymphoma without intracranial mass in a child. Diagnosis by documentation of monoclonality.
        Cancer. 1985; 46: 2804
        • Kahn H.J.
        • Marks A.
        • Thom H.
        • et al.
        Role of antibody to S100 protein in diagnostic pathology.
        Am J Clin Pathol. 1983; 79: 341
        • Kardos T.F.
        • Sprague R.I.
        • Wakely P.E.
        • et al.
        Fine needle aspiration biopsy of lymphoblastic lymphoma and leukemia. A clinical, cytologic, and immunologic study.
        Cancer. 1987; 60: 2448
        • Katz R.L.
        • Raval P.
        • Manning J.T.
        • et al.
        A morphologic, immunologic, and cytometric approach to the classification of non-Hodgkin’s lymphoma in effusions.
        Diagn Cytopathol. 1987; 3: 91
        • Kemshead J.T.
        Monoclonal antibodies to the small round cell tumors of childhood.
        Adv Neuroblastoma Res. 1988; 2: 535
        • Kemshead J.T.
        • Fritschy J.
        • Garson J.A.
        • et al.
        Monoclonal antibody UJ127.11 detects a 220,000-240,000 dalglycoprotein present on a sub-set of neuroectodermally derived cells.
        Int J Cancer. 1983; 31: 187
        • Kemshead J.T.
        • Fritschy J.
        • Goldman A.
        • et al.
        Use of panels of monoclonal antibodies in the differential diagnosis of neuroblastoma and lymphoblastic disorders.
        Lancet. 1983; 1: 12
        • Kline T.S.
        • Lundy J.
        • Lozowski M.
        Monoclonal antibody B72.3. An adjunct for evaluation of suspicious aspiration biopsy cytology from the breast.
        Cancer. 1989; 63: 2253
        • Koprowska I.
        • Zipfel S.
        • Hines T.
        • et al.
        The search for monoclonal antibodies to identify uterine cervical epithelial neoplastic cells.
        Acta Cytol. 1985; 29: 920
        • Koprowska I.
        • Zipfel S.
        • Hines T.
        • et al.
        Use of monoclonal antibodies and immunoper-oxidase staining for demonstration of antigenic cross-reactivity of exfoliated uterine cervical neoplastic cells with other human tumors.
        Acta Cytol. 1984; 28: 653
        • Koprowska I.
        • Zipfel S.
        • Ross A.H.
        • et al.
        Development of monoclonal antibodies that recognize antigens associated with human cervical carcinoma.
        Acta Cytol. 1986; 30: 207
        • Koprowska I.
        • Zipfel S.
        • Hines T.
        • et al.
        Common antigenic sites on exfoliated cells derived from cervical carcinoma and in tumor cells of non-uterine origin as demonstrated by monoclonal antibodies in immunoperoxidase assay.
        Cancer Res. 1985; 45: 5964
        • Koprowska I.
        • Zipfel S.A.
        The potential usefulness of monoclonal antibodies in the determination of histologic types of lung cancer in cytologic preparations.
        Acta Cytol. 1988; 32: 675
        • Kurman R.J.
        • Shah K.H.
        • Lancaster W.B.
        • et al.
        Immunoperoxidase localization of papil lomavirus antigens in cervical dysplasia and vulvar condylomas.
        Am J Obstet Gynecol. 1981; 140: 931
        • Lach E.E.
        • Jenson A.B.
        • Smith H.G.
        • et al.
        Immunoperoxidase localization of human papillomavirus in laryngeal papillomas.
        Intervirology. 1980; 14: 148
        • Land H.
        • Parada L.F.
        • Weinberg R.A.
        Cellular oncogenes and multistep carcinogenesis.
        Science. 1983; 222: 771
        • Lane E.B.
        Monoclonal antibodies provide specific intramolecular markers for the study of epithelial monofilament organization.
        J Cell Biol. 1982; 92: 665
        • Lazarides E.
        Intermediate filaments: A chemically heterogeneous, developmentally regulated class of proteins.
        Ann Rev Biochem. 1982; 51: 219
        • Levallen E.C.
        • Carr D.T.
        Pleural effusion: A statistical study of 436 patients.
        N Engl J Med. 1955; 252: 79
        • Levitt S.
        • Cheng L.
        • DuPuis M.H.
        • et al.
        Fine needle aspiration diagnosis of malignant lymphoma with confirmation by immunoperoxidase staining.
        Acta Cytol. 1985; 29: 895
        • Li C-Y
        • Lazcano-Villareal O.
        • Pierre R.V.
        • et al.
        Immunocytochemical identification of cells in serous effusions. Technical considerations.
        Am J Clin Pathol. 1987; 88: 696
        • Loeffel S.C.
        • Gillespie G.Y.
        • Mirmiran S.A.
        • et al.
        Cellular immunolocalization of S100 protein within fixed tissue sections by monoclonal antibodies.
        Arch Pathol Lab Med. 1985; 109: 117
        • Lopes Cardozo P.L.
        A critical evaluation of 3000 cytologic analyses of pleural fluid, ascitic fluid, and peritoneal fluid.
        Acta Cytol. 1966; 10: 455
        • Lozowski M.S.
        • Mishriki Y.
        • Chao S.
        • et al.
        Estrogen determination in fine needle aspiration biopsies of the breast. Correlation with histologic grade and comparison with biochemical analysis.
        Acta Cytol. 1987; 31: 557
        • Lundy J.
        • Lozowski M.
        • Mushriki Y.
        Monoclonal antibody B72.3 as a diagnostic adjunct in fine needle aspiration biopsies of breast masses.
        Ann Surg. 1986; 203: 399
        • Lundy J.
        • Lozowski M.
        • Mishriki Y.
        Immunocytochemistry with monoclonal antibody B72.3 applied to a spectrum of benign and malignant breast aspirates—strengths and pitfalls.
        Breast Cancer Res Treat. 1988; 12: 259
        • Mariani-Costantini R.
        • Menard S.
        • Clemente C.
        • et al.
        Immunocytochemical identification of breast carcinoma cells in effusions using a monoclonal antibody.
        J Clin Pathol. 1982; 35: 1037
        • Marks A.
        • Law J.
        • Mahoney J.B.
        • et al.
        The structural conservation of S-100 protein during evolution: Analysis by reactivity with a monoclonal antibody.
        Neurochemistry. 1983; 41: 107
        • Marshall R.J.
        • Herbut A.
        • Braye S.G.
        • et al.
        Use of antibodies to carcinoembryonic antigen and human milk fat globule to distinguish carcinoma, mesothelioma, and reactive mesothelium.
        J Clin Pathol. 1984; 37: 1215
        • Martin S.E.
        • Zhang H.Z.
        • Magyarosy E.
        • et al.
        Immunologic methods in cytology: Definitive diagnosis of non-Hodgkin’s lymphomas using immunologic markers for T-and B-cells.
        Am J Clin Pathol. 1984; 82: 666
        • McCarty Jr., K.S.
        • Szabo E.
        • Flowers J.L.
        • et al.
        Use of amonoclonal anti-estrogen receptor antibody in the immunohistochemical evaluation of human tumors.
        Cancer Res. 1986; 46 (Suppl): 5255s
        • McClelland R.A.
        • Berger V.
        • Wilson P.
        • et al.
        Presurgical determination of estrogen receptor status using immunocytochemically stained FNAB smears in patients with breast cancer.
        Cancer Res. 1987; 47: 6118
        • McClelland R.A.
        • Berger U.
        • Miller L.S.
        • et al.
        Immunocytochemical assay for estrogen receptor: Relationship to outcome of therapy in patients with advanced breast cancer.
        Cancer Res. 1986; 46 (Suppl): 4241s
        • McLendon R.E.
        • Burger P.C.
        • Pegram C.N.
        • et al.
        The immunohistochemical application of three anti-GFAP monoclonal antibodies to formalin-fixed, paraffin-embedded normal and neoplastic brain tissue.
        J Neuropathol Exp Neurol. 1986; 45: 692
        • Meittinen M.
        • Lehto V-P
        • Dahl D.
        • et al.
        Differential diagnosis of chordoma, chondroid, and ependymal tumors as aided by anti-intermediate filament antibodies.
        Am J Pathol. 1983; 112: 160
        • Meittinen M.
        • Rapola J.
        Immunohistochemical spectrum of rhabdomyosarcoma and rhabdomyosarcoma-like tumors. Expression of cytokeratin and the 68 Kd neurofilament protein.
        Am J Surg Pathol. 1989; 13: 120
        • Menard S.
        • Rilke F.
        • Della Torre G.
        • et al.
        Sensitivity enhancement of the cytologic detection of cancer cells in effusions by monoclonal antibodies.
        Am J Clin Pathol. 1985; 83: 571
        • Miller L.S.
        • Tribby I.I.
        • Miles M.R.
        • et al.
        Hybridomas producing monoclonal antibodies to human estrogen receptor.
        Fed Proc. 1982; 41: 520
        • Moll R.
        • Franke W.W.
        • Schiller D.L.
        • et al.
        The catalog of human cytokeratins: Patterns of expression in normal epithelia, tumors and cultured cells.
        Cell. 1982; 31: 11
        • Moncrieff D.
        • Ormerod M.G.
        • Coleman D.V.
        Immunocytochemical staining of cervical smears for the diagnosis of cervical intraepithelial neoplasia.
        Analyt Quant Cytol. 1984; 6: 201
        • Monte S.A.
        • Ehya H.
        • Lang W.R.
        Positive effusion cytology as the initial presentation of malignancy.
        Acta Cytol. 1987; 31: 448
        • Morton J.A.
        • Bastin J.
        • Fleming K.A.
        • et al.
        Mallory bodies in alcoholic liver disease: identification of cytoplasmic filament/cell membranes and unique antigenic determinants by monoclonal antibodies.
        Gut. 1981; 22: 1
        • Nadji M.
        • Morales A.R.
        Immunoperoxidase Techniques: A Practical Approach to Tumor Diagnoses. American Society of Clinical Pathologists Press, Chicago1986
        • Nakai Y.
        • Lancaster W.O.
        • Lim L.Y.
        • et al.
        Monoclonal antibodies to genus-type-specific papillomavirus structural antigens.
        Intervirology. 1986; 25: 30
        • Nakajima T.
        • Watanabe S.
        • Sato Y.
        • et al.
        An immunoperoxidase study of S-100 protein distribution in normal and neoplastic tissues.
        Am J Surg Pathol. 1982; 6: 715
        • Nuti M.
        • Mottolese M.
        • Viora R.
        • et al.
        Use of monoclonal antibodies to human breast tumor-associated antigens in FNAB cytology.
        Int J Cancer. 1986; 37: 493
        • Ohuchi N.
        • Thor A.
        • Page D.L.
        • et al.
        Expression of the 21000 molecular weight rasprotein in a spectrum of benign and malignant mammary tissues.
        Cancer Res. 1986; 46: 2511
        • Ordonez N.G.
        The immunohistochemical diagnosis of mesothelioma. Differentiation of mesothelioma and lung adenocarcinoma.
        Am J Surg Pathol. 1989; 13: 276
        • Ordonez N.G.
        • Sneige N.
        • Hickey R.C.
        • et al.
        Use of monoclonal antibody HMB-45 in the cytologic diagnosis of melanoma.
        Acta Cytol. 1989; 32: 684
        • Osborn M.
        • Altmannsberger M.
        • Debus E.
        • et al.
        Differentiation of the major human tumor groups using conventional and monoclonal antibodies specific for individual intermediate filament proteins.
        Ann NY Acad Sci. 1985; 455: 649
        • Osborn M.
        • Weber K.
        Tumor diagnosis of intermediate filament typing: A novel tool for surgical pathology.
        Lab Invest. 1983; 48: 372
        • Otis C.N.
        • Carter D.
        • Cole S.
        • et al.
        Immunohistochemical evaluation of pleural mesothelioma and pulmonary adenocarcinoma.
        Am J Surg Pathol. 1987; 11: 445
        • Oud P.S.
        • Henderik J.B.J.
        • Beck H.L.M.
        • et al.
        Flow cytometric analysis and sorting of human endometrial cells after immunocytochemical labeling for cytokeratiri using a monoclonal antibody.
        Cytometry. 1985; 6: 159
        • Ozzello L.
        • DeRosa C.M.
        • Konrath J.G.
        • et al.
        Detection of estrophilin in frozen sections of breast cancers using an estrogen receptor immunocytochemical assay.
        Cancer Res. 1986; 46 (suppl): 4303s
        • Papasozomenos S.C.H.
        Glial fibrillary acidis (GFA) protein-containing cells in the human pineal gland.
        J Neuropathol Exp Neurol. 1983; 42: 391
        • Perentes E.
        • Rubeinstein L.J.
        Recent applications of immunoperoxidase histochemistry in human neurooncology.
        Arch Pathol Lab Med. 1987; 111: 796
        • Pettigrew N.M.
        Techniques in immunocytochemistry. Application to diagnostic pathology.
        Arch Pathol Lab Med. 1989; 113: 641
        • Pizzolo G.
        • Sloane J.
        • Beverley P.
        • et al.
        Differential diagnosis of malignant lymphoma and non-lymphoid tumours using monoclonal anti-leukocyte antibody.
        Cancer. 1980; 46: 2640
        • Pulford K.A.F.
        • Gatter K.C.
        • Mason D.Y.
        The characterization of two monoclonal antikeratin antibodies and their use in the study of epithelial disorders.
        Histopathology. 1985; 9: 825
        • Radio S.J.
        • Rennard S.I.
        • Kessinger A.
        • et al.
        Breast carcinoma in bronchoalveolar lavage: A cytologic and immunohistochemical study.
        Arch Pathol Lab Med. 1989; 113: 333
        • Ramaekers F.C.S.
        • Beck H.
        • Vooijs G.P.
        • et al.
        Flow cytometric analysis of mixed cell populations using intermediate filament antibodies.
        Exp Cell Res. 1984; 153: 249
        • Reinherz E.L.
        • Schlossman S.F.
        The differentiation and function of human T-lymphocytes.
        Cell. 1980; 19: 821
        • Robey S.S.
        • Cafferty L.L.
        • Beschorner W.E.
        • et al.
        Value of lymphocyte marker studies in diagnostic cytopathology.
        Acta Cytol. 1987; 31: 453
        • Rosens S.T.
        • Mulshine J.L.
        • Cuttitta F.
        • et al.
        Analysis of human small cell lung cancer differentiation antigens using a panel of rat monoclonal antibodies.
        Cancer Res. 1984; 44: 2052
        • Roseto A.
        • Porthier P.
        • Guillemin M-C
        • et al.
        Monoclonal antibody to the major capsid protein of human papillomovirus type 1.
        J Gen Virol. 1984; 651: 1319
        • Rubeinstein L.J.
        • Brucher J.M.
        Focal ependymal differentiation in choroid plexus papillomas.
        Acta Neuropathol. 1981; 53: 29
        • Salisbury J.R.
        • Isaacson P.G.
        Demonstration of cytokeratins and an epithelial membrane antigen in chordomas and human fetal notochord.
        Am J Surg Pathol. 1985; 9: 791
        • Schlom J.
        • Weeks M.O.
        Potential clinical utility of monoclonal antibodies in the management of human carcinoma.
        in: DeVita V.T. Hellman S. Rosenberg S.A. Important Advances in Oncology 1985. JB Lippincott, Philadelphia1985: 170
        • Schlom J.
        • Colcher D.
        • Teramoto Y.A.
        • et al.
        Generation and characterization of murine and human monoclonal antibodies reactive with human mammary tumor cells.
        in: Mitchell M.S. Oettgen H.F. Hybridomas in Cancer Diagnosis. Raven Press, New York1982: 213
        • Schwechheimer K.
        • Kartenbeck J.
        • Moll R.
        • et al.
        Vimentin filament-desmosome cytoskeleton of diverse types of human meningiomas.
        Lab Invest. 1984; 51: 584
        • Sears D.
        • Hajdu S.I.
        The cytologic diagnosis of malignant neoplasms in pleural and peritoneal effusions.
        Acta Cytol. 1987; 31: 85
        • Sehested M.
        • Ralfkjaer E.
        • Rasmussen J.
        Immunoperoxidase demonstration of carcinoembryonic antigen in pleural and peritoneal effusions.
        Acta Cytol. 1983; 2: 124
        • Sheibani K.
        • Battifora H.
        • Burke J.S.
        Antigenic phenotype of malignant mesotheliomas and pulmonary adenocarcinomas. An immunohistologic analysis demonstrating the value of Leu Ml antigen.
        Am J Pathol. 1986; 123: 212
        • Shih T.
        • Weeks M.
        Oncogenes and cancer: The p21 ras genes.
        Cancer Invest. 1984; 2: 109
        • Slamon D.J.
        • Clark G.M.
        • Wong S.G.
        • et al.
        Human breast cancer: Correlation of relapse and survival with amplification of the HER-3/neu oncogene.
        Science. 1987; 235: 177
        • Spandidos D.A.
        • Kerr T.B.
        Elevated expression of the human ras oncogene family in premalignant and malignant tumours of the colo-rectum.
        Br J Cancer. 1984; 49: 681
        • Spriggs A.I.
        • Boddington M.M.
        The Cytology of Effusions and of Cerebrospinal Fluids. ed 2. Heinemann, London1968
        • Spriggs A.I.
        Diagnosis of malignant effusions [Letter].
        Br Med J. 1981; 282: 1972
        • Stahel R.A.
        • O’Hara C.J.
        • Waibel R.
        • et al.
        Monoclonal antibodies against mesothelial membrane antigen discriminate between malignant mesothelioma and lung adenocarcinoma.
        Int J Cancer. 1988; 41: 218
        • Stark E.
        • Wurster U.
        Preparation procedure for cerebrospinal fluid that yields cytologic samples suitable for all types of staining, including immunologic and enzymatic methods.
        Acta Cytol. 1987; 31: 374
        • Stashenko P.
        • Nodler L.M.
        • Hardy R.
        • et al.
        Characterization of a human B lymphocyte specific antigen.
        J Immunol. 1980; 125: 1678
        • Stuhlmiller G.M.
        • Borowitz M.J.
        • Seigler H.F.
        D6.1, a murine antimelanoma monoclonal antibody from congenitally athymic nude mice immunized with purified melanoma tumor associated with purified melanoma tumor associated antigen.
        Hybridoma. 1984; 3: 333
        • Sun T.
        • Li C-Y
        • Yam L.T.
        Atlas of Cytochemistry and Immunochemistry of Hematologic Neoplasms. American Society of Clinical Pathologists, Chicago1985
        • Szpak C.A.
        • Johnston W.W.
        • Lottich S.C.
        • et al.
        Patterns of reactivity of four novel monoclonal antibodies (B72.3, DF3, B1.1, B6.2) with cells in human malignant and benign effusions.
        Acta Cytol. 1984; 28: 356
        • Szpak C.A.
        • Johnston W.W.
        • Roggli V.
        • et al.
        The diagnostic distinction between malignant mesothelioma of the pleura and adenocarcinoma of the lung as defined by monoclonal antibody B72.3.
        Am J Pathol. 1986; 122: 252
        • Szpak C.A.
        • Johnston W.W.
        • Roggli V.
        • et al.
        The significance of monoclonal antibody B72.3 in the diagnostic distinction between malignant mesothelioma of the pleura and adenocarcinoma of the lung.
        Am J Pathol. 1986; 122: 252
        • Szpak C.A.
        • Soper J.T.
        • Thor A.
        • et al.
        Detection of adenocarcinoma in peritoneal washings by monoclonal antibody B72.3.
        Acta Cytol. 1989; 33: 205
        • Tabatowski K.
        • Vollmer R.T.
        • Tello J.W.
        • et al.
        The use of a panel of monoclonal antibodyies in ultrastructurally characterized small cell carcinomas of the lung.
        Acta Cytol. 1988; 32: 667
        • Tagliabue E.
        • Menard S.
        • Della Torre G.
        • et al.
        Generation of monoclonal antibodies reactivating with human epithelial ovarian cancer.
        Cancer Res. 1985; 45: 379
        • Taylor-Papadimitriou J.
        • Peterson J.A.
        • Arklie J.
        • et al.
        Monoclonal antibodies to epithet lium-specific components of the human milk fat globule membrane: Production and reaction with cells in culture.
        Int J Cancer. 1981; 28: 17
        • Thor A.
        • Ohuchi N.
        • Szpak C.A.
        • et al.
        Monoclonal antibody B72.3 defines the distribution of the oncofetal antigen TAG-72.
        Cancer Res. 1986; 46: 3118
        • Thor A.
        • Gorstein F.
        • Ohuchi N.
        • et al.
        Tumor associated glycoprotein (TAG-72) in ovarian carcinomas defined by MAb B72.3.
        JNCI. 1986; 76: 995
        • Thor A.
        • Viglione M.J.
        • Muraro R.
        • et al.
        Monoclonal antibody B72.3 reactivity with human endometrium: A study of normal and malignant tissues.
        Int J Gynecol Pathol. 1987; 6: 235
        • Thor A.
        • Simpson J.
        • Ohuchi N.
        • et al.
        Monoclonal antibodies and human carcinomas diagnostic experimental applications.
        in: DeLellis R. Advances in Immunohistochemistry. 3. New York, Masson Publishing USA1988 (Inc)
        • Thor A.
        • Horan-Hand P.
        • Wunderlich D.
        • et al.
        Monoclonal antibodies define differential ras gene expression in malignant and benign colonic diseases.
        Nature. 1984; 311: 562
        • Thor A.
        • Ohuchi N.
        • Horan-Hand P.
        • et al.
        Ras gene alterations and enhanced levels of ras p21 expression in a spectrum of benign and malignant human mammary tissues.
        Lab Invest. 1986; 55: 603
        • Todd R.
        • Nadler L.M.
        • Schlossman S.F.
        Antigens on human monocytes identified by monoclonal antibodies.
        J Immunol. 1981; 126: 1435
        • Tong A.W.
        • Lee J.C.
        • Stone M.J.
        Discrimination of human small cell and non-small cell lung tumors by a panel of monoclonal antibodies.
        JNCI. 1986; 77: 1023
        • To A.
        • Dearnaley D.P.
        • Ormerod M.G.
        • et al.
        Indirect immunoalkaline phosphatase staining of cytologic smears of serous effusions for tumor marker studies.
        Acta Cytol. 1983; 27: 109
        • To A.
        • Coleman D.V.
        • Dearnaley D.P.
        • et al.
        Use of antisera to epithelial membrane antigen for the cytodiagnosis of malignancy in serous effusions.
        J Clin Pathol. 1981; 34: 1326
        • To A.
        • Dearnaley D.P.
        • Ormerod M.G.
        • et al.
        Epithelial membrane antigen: its use in the cytodiagnosis of malignancy in serous effusions.
        Am J Clin Pathol. 1982; 78: 21
        • Trojanowski J.Q.
        • Atkinson B.
        • Lee V.M.Y.
        An immunocytochemical study of normal and abnormal human cerebrospinal fluid with monoclonal antibodies to glial fibrillary acidic protein.
        Acta Cytol. 1986; 30: 235
        • Tron V.
        • Wright J.L.
        • Churg A.
        Carcinoembryonic antigen and milk fat globule protein staining of malignant mesothelioma and adenocarcinoma of the lung.
        Arch Pathol Lab Med. 1987; 111: 291
        • Tseng S.C.G.
        • Jarvinen M.J.
        • Nelson W.G.
        • et al.
        Correlation of specific keratins with different types of epithelial differentiation: monoclonal antibody studies.
        Cell. 1982; 30: 361
        • van de Vijver J.M.
        • Peters J.L.
        • Mooi W.J.
        • et al.
        neu-Protein overexpression in breast cancer.
        N Engl J Med. 1988; 319: 1239
        • van der Kwast T.
        • Versnel M.A.
        • Delahage M.
        • et al.
        Expression of epithelial membrane antigen on malignant mesothelioma cells. An immunocytochemical and immunoelectron microscopic study.
        Acta Cytol. 1988; 32: 169
        • Van Eldik B.
        • Ehrenfried B.
        • Jensen R.A.
        Production and characterization of monoclonal antibodies with specificity for the S-100 polypeptide of brain S-100 fractions.
        Proc Natl Acad Sci USA. 1984; 81: 6034
        • Vanstapel M-J
        • Peeters B.
        • Cordell J.
        • et al.
        Production of monoclonal antibodies directed against antigenic determinants common to the α and β chain of bovine brain S-100 protein.
        Lab Invest. 1985; 52: 232
        • Vanstapel M-J
        • Gatter K.C.
        • DeWolf-Peters C.
        • et al.
        New sites of human S-100 immunoactivity detected with monoclonal antibodies.
        Am J Clin Pathol. 1986; 85: 160
        • Vennegoor C.
        • Calafat J.
        • Hageman P.
        • et al.
        Biochemical characterization and cellular localization of a formalin-resistant melanoma-associated antigen reacting with monoclonal antibody NKI/C3.
        Int J Cancer. 1985; 35: 287
        • Vennegoor C.
        • Hageman P.
        • Van Nouhuijs H.
        • et al.
        A monoclonal antibody specific for melanocyte differentiation.
        Am J Pathol. 1988; 130: 179
        • Vick W.W.
        • Bigner S.H.
        • Wikstrand C.J.
        • et al.
        The use of a panel of monoclonal antibodies in the evaluation of cytologic specimens from the central nervous system.
        Acta Cytol. 1987; 31: 815
        • Von Overbeck J.
        • Staehli C.
        • Gudat F.
        • et al.
        Immunohistochemical characterization of an antiepithelial monoclonal antibody (Lu-5).
        Virchows Arch (Pathol Anat). 1985; 407: 1
        • Weiss S.W.
        • Langloss J.M.
        • Enzinger F.M.
        Value of S-100 protein in the diagnosis of softtissue tumors with particular references to benign and malignant Schwann cell tumors.
        Lab Invest. 1983; 49: 299
        • Woods J.C.
        • Spriggs A.J.
        • Harris H.
        • et al.
        A new marker for human cancer cells. 3. Immunocytochemical detection of malignant cells in serous fluids with the Ca 1 antibody.
        Lancet. 1982; 2: 512
        • Yam L.T.
        • English M.C.
        • Janckila A.J.
        • et al.
        Immunocytochemistry of cerebrospinal fluid.
        Acta Cytol. 1987; 31: 825
        • Yam L.T.
        • Lin D.G.
        • Janckila A.J.
        • et al.
        Immunocytochemical diagnosis of lymphoma in serous effusions.
        Acta Cytol. 1985; 29: 833
        • Yam L.T.
        • Winkler C.F.
        Immunocytochemical diagnosis of oat-cell carcinoma in pleural effusion.
        Acta Cytol. 1984; 28: 425

      Article info

      Identification

      DOI: https://doi.org/10.1016/S0272-2712(18)30583-3

      Copyright

      © 1990 Elsevier Inc. Published by Elsevier Inc. All rights reserved.

      ScienceDirect

      Access this article on ScienceDirect

      The content on this site is intended for healthcare professionals.


      We use cookies to help provide and enhance our service and tailor content. To update your cookie settings, please visit the Cookie Preference Center for this site.
      Copyright © 2023 Elsevier Inc. except certain content provided by third parties.


      RELX