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Paraneoplastic Neurologic Disease

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Paraneoplastic Neurologic Disease 3601_e19_p423-437 2/19/02 8:59 AM Page 423 19 Paraneoplastic Neurologic Disease KURT A. JAECKLE The term paraneoplastic neurologic disease (PND) less, the description of specific autoantibodies in PND encompasses several degenerative central or periph- has resulted in separation of a group of patients with eral nervous system disorders that result from indi- PND from others without antibodies. Many PND au- rect effects of systemic cancer on elements of the ner- toantibodies have now been associated with specific vous system. By definition, the dysfunction does not tumors, particularly those from lung, breast, gyneco- result from invasion or metastasis by tumor. The con- logic, and testicular neoplasms. In some circum- cept of a remote or indirect effect of cancer on the stances, this has allowed the clinician to expedite the nervous system arose in the latter nineteenth century discovery of the primary cancer in suspect patients by empiric association between peripheral neuropa- and designate the complicated neurologic illness in thy and lung cancer (Oppenheim, 1888). During the given patients as a paraneoplastic condition. A major first half of the twentieth century, the term paraneo- future challenge still remains—the identification of plastic disease was applied to nearly any neurologic effective therapies for these largely unresponsive con- dysfunction in a cancer patient for which an etiology ditions. Such therapies are likely to result from elu- was not readily apparent. As a result, the category in- cidation of the pathogenetic mechanisms involved in cluded a variety of metabolic, nutritional, vascular, the production of these disorders. and infectious disorders. In the latter half of the twen- tieth century, the autoimmune etiology of many para- neoplastic disorders evolved, beginning with the dis- INCIDENCE covery of antineuronal antibodies in patients with small cell lung cancer (SCLC) (Croft and Wilkinson, Overall, PND is rare. The reported incidence of PND 1965). Several different serum autoantibody markers is higher if all peripheral nerve and neuromuscular have now been associated with the paraneoplastic disorders are included. In one study, more than 50% neurologic clinical syndromes, which has allowed the of patients with ovarian epithelial neoplasms had ev- clinician to confirm the diagnosis in suspect cases. idence of peripheral neuropathy (Cavalleti et al., However, the pathogenetic relationship between 1991). In patients with SCLC, peripheral nerve dis- PND antibodies, clinical syndromes, and neuro- ease has been clinically observed in as many as 45% pathologic abnormalities has not been entirely clari- of patients. At autopsy, changes in dorsal root gan- fied. Furthermore, not all patients with such autoan- glia were observed in 70% and in anterior horn cell tibodies have syndromes consistent with PND. neurons in 45% of patients (Kida et al., 1992). How- Additional etiologies may be involved, such as infec- ever, in many of these patients, peripheral neuropa- tious or parainfectious processes, nutritional defi- thy was likely due to other causes, such as effects ciencies, or direct neurotoxicity from proteins and from neurotoxic medications and metabolic or nu- other substances elaborated by the tumor. Nonethe- tritional disorders. In a series of 1476 cancer pa- 423 3601_e19_p423-437 2/19/02 8:59 AM Page 424 424 SYMPTOMS SECONDARY TO CANCER AND ITS TREATMENT tients, “true” paraneoplastic neuromyopathy was re- (Furneaux et al., 1990). Finally, cytotoxic T cells have ported in 7% (Croft and Wilkinson, 1965). The myas- been shown to transform in response to specific thenic (Lambert-Eaton) syndrome occurs in approx- paraneoplastic antigens, and these cells are capable imately 3% of patients with SCLC (Elrington et al., of inducing tumor cell cytotoxicity (Albert et al., 1991). 2000). If one excludes the neuromyopathies, clinically recognizable central nervous system (CNS) PND oc- curs in Ͻ1 % of patients with cancer (Anderson et PATHOGENESIS al., 1987). Several etiologies have been proposed for the para- neoplastic diseases (Brain and Norris, 1965), in- HISTORIC CONSIDERATIONS cluding toxins (e.g., proteins, lipids, and soluble neu- rotoxins and their products); viruses (e.g., the JC The first report of a paraneoplastic syndrome was polyomavirus in progressive multifocal leukoen- probably the description of peripheral neuropathy in cephalopathy); nutritional deficiencies (e.g., vitamins a lung cancer patient at the end of the nineteenth cen- B1, B6, B12, amino acids); and autoimmunity. By def- tury (Oppenheim, 1888). A series of reports followed inition, many of these potential etiologies (nutritional, that clearly defined the clinical syndromes and asso- progressive multifocal leukoencephalopathy, viral en- ciated cancers. Several paraneoplastic conditions cephalitis) are generally not considered part of the were described, including myasthenia gravis in asso- modern definition of PND. To date, there has not been ciation with thymic tumor (Weigert, 1901); der- a definitive animal model for most manifestations of matomyositis with gastric carcinoma (Stertz, 1916); PND. subacute cerebellar degeneration (Brouwer, 1919), It is possible that several separate pathogenetic later associated with ovarian and SCLC (Brain et al., mechanisms are responsible in different patients. For 1951); sensory neuronopathy with lung cancer example, not all cancer patients with clinical PND have (Denny-Brown, 1948); myasthenic syndrome with demonstrable autoantibodies (Posner and Furneaux, SCLC (Lambert et al., 1956); encephalomyelitis (Hen- 1990). Undetected viral or other infectious etiologies, son et al., 1965); and cancer-associated retinopathy tumor-associated neurotoxins, and neuroendocrine in- (Sawyer et al., 1976). fluences have not been totally excluded. Investigators during the last 40 years have explored An autoimmune disturbance involving “molecular the pathogenesis of PND. This effort began in earnest mimicry” has been proposed. In this model, anti- in the mid-1960s with the discovery of serum au- bodies react with shared protein antigens in tumor toantibodies that reacted with neurons (Wilkinson, and in the CNS or peripheral nervous system. Some 1964). Several investigators later described serum patients have identifiable serum and CSF complement- and cerebrospinal fluid (CSF) autoantibodies with fixing antineuronal antibodies of the pathogenic IgG affinity for central or peripheral nervous system pro- subtype (Dalmau et al., 1991; Jean et al., 1994) that tein antigens (Trotter et al., 1976; Kornguth et al., cross react with autologous tumor antigens. Local 1982; Greenlee and Brashear, 1983; Jaeckle et synthesis of paraneoplastic autoantibodies can be al., 1985; Graus et al., 1985; Voltz et al., 1999; Hon- identified in the CNS (Furneaux et al., 1990). Occa- norat et al., 1996). The antibodies have been used to sional patients show improvement and reduction of identify and characterize corresponding protein anti- antibody titers after tumor removal or therapy gens and also to clone cDNA for production and char- (Greenlee et al., 1986; Tsukamoto et al., 1993). acterization of recombinant protein antigens (Drop- Plasmapheresis, which removes autoantibody, has cho et al., 1987; Szabo et al., 1991; Fathallah-Shaykh also resulted in disease stabilization in rare patients; et al., 1991; Thirkill et al., 1992; Sakai et al., 1992; unfortunately, this treatment is usually unsuccessful Buckanovich et al., 1993) (Table 19–1). (Jaeckle et al., 1985; Graus et al., 1992). Other im- In some cases, PND antibodies show relative affin- mune suppressive therapies and intravenous im- ity for sites of pathologic nervous system involvement munoglobulin have been tried but are also largely (Dalmau et al., 1991). In addition, the antineuronal ineffective (Grisold et al., 1995; Keime-Guibert et al., antibodies are also reactive with autologous tumor 2000). 3601_e19_p423-437 2/19/028:59AMPage425 Table 19–1. Paraneoplastic Neurologic Antibodies Clinical Tumor Western Blot Recombinant Syndrome Type Antibody Antigen (kD) Antigen Reference Encephalomyelitis SCLC, breast Anti-Hu 37–42 HuD; PLE21/HuC Szabo et al., 1991 SCLC, breast, Anti-Hel-N1 37–42 Hel-N1 Levine et al., 1993 other Anti-CV2 66 Ulip/CRMP Honnorat et al., 1999 Limbic encephalitis Testicular, breast Anti-Ma 2 (Ta) 40 Ma2 Sutton et al., 2000 Cerebellar degeneration Breast, Gyn Anti-Yo 62 Cdr2 Fathallah-Shaykh et al., 1991 Breast, Gyn Anti-Yo 34 pCDR13 Dropcho et al., 1987 Breast, Gyn Anti-PCA-1 52 p52 Sakai et al., 1992 SCLC, breast, colon, other Anti-Ma 1 40 Ma 1 Voltz et al., 1999 — — 58 p58 Sato et al., 1991 Opsoclonus-Myoclonus-ataxia Breast, lung, GI Anti-Ri 55 Nova 1, 2 Buckanovich et al., 1993 Cancer-associated retinopathy Lung, melanoma Anti-CAR 23–26 CAR Thirkill et al., 1992 Lambert-Eaton SCLC Anti-P/Q VGCC (Bioassay) — Leys et al., 1991 kD, kiloDaltons; SCLC, small cell lung cancer; Gyn, gynecologic malignancies; GI, gastroenteric malignancies; VGCC, voltage-gated calcium channel. 3601_e19_p423-437 2/19/02 8:59 AM Page 426 426 SYMPTOMS SECONDARY TO CANCER AND ITS TREATMENT Theoretically, quiescent memory T cells, which ods for detection of PND (King et al., 1999). None- were transiently exposed in the fetus to developmen- theless, commercial laboratories have been established tal antigens, might escape thymic deletion and reside that offer “clinical panels” for antibody detection by in the periphery until tumor-associated antigens are a variety of different methods. again
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