Clinical Presentation and Natural History of Mesothelioma: Abdominal

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1 25 Clinical Presentation and Natural History of Mesothelioma: Abdominal Claire F. Verschraegen, Charles R. Key, and Raffit Hassan Epidemiology and Etiology The Surveillance, Epidemiology, and End Results (SEER) database showed 5266 cases of mesothelioma (all sites) recorded from 1973 to The age-adjusted incidence rate of the year 2000 United States standard is 9.7 cases per 1,000,000. The 95% confidence interval rates are 9.4 to 10 cases per 1,000,000. These numbers have not changed much from a previous survey done over 15 years ago (1). Table 25.1 shows the incidence around the country. Seattle and the San Francisco Bay area have higher incidence rates than other regions, especially for males. This increased incidence is related to shipyard work, especially since World War II (2). Usage of asbestos for ship building resulted in long-term exposure of workers for the past 60 years. Mesothelioma occurs in different anatomic sites that contain mesothelial layers. The most common site is the pleura, followed by the peritoneum, the pericardium, the male genitalia, miscellaneous, and female genitalia. The peritoneal incidence by gender is different from the pleural incidence (Table 25.2). Proportionally, more women develop peritoneal mesothelioma, with an incidence of 24% versus 8% for males, using mesothelioma from any anatomic site as the denominator. In absolute numbers, more males are diagnosed with abdominal mesothelioma, with a frequency of 54.7% versus 45.3% for women (3) (Table 25.3). In the SEER database, the median age at diagnosis was between 65 and 69 years old for males and females. This is slightly higher than the age of the reported case in the literature (Table 25.4). By race, the incidence rates are highest for whites, followed by blacks, and then others. Asbestos is the best-known environmental agent linked to the development of mesothelioma (see Chapter 2) (4). The literature on asbestos as a cause of pleural/pericardial plaques, asbestosis, and mesothelioma is extensive, and the causal relationship is not discussed in this chapter (5). The number of patients with mesothelioma differs by anatomic site 391

2 392 Chapter 25 Clinical Presentation of Abdominal Mesothelioma Table Mesothelioma rates per 1,000,000 (age-adjusted to the 2000 U.S. standard) SEER database Rate SD Lower CI Upper CI Count Population Males Nine SEER registries , ,413,683 San Francisco Oakland SMSA ,961,380 Connecticut ,759,293 Detroit (Metropolitan) ,102,198 Hawaii ,400,110 Iowa ,370,945 New Mexico ,228,865 Seattle (Puget Sound) ,551,415 Utah ,128,033 Atlanta (Metropolitan) ,911,444 Females Nine SEER registries , ,419,050 San Francisco Oakland SMSA ,509,072 Connecticut ,547,659 Detroit (Metropolitan) ,047,986 Hawaii ,860,703 Iowa ,570,791 New Mexico ,807,655 Seattle (Puget Sound) ,064,742 Utah ,425,156 Atlanta (Metropolitan) ,585,286 SD, standard deviation; CI, confidence interval; confidence intervals are 95% for rates; SMSA. Rates in bold are higher than the mean incidence. Table Incidence by anatomic sites SEER database Male and female Male Female All sites Digestive system Abdominal organs Retroperitoneum Peritoneum, omentum, and mesentery Respiratory system Lung and Bronchus Pleura Respiratory organs Soft tissue including heart Female genital system Corpus and Uterus, NOS Ovary Other female genital organs Male genital system Testis Other male genital organs Miscellaneous

3 C.F. Verschraegen et al 393 Table Relative frequencies of mesothelioma diagnosis per site for males and females Number of Number of Percent Percent mesothelioma mesothelioma Percent Percent all sites all sites Site (male) (female) (male) (female) (male) (female) Abdominal Thoracic Heart Female genital Male genital Other All sites and by gender (Table 25.3). A higher proportion of women develop the disease in the peritoneal cavity. Although not all mesotheliomas have been linked to asbestos exposure, for patients developing a peritoneal mesothelioma induced by asbestos, exposure to this substance was usually heavier and longer (6,7). The latency between asbestos exposure and onset of disease is shorter for peritoneal than for pleural mesothelioma (20 to 30 versus 30 to 40 years) (8). Table Clinical presentation of diffuse malignant mesothelioma Number of No. of patients publications Percent with Characteristic (denominator a ) (8,17 22) characteristic Duration of symptoms Under 6 months 53/ Over 6 months 23/76 30 Age Under 45 years 26/ years 40/97 41 Over 60 years 31/97 32 Symptoms Abdominal pain 76/ Abdominal mass 31/ Increasing abdominal girth 73/ Ascites 46/ Digestive disturbances b 10/ Fever 11/ Weight loss 27/ Thrombocytosis 8/ Leukocytosis 4/ Pathology Epithelial 67/ Sarcomatous 8/89 9 Mixed 14/89 16 a If a symptom is not stated in a publication, the number of patients cited in the publication is not included in the denominator. b Including anorexia.

4 394 Chapter 25 Clinical Presentation of Abdominal Mesothelioma Pathology To establish the diagnosis, a tissue biopsy is essential (see also Pathology of Mesothelioma Section). Without a tissue sample, malignant stromal invasion cannot be detected (9). The biopsy is usually done by a laparoscopic exploratory endoscopy of the peritoneal cavity. The histology of mesothelioma encompasses a spectrum that goes from benign mesothelial hyperplasia (no stromal invasion) to undifferentiated malignant disease. Mesothelial hyperplasia is usually a tissue response to inflammation or trauma, and can be associated with other cancers, presenting a diagnostic challenge. The differential diagnosis includes diffuse malignant mesothelioma, which also can be a diagnostic challenge. Mesothelial hyperplasia may be present for years and it occasionally precedes the diagnosis of diffuse malignant mesothelioma. The different morphologic types of abdominal mesothelial neoplasms that have been described include localized fibrous tumor, adenomatoid tumor, well-differentiated papillary mesothelioma, low-grade cystic mesothelioma, and diffuse malignant mesothelioma (10). The localized fibrous tumor is extremely rare in the abdominal cavity, in comparison to the pleural cavity. The adenomatoid tumor type is encountered most commonly in the genital system, but has been observed on the mesenteric surface or the omentum. Low-grade cystic mesothelioma is also very rare and should not be confused with multilocular peritoneal inclusion cysts, a benign condition. Well-differentiated papillary mesothelioma is the most common variant after diffuse malignant mesothelioma (11,12). It is usually seen in premenopausal women, and could be an incidental finding. When it is symptomatic, it usually presents with ascites, or abdominal pain. Asbestos exposure may not be evident in many well-differentiated cases. Microscopic examination reveals fibrous papillae covered by a mesothelial cell monolayer; the nuclear features are bland and mitoses are rare or absent. A tubulopapillary pattern, branching cords, solid sheets of cells, and deciduoid morphology (13) are sometimes seen. Most well-differentiated papillary mesotheliomas are benign or very low grade and should be observed after diagnostic resection. The differential diagnosis includes a low-grade papillary serous carcinoma of the ovary or peritoneum. There have been three major variants of diffuse malignant mesothelioma described: the epithelial, the sarcomatous types, and the mixed epithelial/sarcomatous type. Pathology and histologic diagnosis is described in Chapter 31. Differential Diagnosis The main differential diagnosis is with adenocarcinoma that invades the peritoneal cavity, such as primary peritoneal tumor, primary ovarian carcinoma especially of the papillary serous type (14), adenocarcinoma of digestive origin, and, rarely, a peritoneal sarcomatosis or a gastrointestinal autonomic nerve tumor (13). Sclerosing mesenteritis sometimes presents a diagnostic problem (15), because of the resulting mesothelial hyperplasia.

5 C.F. Verschraegen et al 395 Clinical Presentation Typically, the diagnosis takes a long time to establish. Most of my patients have complained of symptoms for 6 months to more than 2 years prior to diagnosis. In rare instances, patients describe a spontaneous remission with a recurrence more than 5 years later. When the disease becomes symptomatic, patients present with abdominal girth enlargement, ascites, fatigue, anemia, weight loss, night sweats and nocturnal fever, and digestive disturbances. It is fairly common for males to first present with an inguinal hernia, and less often with an umbilical hernia. Women are sometimes diagnosed because of the finding of a pelvic mass. Transmural invasion with involvement of the abdominal musculature is not uncommon, and these patients are usually diagnosed with a sarcoma, despite the epithelial nature of their mesothelioma (Fig. 25.1). Some patients have indolent disease, despite a heavy tumor burden (16). Table 25.4 presents a compilation of peritoneal cases reported in seven medical publications (8,17 22). The most frequent signs are increased abdominal girth with ascites and abdominal pain. Late complications of mesothelioma are bowel obstruction, and a hypercoagulable state. Care should be taken to prevent deep venous thrombosis and arterial thrombosis, which are relatively frequent in this patient population. Figure Abdominal wall involvement in a patient diagnosed with peritoneal mesothelioma. Thin arrow, parietal involvement.

6 396 Chapter 25 Clinical Presentation of Abdominal Mesothelioma The laboratory investigations show an increased platelet count in about 50% of patients, and sometime an increase in white blood cells. Low-grade anemia is common. Another feature of peritoneal mesothelioma is that it causes a low serum albumin, in relationship to the peritoneal infiltration. This hypoalbuminemia is usually asymptomatic. The most commonly elevated tumor marker is CA-125, probably a sign of peritoneal irritation by the cancer; it is seen in fewer than half the patients. The staging of peritoneal mesothelioma has not been established in a reproducible fashion. I distinguish four categories: a localized lesion that can be fully resected [equivalent to stage I of the Butchart et al (23) classification], disease contained into the abdominal cavity on the peritoneal and organ surfaces that can only be debulked at best (equivalent to stage I), disease contained into the abdominal cavity with intraparenchymal invasion of organs such as liver metastases (equivalent to stage IV), and disease extending outside of the peritoneal cavity including lymph node involvement (equivalent to stage III or IV). The last two categories seem to have a worse prognosis. The SEER registry differentiates among localized, regional, distant, or unstaged disease. Of 621 abdominal mesotheliomas, 60 (9.7%) were localized (primary tumor confined to an organ), 72 (11.6%) were regional (tumor involving adjacent structures, or with regional lymph nodes), 402 (65%) were distant (skipped areas between primary tumor and other lesions), and 87 (14%) were unstaged. Because of the uncertainty of these definitions, these numbers have to be taken cautiously. The principal indication from these numbers is that localized peritoneal mesothelioma is very rare. Pathophysiology Though the pathophysiology of malignant peritoneal mesotheliomas is not well understood, there have been advances in identifying markers associated with malignant proliferation of mesothelial cells (24). One such molecule is mesothelin, a cell surface glycoprotein present on normal mesothelial cells, which is highly expressed in the majority of patients with epithelial mesotheliomas (25,26). Mesothelin overexpression is also seen in other tumors including serous ovarian carcinomas, pancreatic adenocarcinomas and some squamous cell carcinomas. The exact function of mesothelin is not known but it may be involved in tumor dissemination. Initially, mesothelin is formed as a 69-kd polypeptide with a hydrophobic tail, which is probably removed and replaced by phosphatidylinositol. After glycosylation at one or more of its four putative N-linked glycosylation sites, it is cleaved by a protease to yield the cell-bound 40-kd fragment and a smaller N-terminal fragment, which is shed. This N-terminal fragment was called the megakaryocyte potentiating factor (MPF) since it stimulated the megakaryocyte colony-forming activity of murine interleukin-3 in mouse bone marrow cell culture (27). Also, MPF could play a role in the thrombocytosis seen in the majority of patients with malignant

7 mesothelioma. Soluble molecules of the mesothelin/mpf family have also been detected in the serum of patients with ovarian cancer, and studies are ongoing to see whether mesothelin levels are elevated in patients with mesothelioma. If this is the case, mesothelin could serve as a tumor marker for this disease (28). Mesothelin is also an attractive candidate for targeted therapy, given its high expression in patients with mesothelioma and limited expression in normal tissues except normal mesothelial cells. Currently, a phase I study of a recombinant antimesothelin immunotoxin is ongoing in patients with mesotheliomas whose tumors overexpress mesothelin (29). C.F. Verschraegen et al 397 Treatment Currently, there is no curative treatment for peritoneal mesothelioma that is appropriate for the majority of patients. Different modalities have been tried, including surgery, chemotherapy, radiation therapy, immunotherapy, and hormonal therapy (30,31). Many patients receive no treatment. The SEER database collected the following information. Of 601 patients for whom treatment records were available, 201 (33%) did not receive any definitive cancer-directed treatment; however, some outpatient chemotherapy treatments may have been missed during data collection. One hundred seven (18%) patients were treated by surgery only, with a total of 195 patients having surgery during the course of therapy. One hundred sixty-two patients (27%) received a medical treatment including chemotherapy with or without hormonal therapy. Forty-two patients were irradiated with (n = 26) or without (n = 16) other therapeutic modalities. Ninety-six patients (16%) received two or more treatment modalities. The treatment was unknown in 17 patients, and two patients received other treatments. Despite these therapeutic efforts, survival remains poor, as described in the next section. Survival The 5-year average age-adjusted relative survival rate for all mesothelioma collected in the SEER database over 27 years was 8% overall, 5% for men, and 17% for women. For patients diagnosed with peritoneal mesothelioma, including the digestive system category, the 5-year survival rates are 16% overall, 10% for men, and 22% for women. These data indicated that the overall prognosis for patients diagnosed with peritoneal mesothelioma is better than for patients diagnosed with pleural disease. This fact has not well been established in the literature so far (32). Women did better than men, which is also controversial (17,33) (Fig. 25.2). Survival data were analyzed for patients who received a mesothelioma-specific treatment versus patients who were not specifically treated for mesothelioma. Of 601 patients with an abdominal mesothe-

8 398 Chapter 25 Clinical Presentation of Abdominal Mesothelioma % survival All population Men Women Years after Diagnosis Figure Survival of patients diagnosed with peritoneal mesothelioma. lioma, 87 were excluded from the survival analysis for the following reasons: 68 received a diagnosis of a second primary, seven received a diagnosis at autopsy, six lacked follow-up, and six patients mesothelioma had other causes. Of 514 analyzable patients, 339 received a mesothelioma-specific treatment, 162 did not, and for 13 patients the treatment was unknown. Median survival was 11 months for treated patients versus 8 months for untreated patients. At 1 year, survival was 47% (±5.5%) for treated patients versus 25% (±7%) for untreated patients (Fig. 25.3). At 5 years, there was no difference, with 16.5% (±4.5%) of treated and 11% (±6.4%) of untreated patients surviving. Analyzing these data over time shows that there has not been any therapeutic progress within the past 30 years. One-year survival rates % Survival Mesothelioma-specific treatment No treatment Years after Diagnosis Figure Relative survival of untreated versus mesothelioma-specific treated patients.

9 for treated patients were 47% in the 1970s, 49% in the 1980s, and 44% in the 1990s. C.F. Verschraegen et al 399 Conclusion Peritoneal mesothelioma is a disease that can present with a variety of abdominal symptoms, the most common one being increasing girth, or with constitutional symptoms such as fever, night sweats, or weight loss. The prognosis is variable and cannot be predicted accurately despite the symptomatology (16). In absolute numbers, more men than women are affected with this disease; however, the ratio of peritoneal/pleural mesothelioma is greater in women. There are two main types of peritoneal mesothelioma: the diffuse malignant mesothelioma and the well-differentiated mesothelioma seen usually in premenopausal women. The prognosis of patients with well-differentiated disease is better, and these patients should be observed as there is no evidence that treatment improves the prognosis. Patients with diffuse malignant peritoneal disease should be treated on research protocols, as the disease is usually fatal and no treatment has been shown to prolong survival. Multimodality therapy is usually needed in the care of these patients. Acknowledgments The authors thank Dr. Harriett Smith for advice with the SEER database, and Dr. Evelyne Loyer for Figure References 1. Connelly RR, Spirtas R, Myers MH, Percy CL, Fraumeni JF Jr. Demographic patterns for mesothelioma in the United States. J Natl Cancer Inst 1987; 78(6): Roggli VL. Malignant mesothelioma and duration of asbestos exposure: correlation with tissue mineral fibre content. Ann Occup Hyg 1995;39(3): Roggli VL, Oury TD, Moffatt EJ. Malignant mesothelioma in women. Anat Pathol 1997;2: Suzuki Y. Pathology of human malignant mesothelioma preliminary analysis of 1517 mesothelioma cases. Ind Health 2001;39(2): Roggli VL, Sharma A, Butnor KJ, Sporn T, Vollmer RT. Malignant mesothelioma and occupational exposure to asbestos: a clinicopathological correlation of 1445 cases. Ultrastruct Pathol 2002;26(2): Britton M. The epidemiology of mesothelioma. Semin Oncol 2002;29(1): Neumann V, Gunthe S, Mulle KM, Fischer M. Malignant mesothelioma German mesothelioma register Int Arch Occup Environ Health 2001;74(6): Chahinian AP, Pajak TF, Holland JF, Norton L, Ambinder RM, Mandel EM. Diffuse malignant mesothelioma. Prospective evaluation of 69 patients. Ann Intern Med 1982;96(6 Pt 1):

10 400 Chapter 25 Clinical Presentation of Abdominal Mesothelioma 9. Churg A, Colby TV, Cagle P, et al. The separation of benign and malignant mesothelial proliferations. Am J Surg Pathol 2000;24(9): Clement PB. Diseases of the peritoneum. In: Kurman RJ, ed. Pathology of the Female Genital Tract, 4th ed. New York: Springer-Verlag, 1994: Butnor KJ, Sporn TA, Hammar SP, Roggli VL. Well-differentiated papillary mesothelioma. Am J Surg Pathol 2001;25(10): Daya D, McCaughey WT. Well-differentiated papillary mesothelioma of the peritoneum. A clinicopathologic study of 22 cases. Cancer 1990;65(2): Shanks JH, Harris M, Banerjee SS, et al. Mesotheliomas with deciduoid morphology: a morphologic spectrum and a variant not confined to young females. Am J Surg Pathol 2000;24(2): Bollinger DJ, Wick MR, Dehner LP, Mills SE, Swanson PE, Clarke RE. Peritoneal malignant mesothelioma versus serous papillary adenocarcinoma. A histochemical and immunohistochemical comparison. Am J Surg Pathol 1989;13(8): Emory TS, Monihan JM, Carr NJ, Sobin LH. Sclerosing mesenteritis, mesenteric panniculitis and mesenteric lipodystrophy: a single entity? Am J Surg Pathol 1997;21(4): Kerrigan SA, Turnnir RT, Clement PB, Young RH, Churg A. Diffuse malignant epithelial mesotheliomas of the peritoneum in women: a clinicopathologic study of 25 patients. Cancer 2002;94(2): Antman K, Shemin R, Ryan L, et al. Malignant mesothelioma: prognostic variables in a registry of 180 patients, the Dana-Farber Cancer Institute and Brigham and Women s Hospital experience over two decades, J Clin Oncol 1988;6(1): Antman KH, Corson JM, Li FP, et al. Malignant mesothelioma following radiation exposure. J Clin Oncol 1983;1(11): Eltabbakh GH, Piver MS, Hempling RE, Recio FO, Intengen ME. Clinical picture, response to therapy, and survival of women with diffuse malignant peritoneal mesothelioma. J Surg Oncol 1999;70(1): Jones DE, Silver D. Peritoneal mesotheliomas. Surgery 1979;86(4): Piccigallo E, Jeffers LJ, Reddy KR, Caldironi MW, Parenti A, Schiff ER. Malignant peritoneal mesothelioma. A clinical and laparoscopic study of ten cases. Dig Dis Sci, 1988;33(5): van Gelder T, Hoogsteden HC, Versnel MA, de Beer PH, Vandenbroucke JP, Planteydt HT. Malignant peritoneal mesothelioma: a series of 19 cases. Digestion 1989;43(4): Butchart EG, Ashcroft T, Barnsley WC, Holden MP. Pleuropneumonectomy in the management of diffuse malignant mesothelioma of the pleura. Experience with 29 patients. Thorax 1976;31(1): Krismann M, Muller KM, Jaworska M, Johnen G. Molecular cytogenetic differences between histological subtypes of malignant mesotheliomas: DNA cytometry and comparative genomic hybridization of 90 cases. J Pathol 2002;197(3): Chang K, Pai LH, Pass H, et al. Monoclonal antibody K1 reacts with epithelial mesothelioma but not with lung adenocarcinoma. Am J Surg Pathol 1992;16(3): Chang K, Pastan I. Molecular cloning of mesothelin, a differentiation antigen present on mesothelium, mesotheliomas, and ovarian cancers. Proc Nat Acad Sci USA 1996;93(1): Kojima T, Oh-eda M, Hattori K, et al. Molecular cloning and expression of megakaryocyte potentiating factor cdna. J Biol Chem 1995;270(37):

11 28. Scholler N, Fu N, Yang Y, et al. Soluble member(s) of the mesothelin/ megakaryocyte potentiating factor family are detectable in sera from patients with ovarian carcinoma. Proc Nat Acad Sci USA 1999;96(20): Hassan R, Kreitman R, Strauss L, et al. SS1(dsFv)PE38 anti-mesothelin immunotoxin in advanced malignancies: phase I and pharmacokinetic study of alternate-day infusion. Proc Am Soc Clin Oncol 2002;21(A29). 30. Sugarbaker PH, Acherman YI, Gonzalez-Moreno S, et al. Diagnosis and treatment of peritoneal mesothelioma: the Washington Cancer Institute experience. Semin Oncol 2002;29(1): Taub RN, Keohan ML, Chabot JC, Fountain KS, Plitsas M. Peritoneal mesothelioma. Curr Treat Options Oncol 2000;1(4): Hillerdal G. Malignant mesothelioma 1982: review of 4710 published cases. Br J Dis Chest 1983;77(4): Sebbag G, Yan H, Shmookler BM, Chang D, Sugarbaker PH, Results of treatment of 33 patients with peritoneal mesothelioma. Br J Surg 2000; 87(11): C.F. Verschraegen et al 401

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