Islet Cell Tumors of the Pancreas: Clinico-Biochemical Correlations
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1 ANNALS OF CLINICAL AND LABORATORY SCIENCE, Vol. 9, No. 3 Copyright 1979, Institute for Clinical Science, Inc. Islet Cell Tumors of the Pancreas: Clinico-Biochemical Correlations JANARDAN D. KHANDEKAR, M.D. Division o f Medical Oncology, Evanston Hospital, Evanston, IL and Department o f Medicine, Northwestern University Medical School, Chicago, IL ABSTRACT Islet cell tumors produce a spectrum of clinical syndromes. Intensive investigations of these tumors have enhanced our understanding of cellular origin, physiology and biochem istry of the islet hormones. Biochemical studies on the hormones are helpful in the diagnosis and treatm ent planning of the islet tumors. For example, insulinoma and glucagonoma can be diagnosed more readily by dem onstration of pro insulin and proglucagon-like components, respectively, in the blood. Similarly, m easurem ent of vasoactive intestinal polypeptide is not only useful in the diagnosis, but also in the follow-up of patients w ith pancreatic cholera syndrome. This m ini-review examines these and other clinico-biochem ical correlates seen in islet tumors. The islet cell tumors are rare, with a prevalence rate of less than 1:100,000 population.29 However, these tumors have been the subject of great attention, since they pose a challenge to both basic scientists and clinicians. Investigations of these tumors have enhanced our understanding of embryogenesis of different cells of the islets of th e L an g erh an s and about physiology and pathology of the hormones produced by the islet cells. The tumors produce a variety of clinical syndromes, the m anagem ent of which is dem anding to a clinician. In this paper, the biochemical and physiological actions of the islet hormones have been correlated with the corresponding clinical syndrom es produced 212 by the excessive hormonal secretions. This is not an extensive review of the subject, but it is aim ed at developing the concept of clinico-biochemical correlations for islet cell tumors. Embryology of the Islet Cells The islet cells of Langerhans are probably a part of a system acronym ed as APUD, which stands for amine precursor uptake and decarboxylation.23 This system is deriv ed from neurally programmed cells of the epiblastic origin. APUD cells are present in many organs and tumors, such as pituitary, thyroid, adrenal m edulla, sm all cell lung car /79/ $01.20 Institute for Clinical Science, Inc.
2 ISLET CELL TUMORS OF THE PANCREAS 213 cinom a, etc. T h ese cells share m any h isto ch em ical sta in in g p ro p e rtie s.23 F urther support of their essentially neural nature is provided by the recent findings of at least two peptides common to brain and islets of Langerhans.28 The Clinical Spectrum of the Islet Cell Tumors Almost all of the benign and about three-fourths of the m alignant islet cell tumors are recognized during life by the syndrome related to hypersecretion of one or more hormones. In table I are shown the cellular origin of various hormones of the islets, along w ith the syndrom e produced by their excessive production.15 Many tumors may secrete more than one hormone. For example, several malignant insulinomas have been associated with secretion of m ultiple peptide hormones, including gastrin, glucagon, glucagon and gastrin, ACTH and serotonin.29 Occasionally, the tumor may occur as a part of the m ultiple endocrine adenomatosis (MEA- I) syndrome. The MEA-I syndrom e is comprised of pituitary adenoma, islet cell adenoma, or carcinoma and parathyroid adenoma, or hyperplasia.29 About 20 percent of islet cell carcinomas do not secrete hormones, or at least not in high enough quantities that allow m easurem ent with the present techniques, and present with abdominal mass, pain, jaundice or other symptoms.1 These tumors do not secrete human chorionic gonadotrophin (HCG) or one of its subunits (HCG -a or HCG-/3).12 Insulinom as This is the m ost com m on islet cell tum or, although Z ollinger-e llison syndrome is also approaching the same prevalence rate in recent years. T he peak occurrence of this syndrome is in the fourth to sixth decade.29 Anatomically, it may present as:5 (A) adenomas single or multiple (are responsible for 80 percent of the insulinom as); (B) m icroadenom atosis; (C) TABLE I Spectrum o f I s l e t C ell Tumors C e l l H o rm o n es S y n d ro m e A Glucagon Glucagonoma B Insulin Insulinoma D Somatostatin Somatostatinoma D1 Vasoactive Pancreatic cholera intestinal D2 (mainly polypeptide Pancreatic?Marker for non-islets) polypeptide endocrine tumors Non-B Gastrin Zollinger-Ellison Non-B ACTH serotonin Part of carcinoid syndrome Any of the above Nonfunctioning carcinoma; (D) any of these associated w ith MEA-1 syndrom e; and (E) hyperplasia. Additionally, in children, n e sid io b la sto sis, a c o n d itio n c h a ra c terized by genesis of beta cells and small islets from the pancreatic ductules, can cause intractable hypoglycem ia.10 The symptoms of insulinom as are usually related to hypoglycem ia and can mimic a wide variety of psychiatric and neurological disorders. With the exception of carcinomas, which may present with a space-occupying lesion, all other anatomical forms of insulinomas present w ith hypoglycem ic sym ptom s p recip itated by periods of long fasting.5 Insulin produces hypoglycem ia by interfering with a variety of mechanisms responsible for glucose homeostasis.5 Insulin interferes w ith processes involved in glucose production by decreasing inflow to the liver of substances needed for glucogenesis, as well as by decreasing the activities of the hepatic enzymes responsible for glucose production. Insulin also increases glucose and aminoacid intake and utilization in various tissues (see figure 1). Diagnosis of Insulinom as In a patient presenting with symptoms of fasting hypoglycemia, the diagnosis of insulinom a should be considered. In m any patients, th e plasm a/glucose (G)
3 214 KHANDEKAR level after an overnight fast is usually below 60 mg per dl. However, in many patients, a prolonged fasting up to 14 hours is required to demonstrate a reduction of plasma glucose to below 50 mg per dl. A low plasm a glucose, along with an elevated immunoreactive plasma insulin (IR I) is q u ite pathognom ic of in sulinomas.5 A brief discussion pertaining to the role of insulin in glucose homeostasis is essential to appreciate the IRI/G ratio. In normal individuals, secretion of insulin is determ ined by extracellular glucose. Most of the insulinomas are autonomas;31 therefore, a norm al plasm a insulin associated with fasting blood glucose in the hypoglycemic range is evidence that the secretion of insulin is inappropriate for the simultaneous blood glucose level.5 Others have suggested that an amended IR I/G calculated as: plasma IRI u.u per ml x 100 divided by plasm a glucose mg per dl minus 30 (with an upper lim it of 50), would be a better ratio for the diagnosis. The subtraction of 30 mg per dl from the plasm a glucose is based on the observation that at 30 mg per dl of plasma glucose, in su lin se cre tio n is alm ost totally sw itched off in healthy subjects.3 There are a num ber of other provocative and suppressive tests which may be useful in the diagnosis of insulinom as.4,3 Assays of C-peptide and proinsulin are of considerable interest, since they dem onstrate application of basic sciences to the clinical medicine. A brief discussion pertaining to the insulin synthesis and secretion will illustrate this point. INCREASED INSULN I I I 1 DECREASED DECREASED INCREASED GLUCOSE INCREASED UPTAKE OF GLYCOGENOLYSIS NE0GLUC0GENES1S UPTAKE AND AMINOAClDS BY MUSCLE UTILIZATION IN UVER, MUSCLE, ADPOSE TISSUE DECREASED AMNO DECREASED DECREASED HEPATIC DECREASED ACTIVITY AC MOBILIZATION GLYCEROL UPTAKE OF AMN0ACI0S OF HEPATIC ENZYMES F ig u r e 1. hypoglycem ia. M echan ism s o f in su lin -in d u ced Many different proteins of diverging biological importance, such as hormones, a n tib o d ie s, m em b ran e p ro te in s, are synthesized in the form of larger precursors that are subsequently modified by cleavage to smaller forms.11 Many recent studies have clearly dem onstrated that initiation of protein synthesis occurs on polyribosomes in the cell matrix, and that the translation products of the m-rna for various secretory proteins carry a 20 to 30 residue N H 2 term inal extensions that contain a high proportion of hydrophobic aminoacids.2,21,33 This hydrophobic N H 2 term inal of preproinsulin serves as a leader at the ribosome membrane junction, leading to the vectorial discharge of the polypeptide in the rough endoplasmic reticulum (RER).2 Im m ediately following the entry of the preproinsulin in the cisternae of the RER, the le a d e r seq u en c e is rem o v ed by specific peptidase, resulting in the formation of proinsulin.22 The prohormone then moves within the cisterne of the RER to the Golgi complex, w here the am inoterm inal peptide is further cleaved by trypsin and carboxypeptidase B, resulting in the production of insulin.2,10 The final hormonal product is packed into secretory granules and transported to the periphery of the cell. I t is released into the extracellular space by the process of exocytosis,21 in response to an increased concentration of glucose in the extracellular fluid. Normally, plasm a proinsulin-like com ponents (PLC) constitute less than 20 percent of the IRI.6 In almost all patients with insulinom a, plasm a PLC c o n trib u tes more than 25 percent of total IRI as measured by specific radioimmunoassay or by gel filtration.6,24 Although higher PLC activity is seen in other hypoglycemic states and rarely in other conditions, dem onstration of this fraction in insulinoma patients is characteristic.6 More recently, gel filtration studies have dem onstrated the presence of a high m olecular w eight IRI,
4 ISLET CELL TUMORS OF THE PANCREAS 215 which could represent a counterpart of p re p ro in su lin d isc o v e red in rat in sulinoma.2'24 The inappropriate basal and stim ulated release of insu lin and pro insulin could be explained by a num ber of m echanism s. However, m ost of the evidence favors the hypothesis that in the insulinom as, there is a loss of storage capacity, com bined w ith uncontrolled release of the hormones, owing to a defect in the intracellular insulin transport and release processes.6 The proinsulin molecule is composed of a C-peptide which links A and B chains of the insulin. The function of the C-peptide appears to be proper alignm ent of the chains, resulting in efficient form ation of disulfide linkages.33 W hen the proinsulin is converted to insulin by cleavage of C-peptide by trypsin carboxypeptidase B, the peptide is also released in circulation, and its release is proportional to endogenous insulin secretion.26 In normal volunteers, insulin infusion suppresses endogenous insulin secretion. Since most of the insulinomas are autonomous, there is an im pairm ent of the feedback inhibition of endogenous insulin secretion.5 Service et al have used this principle in the diagnosis of insulinomas. They adm inistered porcine insulin and m easured C -p e p tid e.31 D uring h y p o glycemia (plasma glucose of less than 40 mg per dl), the mean C-peptide immunoreactivity (CPR) of normal subjects was less than 1.2 ng per ml, whereas with one exception, all patients with insulinoma had a mean CPR of more than 1.9 ng per ml. Glucagonomas Although glucagonomas were described m any years ago, M allinson and his coworkers described for the first time in detail the clinical glucagonoma syndrom e.17 It is characterized by necrolytic migratory erythema, stomatitis, anemia, hypoaminoacidem ia, m ild diabetes m ellitus, and weight loss. The single most characteristic feature seems to be the skin changes, and many of these patients may rem ain undiagnosed while attending dermatology clinics.36 The findings of hypoam inoacidemia and mild diabetes mellitus can be explained on the basis of increased glucagon levels, since the horm one is known to be antagonistic to insulin.36 The m echanism of derm atitis and anem ia remains unknown. More recently, a patient was seen by us with glucagonoma who also m anifested a diffuse neurological syndrome. Although the cerebral spinal fluid (CSF) glucagon in this patient was elevated, the exact m echanism of the neurological syndrom e rem ains to be defined.12"4 T he diagnosis of glucagonom a is provided by im m unocytochem istry and radioimmunoassay of glucagon.3,15*39 As with insulinomas, patients with glucagonomas also secrete high m olecular w eight precursor forms, and these can also be used for the diagnosis of the syndrom e.3,39 The glucagon m easurem ents (IRG) may also serve in the follow-up of patients and to assess tu m o r re sp o n se to various therapies.3 Our patient with glucagonoma received chem otherapy w ith m ultiple courses of 5-fluorouracil and streptozotocin, and plasma IRG was serially followed. The decline in the plasma IRG preceded his clinical improvement and has served as a useful m arker for treatm ent planning.12"1 Serial follow-up w ith the m arkers, such as alpha fetoprotein or carcinoem bryonic antigen, has b een useful in the m anagem ent of neoplasia and in other various tum ors.18,20 Zollinger-Ellison (ZE) Syndrome The frequency of the ZE syndrome is fast approaching that of insulinoma. This syndrome results from the prolonged and excessive release of gastrin from a tumor also known as gastrinoma.30,38 Most of the clinical m anifestations of th e ZE syndrome are secondary to hypersecretions of gastric acid.30 Entry of large volumes of acid gastric juice is directly responsible for
5 216 KHANDEKAR duodenitis, duodenal and jejunal ulceration, and for the diarrhea frequently observed.25,38 Although volum e and bicarbonate output of the pancreatic juice are also increased in gastrinomas, the capacity to secrete bicarbonate does not equal the capacity to secrete acid in these patients.38 This im balance in acid bicarbonate secretion leads to low intralum inal ph, resulting in injury to the proximal intestinal m u cosa. This impairs its ability to release normal amounts of secretin and to dissipate acid. The diarrhea and steatorrhea associated with ZE are also secondary to excessive gastrin production.25 Gastrin inhibits salt and w ater absorption by the intestine. Similarly, large am ounts of gastric contents (up to 10 liters per day) presented to the intestine and rapid intestinal transit tim es m ay also b e in v o lv ed in the pathogenesis of diarrhea.30 T he low intestinal luminal ph caused by excessive gastric acid secretion, results in an activation of lipase and precipitation of bile salts. These factors, along with the damage to the intestinal mucosal cells, result in impaired ability to form chylom icrons, causing steatorrhea.38 Tum ors of the extra pancreatic endocrine glands are found in 20 to 48 percent of patients w ith the ZE syndrom e.14 Although total gastrectomy has been the treatm ent of choice in managing patients with the ZE syndrome, recently cimetidine, an H 2-receptor antagonist, has been found tc be useful.19 These subjects are beyond the scope of the present review. Somatostatinoma Only three cases of somatostatinoma have been described.8' 13,16 Two of these patients had a diabetic glucose tolerance curve,8 16 and in one case, steatorrhea and achlorohydria were also present.16 Two p a tie n ts had exhau stiv e e n d o crin e w ork-up. E xcessive p ro d u ctio n of som atostatin in these patients was probably responsible for the m arked suppression of basal and stim ulated IRI, IRG and hum an growth hormone secretion.7,15,16 T hese cases have confirm ed the physiological actions seen after the infusion of som atostatin in hum ans.36 P ancreatic C holera (W erner-m orrison Syndrome) This syndrome, described first in 1958, is characterized by severe intractable, w atery d iarrh ea, w ith hypokalem ia, h y p o c h lo ro h y d ria an d o ccasionally hypoglycem ia, h y p ercalcem ia and episodes of flushing.27,28,37 The diarrhea is mostly of secretory type and results in the m arked loss of water and electrolytes from the small and large intestines.28 The lesion most commonly underlying this syndrom e is an islet cell adenom a or adenocarcinom a.27 A num ber of other tumors arising from APIJD system may also cause this syndrom e.15 T here is considerable evidence that the syndrom e is caused by excessive secretio n of vasoactive in testin al polypeptide (VIP).27,28 VIP in experim ental anim als causes in d u ctio n of m ucosal adenylate cyclase, which through cyclic AMP stimulates water and electrolyte secretion from the small and large intestines.23,28,32 There is also evidence that the VIP-cyclic AMP system may also be responsible for hypochlorohydria and hypoglycem ia seen in this syndrom e.32 Some doubts have been expressed regarding the diagnostic value of plasma V IP m easurem ents in the p ancreatic cholera syndrome. Straus has pointed out the problem s associated w ith the radioim m unoassay of VIP.34 It, th erefo re, seems that until more conclusive data are obtained, therapeutic decisions in cases of pancreatic cholera syndrome should be made more on clin ical grounds than on the basis of VIP concentration. M oreover, cases have now been reported in which VIP levels were normal, whereas elevated
6 ISLET CELL TUMORS OF TH E PANCREAS 217 levels of prostaglandins of E series were found.11 Conclusion The islet cell tumors produce a spectrum of clinical disorders. Many of the symptoms and signs, characteristics of the specific islet cell tumors, can be explained by biochem ical and physiological actions produced by the respective hormones of the tumors. In addition, many of the tests used in the diagnosis of these tumors are dependent on the biochemical actions of these hormones. A study of these tumors has led to a greater understanding of the biochemical and physiologic mechanisms of these horm ones. References 1. Broder, L. E. and Ca rter, S. K.: Pancreatic islet cell carcinoma clinical features of 52 patients. Ann. Int. Med. 79: , C h a n, S. J., Keim, P., and St e in e r, D. F.: Cellfree synthesis of rat preproinsulins: characterization and partial amino acid sequence determination. Proc. Nat. Acad. Sci. 73: , D a n fo r th, D. N., Jr., T rich e, T., Doppman, J. L., ET AL: Elevated plasma proglucagon-like component with a glucagon-secreting tumor. New Eng. J. Med. 295: , E d is, A. J., M c Ilr a th, D. C., van H e e r d e n, J. A., ET AL: Insulinoma current diagnosis and surgical management. Current Problems in Surgery. Chicago, Year Book Medical Publishers, Inc., F a jans, S. S. and FLOYD, J. C.: Fasting hypoglycem ia in adults. N ew E ng. J. Med. 294: , F r eric h s, H. and Cr e u t z f e l d t, W.: Hypoglycaemia. 1. Insulin secreting tumours. Clin. Endocr. Metab. 5: , Ga n d a, O. P. and SOELDNER, J. S.: Somatostatinoma: Follow-up studies. New Eng. J. Med. 297: , Ga n d a, O. P., Weir, G. C., So eld n er, J. S., et AL: Som atostatinom a: A som atostatin - containing tumor o f the endocrine pancreas. N ew Eng. J. Med. 296: , Habener, J. F. and Potts, J. T.: Biosynthesis o f parathyroid hormone. N ew Eng. J Med. 299: , H irsch, H. J., Loo, S., Evans, N., et a l: H ypoglycem ia o f infancy and nesidioblastosis Studies with somatostatin. New Eng. J. Med. 296: , J a f f e, B. M. and CONDON, S.: Prostaglandins E and F in endocrine diarrhea-genic syndromes. Ann. Surgery 84: , Ka h n, C. R., R o s e n, S. W., W e in t r a u b, B. D., ET AL: Ectopic production of chorionic gonadotropin and its subunits by islet-cell tumors. New Eng. J. Med. 297: , a. Kh a n dek ar, J. D., O yer, D., Mil l e r, H., and VlCK, N. A.: Neurologic involvement in glucagonoma syndrome: Response to combination chemotherapy with 5-fluorouracil and streptozotocin. Cancer (in press). 13. K o v a c s, K., H o r v a t h, E., E z r in, C., e t a l : Immunoreactive somatostatin in pancreatic islet-cell carcinoma accompanied by ectopic A C T H syndrome. Lancet , L a m e r s, C. B., St a d il, F and T o n g e r e n, J. H.: Prevalence of endocrine abnormalities in patients with the Zollinger-Ellison syndrome and in their families. Amer. J. Med. 64: , La r s s o n, L. I.: Endocrine pancreatic tumors. Human Path. 9 : , L a r s s o n, L.I., H o l s t, J. J., H i r s c h, M. A., e t AL: Pancreatic som atostatinom a. L ancet 1 : , Ma l l in so n, C. N., Bloom, S. R., Wa rin, A. P., ET AL: A glu cagonom a sy n d rom e. L ancet 2:1-5, Ma u g h, T. H., II: Biochemical markers: Early warning signs of cancer. Science i97: , M c C a r t h y, D. M.: Report on the United States experience w ith cim etidine in Zollinger-Ellison syndrome and other hypersecretory states. Gastroenterology 74: , M o o r e, M. R., W a l t o n, K. N., M c I n t i r e, R. K., ET AL: Evaluation of human chorionic gonadotropin and alpha fetoprotein in benign and m alignant testicular disorders. Surg. Gynec. Obstet. 147: , Pa l a d e, G.: Intracellular aspects of the process of protein synthesis. Science 189: , Pa t z e l t, C., La brecque, A. D., D u g u id, J. R., ET AL: Detection and kinetic behavior of preproinsulin in pancreatic islets. Proc. Nat. Acad. Sci. 75: , P e a r s e, A. G. E., P o l a k, J. M., and B l o o m, S. R.: The newer gut hormones: cellular sources, physiology, pathology, and clinical aspects. Gastroenterology 72: , PERMUTT, M., BlESBROECK, J., and C h y n, R.: Characteristics of high molecular weight insulins in insulinoma patients. J. Chem. Eng. Med. 44: , R e g a n, P. T. and MALAGELADA, J. R.: Clinical aspects of Zollinger-Ellison syndrome. Mayo Clin. Proceed. 53:19-23, Ru b e n s t e in, A. H., Block, M. B., Starr, J., ET AL: Proinsulin and C-peptide in blood. D i abetes 21 :661, S a id, S. I. and F a l o o n a, G. R.: Elevated plasma and tissue levels of vasoactive intesti
7 2 1 8 KHANDEKAR nal polypeptide in the watery-diarrhea syndrome due to pancreatic, bronchogenic and other tumors. New Eng. J. Med. 293: , Sa id, S. I. and Zf a ss, A. M.: Gastrointestinal hormones. Disease-A-Month, vol. XXIV, no. 10. Chicago, Year Book Medical Publishers, Inc., Sc h e in, P. S., D e L e l l is, R. A., Ka h n, C. R., e t AL: Islet cell tumors: current concepts and management. Ann. Intern. Med. 79: , Se n b e r g, J. I., Wa l sh, J. H., Gr ossm an, M. J.: Zollinger-Ellison syndrome. Gastroenterology 65: , Service, F. J., Horw itz, D. L., Rubenstein, A. H., ET AL: C-peptide suppression test for insulinoma. J. Lab. Clin. Med. 90: , SlMON, B. and Ka t h e r, H.: Activation of human adenylate cyclase in the upper gastrointestinal tract by vasoactive intestinal polypeptide. Gastroenterology 74: , St e in e r, D. F. and Clark, J. L.: The spontaneous reoxidation of reduced beef and rat proinsulins. Proc. Nat. Acad. Sei. 60: , Str a u s, E.: Radioimmunoassay of gastrointestinal horm ones. G astroenterology 74: , U llr ic h, A., Sh in e, J., C h ir g w in, J., e t a l : Rat insulin genes: construction of plasmids containing the coding sequences. Science i 96: , U n g e r, R. H.: Glucagon and somatostatin. Disease-A-Month, vol. XXIV, no. 8. Chicago, Year Book Medical Publishers, Inc., V e r n e r, J. V. and M ORRISON, A. B.: Endocrine pancreatic islet disease with diarrhea. Arch. Intern. Med. 133: , Wa l sh, J. H. and Grossm an, M. I.: Gastrin. New Eng. J. Med. 292: & , Weir, G. C., Horto n, E. S., Aoki, T. T., e t a l : Secretion by glucagonom as of a p ossib le glucagon precursor. J. Clin. Invest. 59: , 1977.
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