Medullary Carcinoma of the Thyroid in the Multiple Mucosal Neuromas Syndrome*
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1 ANNALS OF CLINICAL AND LABORATORY SCIENCE, Vol. 9, No. 5 Copyright 1979, Institute for Clinical Science, Inc. Medullary Carcinoma of the Thyroid in the Multiple Mucosal Neuromas Syndrome* MICHAEL L. NETZLOFF, M.D.,f ADOLFO D. GARNICA, M.D.,t B. M. RODGERS,! and JAIME L. FRIAS, M.D.f t Department of Pediatrics, Division of Genetics, and $ Department of Surgery, Division of Pediatric Surgery, University of Florida College of Medicine, Gainesville, FL ABSTRACT The clinical features of the multiple mucosal neuromas (MMN) syndrome permit the recognition of these patients and their potential development of the associated medullary thyroid carcinoma (MTC). The distinctive physical appearance caused by the mucosal neuromas, the Marfanoid habitus and, occasionally, the positive family history aid in establishing the diagnosis. Neurogangliomas are frequently present in the gastrointestinal tract of these patients who may have megacolon, constipation and diarrhea. The third instance of the MMN syndrome is reported in the newborn as intestinal obstruction. It is suggested that the syndrome be considered in the differential diagnosis of Hirschsprung s disease and bowel obstruction in the neonate. Serum calcitonin measurements following stimulation by calcium or pentagastrin infusion reliably detect incipient MTC and may be used to select those MMN patients requiring thyroid surgery. Recognition of patients with the MMN syndrome and subsequent calcitonin screening and early surgical intervention will significantly reduce the chance of their developing terminal MTC. All MMN patients with mucosal neuromas or intestinal neurogangliomas should have such evaluations at least yearly. Relatives who are at risk for inheriting this dominant disease should be similarly evaluated, regardless of their normal appearance. Introduction The opportunity to recogn ize and evaluate the potential of malignancy based on an identifiable phenotype oc * Reprint requests to: Michael L. Netzloff, M.D., Department of Pediatrics (Genetics), Box J-296, JHM Health Center, University of Florida College of Medicine, Gainesville, FL curs infrequently in clinical medicine. However, certain conditions in which cancer may develop do have clinically definable characteristics, based on the presence of physical or biochemical markers. One example is the syndrome of multiple mucosal neuromas (MMN), in which patients may have associated medullary /79/ $01.20 Institute for Clinical Science, Inc.
2 M ULTIPLE MUCOSAL NEUROM AS SYNDROME 369 thyroid carcinom a (MTC), pheochrom ocytoma and a characteristic m orphologic appearance. This report will em phasize th e ty p ic a l d y sm o rp h ic fe a tu re s and gastrointestinal symptoms w hich aid in the diagnosis o fthe MMN syndrom e. This disease has been recently seen in a family and the present authors report the third instance of the MMN syndrom e p resent ing as neonatal intestinal obstruction.5,12 Case Report J. B. was hospitalized at the Shands Teaching Hospital, University of Florida, at two days of age because of intestinal obstruction. At surgery, a sten otic area of the descending colon was resected, sent for pathologic diagnosis and a colostomy was per formed. Histology of the tissue showed increased neural elem ents in the myenteric plexi. Rectal biop sies obtained during this surgery demonstrated plexiform ganglioneurofibrom atosis, and the diagn osis o f m u ltip le m ucosal neurom as was suggested. He was subsequently readmitted at the age of eight months for a colon biopsy, which con firmed the previous impression. At age 21 months, the patient and his family were examined by the Genetics Service. In figure 1 is shown J. B. s facial appearance which was similar to his mother s and characterized by patulous, thick lips, particularly the lower lip which also had several subcutaneous nodules. Several nodules were also located beneath the buccal mucosa. His face ap peared elongated and the palate was high-arched. His mother s facial appearance was similar to, but more striking than, that of the patient. In addition, she had m ultiple subcutaneous nodules on her tongue, particularly the anterior border (figure 2). Her face had a coarse appearance (figure 3) and she had the arachnodactyly and tall stature typifying the Marfan syndrome-like habitus. Her history was remarkable for removal o f bilateral pheochromocytomas and thyroid surgery for a tumor. The patient s siblings, ages 7Y2 and 10 years, were normal in appearance and had normal ratios of upper to lower body segments. J. B. was readmitted at age 2 Vi years for diarrhea and perineal excoriation. P ertinent laboratory studies on admission included normal electrolytes, BUN, creatinine, total protein, albumin, carotene, hematocrit, white blood cell count, triglycerides and stool cultures. Urinary excretion of vanilmandelic acid (VMA) was 3.0 mg per 24 hrs (normal 0.5 to 7.5) and homovanillic acid (HVA), 2.0 mg per 24 hrs (normal 0-15). Fasting serum calcitonin was 334 pg per ml (normal less than 400 pg per ml).11 A Pentagastin stimulation test, using 0.5 /xg per kg by IV push, resulted in serum calcitonin responses as fol lows: 5 min: 381; 10 min: 349; 15 min: 303; 30 min: 300 pg per ml (normal stimulated values less than 580 pg per ml; mean ± 2 S.D. o f 220 ± 360 pg per ml).11 The diarrhea subsequently cleared and the F IG U R E 1. P atient J. B. at age 20 m onths. Thickening, particularly o f lower lip, and elongated face are visible. family has refused either further testing or consider ation of thyroidectomy. Discussion In 1961, S ip p le 16 reported a 14-fold increase in the frequency of adrenal pheochrom ocytom a among patients w ith car cinom a of the thyroid. W illiam s19 in 1965 show ed that the thyroid carcinom a was of the m edullary type originating in the para follicular, calcitonin-producing cells (Ccells). S ubsequent reports2,4,10,14 estab lis h e d th a t th e m u ltip le e n d o c rin e neoplasia (MEN) syndromes are familial an d m ay sh o w a u to so m al d o m in a n t inheritance. In table I are shown the three major M EN syndrom es and their associated le sions. MEN-1, or W erm er s syndrom e, is com prised of lesions in the parathyroids, pancreatic islets, anterior pituitary and adrenal. In contrast, Sipple s syndrom e, or
3 370 N E T Z L O F F, CARNICA, RODGERS A ND FRIAS F i g u r e 2. Mother o f patient J. B. Numerous subcutaneous nodules are located on the anterior border of her tongue. F ig u r e 3. Facial features of patient s mother. Elongation and coarseness of the face are apparent. Note also the left lateral thyroidectomy scar. MEN-2 or 2a, is characterized by pheochrom ocytom a an d m ed u llary th y roid carcinom a, in a d d itio n to parath y ro id hyperplasia or adenoma. T he MMN syndrom e is a variant of M EN-2 and has also b een d esig n ated M EN -2b or M EN -3.3 It p resen ts w ith m ucosal neurom as over the eyelids, lips, tongue and buccal m ucosa, associated with a m edullary thyroid carcinom a and b ila te ra l a d re n a l pheochrom ocytom as. These patients may also have thickened corneal nerv es.15 T he Marfanoid habitus is reported to occur in 83 percent of pa tients with the MMN syndrom e and con sists of tall, asthenic appearance, abnor mal upper-to-low er body segm ent ratio an d p o o r m u sc le d e v e lo p m e n t, w ith arachnodactyly, jo in t laxity and hypo tonia.7 Additional anom alies may include k y p h o sc o lio sis, p e c tu s excavatum or carinatum, pes cavus, high arched palate and coarse facies features. O ther features of true Marfan syndrom e, such as aortic aneurysm and ectopia lentis, have not b een described in the MMN syndrom e.7 T he distinctive appearance aids in recog nition of the diagnosis, as do the gastro intestinal m anifestations resulting from ab n o rm alities of th e in te stin a l neural plexi. T he in te stin a l ganglioneurom as (p o ssib ly m o re a p p ro p ria te ly c a lle d neu ro g an g lio m as to in d ic a te th e p re dom inance of neural tissu e 7) are sim ilar to the mucosal neurom as found in other loca tions in the MMN syndrom e but are as sociated w ith functional abnorm alities. T hey m ay cause sym ptom s sim ulating H irschsprung s disease w ith megacolon and constipation or diarrhea.9,18 Sympto matic alim entary tract involvem ent was found to dom inate the clinical presenta tion in 12 of the 16 cases of MMN syn drome reported by C arney et al.5 In addition to the gastrointestinal m ani festations and the distinctive phenotype, w hich may aid in the diagnosis of MMN, the family history may also be helpful. The majority of cases appear to arise by spontaneous m utation, b ut the rem ainder
4 MULTIPLE MUCOSAL NEUROMAS SYNDROME 371 are inherited by an autosomal dominant m ode.4,10,14 The presence of the completely developed phenotype in the parent of a suspected patient is invaluable in establishing the diagnosis. T h e MMN syndrom e is usually discernible during the first few years of life because of the more common phenotypic expressions m entioned previously. Our patient developed a large bow el obstruction on the second day of life, similar tc both that in the neonate with MMN syndrome reported by Moyes and Alexan der,12 and that in case No. 8 in the series oi Carney et al.5 In addition, our patient was found to have a functionally aganglio n ic constricted segm ent of bow el identified at surgery. Various other gastrointestinal symptoms were present at or shortly after birth in 10 of the 16 cases reported by C arney e t al.5 B artlett2 reported a four-year-old male child who also had a p o sitiv e fam ily h istory and docum ented intestinal neurogangliomas but who presented with diarrhea. Other MMN patients reported w ith neurogangliomas have not p resented w ith obstruction in the neonatal period.12,18 Ours is only the third such case and the first new born to have d e m o n stra ted a gross anatom ic lesion of the colon. These findings indicate that the developm ent of intestinal neurogangliomas may frequently antedate the appearance of the other lesions associated w ith the MMN syndrome, including endocrine disease. The mucosal neuromas can also be present at birth, prior to d ev elo p m en t of pheochromocytomas or MTC.2 In newborns and older patients, the diffuse gastrointestinal neuroganglioma are always reported in association with mucosal neurom as;18 isolated intestinal ganglioneuromatosis, however, is not associated with MTC.7 T hese observations indicate that intestinal neurogangliomatosis may represent a variation of the mucosal neurom a component of the MMN syndrom e. Disturbances in gut motility, including diarrhea and constipation are common S y n d r o m e MEN-1 (Wermer's Syndrome) MEN-2* (Sipple's Syndrome) MEN-3+ (Multiple Mucosal Neuroma Syndrome) *MEN-2a TABLE I L esions in M u ltip le Endocrine N eoplasia (MEN) Syndromes L e s i o n s Parathyroid adenomas/hyperplasia Pancreatic islet cell tumors Pituitary tumors Adrenal cortical adenomas Thyroid adenomas Medullary thyroid carcinoma Pheochromocytoma Parathyroid adenomas/hyperplasia Medullary thyroid carcinoma Pheochromocytoma Mucosal neuromas Intestinal neurogangliomas +MEN-2b com plaints in older patients with intestinal neurogangliom as associated w ith MEN-2 syndromes.2,5,18 These functional abnorm alities may occur in the absence of radiographic evidence of diverticula and other bowel disease which are relatively common findings in patients with M TC.18 In the absence of dem onstrable pathology, the diarrhea in some patients has b e e n a ttrib u te d to n euro activ e com pounds such as prostaglandin and serotonin,7 secreted by the tumor. The pheochromocytomas associated with the MMN syndrom e may also cause diarrhea by p ro d u ctio n of e p in e p h rin e an d /o r norepinephrine,10 or vasoactive peptides.7 In contrast to older patients with MMN syndrom e, the gastrointestinal sym ptom a tology in the newborn usually consists of constipation and, occasionally, of obstruction, as in our patient. The relative infrequency of diarrhea in newborn patients with the MMN syndrome who do not yet have MTC suggests that the latter lesion is necessary for the developm ent of diarrhea in the MMN syndrom e. Chronic constipation and megacolon have been reported to predom inate in a case of neurogangliomatosis and pheochromocytoma without MTC.9 T he frequency of occurrence of in testinal neurogangliom atosis in the MMN
5 372 NETZLO FF, GARNICA, RODGERS AND FRIAS syndrom e has been previously u n d erestim ated. Gorlin et a l10 noted only one example in their analysis of 17 cases but suggest that this might be based on a limited assessm ent; recent estim ates have been as high as 100 percent.3,5 The MMN syndrome itself may be more common than presen tly a p p re c ia te d 4 and, also based on our observations, should properly be included in the differential diagnosis of H irschsprung s disease or intestinal obstruction, particularly in the new-born period. T he involvem ent of m ultiple endocrine and gastrointestinal sites in the MMN syndrom e may have a unifying explanation. The tumors involved all arise from cells w h ich P e a rs e 13 has term ed the APUD series (^m ines recursion juptake decarboxylase of L-aromatic amino acids). This term is used to m ean that these cells have the capacity to take up precursors of biogenic amines and convert them to amine neurotransm itters through enzymatic decarboxylation.1 These cells also synthesize and secrete low m olecular weight peptide hormones. The capacity of such cells to synthesize biogenic amines w ould thus seem to relate them to nervous tissue, and suggests that they are derived from neural crest tissue during embryogenesis. This has been shown to be the case for the C-cells from w hich MTC originates,13 and the m edulla of the adrenal gland, where pheochromocytomas originate.7 A defect in the developing neural crest could lead to abnormalities in both sites. The finding of neuromas and intestinal neurogangliomas in the MMN syndrom e is c o n siste n t w ith this hypothesis. The less frequent finding of parathyroid abnorm alities in MMN syndrom e than MEN-2a suggests that the p arathyroid lesion may be a reactive hyperplasia secondary to chronically high calcitonin levels and not the result of a primary defect in the embryologic neural crest.3 Since MTC is a neoplasm involving the C-cells of the thyroid gland, the tumor produces abnorm ally large quantities of calcitonin.7 In most patients with MTC, basal levels of calcitonin are sufficiently elevated to be diagnostic. In fact, the radioim m unoassay for calcitonin can establish the presence of MTC with such a high degree of accuracy that it is probably the most clinically reliable serologic test for the diagnosis of cancer.7 Unfortunately a significant percentage of patients with MTC have basal calcitonin levels which are indistinguishable from normal. Also, the levels in any one patient may be only interm ittently abnormal. Many cases of interm ittently high levels may represent early stages in the developm ent of the tumor or even C-cell hyperplasia, either of which one would like most to diagnose since they are am enable to surgical cure.7 Provocative testin g decreases the incidence of false negative diagnosis17 and takes advantage of the fact that the tumor is not autonomous. Secretion of calcitonin by C-cells in MTC is stim ulated by hypercalcem ia and other secretagogues. One of the first agents to be used for the stim ulation of calcitonin secretion was glucagon, but its effect was variable and unreliable. In addition, in patients with associated pheochromocytomas, glucagon can cause the release of catecholamines and precipitate an adrenergic crisis.7 Calcium infusions, particularly the recently described short term procedures, reliably stimulate calcitonin secretion, despite an elevation in the plasma calcium of less than 1 mg per dl. Side effects caused by hypercalcem ia, such as hypertension, nausea and vom iting, have been substantially reduced by the abbreviated procedures. Another widely used stimulus to calcitonin secretion in MTC patients is pentagastrin, 0.5 fig per kg IV, which appears to be as effective as calcium infusion as a calcitonin secretagogue. T he response to both agents appears dependent on the rapidity of infusion.7 E ither pentagastrin or calcium tests will define the presence of tum or in most instances, but false negatives occur w ith both procedures.7,11 Thus, w hen there is clinical suspicion o f M TC a n d one procedure
6 MULTIPLE MUCOSAL NEUROMAS SYNDROME 373 gives negative results, the alternative procedure should be used before excluding the diagnosis. Earlier estim ates10 of approximately 50 percent for the frequency of MTC in patients with MMN were undoubtedly too low and the true incidence is probably close to 100 percent.3,5 In addition, the developm ent of the thyroid carcinom a com ponent of the MMN syndrom e, usually reported to be betw een 18 and 25 years,10 has recently been reported as early as ten years.8 Moreover, the neonate recently reported by Moyes and Alexand e r 12 had a resectio n of a m edullary thyroid carcinoma at 15 months of age. M arkedly elevated calcitonin levels were m easured at the age of eight months in their patient. Early death in patients with the MMN is related to developm ent of MTC.4 Graze et al have dem onstrated the effectiveness of a calcitonin screening program for detecting fam ilial M TC in a prem etastatic _ stage.11 M easurem ent of calcitonin after calcium or pentagastrin provocation offers a reliable means of detecting this thyroid malignancy even during its hyperplastic, pre-m alignant stages. Serial m easurements of calcitonin following stimulation may be used to select those patients re quiring surgery, and early surgical intervention in those MMN patients with positive calcitonin screening tests will prevent the developm ent of fatal m edullary thyroid carcinom a.11 All patients with mucosal neurom as or intestinal neurogangliomas should have calcitonin levels m onitored at least yearly. Since an occasional MMN patient has no abnormalities of the face, oral m ucosa or skeletal system,5,6,7 fam ily m em bers who have a chance of inheriting the gene for this dominant disease should have the same evaluation despite th eir norm al appearance. References 1. At k in s, F. L., Be a v e n, M. A., and Ke is e r, H. R.: Dopa decarboxylase in medullary carcinom a o f the thyroid. New Eng. J. Med. 289: , Ba r t l e t t, R. C., M y a l l, R. W. T., Be a n, L. R., and M a n d l e st a m, P.: A neuropolyendocrine syndrome; mucosal neuromas; pheochromocytoma, and medullary thyroid carcinoma. Oral Surg. 31: , B a y l i n, S. B.: T he m ultiple en docrine neoplasia syndromes: implications for the study of inherited tumors. Sem. Oncol. 5:35-45, B r o w n, R. S., C o l l e, E., Ta sh jia n, A. H., Jr.: The syndrome of multiple mucosal neuromas and medullary thyroid carcinoma in childhood. J. Pediat. 86:77-83, C a r n e y, J. A., Go, V. L. W., Siz e m o r e, G. W., and H a y l e s, A. B.: Alimentary tract ganglioneuromatosis: a major component of the syndrome of multiple endocrine neoplasia, type 2b. New Eng. J. Med. 295: , C a r n e y, J. A., S i z e m o r e, G. W., and L o v e - STED T, S. A.: Mucosal ganglioneuromatosis, medullary thyroid carcinoma, and pheochromocytoma: multiple endocrine neoplasia, type 2b. Oral Surg , D e f t o s, L. J.: Calcitonin in clinical medicine. Advances Intern. Med. 23: , D e n t, C. E., F a c c in i, J., and H o d s m a n, A.: Medullary carcinoma of thyroid gland in a girl aged ten years. Arch. Dis. Child. 52 : , D u f f y, T. J., E r ic k s o n, E. C., Jo r d a n, G. L., and Be n n e t t, H. D.: Megacolon and bilateral pheochromocytoma. Amer. J. Gastroenterol. 38: , G o r l in, R. J. and Vic k e r s, R. A.: Multiple m ucosal neurom as, pheochrom ocytom a, medullary carcinoma of the thyroid and Marfanoid body b u ild w ith m uscle wasting: reexamination of a syndrome of neural crest malmigration. Birth Defects: Original Article Series VII(6):69-72, G r a z e, K., Sp il e r, I. J., T a sh jia n, A. H., Jr., e t AL.: Natural history o f familial medullary thyroid carcinoma: effect of a program for early diagnosis. New Eng. J. Med. 299: , M o y e s, C. D. and A l e x a n d e r, F. W.: Mucosal neuroma syndrome presenting in a neonate. Dev. Med. Child Neurol. 29: , P e a r s e, A. G. E. and P o l u k, J. M.: Cytochemical evidence for the neural crest origin of mammalian ultimobranchial C-cells. Histochem. 27:96-102, Sc h im k e, R. N.: Multiple endocrine adenomatosis syndromes. Advances Intern. Med. 2 1 : , S c h w e it z e r, N. M. J. and V a n D e r Po l, B. A. E.: Multiple mucosal neuroma (MMN) or multiple endocrine neoplasia (MEN) Type 3 syndrome. Doc. Ophthalmol. 44: , SlPPLE, J. H.: The association of pheochromocytoma with carcinoma of the thyroid gland. Amer. J. Med. 31: , S iz e m o r e, G. W. and Go, V. L. W.: Stim u lation tests for d iagnosis o f m edullary thyroid carcinom a. M ayo C lin ic Proc. 50:53-56, W h i t t l e, T. S., Jr. and G oodw in, M. N., Jr.: Intestinal ganglioneurom atosis w ith the mucosal neuroma medullary thyroid carcinoma pheochromocytoma syndrome. Amer. J. Gastroenterol. 65: , WILLIAMS, E. D.: A review of seventeen cases of carcinoma of the thyroid and pheochromocytoma. J. Clin. Path. 18: , 1965.
Calcitonin. 1
Calcitonin Medullary thyroid carcinoma (MTC) is characterized by a high concentration of serum calcitonin. Routine measurement of serum calcitonin concentration has been advocated for detection of MTC
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