The melanotic neuroectodermal tumor of infancy

Int. J. Oral Surg. 1981: 10: 432-446 (Key words: melanotic neuroectodermal tumor of tnfoncv: tumor, benign .. childhood neoplasms; neoplasm of ernbryoidal ussuev

The melanotic neuroectodermal tumor of infancy Report of two cases and review of the literature JAMES R. HUPP, RICHARD G. TOPAZIAN AND DAVID J. KRUTCHKOFF Department ofOral and M axtllofacial Surgery and Department ofOral Diagnosis, Oral Pathology Section, School of Dental Medicine, University of Connecticut Health Center, Farmington, Connecticut, USA

ABSTRACT - The melanotic neuroectodermal tumor of infancy (MNTI) is a rare childhood neoplasm with an alarming but classical clinical presentation. It appears as a rapidly enlarging mass in the jaws or skull of infants and unless MNTI isconsideredin the diITerential diagnosis, thelesioncan easily bemistaken for a malignant neoplasm. Although possessing an aggressive growth rate and radiographic appearance, the MNTI almost alwaysbehavesin a benign fashion and can be treated with local excision. However, recent reports of malignant behavior as well as of occasional recurrences make close follow-up important. Approximately 139 cases of the MNTI have been reviewed and tabulated with respect to ageat discovery, sex, tumor location, length offollow-up, and whether recurrence occurred. 2 additional cases. 1 of which was in the mandible, are presented along with theories of origin and recommended therapy.

(Received for publication 7 May, accepted 16 July 1981)

Few neoplasms of the head and neck have produced as much controversy with respect to origin as has the melanotic neuroectodermal tumor of infancy (MNTI). This is reflected in the variety of terms this lesion has engendered including, among others, retinal anlage tumor, melanotic (pigmented) ameloblastoma, melanoameloblastoma, benign melanotic tumor of the infantile jaw, pigmented congenital epulis, melanotic progonoma, congenital melanocarcinoma and melanotic epithelial odontomav-" .89,90,96,11,.123,126, The term, melanotic neuroectodermal tumor of infancy has been widely accepted recently as properly describing the lesion and thus will be used throughout this

report". The purpose is to summarize reported findings of this uncommon tumor, to describe the current knowledge regarding this lesion, and to report 2 additional cases, 1 ofwhich occurred in the mandible. Despite the uncertainty of origin, the MNTI is remarkably consistent in its clinical presentation, histopathology, and course following treatment. MNTI usually presents as a rapidly enlarging mass in the anterior maxilla of infants, but other sites have been reported. It most commonly appears between the ages of 3 weeks to 12 months, frequently interferes with feeding, and is without apparent sex predilection. Clinically the mass usually appears irregul-

0300-9785/81/060432-15$02.50/0 © 1981 Munksgaard, Copenhagen

MELANOTIC NEUROECTODERMAL TUMOR

arly pigmented in a patchwork of dark blues and blaek and may contain prem aturely erupted or displaced primary teeth. The tumor is of a rubbery consistency and may have an ulcerated sur fa ce. Invasion of cancellous bone with expansion of cortical plates may occur. The growth is non-tender, non-pulsatile and does not yield fluid on aspira tio n. There are several features wh ich give cause for concern. The swift growth and poorly demarcated radiographic appea rance suggest an aggressive malignancy rather than a process controllable hy more conservative means. Another potentially misleading feature is a common osteogenic reaction which exhibits a "sunray" radiographic pattern that may be mistaken for osteosarcoma. I n spite of disconcerting clinical and rad iographic features, MNTI is usually a benign process that is readily treatable by conservative excision ; nonetheless, recent reports of malignant beh avior of MNTI make close follow-up important'"-" .

Case reports Case I A 3-month old female was ad mitted to the University of Connecticut's John N. Demp sey Ho spital in January, 1978 with a ra pid ly grow ing, intra-oral

Fig. 1. 2-month old female (Case I) showing facial asym metry due to left maxill ary mass.

433

Fig. 2. Intraoral appearance of tumor exhibiting

pigmentation and displaced tooth.

maxillary mass causing left rnidfacial swelling . The ch ild had appeared normal at birth and no history of disease in the perinat al period was obtained . At the age 01'2 months a mass was first noted, Th e in fa nt was then seen by th e surgical service of another hospital , and thejaw lesion was biopsied and the specimen sent to Sloan Kettering Institute where the diagnosis of MNTI was ma de. The infant appeared well-developed but moderately uncomfortable. The left rnidface was deformed by the underlying lesion but the skin appeared norm al in color and consistency and could he moved freely over the mass ( Fig. I). Intraoral exam ination revealed a large mass a pproximatcly 3 x 4 ern in size centered over the left maxillary alveolar process extending from the can ine region to the Icft max illary tuberos ity (Fig. 2). The lesion exhibited a bluc-blaek pigmentation and a somewhat rubbery con sistency. A primary molar had erupted to the surface of the tumor, and there was a pronounced ulce ration of the opposing mandibular alveolar ridge. Superiorly, the left side of the palate and the alveolar process were expanded and the tumor was noted to extend into the area of the zygoma tic process although definite margins were not palpablc. 24 h urinary vanilmandelic acid (VMA) levels were within normal range . The rema inder of the exam inat ion an d laboratory studies were within norm al limits. Radiographic examination revealed a destructive, poorly dem arcat ed slightly radiopaque mass with a pattern reminiscent of the "sunray" appea rance associated with osteosarcoma (Fig. 3). Under general anesthesia with a throat pack in place, an incision was made intra-orally beginning on the alveolar ridge anterio r to th e lesion and extending laterally and posteriorly to the dist al of

434

HlJPP, TOPAZIAN AND KRUTCHKOFF the mucosa undermined and reapproxirnated over a petrolatum coated iodoform gauze pack. The tumor was not markedly vascular and blood loss was minimal. The post-operative course was excellent with pack removal in 2 days. There is no clinical or radiographic evidence of recurrence 2t years after surgery. No oro-antral or oro-nasal fistulae exist. The specimen measured 3.0 x 2.5 x 2.5 ern (Fig. 4) with a densely pigmented color upon cut section, and a partially ulcerated surface evident microscopically. Numerous nests of tightly packed immature cells, surrounded by a proliferative, fibrous stroma con-

Fig. 3. Radiograph of maxillary mass illustrating "sun-ray" appearance of bone that can easily be confused with the radiographic appearance of osteosarcoma.

tuberosity, The mucoperiosteum was reflected superiorly revealing a pigmented tumor mass. This was completely enucleated. The tumor extended into the maxillary sinus, to the medial wall, and approximated but did not involve the floor of the orbit. Palatally, it extended to the midline and supero-laterally involved the sinus wall. Arter initial enucleation, all hony margins were rongeured and currettcd until remaining pigmented and other soft tissues had been completely removed. Several tooth follicles were removed with the mass although attempts were made to avoid disturbing dental follicles which were not involved with the tumor. Homeostasis was achieved,

Fig. 4. Gross appearance of surgical specimen that measured 3 x 2.5 x 2.5 em.

Fig. 5. Representative area ofMNTI (Case I) showing the characteristic biphasic patlern of the tumor. Densely cellular nests of immature neuroectodermal cells containing little cytoplasm are surrounded by larger, more mature cells which contain variable amounts of melanin (hematoxylin and eosin, x 100).

Fig. 6. Higher magnification of representative field of MNTl. Within adjacent stroma are more differentiated cells, some of which contain intracytoplasmic melanin (hematoxylin and eosin, x 240).

MELANOTIC NEUROECTODERMAL TUMOR taining large, melanin-laden cells were found throughout the tumor mass. Nests of tumor were arranged in an alveolar pattern with central cells being exceptionally immature, basophilic, and with little cytoplasm (Figs. 5, 6, 7). Moderate mitotic activity was noted

Fig. 7. Another area reveals encroachment of the

tumor upon a developing primary tooth. Note the atypical dentinal matrix with numerous cellular inclusions (hematoxylin and eosin, x 100).

435

within the nests. Peripheral cells appeared to be undergoing a process of differentiation and enlargement due to increased cytoplasmic volume. The latter cells contained abundant melanin and appeared to proliferate into surrounding stroma assuming a cuboidal shape. Bone was seen which contained tumor within medullary spaces. Diagnosis was MNTI. Case 2 A 5-month old male was first seen in February, 1962 by one of the authors (R.G.T.) at the Christian Medical College Hospital in Vellore, India. A large swelling involving the right body of lite mandible was observed (Fig. 8). The swelling had an insidious onset at the age of 4 months and had progressively enlarged to such an extent that it began to interfere with breast feeding. The perinatal period had been normal. Examination revealed a healthy looking infant with an obvious mass occupying the entire right body of the mandible. It distorted the cheek and prevented mouth closure. The tumor was bluish pink in color, firm in consistency, and non-pulsatile. Numerous blood vessels coursed over the surface of the tumor and a tooth which was surrounded by unusually pale mucosa was situated on the crest of the mass. The mass measured approximately 4 em in diameter. The tumor was fixed to the mandible and the mucosa over the tumor was not freely mobile. The tongue was displaced to the left because of encroachment of the tumor upon the floor of the mouth. Radiographs revealed extensive involvement of the entire right side of the mandible with multiple radiolucent areas surrounded by bone in a "sunray" pattern. The clinical diagnosis was osteogenic sarcoma. Biopsy of the lesion revealed a microscopic picture consistent with MNTI. Treatment consisted of complete removal of the tumor via intra-oral ennucleation. The patient was lost to follow-up.

Discussion 5 principal theories regarding the origtn of MNTI have arisen from the 139 cases reported in the literature (Table 1). These may be described as (1) malignant transformation of odontogenic epithelium":":" t , l2o, (2) ameloblastoma variant",67,7l.••.•,.'6.)J', (3) origin from Fig. 8. 5-month old male (Case 2) showing large

mandibular mass.

Jacobson's vomeronasal organ'?", (4) origin from retinal anlage (progonoma)", and (5) origin from neuroectodermal rests":". Little, if'

Year of report

1918 1926 1935 1941

1947 1948 1949 1950 1950 1951 1951 1953 1953 1953 1953 1953 1954 1954 1955 1956 1956 1956

1957 1957

1958 1958

Author

Krompecher Mummery et al. Dudits et at. Soderberg et at.

Halpert et al. Wass DeAtaide Field Martin et al. Battle et al. Clarke et al. Notter et al. Shafer et al. MacDonald et at. Hunderwadel Aisenberg Kuhn Traube et at. Caldwell Vanek Bhat Tiecke et al.

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2 months 2 months 3 weeks 1 week 3 months 4 months 1 month 2 months I month 1 month 9 months 5 months I month 3 months I month 4 months 1 month birth 3 months 3 months 4 months 4 months 3 months 3 months 1 year 2 weeks 3 months 2 months 4 months 2 months 3 months 2 weeks 3 weeks 4 months

Age when tumor discovered*

Table 1. Documented cases of melanotic neuroectodermal tumor of infancy

maxilla maxilla maxilla maxilla maxilla maxilla mandible maxilla maxilla maxilla mandible ant. fontanel maxilla maxilla maxilla maxilla maxilla ant. fontanel maxilla maxilla maxilla maxilla mandible mandible maxilla maxilla maxilla maxilla maxilla maxilla maxilla maxilla maxilla shoulder

F F F F F F M F F M M M F M F M F F M M M M F F F M M F M F F M M

Location of tumor

Sex of child

3 years 2 years recurred 30 months post-op I year 3 years recurred soon post-op 3 months 8 years 3 years I year

-

recurred 9 months post-op recurred 10 months post-op 5 years I year

-

3 months 4 years 7 months 6 years 6 months 8 months 2 months died at 8 months untreated 5 months 7 years recurred soon post-op 14 months 9 months 5 years recurred 16 months post-op 9 years 10 years

Length of follow-up or when recurrence occurred

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1964 1964 1965 1965 1965

1965 1965 1965 1965

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Valetti et al. Eder et al. Henry et al. Mitchell et al. Miyake et al. Foote Mancini et al. Jones et al. Davis Medenis Porter et al. Tipman Kerr et al, Kilmer Leskien Reeyes et al. Panabokke et al. Godin

Kerr et al.

Schulenberg et al. Dah1back et al. Korlof et al. Pontius et al, Dodge

Misugi et al. Held Martensson et al. Fievez et af.

Perl Sato et al. Husted et al. Quinn Borello et al. Agawal et al.

5 months 2 weeks 6 months 2 months 2 months 6 weeks 6 months 1 month 3 months 4 months 7 months 5 months 2 months 5 months 2 months 1 month 2 weeks 3 months 5 months 3 months 2 months birth birth 2 weeks 3 months 2 months 3 months 2 months 5 months 4 months 3 months 9 months 3 months 1 month 6 months 3 months 1 month 5 months 3 months

F

F M

F

M F

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M M M F

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F M F M F M M F F F M M F F M M F F

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maxilla maxilla maxilla maxilla maxilla maxilla maxilla maxilla ant. fontanel maxilla maxilla maxilla mandible maxilla maxilla ant. fontanel mandible maxilla maxilla maxilla maxilla maxilla maxilla maxilla maxilla maxilla maxilla maxilla mediastinum maxilla maxilla maxilla maxilla maxilla mandible maxilla maxilla maxilla maxilla

-

recurred 1 month post-op

14 years 6 months 9 months

6 months recurred 4 months post-op 10 years

-

6 years 3 years 2 years recurred

-

recurred 2 years 8 years 18 months

-

30 months recurred 2 years

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2 years

recurred 4 months post-op

21 months 4 months 21 months 10 months recurred

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Baugh et al. Ross et al. Stokke Hayward et al. Costa Allen et al.

Smirne Vlachos et al. Wejroch-Kowalska Carlier et al. James et al. Best Anagnostopoulus Grave et al.

Gilmor et al.

Shivde et al. Dehner Nagathau et al. Elomaa et al. Heydenrych

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Table 1. Cont.

5 months 3 months 2 months 6 weeks 5 months

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2 months 5 months 2 months 8 months 1 month 1 month 8 months 6 months 6 months 6 weeks 6 weeks 5 months 3 months 6 weeks 2 months 6 months 3 months 2 months 6 months 3 months 3 months 10 months 5 weeks birth 4 months 5 months 11 months birth

Age when tumor discovered* maxilla maxilla maxilla maxilla maxilla maxilla maxilla ant. fontanel maxilla maxilla temporal bone maxilla maxilla maxilla maxilla maxilla maxilla ant. fontanel mandible maxilla maxilla maxilla maxilla maxilla ant. fontanel temporal bone maxilla occipital bone skull maxilla maxilla maxilla maxilla maxilla

Location of tumor

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Lopez Singh et al. Alipilenko et al. Kitano et al.

Lee et al. Nikai et al. Karma et al. Kukreja et al. Van Middlesworth De Pasculis et al. Zajtchuk et al. Dooling et al. Adeloye et al. Bhargava et al. Kasumova et al. Baughman et al. Dehner/Bleck Ramon et af. Gotcher et al. Cutler et al.

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4 months 7 months birth 3 months 6 months 6 weeks 5 months 3 months 4 months 3 months I month birth

2 months 2 months I month 2 months 5 months 2 months 2 months M F M M F M

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M F M M

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3 months birth 2 months 3 months 4 months 4 months 3 months 3 months 7 months 2 months 5 months 6 months

* Age when any sign of abnormality noted, whether by parent or doctor.

Cutler/Hupp Hupp et al.

1973 1974

Harilal et al. Ostrander et al.

maxilla maxilla maxilla maxilla maxilla maxilla maxilla temporal bone maxilla maxilla maxilla maxilla ant. fontanel maxilla maxilla oropharynx maxilla maxilla maxilla maxilla ant. fontanel ant. fontanel frontal bone ant. fontanel maxilla ant. fontanel mandible ant. fontanel maxilla maxilla maxilla maxilla mandible

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1 year I year recurred 3 months post-op 6 months

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2i years 2 years

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I year

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recurred 3 years 3 months died soon post-op 9 years 16 years

recurred 1 month post-op I year

440

HUPP. TOPAZIAN AND KRUTCHKOFF

with a MNTI. VMA levels returned to normal after excision of the tumor. This finding is highly suggestive of a neural crest origin since known tumors from this tissue (e.g, pheochromocytoma, ganglioneuroblastoma, neuroblastoma) commonly secrete norepinephrine-like hormones which are metabolized to VMA and subsequently excreted in the urine. The markedly elevated urinary VMA in patients with MNTI is strong circumstantial evidence for a neuroectodermal origin. Previous reports of MNTI have included cases in which the diagnosis is subject to question9 .28 .J5.39.4o.47.48.55. 73,82,.,,86,1"0114.124,13 7. If

any, evidence exists to support the first 3 theories ; however, the notion that MNTI may originate from neuroectoderm has considerable merit . The 4th and 5th theories are based on this view. HALPERT & PATZER " suggested that MNTI represented the prolifer at ion of retinal anlage since ciliary process-like structures including layers of pigmented cuboidal cells are found. This theory is weakened by the recognition that the lesion appears in extramaxillary sites where displaced retinal anlage would be unlikely to migrate during embryogenesis"; Also, during fetal development the retina is already well organized by the time the maxilla is just beginning to form". Finally, the absence of more differentiated retinal components tends to discredit this theory. BORELLO & GORLIN2 1 reported high urinary vanilmandelic acid (YMA) levels in a patient

one excludes these doubtful cases, there are still about 139 cases of MNTI which fulfill recognized diagnostic criteria for this lesion. MNTI is most frequent in the first 6 months of life with an age range extending from birth to I year (Fig. 9). The vast majority occur in the maxilla, with

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Age when t umor fi r st di scovered (i n months ) Fig. 9. Age when the melanotic neuroectodermal tumor of infancy was first discovered in 139 cases reported in

the literature. In 3 cases age of discovery not specified.

MELANOTIC NEUROECTODERMAL TUMOR Table 2. Location and sex of child in 139 cases of melanotic neuroectodermal tumor of infancy Skull Anterior fontanel Temporal bone Occipital bone Frontal bone Unspecified

13 (9%) 3 (2%) 1 I I

Jaws Maxilla Mandible Other Oropharynx Mediastinum Shoulder Sex Female Male Not able to identify from report

108 (78%) 10 (8%)

64 65 10

occasional cases in the mandible, anterior fontanel, calvaria, mediastinum and shoulder (Table 2). There is no predilection with respect to sex. The recurrence rate is 15% (Table 1). MNTI usually presents in a relatively consistent and predictable manner so diagnosis is usually not a problem for those familiar with the entity. The differential diagnosis should also include infectious processes and benign or malignant neoplasms of odontoblastic, neuroblastic or osteoblastic tissue. Malignant melanoma, lymphoma and (especially with respect to the age range and radiographic appearance) osteosarcoma must also be considered. The mere presence of melanin however, is in itself insufficient evidence for a diagnosis of MNTI since several other neoplasms including ameloblastoma can contain pigment: occasionally this causes such lesions to be misdiagnosed as examples ofMNTI. Unfortunately, errors such as these become perpetuated in the literature and give rise to misleading impressions regarding the incidence, age range, sites of origin and almost universal benign behavior of MNTI. In our 2 cases, the clinical presentation of a rapidly enlarging, pigmented mass of the jaw in

441

an infant was characteristic as were the radiographic features suggesting aggressive bony invasion and osteogenesis within the neoplasm. Finally, the histological findings of nests of immature cells with high nuclear/cytoplasmic ratios interspersed among larger, more mature cells containing melanin also coincide with accepted criteria for the diagnosis of MNTI. With respect to Case 1, relatively conservative treatment appears to have been successful at 2t years, since the patient healed without recurrence, even though it is likely that residual remnants of tumor were present at the margins following surgery. The characteristic success in treatment of MNTI following conservative excision may be due to a "debulking effect" allowing the body an opportunity to destroy the few remaining neoplastic cells as is seen in a malignant neuroectodermal tumor, the neuroblastoma'"-". Neuroblastomas, the most frequent solid neoplasms of children, represent the uncontrolled proliferation of fetal-like cells and have one of the highest rates of spontaneous regression seen in malignancies". The cells of MNTI are also fetal-like and residual neoplastic cells seem to spontaneously regress after debulking. The success of local excision may also represent removal of a group of stimulatory cells contained within the main tumor mass which the peripheral cellsrequire to survive'w. The theoretical possibilityis that, in the process of removing most of the tumor, the microenvironment is disrupted in such a way that the remaining tissue cannot survive. Although the MNTI displays a disturbing rapid growth potential and invasive radiographic appearance, it exhibits benign behavior in the vast majority of cases, permitting more conservative management than that which would otherwise be required for a malignant neoplasm. Some authors have advocated simple currettage of the involved bony areas along with excision of the soft tissue mass with little or no margin of healthy tissue. Because the marked pigmentation of the neoplasm allows visualiz-

442

HUPP, TOPAZIAN AND KRUTCHKOFF

ation of the margins, dissection usually proceeds with relative ease. Others, fearing the 15% recurrence rate or the 2% malignancy rate, proceed with more aggressive surgical treatment and include a 5 mm margin of clinically normal tissue along with the specimen. The need for aggressive management can be seriously questioned, however, since conservative local excision of recurrences is almost invariably curative.

9. 10.

1I.

12.

Radiotherapy has also been proposed and used in the treatment of MNTI due to the marked radiosensitivity of immature cells con-

13.

tained within the tumor. Although the MNTI is reduced in size after radiotherapy, surgery is

14.

still necessary to cure the patient. Also, the

15.

harmful effects of radiation on normal growth and development, particularly in infants, and the fact that surgery alone is relatively successful, would mitigate against radiation therapy for

MNTI in most cases.

16.

17.

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Address: Richard G. Topazian Department of Oral and Maxillofacial Surgery School of Dental Medicine University of Connecticut Health Center Farmington, Connecticut 06032 USA