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Squamous Cell Carcinoma Arising in Recurrent CASE REPORT Squamous Cell Carcinoma Arising in Recurrent Respiratory Papillomatosis with Pulmonary Involvement: Emerging Common Pattern of Clinical Features and Human Papillomavirus Serotype Association James R. Cook, M.D., Ph.D., D. Ashley Hill, M.D., Peter A. Humphrey, M.D., Ph.D., John D. Pfeifer, M.D., Ph.D., Samir K. El-Mofty, D.M.D., Ph.D. Lauren V. Ackerman Laboratory of Surgical Pathology, Department of Pathology, Washington University School of Medicine, St. Louis, Missouri of vaginal delivery in the presence of genital lesions, Squamous papillomas of the lung are an uncom- and patients typically present with symptoms of mon feature of recurrent respiratory papillomato- hoarseness or respiratory obstruction in childhood sis, occurring in fewer than 1% of cases. We describe or adolescence. In the majority of cases, the papil- a 23-year-old patient with pulmonary papillomas lomas are confined to the larynx; only 5% of pa- who developed a fatal squamous cell carcinoma of tients exhibit more distal involvement of the tra- the lung. PCR-based human papillomavirus (HPV) chea, and involvement of lung parenchyma occurs typing showed the presence of HPV 11 DNA in both in fewer than 1% of cases (1, 2). benign papillomas and invasive carcinoma. A re- Pulmonary involvement by RRP is twice as fre- view of the literature reveals four reports of malig- quent in males than in females and is associated nant transformation of juvenile-onset recurrent re- with an aggressive clinical course. Most patients spiratory papillomatosis in which HPV typing was require numerous excisions, frequently require tra- performed. Similar clinical features are noted in all cheostomy, and ultimately die as a result of respi- of the reports; specifically, each case has arisen in a ratory insufficiency or infections (2). Malignant young adult man with a history of papillomatosis transformation of laryngeal or pulmonary lesions is since childhood. In each of the cases, HPV 11 was a very rare event in the absence of prior irradiation; identified in association with the squamous cell car- fewer than 20 cases are reported in the English cinoma. Although HPV 11 is uncommonly associ- literature (3–6). It remains unclear whether the risk ated with the development of invasive carcinoma at of malignant transformation is dependent on the other sites, these findings suggest that it is corre- HPV serotype involved. lated with malignant transformation in the setting We describe a patient with pulmonary involve- of juvenile-onset recurrent respiratory papilloma- ment by RRP who developed a squamous cell car- tosis. cinoma of the lung. Polymerase chain reaction (PCR) typing performed at postmortem examina- KEY WORDS: Human papillomavirus 11, Recurrent tion showed the presence of HPV 11 DNA in both respiratory papillomatosis, Squamous cell carcinoma. the papillomas and squamous cell carcinoma. This Mod Pathol 2000;13(8):914–918 is the fifth report of an association between HPV 11 and malignant transformation of pulmonary papil- Juvenile-onset recurrent respiratory papillomatosis lomas (3, 4, 6, 7). Together, these five cases suggest (RRP) is characterized by numerous squamous pap- a stereotypical clinical setting for the emergence of illomas of the respiratory tract secondary to infec- invasive carcinoma from RRP. tion with human papillomavirus (HPV) types 6 and 11 (1, 2). HPV is thought to be acquired at the time CASE REPORT Copyright © 2000 by The United States and Canadian Academy of The patient was a 23-year-old white man with a Pathology, Inc. VOL. 13, NO. 8, P. 914, 2000 Printed in the U.S.A. history of RRP, initially diagnosed at age 5. By age Date of acceptance: February 11, 2000. 10, he had developed laryngeal, tracheal, and pul- Address reprint requests to: James R. Cook, M.D., Ph.D., Division of Surgical Pathology, Box 8118, Barnes-Jewish Hospital, 660 South Euclid Avenue, St. monary papillomas. He underwent more than 100 Louis, MO 63110; e-mail: [email protected]; fax: 314-362-8950. surgical excisions and laser ablations, required 914 multiple tracheotomies for tracheal obstruction, and sequenced using the Taq DyeDeoxy terminator and was frequently treated for postobstructive cycle sequencing kit (Applied Biosystems Inc., Fos- pneumonia and pulmonary abscesses. He was also ter City, CA) and an automated fluorescent DNA treated with interferon-␣, acyclovir, indol-3- sequencer (Model 373A; Applied Biosystems Inc.). carbanol, and an adjunctive trial of measles vaccine DNA sequence analysis was facilitated by BLAST injection. Clinical response was noted only to ther- sequence similarity searches using the National apy with interferon-␣, which reduced the bulk of Center for Biotechnology Information database his papillomas and the frequency of required sur- (http://www.ncbi.nlm.nih.gov/BLAST/). gical interventions. During late adolescence and into young adulthood, the patient smoked approx- RESULTS imately one half to one pack of cigarettes per day Ͻ ( 10 pack-year history total). Autopsy Findings At age 22, the patient began to complain of Postmortem examination was limited to the weight loss and thoracic pain radiating to the scap- lungs, larynx, trachea, thyroid, and a portion of ula. Chest radiographs demonstrated an enlarging vertebral bone. Examination of the larynx and tra- right upper lobe mass, and a bronchial washing chea revealed numerous papillomas, ranging in di- showed invasive squamous cell carcinoma. He was ameter from less than 0.1 to 0.4 cm, extending from treated with radiotherapy for control of pain and the larynx to the level of the carina. Several of the local control of the tumor. Subsequent chest radio- papillomas showed mild to moderate dysplasia graphs demonstrated continuing enlargement of (Fig. 1A, B). The right and left mainstem bronchi did the mass, which seemed to compress the right main not contain papillomas. The lungs were firm and bronchus. He experienced progressive respiratory heavy (1450 g, combined weight). Both lungs were compromise and died approximately 1 year after involved by numerous cavitary papillomas, ranging the diagnosis of carcinoma. from 0.1 to 1.5 cm in diameter. The pulmonary papillomas consisted of squamous epithelium with MATERIALS AND METHODS underlying nests of squamous cells within alveolar spaces (Fig. 1C, D). A rim of compressed uninvolved DNA Extraction parenchyma in turn surrounded these areas. The ␮ Five, 10- sections of formalin-fixed, paraffin- squamous nests were distinguished from an inva- embedded tissue obtained at autopsy were depar- sive carcinoma by the presence of intact alveolar affinized using xylene and ethanol washes and were septa, low-grade cytology, a pushing border, and digested overnight at 65° C in digestion buffer (Tris the absence of desmoplasia. pH 7.5, 20 mM EDTA, 1% SDS) containing 200 The pleura of the right lung was thickened by ␮ ␮ g/ L proteinase K. Samples were boiled with fibrosis, ranging from 0.2 to 0.5 cm in thickness. A Chelex 100 resin for 20 min and centrifuged, the 4.5-cm firm, partially necrotic, well-differentiated aqueous phase was transferred to a new tube, and squamous cell carcinoma was present in the right DNA was quantitated by spectrophotometry. upper lobe that encircled but did not invade the right mainstem bronchus (Fig. 2). The carcinoma PCR Amplification PCR analysis was carried out using the GeneAmp kit (Perkin-Elmer, Foster City, CA) with HPV con- sensus primers as described by Manos et al. (8): MY09—CGTCCMARRGGAWACTGATC; MY11—GCM- CAGGGWCATAAYAATGG where R ϭ AϩG, W ϭ AϩT, M ϭ AϩC, and Y ϭ CϩT. As a control for intact ampli- fiable DNA, primers for the ␤-globin gene were also used in the same reaction: globin1—ACACAACTGTGTTCAC- TAGC; globin2—CAACTTCATCCACGTTCACC. Reac- tions were carried out in 50-␮L volumes with 0.5 ␮M primers and 2 mM MgCl2. The reaction parameters were as follows: initial denaturation at 95° C for 5 min; 35 cycles each at 95° C for 1 min, 50° C for 1 min, and 72° C for 1 min; final extension at 72° C for 5 min. FIGURE 1. Sections of the larynx and trachea showing numerous DNA Sequencing squamous papillomas with mild nuclear pleomorphism (A and B). The lung contained cavitary papillomas lined by squamous epithelium (C) PCR products were cloned into vector pCR2.1 with underlying nests of noninvasive squamous cells within intact using the TA cloning kit (Invitrogen, Carlsbad, CA) alveolar spaces (D). Carcinoma in Pulmonary Papillomatosis (J.R. Cook et al.) 915 FIGURE 3. Polymerase chain reaction analysis for the presence of human papillomavirus DNA (450 bp) and human ␤-globin (107 bp). Human papillomavirus DNA is detected in the invasive squamous cell carcinoma and laryngeal papillomas, but not in thyroid. ␤-globin was amplified from each tissue, as expected. Lane M, molecular weight markers; Lane 1, invasive squamous cell carcinoma; Lane 2, laryngeal papilloma; Lane 3, thyroid; Lane 4, water (omitted DNA template) control. DISCUSSION In this article, we describe a patient with RRP with pulmonary involvement who developed well- FIGURE 2. The right upper lobe contained a 4.5-cm invasive, well- differentiated squamous cell carcinoma of the lung differentiated squamous cell carcinoma (A) with marked nuclear approximately 17 years after the onset of papillo- pleomorphism (B). matosis. HPV 11 DNA was detected in both benign papillomas and squamous cell carcinoma. Numer- ous studies have examined the HPV serotypes as- consisted of irregular, invasive tongues of keratin- sociated with RRP and have identified HPV 6 and 11 izing squamous cells with moderate to severe cyto- as the causative agents both in cases limited to the logic atypia. In contrast to the pulmonary squa- larynx (9) and in cases with involvement of the lung mous papillomas, the carcinoma was associated (1, 10, 11). The frequency of individual HPV sero- with a marked desmoplastic reaction and showed types in juvenile-onset papillomas has been re- invasive destruction of surrounding alveolar paren- ported as 50 to 84% for HPV 6 and 25 to 37% for chyma.
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