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Marlinda Adham 1 , Antonius N. Kurniawan 2 , Arina Ika Muhtadi 1 , Averdi Roezin 1 , Bambang Hermani 1 , Soehartati Gondhowiardj

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Marlinda Adham 1 , Antonius N. Kurniawan 2 , Arina Ika Muhtadi 1 , Averdi Roezin 1 , Bambang Hermani 1 , Soehartati Gondhowiardj Chinese Journal of Cancer Original Article Marlinda Adham 1, Antonius N. Kurniawan2 , Arina Ika Muhtadi1 , Averdi Roezin 1, Bambang Hermani1 , Soehartati Gondhowiardjo 3, I Bing Tan4 and Jaap M. Middeldorp 5 Abstract Among all head and neck (H&N) cancers, nasopharyngeal carcinoma (NPC) represents a distinct entity regarding epidemiology, clinical presentation, biological markers, carcinogenic risk factors, and prognostic factors. NPC is endemic in certain regions of the world, especially in Southeast Asia, and has a poor prognosis. In Indonesia, the recorded mean prevalence is 6.2/100 000, with 13 000 yearly new NPC cases, but otherwise little is documented on NPC in Indonesia. Here, we report on a group of 1121 NPC patients diagnosed and treated at Dr. Cipto Mangunkusumo Hospital, Jakarta, Indonesia between 1996 and 2005. We studied NPC incidence among all H&N cancer cases (n =6000) observed in that period, focusing on age and gender distribution, the ethnic background of patients, and the disease etiology. We also analyzed most prevalent signs and symptoms and staging of NPC patients at first presentation. In this study population, NPC was the most frequent H&N cancer (28.4%), with a male鄄to鄄 female ratio of 2.4, and was endemic in the Javanese population. Interestingly, NPC appeared to affect patients at a relatively young age (20% juvenile cases) without a bimodal age distribution. Mostly, NPC initiated in the fossa of Rosenmuller and spreaded intracranially or locally as a mass in the head. Occasionally, NPC developed at the submucosal level spreading outside the anatomic limits of the nasopharynx. At presentation, NPC associated with hearing problems, serous otitis media, tinnitus, nasal obstruction, anosmia, bleeding, difficulty in swallowing and dysphonia, and even eye symptoms with diplopia and pain. The initial diagnosis is difficult to make because early signs and symptoms of NPC are not specific to the disease. Early鄄ag e Epstein鄄B arr virus (EBV) infection combined with frequent exposure to environmental carcinogenic co鄄fa ctors is suggested to cause NPC development. Undifferentiated NPC is the most frequent histological type and is closely associated with EBV. Expression of the EBV鄄en coded latent membrane protein 1(LMP1) oncogene in biopsy material was compared between NPC patients of < 30 years old and those of 30 years old, matched for sex and tumor stage. Higher LMP1 expression in 逸 patients of <30 years old was observed, which was related to more locoregional progressivity. Increased medical awareness of prevailing early stage signs and symptoms coupled to use of EBV鄄re lated diagnostic tumor markers may lead to down鄄sta ging and timely treatment to improve survival of patients with this aggressive disease. Key words Nasopharyngeal carcinoma, incidence, epidemiology, Indonesia 1Depa rtment of Otorhinolaryngology, 2De partment of Anatomy Pathology, 3Depa rtment of Radiotherapy, Faculty of Medicine, Nasopharyngeal carcinoma (NPC) is a rare University of Indonesia, Dr. Cipto Mangunkusumo Hospital, Jakarta, malignancy throughout most parts of the world, with a Indonesia; 4A ntoni van Leeuwenhoek Hospital, Netherlands Cancer prevalence usually less than 1/100 000 [1,2] . NPC is a highly 5 Institute, Department of Pathology, VU University Medical Center, prevalent malignant disease and a leading cause of Amsterdam, Netherlands. death in several regions in southern China, and recently Jaap M. Middeldorp, Department of Pathology, VU improved registry data indicate medium to high University Medical Center, De Boelelaan 1117, 1081 HV Amsterdam, The Netherlands. Tel: +31鄄2044 44052; Fax: +31鄄20 鄄444 2964; Email: j. prevalence in other countries in Southeast Asia as well. [email protected]. The Guangdong province in South China has the highest 10.5732/cjc.011.10328 prevalence in the world, with approximately 20 to 40 www.cjcsysu.com CACA Chinese Anti鄄Ca ncer Association 185 Marlinda Adham et al. Nasopharyngeal carcinoma in Indonesia cases per 100 000 inhabitants depending on the region [3­7] . syndrome (Duncan s Syndrome). In humans, EBV Earlier work showed that Cantonese boat people had infection initiates at 爷the oropharyngeal epithelium upon the highest incidence of NPC (54.7/100 野 000) [8] . The冶 data transmission in the saliva. During this infection, the EBV from Guangdong were recently paralleled by findings in virus infiltrates and transforms submucosal B native Bidayuh people of Serawak, Malaysia, who also lymphocytes that are important for viral latent persistence had a high incidence of NPC (23.1/100 000) [9] , and further dissemination of the infection to distal suggesting that improved diagnosis and registry may epithelial surfaces including the nasopharynx [4] . After reveal additional hot­spots of high NPC incidence. primary infection, EBV persists for life as a Besides southern 野China, high冶 incidence was also predominantly latent infection of B lymphocytes, with reported among Inuits and other native populations of the variable but persistent shedding in the saliva. Arctic region. EBV is the first human virus to be linked to Intermediate incidence rates of NPC are seen in South­ oncogenesis due to its close association with Burkitt east Asia, including Singapore (15/100 000), Malaysia lymphoma and subsequent linkage to the etiology of (9.7/100 000), Vietnam (7.5/100 000), Taiwan (7/100 000), other lymphoid and epithelial malignancies. In immun and the Philippines (6.4/100 000). This trend also applies osuppressed hosts, such as transplant recipients and 鄄 in Africa, including the eastern country Kenya (5.4/100 000) untreated human immunodeficiency virus (HIV)­infected and northern countries Algeria, Morocco, and Tunisia individuals, EBV is a major risk factor for the (5.1/100 000) [10] . Therefore, epidemiologically, NPC is an development of lymphoproliferative diseases, which may interesting cancer because of this defined geographic turn into malignant lymphomas if left untreated [20,21] . In and racial distribution, pointing to genetic, social, and immunocompetent individuals, the virus is associated environmental factors in the etiology of this tumor type. with classic Hodgkin lymphoma, Burkitt lymphoma, and The incidence of NPC in other countries is generally low, extranodal B and T/natural killer (NK) cell non­Hodgkin s and it is therefore considered a rare cancer in lymphomas, as well as a few gastric adenocarcinomas 爷 populations of the Americas, Japan, Korea, and Europe and most undifferentiated and poorly differentiated NPCs [1,11­14] . worldwide. Patients (in developing countries) exposed to NPC is a frequent cancer in Indonesia, rating as the chronic inflammation and infection have been reported to fourth most common tumor after cervical cancer, breast be more prone to develop EBV­driven malignancies [21] , a cancer, and skin cancer, and is the most common situation that might apply to Indonesia as well, but has malignancy in the head and neck. The disease is 100% not been analyzed in any detail yet. EBV is active in the related to Epstein­Barr virus (EBV) infection, especially malignant cells of all described tumor types, and each the most common undifferentiated type of NPC (WHO type of tumor has a distinct pattern of EBV gene type III) [14,15] . In Indonesia, which has an ethnically diverse expression. Individual EBV genes associated with the population of 225 million people, NPC is prevalent three main latency programs of EBV can contribute to among different native people (s) and presents a major the malignant phenotype, albeit in a different fashion in socioeconomic problem, with an overall incidence distinct tumor types [20,21] . EBV has been classified since estimated at 6.2/100 000 or about 12 000 new cases per 1997 as group 1 human carcinogen by the International year [16] . Unfortunately, many of these cases go unregistered Agency on Research on Cancer. Recently, the presence due to limited medical awareness as well as the lack of of latent EBV in tonsil epithelial cells was demonstrated [22] , hospital facilities and a nationwide cancer diagnostic and providing a basis for understanding the link between EBV registration system. Virtually all cases of NPC show and carcinogenesis. The data from that study support genetic positivity for EBV, with multiple viral genes being the model of dual epithelial­lymphoid tropism for the expressed in each tumor cell [8] . virus , indicating the possibility that healthy tonsil EBV was identified by Sir Epstein and colleagues in epithelium may play a role in transmission of the virus as 1964 in cells cultured from African Burkitt lymphoma part of the viral life cycle, and suggesting that EBV can tumor explants and the virus was subsequently found to play an initiating role in associated epithelial lesions like infect more than 90% of the world population though was NPC and oral hairy leukoplakia. Transformation of rarely considered pathogenic [17] . Primary infection usually epithelial cells into a malignant disease by EBV may occurs at childhood and is asymptomatic or presents as be enhanced by environmental co­carcinogens, and a mild inflammation or upper respiratory infection [18] . In premalignant dysplasia may progress rapidly into Indonesia, 100% of children at 5 years of age are cancer [8,13,14,21] . infected with EBV and carry latent virus for life [19] . NPC oncogenesis is not simply a consequence of Delayed primary infection may cause a mild self­limiting EBV infection alone. More than 95% of adults in all illness known as infectious
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