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Published in: BMC Oral Health 1/2014

Open Access 01-12-2014 | Research article

Screening for oral potentially malignant disorders among areca (betel) nut chewers in Guam and Saipan

Authors: Yvette C Paulino, Eric L Hurwitz, Saman Warnakulasuriya, Robert R Gatewood, Kenneth D Pierson, Lynnette F Tenorio, Rachel Novotny, Neal A Palafox, Lynne R Wilkens, Grazyna Badowski

Published in: BMC Oral Health | Issue 1/2014

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Abstract

Background

The Mariana Islands, including Guam and Saipan, are home to many ethnic subpopulations of Micronesia. Oral cancer incidence rates vary among subpopulations, and areca (betel) nut chewing, a habit with carcinogenic risks, is common. Our objectives were to conduct a screening program to detect oral potentially malignant disorders (OPMD) in betel nut chewers, measure their betel nut chewing practices, and assess the prevalence of the oral human papillomavirus (HPV) infection in a subset of betel nut chewers in these islands.

Methods

A cross-section of 300 betel nut chewers ≥18 years old [in Guam (n = 137) and in Saipan (n = 163)] were recruited between January 2011-June 2012. We collected demographic, socioeconomic, and oral behavioural characteristics. Latent class analysis was used to identify chewing patterns from selected chewing behaviours. Following calibration of OPMD against an expert, a registered oral hygienist conducted oral examinations by house to house visits and referred positive cases to the study dentist for a second oral examination. Buccal smears were collected from a subset (n = 123) for HPV testing.

Results

Two classes of betel nut chewers were identified on 7 betel nut behaviours, smoking, and alcohol use; a key difference between the two Classes was the addition of ingredients to the betel quid among those in Class 2. When compared on other characteristics, Class 1 chewers were older, had been chewing for more years, and chewed fewer nuts per day although chewing episodes lasted longer than Class 2 chewers. More Class 1 chewers visited the dentist regularly than Class 2 chewers. Of the 300 participants, 46 (15.3%; 3.8% for Class 1 and 19.4% for Class 2) had OPMD and one (0.3%) was confirmed to have squamous cell carcinoma. The prevalence of oral HPV was 5.7% (7/123), although none were high-risk types.

Conclusions

We found two patterns of betel nut chewing behaviour; Class 2 had a higher frequency of OPMD. Additional epidemiologic research is needed to examine the relationship between pattern of chewing behaviours and oral cancer incidence. Based on risk stratification, oral screening in Guam and Saipan can be targeted to Class 2 chewers.
Literature
1.
go back to reference Gupta PC, Warnakulasuriya S: Global epidemiology of betel nut usage. Addict Biol. 2002, 7: 77-83. 10.1080/13556210020091437.CrossRefPubMed Gupta PC, Warnakulasuriya S: Global epidemiology of betel nut usage. Addict Biol. 2002, 7: 77-83. 10.1080/13556210020091437.CrossRefPubMed
2.
go back to reference International Agency for Research on Cancer: Betel-Quid and Areca-nut Chewing and Some Areca-nut-Derived Nitrosamines. 2004, Lyon, France: IARC Press, [IRAC Monogr Eval Carcinog Risks Hum, vol 85] International Agency for Research on Cancer: Betel-Quid and Areca-nut Chewing and Some Areca-nut-Derived Nitrosamines. 2004, Lyon, France: IARC Press, [IRAC Monogr Eval Carcinog Risks Hum, vol 85]
3.
go back to reference International Agency for Research on Cancer: Tobacco Habits other than Smoking; Betel - Quid and Areca-Nut Chewing; and some Related Nitrosamines. 1998, Lyon, France: IRAC Press, [IRAC Monogr Eval Carcinog Risks Hum, vol 37] International Agency for Research on Cancer: Tobacco Habits other than Smoking; Betel - Quid and Areca-Nut Chewing; and some Related Nitrosamines. 1998, Lyon, France: IRAC Press, [IRAC Monogr Eval Carcinog Risks Hum, vol 37]
4.
go back to reference Warnakulasuriya S, Johnson NW, van der Waal I: Nomenclature and classification of potentially malignant disorders of the oral mucosa. J Oral Pathol Med. 2007, 36: 575-580. 10.1111/j.1600-0714.2007.00582.x.CrossRefPubMed Warnakulasuriya S, Johnson NW, van der Waal I: Nomenclature and classification of potentially malignant disorders of the oral mucosa. J Oral Pathol Med. 2007, 36: 575-580. 10.1111/j.1600-0714.2007.00582.x.CrossRefPubMed
5.
go back to reference Warnakulasuriya S: Oral precancer: terminology, diagnosis, and prognosis. The Inside Summit on Oral Cancer Discovery and Management. 2007, 3 (Suppl 2): 1-6. Warnakulasuriya S: Oral precancer: terminology, diagnosis, and prognosis. The Inside Summit on Oral Cancer Discovery and Management. 2007, 3 (Suppl 2): 1-6.
6.
go back to reference Paulino YC: Describing and measuring variability of Areca catechu (betel nut) chewing in Micronesian populations in Guam. 2010, Ann Harbor: UMI Dissertation Publishing Paulino YC: Describing and measuring variability of Areca catechu (betel nut) chewing in Micronesian populations in Guam. 2010, Ann Harbor: UMI Dissertation Publishing
7.
go back to reference Paulino YC, Novotny R, Miller MJ, Murphy SP: Areca (betel) nut chewing practices in Micronesian Populations. Hawaii Journal of Public Health. 2011, 3: 19-29.PubMedPubMedCentral Paulino YC, Novotny R, Miller MJ, Murphy SP: Areca (betel) nut chewing practices in Micronesian Populations. Hawaii Journal of Public Health. 2011, 3: 19-29.PubMedPubMedCentral
8.
go back to reference Katz AR, Palafox NA, Johnson DB, Yamada S, Ou AC, Minami JS: Cancer epidemiology in the freely associated U.S. Pacific Islands jurisdictions: challenges and methodologic issues. Pac Health Dialog. 2004, 11: 84-87.PubMed Katz AR, Palafox NA, Johnson DB, Yamada S, Ou AC, Minami JS: Cancer epidemiology in the freely associated U.S. Pacific Islands jurisdictions: challenges and methodologic issues. Pac Health Dialog. 2004, 11: 84-87.PubMed
9.
go back to reference Haddock RL: Oral cancer incidence disparity among ethnic groups on Guam. Pac Health Dialog. 2005, 12: 153-154.PubMed Haddock RL: Oral cancer incidence disparity among ethnic groups on Guam. Pac Health Dialog. 2005, 12: 153-154.PubMed
10.
go back to reference Haddock R, Hoffman JH, Williams WR: Betel nut chewing on Guam. Fiji Medical Journal. 1981, 9: 139-149. Haddock R, Hoffman JH, Williams WR: Betel nut chewing on Guam. Fiji Medical Journal. 1981, 9: 139-149.
11.
go back to reference Pacific Islands Nutrition, No.49: Betel Chewing and Cancer. 2001, Noumea, New Caledonia: Secretariat of the Pacific Community Pacific Islands Nutrition, No.49: Betel Chewing and Cancer. 2001, Noumea, New Caledonia: Secretariat of the Pacific Community
12.
go back to reference Government of the Republic of Palau: RPPL no. 8–27 An Act to Adopt Measures Consistent With the Objective of the World Health Organization’s Framework Convention on Tobacco Control (FCTC), to Which the Republic is a Party, to Protect Present and Future Generations Against the Devastating Health, Social, Environmental and Economic Consequences of Tobacco Consumption and Exposure to Tobacco Smoke; to Amend, Repeal and Replace Sections of Chapter l 0 of Title ll of the Palau National Code and for Other Related Purposes. 2011, Palau: 8th Olbiil Era Kelulau Government of the Republic of Palau: RPPL no. 8–27 An Act to Adopt Measures Consistent With the Objective of the World Health Organization’s Framework Convention on Tobacco Control (FCTC), to Which the Republic is a Party, to Protect Present and Future Generations Against the Devastating Health, Social, Environmental and Economic Consequences of Tobacco Consumption and Exposure to Tobacco Smoke; to Amend, Repeal and Replace Sections of Chapter l 0 of Title ll of the Palau National Code and for Other Related Purposes. 2011, Palau: 8th Olbiil Era Kelulau
13.
go back to reference Oakley E, Demaine L, Warnakulasuriya S: Areca (betel) nut chewing habit among high-school children in the Commonwealth of the Northern Mariana Islands (Micronesia). In Bull World Health Organ. 2005, 83: 656-660. Oakley E, Demaine L, Warnakulasuriya S: Areca (betel) nut chewing habit among high-school children in the Commonwealth of the Northern Mariana Islands (Micronesia). In Bull World Health Organ. 2005, 83: 656-660.
14.
go back to reference Novotny R, Coleman P, Tenorio L, Davison N, Camacho T, Ramirez V, Vijayadeva V, Untalan P, Tudela MD: Breastfeeding is associated with lower body mass index among children of the Commonwealth of the Northern Mariana Islands. J Am Diet Assoc. 2007, 107: 1743-1746. 10.1016/j.jada.2007.07.018.CrossRefPubMed Novotny R, Coleman P, Tenorio L, Davison N, Camacho T, Ramirez V, Vijayadeva V, Untalan P, Tudela MD: Breastfeeding is associated with lower body mass index among children of the Commonwealth of the Northern Mariana Islands. J Am Diet Assoc. 2007, 107: 1743-1746. 10.1016/j.jada.2007.07.018.CrossRefPubMed
15.
go back to reference Paulino YC, Patricia C, Davison NH, Lee SK, Camacho TB, Tenorio LF, Murphy SP, Novotny R: Nutritional characteristics and body mass index of children in the Commonwealth of the Northern Mariana Islands. J Am Diet Assoc. 2008, 108: 2100-2104. 10.1016/j.jada.2008.09.014.CrossRefPubMed Paulino YC, Patricia C, Davison NH, Lee SK, Camacho TB, Tenorio LF, Murphy SP, Novotny R: Nutritional characteristics and body mass index of children in the Commonwealth of the Northern Mariana Islands. J Am Diet Assoc. 2008, 108: 2100-2104. 10.1016/j.jada.2008.09.014.CrossRefPubMed
17.
go back to reference Paulino YC, Novotny R, Katz AR, Wilkens LR, Hurwitz EL: Development and Validation of an Areca (Betel) nut Usage Measurement Tool for Micronesia [Abstract]. Proceedings of the 6th American Association for Cancer Research Conference on the Science of Cancer Health Disparities in Racial/Ethnic Minorities and the Medically Underserved; 2013 Dec 6–9; Atlanta, GA. 2013, Philadelphia (PA): AACR, 169-Abstract nr B15 Paulino YC, Novotny R, Katz AR, Wilkens LR, Hurwitz EL: Development and Validation of an Areca (Betel) nut Usage Measurement Tool for Micronesia [Abstract]. Proceedings of the 6th American Association for Cancer Research Conference on the Science of Cancer Health Disparities in Racial/Ethnic Minorities and the Medically Underserved; 2013 Dec 6–9; Atlanta, GA. 2013, Philadelphia (PA): AACR, 169-Abstract nr B15
18.
go back to reference Landis JR, Koch GG: The measurement of observer agreement for categorical data. Biometrics. 1977, 33: 159-174. 10.2307/2529310.CrossRefPubMed Landis JR, Koch GG: The measurement of observer agreement for categorical data. Biometrics. 1977, 33: 159-174. 10.2307/2529310.CrossRefPubMed
19.
go back to reference Warnakulasuriya S: Screening for Oral Cancer and Precancer. University of Guam Presentation. 2010, Guam Warnakulasuriya S: Screening for Oral Cancer and Precancer. University of Guam Presentation. 2010, Guam
20.
go back to reference Hernandez BY, McDuffie K, Zhu X, Wilkens LR, Killeen J, Kessel B, Wakabayashi MT, Bertram CC, Easa D, Ning L, Boyd J, Sunoo C, Kamemoto L, Goodman MT: Anal human papillomavirus infection in women and its relationship with cervical infection. In Cancer Epidemiol Biomarkers Prev. 2005, 14: 2550-2556. 10.1158/1055-9965.EPI-05-0460.CrossRef Hernandez BY, McDuffie K, Zhu X, Wilkens LR, Killeen J, Kessel B, Wakabayashi MT, Bertram CC, Easa D, Ning L, Boyd J, Sunoo C, Kamemoto L, Goodman MT: Anal human papillomavirus infection in women and its relationship with cervical infection. In Cancer Epidemiol Biomarkers Prev. 2005, 14: 2550-2556. 10.1158/1055-9965.EPI-05-0460.CrossRef
21.
go back to reference Gravitt P, Peyton CL, Alessi TQ, Wheeler CM, Coutlee F, Hildesheim A, Schiffman MH, Scott DR, Apple RJ: Improved amplification of genital human papillomaviruses. J Clin Microbiol. 2000, 38: 357-361.PubMedPubMedCentral Gravitt P, Peyton CL, Alessi TQ, Wheeler CM, Coutlee F, Hildesheim A, Schiffman MH, Scott DR, Apple RJ: Improved amplification of genital human papillomaviruses. J Clin Microbiol. 2000, 38: 357-361.PubMedPubMedCentral
22.
go back to reference Gravitt PE, Peyton CL, Apple RJ, Wheeler CM: Genotyping of 27 human papillomavirus types by using L1 consensus PCR products by single hybridization, reverse line blot detection method. J Clin Microbiol. 1998, 36: 3020-3027.PubMedPubMedCentral Gravitt PE, Peyton CL, Apple RJ, Wheeler CM: Genotyping of 27 human papillomavirus types by using L1 consensus PCR products by single hybridization, reverse line blot detection method. J Clin Microbiol. 1998, 36: 3020-3027.PubMedPubMedCentral
23.
go back to reference McCutcheon AL: Latent Class Analysis. 1987, Newbury Park: Sage PublicationsCrossRef McCutcheon AL: Latent Class Analysis. 1987, Newbury Park: Sage PublicationsCrossRef
24.
go back to reference Muthen B: Latent Variable Mixture Modeling. New Developments and Techniques in Structural Equation Modeling. Edited by: Marcoulides GA, Schumacker RE. 2001, New Jersey: Lawrence Erlbaum Associates, 1-33. Muthen B: Latent Variable Mixture Modeling. New Developments and Techniques in Structural Equation Modeling. Edited by: Marcoulides GA, Schumacker RE. 2001, New Jersey: Lawrence Erlbaum Associates, 1-33.
25.
go back to reference Chung CH, Yang YH, Wang TY, Shieh TY, Warnakulasuriya S: Oral precancerous disorders associated with areca quid chewing, smoking, and alcohol drinking in Southern Taiwan. J Oral Pathol Med. 2005, 34 (8): 460-466. 10.1111/j.1600-0714.2005.00332.x.CrossRefPubMed Chung CH, Yang YH, Wang TY, Shieh TY, Warnakulasuriya S: Oral precancerous disorders associated with areca quid chewing, smoking, and alcohol drinking in Southern Taiwan. J Oral Pathol Med. 2005, 34 (8): 460-466. 10.1111/j.1600-0714.2005.00332.x.CrossRefPubMed
26.
go back to reference Lee C-H, Ko AM, Warnakulasuriya S, Yin BL, Sunarjo , Zain RB, Ibrahim SO, Liu ZW, Li WH, Zhang SS, Kuntoro , Utomo B, Rajapakse PS, Warusavithana SA, Razak IA, Abdullah N, Shrestha P, Kwan AL, Shieh TY, KO YC, Chen MK: Intercountry prevalences and practices of betel-quid use in south, southeast and eastern Asia regions and associated oral preneoplastic disorders: an international collaborative study by Asian betel-quid consortium of south andeast Asia. Int J Cancer. 2011, 129 (7): 1741-1751. 10.1002/ijc.25809.CrossRefPubMed Lee C-H, Ko AM, Warnakulasuriya S, Yin BL, Sunarjo , Zain RB, Ibrahim SO, Liu ZW, Li WH, Zhang SS, Kuntoro , Utomo B, Rajapakse PS, Warusavithana SA, Razak IA, Abdullah N, Shrestha P, Kwan AL, Shieh TY, KO YC, Chen MK: Intercountry prevalences and practices of betel-quid use in south, southeast and eastern Asia regions and associated oral preneoplastic disorders: an international collaborative study by Asian betel-quid consortium of south andeast Asia. Int J Cancer. 2011, 129 (7): 1741-1751. 10.1002/ijc.25809.CrossRefPubMed
27.
go back to reference Scheifele C, Reichart PA, Dietrich T: Low prevalence of oral leukoplakia in a representative sample of the US. population. Oral Oncol. 2003, 39 (6): 619-2. 10.1016/S1368-8375(03)00050-2.CrossRefPubMed Scheifele C, Reichart PA, Dietrich T: Low prevalence of oral leukoplakia in a representative sample of the US. population. Oral Oncol. 2003, 39 (6): 619-2. 10.1016/S1368-8375(03)00050-2.CrossRefPubMed
28.
go back to reference Lin W-J, Jiang R-S, Wu S-H, Chen F-J, Liu S-A: Smoking, alcohol, and betel quid and OralCancer: a prospective cohort study. In J Oncol. 2011, 2011: 525976-doi:10.1155/2011/525976CrossRef Lin W-J, Jiang R-S, Wu S-H, Chen F-J, Liu S-A: Smoking, alcohol, and betel quid and OralCancer: a prospective cohort study. In J Oncol. 2011, 2011: 525976-doi:10.1155/2011/525976CrossRef
30.
go back to reference Subramanian S, Sankaranarayanan R, Bapat B, Somanathan T, Thomas G, Mathew B, Vinoda J, Ramadas K: Cost-effectiveness of oral cancer screening: results from a cluster randomized controlled trial in India. Bull World Health Organ. 2009, 87 (3): 200-206. 10.2471/BLT.08.053231.CrossRefPubMedPubMedCentral Subramanian S, Sankaranarayanan R, Bapat B, Somanathan T, Thomas G, Mathew B, Vinoda J, Ramadas K: Cost-effectiveness of oral cancer screening: results from a cluster randomized controlled trial in India. Bull World Health Organ. 2009, 87 (3): 200-206. 10.2471/BLT.08.053231.CrossRefPubMedPubMedCentral
31.
go back to reference Dedhia RC, Smith KJ, Johnson JT, Roberts M: The cost-effectiveness of community-based screening for oral cancer in high-risk males in the united states: a Markov decision analysis approach. Laryngoscope. 2011, 121 (5): 952-960. 10.1002/lary.21412.CrossRefPubMedPubMedCentral Dedhia RC, Smith KJ, Johnson JT, Roberts M: The cost-effectiveness of community-based screening for oral cancer in high-risk males in the united states: a Markov decision analysis approach. Laryngoscope. 2011, 121 (5): 952-960. 10.1002/lary.21412.CrossRefPubMedPubMedCentral
32.
go back to reference Nunn H, Lalli A, Fortune F, Croucher R: Oral cancer screening in the bangladeshi community of tower hamlets: a social model. Br J Cancer. 2009, 101 (Suppl 2): S68-S72.CrossRefPubMedPubMedCentral Nunn H, Lalli A, Fortune F, Croucher R: Oral cancer screening in the bangladeshi community of tower hamlets: a social model. Br J Cancer. 2009, 101 (Suppl 2): S68-S72.CrossRefPubMedPubMedCentral
33.
go back to reference Sankaranarayanan R, Ramadas K, Thomas G, Muwonge R, Thara S, Mathew B, Rajan B, Trivandrum Oral Cancer Screening Study Group: Effect of screening on oral cancer mortality in Kerala, India: a cluster-randomised controlled trial. Lancet. 2005, 365 (9475): 1927-1933. 10.1016/S0140-6736(05)66658-5.CrossRefPubMed Sankaranarayanan R, Ramadas K, Thomas G, Muwonge R, Thara S, Mathew B, Rajan B, Trivandrum Oral Cancer Screening Study Group: Effect of screening on oral cancer mortality in Kerala, India: a cluster-randomised controlled trial. Lancet. 2005, 365 (9475): 1927-1933. 10.1016/S0140-6736(05)66658-5.CrossRefPubMed
34.
go back to reference Warnakulasuriya KA, Ekanayake AN, Sivayoham S, Sivayoham S, Stjernswärd J, Pindborg JJ, Sobin LH, Perera KS: Utilization of primary health care workers for early detection of oral cancer and precancer cases in Sri Lanka. Bull World Health Organ. 1984, 62 (2): 243-250.PubMedPubMedCentral Warnakulasuriya KA, Ekanayake AN, Sivayoham S, Sivayoham S, Stjernswärd J, Pindborg JJ, Sobin LH, Perera KS: Utilization of primary health care workers for early detection of oral cancer and precancer cases in Sri Lanka. Bull World Health Organ. 1984, 62 (2): 243-250.PubMedPubMedCentral
35.
go back to reference Warnakulasuriya S, Ekanayake A, Stjernsward J, Pindborg JJ, Sivayoham S: Compliance following referral in the early detection of oral cancer and precancer in Sri Lanka. Community Dent Oral Epidemiol. 1988, 6: 326-329.CrossRef Warnakulasuriya S, Ekanayake A, Stjernsward J, Pindborg JJ, Sivayoham S: Compliance following referral in the early detection of oral cancer and precancer in Sri Lanka. Community Dent Oral Epidemiol. 1988, 6: 326-329.CrossRef
36.
go back to reference Syrjänen S, Lodi G, von Bültzingslöwen I, Aliko A, Arduino P, Campisi G, Challacombe S, Ficarra G, Flaitz C, Zhou MH, Maeda H, Miller C, Jontell M: Human papillomaviruses in oral carcinoma and oral potentially malignant disorders: a systematic review. Oral Dis. 2011, 17 (Suppl 1): 58-72.CrossRefPubMed Syrjänen S, Lodi G, von Bültzingslöwen I, Aliko A, Arduino P, Campisi G, Challacombe S, Ficarra G, Flaitz C, Zhou MH, Maeda H, Miller C, Jontell M: Human papillomaviruses in oral carcinoma and oral potentially malignant disorders: a systematic review. Oral Dis. 2011, 17 (Suppl 1): 58-72.CrossRefPubMed
38.
go back to reference Gillison ML, Broutian T, Pickard RK, Tong ZY, Xiao W, Kahle L, Graubard BI, Chaturvedi AK: Prevalence of oral HPV in the United States, 2009–2010. J Amer Medl Assoc. 2012, 307 (7): 693-703. 10.1001/jama.2012.101.CrossRef Gillison ML, Broutian T, Pickard RK, Tong ZY, Xiao W, Kahle L, Graubard BI, Chaturvedi AK: Prevalence of oral HPV in the United States, 2009–2010. J Amer Medl Assoc. 2012, 307 (7): 693-703. 10.1001/jama.2012.101.CrossRef
39.
go back to reference Centers for Disease Control and Prevention: Sexually Transmitted Disease Surveillance 2011. 2012, Atlanta: U.S. Department of Health and Human Services Centers for Disease Control and Prevention: Sexually Transmitted Disease Surveillance 2011. 2012, Atlanta: U.S. Department of Health and Human Services
40.
go back to reference Guam Comprehensive Cancer Control Coalition: Guam Cancer Facts and Figures 2003–2007 (Revised February 2011). 2011, Guam: Guam Comprehensive Cancer Control Coalition Guam Comprehensive Cancer Control Coalition: Guam Cancer Facts and Figures 2003–2007 (Revised February 2011). 2011, Guam: Guam Comprehensive Cancer Control Coalition
45.
go back to reference International Agency for Research on Cancer: Human Papillomaviruses. 2007, Lyon, France: IARC Press, [IARC Monogr Eval Carcinog Risks Hum, vol 90] International Agency for Research on Cancer: Human Papillomaviruses. 2007, Lyon, France: IARC Press, [IARC Monogr Eval Carcinog Risks Hum, vol 90]
46.
go back to reference Kerr AR: Life saving oral cancer screening. N Y State Dent J. 2000, 66: 26-30.PubMed Kerr AR: Life saving oral cancer screening. N Y State Dent J. 2000, 66: 26-30.PubMed
Metadata
Title
Screening for oral potentially malignant disorders among areca (betel) nut chewers in Guam and Saipan
Authors
Yvette C Paulino
Eric L Hurwitz
Saman Warnakulasuriya
Robert R Gatewood
Kenneth D Pierson
Lynnette F Tenorio
Rachel Novotny
Neal A Palafox
Lynne R Wilkens
Grazyna Badowski
Publication date
01-12-2014
Publisher
BioMed Central
Published in
BMC Oral Health / Issue 1/2014
Electronic ISSN: 1472-6831
DOI
https://doi.org/10.1186/1472-6831-14-151

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