- Email: [email protected]
Primary Oral Malignancy Imitating Peri-Implantitis
1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56
CASE REPORT
Primary Oral Malignancy Imitating Peri-Implantitis Vadim Raiser,* Immad Abu-El Naaj,y Benjamin Shlomi,z Dan M. Fliss,x and Ilana Kaplank
Q10
Q2
Purpose:
To describe new cases of primary malignancy arising around dental implants.
Materials and Methods:
Three patients presented with asymptomatic lesions around longstanding dental implants that resembled peri-implantitis. One case was primary large B-cell lymphoma and the remaining cases were primary squamous cell carcinoma in patients with oral lichen planus. The literature was reviewed for cases mimicking peri-implantitis.
Results:
Of 42 implant-associated malignancies reported from 2000 through 2014, 85.7% were squamous cell carcinoma (69% primary and 9.4% metastatic). Most patients presented with pre-existing risk factors for oral cancer. Lymphoma was not associated with dental implants.
Q4
Conclusions: Primary and metastatic malignancies can occur in peri-implant mucosa, often with clinical and radiographic features resembling peri-implantitis. Clinicians should have a high index of suspicion for changes in peri-implant mucosa in patients with existing risk factors; however, rare cases such as lymphoma might present outside this risk population. Histopathologic analysis should be included in the management of selected peri-implant lesions to avoid delayed diagnosis of malignancy. Ó 2016 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg -:1-8, 2016
Peri-implantitis (PI) is a common long-term complication dental implantation. It is recognized that a large proportion of dental implants will develop PI over time, involving the surrounding mucosa and alveolar bone. Characteristics of PI include swelling, erythema, and often suppuration. Bone loss and pocket formation are typical.1 The etiology is multifactorial and not fully understood, with bacterial factors, surgical factors, implant surface characteristics, prosthetic design, and genetic predisposition suggested as contributory etiologic factors.2 There are no universal protocols for treatment, and peri-implant tissue is usually removed during treatment and not routinely submitted for histopathologic examination. There is only sparse information in the literature on the microscopic findings of PI.
Q3
A study of 117 biopsy samples from PI cases reported that, rather than simple inflammatory changes, close to half the cases presented with potentially aggressive lesions, such as pyogenic granuloma, giant cell granuloma, and Actinomyces-related inflammation.3 These entities exhibited clinical and radiographic characteristics that mimicked PI did not respond to conventional treatment modalities for PI (debridement, improved hygiene, antiseptic or antibiotic therapy, and various treatments for the implant surface); these require further investigation, including histopathologic evaluation. Rarely, primary or metastatic peri-implant malignancies closely resembling PI also have been associated with dental implants. The objectives of the present study were to describe 3 new cases of primary malignancy of the peri-implant
*Senior, Oral and Maxillofacial Surgery Unit, Tel-Aviv Sourasky
kProfessor, Institute of Pathology, Tel-Aviv Sourasky Medical
Medical Center, Tel-Aviv, Israel. yDepartment Head, Department of Oral and Maxillofacial Surgery,
Center, Tel-Aviv; Goldschleger School of Dental Medicine; Sackler School of Medicine, Tel-Aviv University, Tel-Aviv, Israel.
The Baruch Padeh Medical Center, Poriya, Israel.
Address correspondence and reprint requests to Prof Kaplan:
zDepartment Head, Unit of Oral and Maxillofacial Surgery, Tel-
Institute of Pathology, Tel-Aviv Sourasky Medical Center, 5 Daphna
Aviv Sourasky Medical Center; Sackler School of Medicine, Tel-Aviv
Street, Tel-Aviv, Israel; e-mail: [email protected]
University, Tel-Aviv, Israel.
Received January 17 2016
xProfessor and Division Head, Division of Otolaryngology and
Accepted February 11 2016
Head and Neck Surgery, Tel-Aviv Sourasky Medical Center; Sackler
Ó 2016 American Association of Oral and Maxillofacial Surgeons
School of Medicine, Tel-Aviv University, Tel-Aviv, Israel.
0278-2391/16/00177-4 http://dx.doi.org/10.1016/j.joms.2016.02.008
1 CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112
print & web 4C=FPO
PRIMARY MALIGNANCY IMITATING PERI-IMPLANTITIS
FIGURE 1. A, Well-circumscribed gingival mass in the left anterior maxilla, with minute focal surface ulcerations diagnosed as large B-cell Q8 lymphoma. B, Complete resolution after treatment. Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
Q5
mucosa and bone, review the literature, and discuss the implications resulting from clinical overlap with conventional PI. This report was written in accordance with the ethical requirements (Israeli and GCP-ICH standards) of clinical trials.
Report of Cases CASE 1 Q6
A 72-year-old man with longstanding implantsupported PFM restoration and poor oral hygiene presented with a firm erythematous gingival overgrowth in the left maxillary canine area. He noticed it several months previously but did not seek dental or medical advice because it was asymptomatic. He presented for examination in the oral and maxillofacial surgery clinic
in a major hospital when bleeding while brushing his teeth became a problem. In addition to the slightly ulcerated gingival mass, pocket formation and radiographic bone loss were documented. The clinical impression was PI, giant cell granuloma, or pyogenic granuloma (Fig 1). Biopsy examination of the lesion yielded a surprising diagnosis of large B-cell lymphoma. Thorough workup showed that no other organ was affected; thus, the diagnosis of primary peri-implant large B-cell lymphoma was established. The patient successfully completed the hemato-oncologic treatment protocol, the lesion completely regressed, and he has been free of disease for 36 months. CASE 2
A 55-year-old woman with a medical history of systemic lupus erythematosus and oral lichen planus
print & web 4C=FPO
113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168
2
FIGURE 2. A, Gingival overgrowth with a yellowish-white surface around left mandibular implants diagnosed as squamous cell carcinoma. (Fig 2 continued on next page.) Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
Q1
169 170 171 172 173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224
3
RAISER ET AL
225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280
FIGURE 2 (cont’d). B, Radiograph displays substantial vertical peri-implant bone loss. Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
(OLP) had a longstanding implant-supported complete mandibular PFM restoration. She presented at the oral and maxillofacial dental department (where she was being followed) with an asymptomatic, white, thick gingival overgrowth with pocket formation and substantial bone loss. Because OLP is a potentially malignant condition, a biopsy examination was performed and the diagnosis was welldifferentiated squamous cell carcinoma (SCC). No other organs were affected, and after mandibulectomy and node dissection, the patient has been free of disease for 8 years (Fig 2). CASE 3
A 70-year-old woman with a 7-year history of OLP presented with an irregular erythematous nonulcerated mass on the buccal and lingual sides of an implant-supported PFM restoration in the posterior right mandible (Fig 3). Some horizontal bone loss was noted on the panoramic radiograph. Biopsy examination resulted in a diagnosis of SCC. At surgery, the lesion was found to involve the retromolar trigon, the floor of the mouth, and mandible, without lymph node involvement. After mandibulectomy with node
dissection and radiation therapy, the patient has been free of disease for 3 years.
Literature Analysis A literature search of PubMed and Google Scholar from 2000 through 2014 retrieved 42 cases of oral malignancy involving dental implants4-25 (Table 1). Before 2000, only 4 cases were described,26,27 but the number of such cases in the literature has increased sharply since then (Fig 4). The patients were typically older adults (mean age, 68 yr; female predominance, 1:1.5). Most cases (92.8%) involved the mandible and the remaining cases (7.2%) occurred in the maxilla. The most prevalent type of malignancy reported around dental implants was SCC (85.7%); the second in frequency (9.5%) was metastasis from primary breast and lung tumors. The remaining malignancy types reported were 1 case each of osteosarcoma and plasmacytoma (2.4%). Lymphoma was not associated with dental implants. Primary large B-cell lymphoma is extremely rare in the gingiva, with only 13 such cases ever reported.28
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336
PRIMARY MALIGNANCY IMITATING PERI-IMPLANTITIS
print & web 4C=FPO
337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392
4
FIGURE 3. A, Granular and erythematous tissue surrounding left posterior mandibular implants diagnosed as squamous cell carcinoma. The red-and-white lesion on the buccal mucosa is related to the patient’s history of oral lichen planus. (Fig 3 continued on next page.) Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
Peri-implant malignancies usually were primary tumors (69%). The remaining were recurrent or second primary tumors in patients with previous oral malignancy (21.4%) and metastasis from nonoral distant tumors (9.5%). The literature search showed that 45.3% of cases occurred in a population with recognized risk factors for oral cancer; potentially malignant conditions were erythroplakia, leukoplakia, OLP, and proliferative verrucous leukoplakia (PVL). In addition, 47.6% of cases had a previous oral malignancy and 19% had a history of a nonoral malignancy that could metastasize to the jaws or gingiva. Thus, the vast majority, but not all, cases occurred in a population in which a high level of suspicion for oral cancer should be maintained. Additional life style factors such as previous or current smoking were reported in 35.7% of cases and alcohol use in 19%, with coexisting risk factors in several cases. However, detailed quantitative information on the history of smoking or alcohol use (or abuse) was not included in most cases reviewed.
Discussion The incidence of peri-implant malignancy seems to be extremely low, with only 46 cases ever reported.4-27 Bhatavadekar21 calculated the theoretical standardized incidence ratio (SIR) to be 0.00017 per million per year. This is a very low figure, for example, compared with cancer related to background radiation, for
which the calculated SIR was 20 per million per year.21 Data from a study by Moergel et al24 provide Q7 information on the actual incidence: in a cohort of 10,986 implants placed during a 15-year period, 15 cases of peri-implant SCC were recorded, 9 (3%) in patients with previous oral SCC and 6 (0.056%) for the remaining 10,689 implants. The incidence in patients with a previous oral malignancy is considerably higher (although low compared with the expected recurrence of oral SCC) and seems to be very low outside this risk group. From analysis of peri-implant malignancy in the literature, including the new cases reported in the present study, the affected individuals tend to be elderly adults (mean age, 68 yr). The gender distribution shows a clear 1:1.5 female predominance as opposed to the characteristic male predominance of oral cancer in general. There also is a clear predilection for the mandible. Most patients in the literature had at least 1 recognized predisposing factor for oral cancer: erythroplakia, OLP, PVL and previous oral malignancy. This was true for cases 2 and 3 in the present series who had a history of OLP. Most malignancies in conjunction with dental implants in the literature have been SCC, and most of these were primary tumors, which is in agreement with the distribution of cancer types in oral cancer in general. Cases 2 and 3 have these typical features for peri-implant malignancy. In contrast, case 1, who was diagnosed with a primary large B-cell lymphoma, had no known risk
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448
5
RAISER ET AL
449 450 451 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 504
FIGURE 3 (cont’d). B, Radiograph shows only moderate vertical bone loss around the implants. Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
factors at the time he was diagnosed. The oral cavity accounts for only 1% of extranodal non-Hodgkin lymphoma (NHL), and these are very rarely located in the gingiva. Only 13 gingival cases of NHL have ever been reported,28 and none in the context of dental implants. The existing data suggest that the incidence of periimplant malignancy is very low, and there is no epidemiologic evidence that dental implants pose any specific risk for cancer. However, attention should focus on the fact that the clinical presentation in most cases reported and the new cases described in the present report bears many similarities to PI, such as gingival overgrowth, bone loss, and a tendency to bleed. This clinical presentation also has been described primarily for longstanding implants, which also are the circumstances in which PI is most frequent. Malignancy masquerading as PI carries the risk of being ignored or treated as PI without histopathologic analysis, leading to delayed diagnosis. In the case of malignancy, delays in diagnosis have dire implications for patient survival.
In the 3 present cases, the examination was carried out by oral and maxillofacial surgeons in a large hospital facility, where biopsy services are readily available. However, most patients with dental-supported restorations are usually cared for by dentists in the community who would have little experience with oral cancer or biopsy procedures or immediate access to pathology services. It is impossible to differentiate simple PI clinically from its benign and malignant mimickers without proper histopathologic analysis. The purpose of this report is to raise awareness that lesions that imitate PI might represent other aggressive lesions, malignant and benign but aggressive, such as giant cell granuloma.3 Especially high suspicion should be raised for lesions that do not respond to conventional treatment modalities for PI, lesions in patients with medical histories positive for potentially malignant conditions, and patients with previous oral and nonoral cancer. These cases should be referred immediately for biopsy examination and histopathologic analysis.
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
505 506 507 508 509 510 511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537 538 539 540 541 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558 559 560
561 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 615 616
6
PRIMARY MALIGNANCY IMITATING PERI-IMPLANTITIS
Table 1. SUMMARY OF CASES PUBLISHED FROM 2000 THROUGH 2014
Age (yr)/ Gender
Source
Location
Risk Factors
Clinical Presentation
Diagnosis
82/M
Mandible
VC 3, leukoplakia, previous smoking
Mimicked PI
SCC
69/M
Mandible
Previous SCC
Rec SCC
69/F
Mandible
Rec SCC
F
Mandible
Previous VC, leukoplakia, SCC OLP, smoking
Mimicked PI, pathologic fracture Mimicked PI
Mimicked PI
Primary SCC
M
Mandible
Mimicked PI
Rec SCC
Verhoeven et al, 20078 Dib et al, 200710
67/F
Mandible
Mimicked PI
Metastasis from lung
NA/F
Mandible
Swelling and pain
Abu El-Naaj et al, 20077
70/F
Mandible
Metastasis from breast cancer SCC
72/M 75/F
Mandible Mandible
Schache et al, 200815
77/M
Mandible
Breast adenocarcinoma Thyroid and breast cancer OLP, smoking Solitary plasmacytoma spine None
Gallego et al, 200812 Kwok et al, 200813
81/F
Mandible
OLP, previous SCC
71/M
Mandible
67/F
Mandible
62/M 38/F
Mandible Maxilla
Previous smoking, alcohol Previous tongue SCC (2), breast cancer, previous smoking, alcohol Alcohol and tobacco None
76/M
Mandible
None
70/F
Mandible
None
62/F
Mandible
77/F
Mandible
Previous SCC, smoking Previous SCC
71/M
Mandible
Previous SCC
62/F 69/F
Mandible Mandible, floor of mouth Mandible
Previous SCC Previous SCC
Block and Scheufler, 20014 Shaw et al, 20045
Czerninski et al, 20066
Poggio, 20079
McGuff et al, 200814 Eguia del Valle et al, 200811 Gallego et al, 200916 Gulati et al, 200917 De Ceulaer et al, 201018
Meijer et al, 201019 Orhan et al, 201120
69/F
Previous colon and oral cancer Lung cancer
Breast cancer
Exophytic white lesion, bone loss Ulcerated mass Peri-implant mass, bleeding, bone loss Peri-implant mass, discomfort, bony erosion Peri-implant mass
SCC Solitary plasmacytoma SCC
Rec SCC
‘‘Inflammatory process’’ Exophytic mass, ‘‘granulation tissue’’
SCC
Nonhealing ulcer Mass
SCC Osteosarcoma
White exophytic mass, ulcer, bone loss Ulcer and pain related to cantilever Mimicked PI
SCC
Rec SCC
Mimicked PI
Rec SCC
Mucosal nonulcerated swelling Mimicked PI Exophytic mass
Rec SCC
Numb chin syndrome, with mixed RO-RL lesion
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
Second primary SCC
SCC
Rec SCC SCC
Metastatic breast cancer
617 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640 641 642 643 644 645 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 672
7
RAISER ET AL
Table 1. Cont’d
Age (yr)/ Gender
Source
Location
Risk Factors
Pfammatter et al, 201223
55/F
Mandible
Pancreatic cancer, NSCLC
Bhatavadekar, 201221 Marini et al, 201325 Moergel et al, 201424
54/M
Maxilla
None
55/F
Mandible
15 cases (8 F, 7 M)
Mandible, 14; maxilla, 1
Summary
17 M, 25 F
Maxilla, 3; mandible, 39
OLP, long-term steroids Previous SCC, 9; leukoplakia, 10; erythroplakia, 2; OLP, 3 Previous SCC, 20; potentially malignant lesions, 19; nonoral cancer, 8; tobacco and alcohol, 5; no risk factors, 5
Clinical Presentation
Diagnosis
Initial presentation mimicked PI, later developed numbness Swelling and ulcer
Metastasis from NSCLC
SCC
Mimicked PI
SCC
Exophytic mass, 10; nonhealing ulcer, 4; mimicked PI, 1 Mass or swelling, 16; mimicked PI, 16; ulcer or ulcerated mass, 8; numb chin syndrome, 1
SCC
Primary SCC, 27; Rec and second SCC, 9; metastasis, 4; plasmacytoma, 1; osteosarcoma, 1
Abbreviations: F, female; M, male; NA, ---; NSCLC, ---; OLP, oral lichen planus; PI, peri-implantitis; Rec, recurrent; RL, Q9 ---; RO, ---; SCC, squamous cell carcinoma; VC, verrucous carcinoma. Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
Cases of Perimplant Malignancy, 1995 - 2014 25
20
No.Cases
15
10
print & web 4C=FPO
673 674 675 676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 707 708 709 710 711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728
5
0 1995-1999
2000-2004
2005-2009
2010-2014
FIGURE 4. A sharp increase in the number of reported cases of peri-implant malignancy. Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
729 730 731 732 733 734 735 736 737 738 739 740 741 742 743 744 745 746 747 748 749 750 751 752 753 754 755 756 757 758 759 760 761 762 763 764 765 766 767 768 769 770 771 772 773 774 775 776 777 778 779 780 781 782 783 784
785 786 787 788 789 790 791 792 793 794 795 796 797 798 799 800 801 802 803 804 805 806 807 808 809 810 811 812 813 814 815 816 817 818 819 820 821 822 823 824
8
PRIMARY MALIGNANCY IMITATING PERI-IMPLANTITIS
References 1. Albrektsson T, Isidor F: Consensus report of session IV, in Lang NP, Charring T (eds): Proceedings of the First European Workshop on Periodontology. London, UK, Quintessence, 1994, pp 365–369 2. Berglundh T, Zitzmann NU, Donati M: Are peri-implantitis lesions different from periodontitis lesions? J Clin Periodontol 38(suppl 11):188, 2011 3. Kaplan I, Hirshberg A, Shlomi B, et al: The importance of histopathological diagnosis in the management of lesions presenting as peri-implantitis. Clin Implant Dent Relat Res 17:e126, 2015 4. Block MS, Scheufler E: Squamous cell carcinoma appearing as peri-implant bone loss: A case report. J Oral Maxillofac Surg 59:1349, 2001 5. Shaw R, Sutton D, Brown J, et al: Further malignancy in field change adjacent to osseointegrated implants. Int J Oral Maxillofac Surg 33:353, 2004 6. Czerninski R, Kaplan I, Almoznino G, et al: Oral squamous cell carcinoma around dental implants. Quintessence Int 37:707, 2006 7. Abu El-Naaj I, Trost O, Tagger-Green N, et al: Peri-implantitis or squamous cell carcinoma? Rev Stomatol Chir Maxillofac 108: 458, 2007 8. Verhoeven JW, Cune MS, van Es RJ: An unusual case of implant failure. Int J Prosthodont 20:51, 2007 9. Poggio CE: Plasmacytoma of the mandible with a dental implant failure. Clin Oral Implants Res 18:54, 2007 10. Dib LL, Soares AL, Sandoval RL, et al: Breast metastasis around dental implants: A case report. Clin Implant Dent Relat Res 9: 112, 2007 11. Eguia del Valle A, Martınez-Conde Llamosas R, L opez Vicente J, et al: Primary oral squamous cell carcinoma arising around dental osseointegrated implants mimicking peri-implantitis. Med Oral Patol Oral Cir Bucal 13:E489, 2008 12. Gallego L, Junquera L, Baladr on J, et al: Oral squamous cell carcinoma associated with symphyseal dental implants: An unusual case report. J Am Dent Assoc 139:1061, 2008 13. Kwok J, Eyeson J, Thompson I, et al: Dental implants and squamous cell carcinoma in the at risk patient-report of three cases. Br Dent J 205:543, 2008 14. McGuff HS, Heim-Hall J, Holsinger FC, et al: Maxillary osteosarcoma associated with a dental implant: Report of a case and review of the literature regarding implant-related sarcomas. J Am Dent Assoc 139:1052, 2008
15. Schache A, Thavaraj S, Kalavrezos N: Osseointegrated implants: A potential route of entry for squamous cell carcinoma of the mandible. Br J Oral Maxillofac Surg 46:397, 2008 16. Gallego L, Junquera L, Llorente S: Oral carcinoma associated with implant-supported overdenture trauma: A case report. Dent Traumatol 25:e3, 2009 17. Gulati A, Puthussery FJ, Downie IP, et al: Squamous cell carcinoma presenting as peri-implantitis: A case report. Ann R Coll Surg Engl 91:W8, 2009 18. De Ceulaer J, Magremanne M, van Veen A, et al: Squamous cell carcinoma recurrence around dental implants. J Oral Maxillofac Surg 68:2507, 2010 19. Meijer GJ, Dieleman FJ, Berge SJ, et al: Removal of an oral squamous cell carcinoma including parts of osseointegrated implants in the marginal mandibulectomy: A case report. Oral Maxillofac Surg 14:253, 2010 20. Orhan K, Bayndr H, Aksoy S, et al: Numb chin syndrome as a manifestation of possible breast cancer metastasis around dental implants. J Craniofac Surg 22:942, 2011 21. Bhatavadekar NB: SCC in association with dental implants: An assessment of previously hypothesized carcinogenic mechanisms and a case report. J Oral Implantol 38:792, 2012 22. Javed F, Al-Askar M, Qayyum F, et al: Oral squamous cell carcinoma arising around osseointegrated dental implants. Implant Dent 21:280, 2012 23. Pfammatter C, Lindenm€ uller IH, Lugli A, et al: Metastases and primary tumors around dental implants: A literature review and case report of peri-implant pulmonary metastasis. Quintessence Int 43:563, 2012 24. Moergel M, Karbach J, Kunkel M, et al: Oral squamous cell carcinoma in the vicinity of dental implants. Clin Oral Investig 18: 277, 2014 25. Marini E, Spink MJ, Messina AM: Peri-implant primary squamous cell carcinoma: A case report with 5 years’ follow-up. J Oral Maxillofac Surg 71:322, 2013 26. Clapp C, Wheeler JC, Martof AB, et al: Oral squamous cell carcinoma in association with dental osseointegrated implants. An unusual occurrence. Arch Otolaryngol Head Neck Surg 122: 1402, 1996 27. Moxley JE, Stoelinga PJW, Blijdorp PA: Squamous cell carcinoma associated with a mandibular staple implant. J Oral Maxillofac Surg 55:1020, 1997 28. Sugimoto K-J, Shimada A, Sakurai H, et al: Primary gingival diffuse large B-cell lymphoma: A case report and a review of the literature. Int J Clin Exp Pathol 7:418, 2014
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
825 826 827 828 829 830 831 832 833 834 835 836 837 838 839 840 841 842 843 844 845 846 847 848 849 850 851 852 853 854 855 856 857 858 859 860 861 862 863 864
CASE REPORT
Primary Oral Malignancy Imitating Peri-Implantitis Vadim Raiser,* Immad Abu-El Naaj,y Benjamin Shlomi,z Dan M. Fliss,x and Ilana Kaplank
Q10
Q2
Purpose:
To describe new cases of primary malignancy arising around dental implants.
Materials and Methods:
Three patients presented with asymptomatic lesions around longstanding dental implants that resembled peri-implantitis. One case was primary large B-cell lymphoma and the remaining cases were primary squamous cell carcinoma in patients with oral lichen planus. The literature was reviewed for cases mimicking peri-implantitis.
Results:
Of 42 implant-associated malignancies reported from 2000 through 2014, 85.7% were squamous cell carcinoma (69% primary and 9.4% metastatic). Most patients presented with pre-existing risk factors for oral cancer. Lymphoma was not associated with dental implants.
Q4
Conclusions: Primary and metastatic malignancies can occur in peri-implant mucosa, often with clinical and radiographic features resembling peri-implantitis. Clinicians should have a high index of suspicion for changes in peri-implant mucosa in patients with existing risk factors; however, rare cases such as lymphoma might present outside this risk population. Histopathologic analysis should be included in the management of selected peri-implant lesions to avoid delayed diagnosis of malignancy. Ó 2016 American Association of Oral and Maxillofacial Surgeons J Oral Maxillofac Surg -:1-8, 2016
Peri-implantitis (PI) is a common long-term complication dental implantation. It is recognized that a large proportion of dental implants will develop PI over time, involving the surrounding mucosa and alveolar bone. Characteristics of PI include swelling, erythema, and often suppuration. Bone loss and pocket formation are typical.1 The etiology is multifactorial and not fully understood, with bacterial factors, surgical factors, implant surface characteristics, prosthetic design, and genetic predisposition suggested as contributory etiologic factors.2 There are no universal protocols for treatment, and peri-implant tissue is usually removed during treatment and not routinely submitted for histopathologic examination. There is only sparse information in the literature on the microscopic findings of PI.
Q3
A study of 117 biopsy samples from PI cases reported that, rather than simple inflammatory changes, close to half the cases presented with potentially aggressive lesions, such as pyogenic granuloma, giant cell granuloma, and Actinomyces-related inflammation.3 These entities exhibited clinical and radiographic characteristics that mimicked PI did not respond to conventional treatment modalities for PI (debridement, improved hygiene, antiseptic or antibiotic therapy, and various treatments for the implant surface); these require further investigation, including histopathologic evaluation. Rarely, primary or metastatic peri-implant malignancies closely resembling PI also have been associated with dental implants. The objectives of the present study were to describe 3 new cases of primary malignancy of the peri-implant
*Senior, Oral and Maxillofacial Surgery Unit, Tel-Aviv Sourasky
kProfessor, Institute of Pathology, Tel-Aviv Sourasky Medical
Medical Center, Tel-Aviv, Israel. yDepartment Head, Department of Oral and Maxillofacial Surgery,
Center, Tel-Aviv; Goldschleger School of Dental Medicine; Sackler School of Medicine, Tel-Aviv University, Tel-Aviv, Israel.
The Baruch Padeh Medical Center, Poriya, Israel.
Address correspondence and reprint requests to Prof Kaplan:
zDepartment Head, Unit of Oral and Maxillofacial Surgery, Tel-
Institute of Pathology, Tel-Aviv Sourasky Medical Center, 5 Daphna
Aviv Sourasky Medical Center; Sackler School of Medicine, Tel-Aviv
Street, Tel-Aviv, Israel; e-mail: [email protected]
University, Tel-Aviv, Israel.
Received January 17 2016
xProfessor and Division Head, Division of Otolaryngology and
Accepted February 11 2016
Head and Neck Surgery, Tel-Aviv Sourasky Medical Center; Sackler
Ó 2016 American Association of Oral and Maxillofacial Surgeons
School of Medicine, Tel-Aviv University, Tel-Aviv, Israel.
0278-2391/16/00177-4 http://dx.doi.org/10.1016/j.joms.2016.02.008
1 CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
57 58 59 60 61 62 63 64 65 66 67 68 69 70 71 72 73 74 75 76 77 78 79 80 81 82 83 84 85 86 87 88 89 90 91 92 93 94 95 96 97 98 99 100 101 102 103 104 105 106 107 108 109 110 111 112
print & web 4C=FPO
PRIMARY MALIGNANCY IMITATING PERI-IMPLANTITIS
FIGURE 1. A, Well-circumscribed gingival mass in the left anterior maxilla, with minute focal surface ulcerations diagnosed as large B-cell Q8 lymphoma. B, Complete resolution after treatment. Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
Q5
mucosa and bone, review the literature, and discuss the implications resulting from clinical overlap with conventional PI. This report was written in accordance with the ethical requirements (Israeli and GCP-ICH standards) of clinical trials.
Report of Cases CASE 1 Q6
A 72-year-old man with longstanding implantsupported PFM restoration and poor oral hygiene presented with a firm erythematous gingival overgrowth in the left maxillary canine area. He noticed it several months previously but did not seek dental or medical advice because it was asymptomatic. He presented for examination in the oral and maxillofacial surgery clinic
in a major hospital when bleeding while brushing his teeth became a problem. In addition to the slightly ulcerated gingival mass, pocket formation and radiographic bone loss were documented. The clinical impression was PI, giant cell granuloma, or pyogenic granuloma (Fig 1). Biopsy examination of the lesion yielded a surprising diagnosis of large B-cell lymphoma. Thorough workup showed that no other organ was affected; thus, the diagnosis of primary peri-implant large B-cell lymphoma was established. The patient successfully completed the hemato-oncologic treatment protocol, the lesion completely regressed, and he has been free of disease for 36 months. CASE 2
A 55-year-old woman with a medical history of systemic lupus erythematosus and oral lichen planus
print & web 4C=FPO
113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139 140 141 142 143 144 145 146 147 148 149 150 151 152 153 154 155 156 157 158 159 160 161 162 163 164 165 166 167 168
2
FIGURE 2. A, Gingival overgrowth with a yellowish-white surface around left mandibular implants diagnosed as squamous cell carcinoma. (Fig 2 continued on next page.) Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
Q1
169 170 171 172 173 174 175 176 177 178 179 180 181 182 183 184 185 186 187 188 189 190 191 192 193 194 195 196 197 198 199 200 201 202 203 204 205 206 207 208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224
3
RAISER ET AL
225 226 227 228 229 230 231 232 233 234 235 236 237 238 239 240 241 242 243 244 245 246 247 248 249 250 251 252 253 254 255 256 257 258 259 260 261 262 263 264 265 266 267 268 269 270 271 272 273 274 275 276 277 278 279 280
FIGURE 2 (cont’d). B, Radiograph displays substantial vertical peri-implant bone loss. Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
(OLP) had a longstanding implant-supported complete mandibular PFM restoration. She presented at the oral and maxillofacial dental department (where she was being followed) with an asymptomatic, white, thick gingival overgrowth with pocket formation and substantial bone loss. Because OLP is a potentially malignant condition, a biopsy examination was performed and the diagnosis was welldifferentiated squamous cell carcinoma (SCC). No other organs were affected, and after mandibulectomy and node dissection, the patient has been free of disease for 8 years (Fig 2). CASE 3
A 70-year-old woman with a 7-year history of OLP presented with an irregular erythematous nonulcerated mass on the buccal and lingual sides of an implant-supported PFM restoration in the posterior right mandible (Fig 3). Some horizontal bone loss was noted on the panoramic radiograph. Biopsy examination resulted in a diagnosis of SCC. At surgery, the lesion was found to involve the retromolar trigon, the floor of the mouth, and mandible, without lymph node involvement. After mandibulectomy with node
dissection and radiation therapy, the patient has been free of disease for 3 years.
Literature Analysis A literature search of PubMed and Google Scholar from 2000 through 2014 retrieved 42 cases of oral malignancy involving dental implants4-25 (Table 1). Before 2000, only 4 cases were described,26,27 but the number of such cases in the literature has increased sharply since then (Fig 4). The patients were typically older adults (mean age, 68 yr; female predominance, 1:1.5). Most cases (92.8%) involved the mandible and the remaining cases (7.2%) occurred in the maxilla. The most prevalent type of malignancy reported around dental implants was SCC (85.7%); the second in frequency (9.5%) was metastasis from primary breast and lung tumors. The remaining malignancy types reported were 1 case each of osteosarcoma and plasmacytoma (2.4%). Lymphoma was not associated with dental implants. Primary large B-cell lymphoma is extremely rare in the gingiva, with only 13 such cases ever reported.28
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319 320 321 322 323 324 325 326 327 328 329 330 331 332 333 334 335 336
PRIMARY MALIGNANCY IMITATING PERI-IMPLANTITIS
print & web 4C=FPO
337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352 353 354 355 356 357 358 359 360 361 362 363 364 365 366 367 368 369 370 371 372 373 374 375 376 377 378 379 380 381 382 383 384 385 386 387 388 389 390 391 392
4
FIGURE 3. A, Granular and erythematous tissue surrounding left posterior mandibular implants diagnosed as squamous cell carcinoma. The red-and-white lesion on the buccal mucosa is related to the patient’s history of oral lichen planus. (Fig 3 continued on next page.) Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
Peri-implant malignancies usually were primary tumors (69%). The remaining were recurrent or second primary tumors in patients with previous oral malignancy (21.4%) and metastasis from nonoral distant tumors (9.5%). The literature search showed that 45.3% of cases occurred in a population with recognized risk factors for oral cancer; potentially malignant conditions were erythroplakia, leukoplakia, OLP, and proliferative verrucous leukoplakia (PVL). In addition, 47.6% of cases had a previous oral malignancy and 19% had a history of a nonoral malignancy that could metastasize to the jaws or gingiva. Thus, the vast majority, but not all, cases occurred in a population in which a high level of suspicion for oral cancer should be maintained. Additional life style factors such as previous or current smoking were reported in 35.7% of cases and alcohol use in 19%, with coexisting risk factors in several cases. However, detailed quantitative information on the history of smoking or alcohol use (or abuse) was not included in most cases reviewed.
Discussion The incidence of peri-implant malignancy seems to be extremely low, with only 46 cases ever reported.4-27 Bhatavadekar21 calculated the theoretical standardized incidence ratio (SIR) to be 0.00017 per million per year. This is a very low figure, for example, compared with cancer related to background radiation, for
which the calculated SIR was 20 per million per year.21 Data from a study by Moergel et al24 provide Q7 information on the actual incidence: in a cohort of 10,986 implants placed during a 15-year period, 15 cases of peri-implant SCC were recorded, 9 (3%) in patients with previous oral SCC and 6 (0.056%) for the remaining 10,689 implants. The incidence in patients with a previous oral malignancy is considerably higher (although low compared with the expected recurrence of oral SCC) and seems to be very low outside this risk group. From analysis of peri-implant malignancy in the literature, including the new cases reported in the present study, the affected individuals tend to be elderly adults (mean age, 68 yr). The gender distribution shows a clear 1:1.5 female predominance as opposed to the characteristic male predominance of oral cancer in general. There also is a clear predilection for the mandible. Most patients in the literature had at least 1 recognized predisposing factor for oral cancer: erythroplakia, OLP, PVL and previous oral malignancy. This was true for cases 2 and 3 in the present series who had a history of OLP. Most malignancies in conjunction with dental implants in the literature have been SCC, and most of these were primary tumors, which is in agreement with the distribution of cancer types in oral cancer in general. Cases 2 and 3 have these typical features for peri-implant malignancy. In contrast, case 1, who was diagnosed with a primary large B-cell lymphoma, had no known risk
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
393 394 395 396 397 398 399 400 401 402 403 404 405 406 407 408 409 410 411 412 413 414 415 416 417 418 419 420 421 422 423 424 425 426 427 428 429 430 431 432 433 434 435 436 437 438 439 440 441 442 443 444 445 446 447 448
5
RAISER ET AL
449 450 451 452 453 454 455 456 457 458 459 460 461 462 463 464 465 466 467 468 469 470 471 472 473 474 475 476 477 478 479 480 481 482 483 484 485 486 487 488 489 490 491 492 493 494 495 496 497 498 499 500 501 502 503 504
FIGURE 3 (cont’d). B, Radiograph shows only moderate vertical bone loss around the implants. Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
factors at the time he was diagnosed. The oral cavity accounts for only 1% of extranodal non-Hodgkin lymphoma (NHL), and these are very rarely located in the gingiva. Only 13 gingival cases of NHL have ever been reported,28 and none in the context of dental implants. The existing data suggest that the incidence of periimplant malignancy is very low, and there is no epidemiologic evidence that dental implants pose any specific risk for cancer. However, attention should focus on the fact that the clinical presentation in most cases reported and the new cases described in the present report bears many similarities to PI, such as gingival overgrowth, bone loss, and a tendency to bleed. This clinical presentation also has been described primarily for longstanding implants, which also are the circumstances in which PI is most frequent. Malignancy masquerading as PI carries the risk of being ignored or treated as PI without histopathologic analysis, leading to delayed diagnosis. In the case of malignancy, delays in diagnosis have dire implications for patient survival.
In the 3 present cases, the examination was carried out by oral and maxillofacial surgeons in a large hospital facility, where biopsy services are readily available. However, most patients with dental-supported restorations are usually cared for by dentists in the community who would have little experience with oral cancer or biopsy procedures or immediate access to pathology services. It is impossible to differentiate simple PI clinically from its benign and malignant mimickers without proper histopathologic analysis. The purpose of this report is to raise awareness that lesions that imitate PI might represent other aggressive lesions, malignant and benign but aggressive, such as giant cell granuloma.3 Especially high suspicion should be raised for lesions that do not respond to conventional treatment modalities for PI, lesions in patients with medical histories positive for potentially malignant conditions, and patients with previous oral and nonoral cancer. These cases should be referred immediately for biopsy examination and histopathologic analysis.
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
505 506 507 508 509 510 511 512 513 514 515 516 517 518 519 520 521 522 523 524 525 526 527 528 529 530 531 532 533 534 535 536 537 538 539 540 541 542 543 544 545 546 547 548 549 550 551 552 553 554 555 556 557 558 559 560
561 562 563 564 565 566 567 568 569 570 571 572 573 574 575 576 577 578 579 580 581 582 583 584 585 586 587 588 589 590 591 592 593 594 595 596 597 598 599 600 601 602 603 604 605 606 607 608 609 610 611 612 613 614 615 616
6
PRIMARY MALIGNANCY IMITATING PERI-IMPLANTITIS
Table 1. SUMMARY OF CASES PUBLISHED FROM 2000 THROUGH 2014
Age (yr)/ Gender
Source
Location
Risk Factors
Clinical Presentation
Diagnosis
82/M
Mandible
VC 3, leukoplakia, previous smoking
Mimicked PI
SCC
69/M
Mandible
Previous SCC
Rec SCC
69/F
Mandible
Rec SCC
F
Mandible
Previous VC, leukoplakia, SCC OLP, smoking
Mimicked PI, pathologic fracture Mimicked PI
Mimicked PI
Primary SCC
M
Mandible
Mimicked PI
Rec SCC
Verhoeven et al, 20078 Dib et al, 200710
67/F
Mandible
Mimicked PI
Metastasis from lung
NA/F
Mandible
Swelling and pain
Abu El-Naaj et al, 20077
70/F
Mandible
Metastasis from breast cancer SCC
72/M 75/F
Mandible Mandible
Schache et al, 200815
77/M
Mandible
Breast adenocarcinoma Thyroid and breast cancer OLP, smoking Solitary plasmacytoma spine None
Gallego et al, 200812 Kwok et al, 200813
81/F
Mandible
OLP, previous SCC
71/M
Mandible
67/F
Mandible
62/M 38/F
Mandible Maxilla
Previous smoking, alcohol Previous tongue SCC (2), breast cancer, previous smoking, alcohol Alcohol and tobacco None
76/M
Mandible
None
70/F
Mandible
None
62/F
Mandible
77/F
Mandible
Previous SCC, smoking Previous SCC
71/M
Mandible
Previous SCC
62/F 69/F
Mandible Mandible, floor of mouth Mandible
Previous SCC Previous SCC
Block and Scheufler, 20014 Shaw et al, 20045
Czerninski et al, 20066
Poggio, 20079
McGuff et al, 200814 Eguia del Valle et al, 200811 Gallego et al, 200916 Gulati et al, 200917 De Ceulaer et al, 201018
Meijer et al, 201019 Orhan et al, 201120
69/F
Previous colon and oral cancer Lung cancer
Breast cancer
Exophytic white lesion, bone loss Ulcerated mass Peri-implant mass, bleeding, bone loss Peri-implant mass, discomfort, bony erosion Peri-implant mass
SCC Solitary plasmacytoma SCC
Rec SCC
‘‘Inflammatory process’’ Exophytic mass, ‘‘granulation tissue’’
SCC
Nonhealing ulcer Mass
SCC Osteosarcoma
White exophytic mass, ulcer, bone loss Ulcer and pain related to cantilever Mimicked PI
SCC
Rec SCC
Mimicked PI
Rec SCC
Mucosal nonulcerated swelling Mimicked PI Exophytic mass
Rec SCC
Numb chin syndrome, with mixed RO-RL lesion
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
Second primary SCC
SCC
Rec SCC SCC
Metastatic breast cancer
617 618 619 620 621 622 623 624 625 626 627 628 629 630 631 632 633 634 635 636 637 638 639 640 641 642 643 644 645 646 647 648 649 650 651 652 653 654 655 656 657 658 659 660 661 662 663 664 665 666 667 668 669 670 671 672
7
RAISER ET AL
Table 1. Cont’d
Age (yr)/ Gender
Source
Location
Risk Factors
Pfammatter et al, 201223
55/F
Mandible
Pancreatic cancer, NSCLC
Bhatavadekar, 201221 Marini et al, 201325 Moergel et al, 201424
54/M
Maxilla
None
55/F
Mandible
15 cases (8 F, 7 M)
Mandible, 14; maxilla, 1
Summary
17 M, 25 F
Maxilla, 3; mandible, 39
OLP, long-term steroids Previous SCC, 9; leukoplakia, 10; erythroplakia, 2; OLP, 3 Previous SCC, 20; potentially malignant lesions, 19; nonoral cancer, 8; tobacco and alcohol, 5; no risk factors, 5
Clinical Presentation
Diagnosis
Initial presentation mimicked PI, later developed numbness Swelling and ulcer
Metastasis from NSCLC
SCC
Mimicked PI
SCC
Exophytic mass, 10; nonhealing ulcer, 4; mimicked PI, 1 Mass or swelling, 16; mimicked PI, 16; ulcer or ulcerated mass, 8; numb chin syndrome, 1
SCC
Primary SCC, 27; Rec and second SCC, 9; metastasis, 4; plasmacytoma, 1; osteosarcoma, 1
Abbreviations: F, female; M, male; NA, ---; NSCLC, ---; OLP, oral lichen planus; PI, peri-implantitis; Rec, recurrent; RL, Q9 ---; RO, ---; SCC, squamous cell carcinoma; VC, verrucous carcinoma. Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
Cases of Perimplant Malignancy, 1995 - 2014 25
20
No.Cases
15
10
print & web 4C=FPO
673 674 675 676 677 678 679 680 681 682 683 684 685 686 687 688 689 690 691 692 693 694 695 696 697 698 699 700 701 702 703 704 705 706 707 708 709 710 711 712 713 714 715 716 717 718 719 720 721 722 723 724 725 726 727 728
5
0 1995-1999
2000-2004
2005-2009
2010-2014
FIGURE 4. A sharp increase in the number of reported cases of peri-implant malignancy. Raiser et al. Primary Malignancy Imitating Peri-Implantitis. J Oral Maxillofac Surg 2016.
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
729 730 731 732 733 734 735 736 737 738 739 740 741 742 743 744 745 746 747 748 749 750 751 752 753 754 755 756 757 758 759 760 761 762 763 764 765 766 767 768 769 770 771 772 773 774 775 776 777 778 779 780 781 782 783 784
785 786 787 788 789 790 791 792 793 794 795 796 797 798 799 800 801 802 803 804 805 806 807 808 809 810 811 812 813 814 815 816 817 818 819 820 821 822 823 824
8
PRIMARY MALIGNANCY IMITATING PERI-IMPLANTITIS
References 1. Albrektsson T, Isidor F: Consensus report of session IV, in Lang NP, Charring T (eds): Proceedings of the First European Workshop on Periodontology. London, UK, Quintessence, 1994, pp 365–369 2. Berglundh T, Zitzmann NU, Donati M: Are peri-implantitis lesions different from periodontitis lesions? J Clin Periodontol 38(suppl 11):188, 2011 3. Kaplan I, Hirshberg A, Shlomi B, et al: The importance of histopathological diagnosis in the management of lesions presenting as peri-implantitis. Clin Implant Dent Relat Res 17:e126, 2015 4. Block MS, Scheufler E: Squamous cell carcinoma appearing as peri-implant bone loss: A case report. J Oral Maxillofac Surg 59:1349, 2001 5. Shaw R, Sutton D, Brown J, et al: Further malignancy in field change adjacent to osseointegrated implants. Int J Oral Maxillofac Surg 33:353, 2004 6. Czerninski R, Kaplan I, Almoznino G, et al: Oral squamous cell carcinoma around dental implants. Quintessence Int 37:707, 2006 7. Abu El-Naaj I, Trost O, Tagger-Green N, et al: Peri-implantitis or squamous cell carcinoma? Rev Stomatol Chir Maxillofac 108: 458, 2007 8. Verhoeven JW, Cune MS, van Es RJ: An unusual case of implant failure. Int J Prosthodont 20:51, 2007 9. Poggio CE: Plasmacytoma of the mandible with a dental implant failure. Clin Oral Implants Res 18:54, 2007 10. Dib LL, Soares AL, Sandoval RL, et al: Breast metastasis around dental implants: A case report. Clin Implant Dent Relat Res 9: 112, 2007 11. Eguia del Valle A, Martınez-Conde Llamosas R, L opez Vicente J, et al: Primary oral squamous cell carcinoma arising around dental osseointegrated implants mimicking peri-implantitis. Med Oral Patol Oral Cir Bucal 13:E489, 2008 12. Gallego L, Junquera L, Baladr on J, et al: Oral squamous cell carcinoma associated with symphyseal dental implants: An unusual case report. J Am Dent Assoc 139:1061, 2008 13. Kwok J, Eyeson J, Thompson I, et al: Dental implants and squamous cell carcinoma in the at risk patient-report of three cases. Br Dent J 205:543, 2008 14. McGuff HS, Heim-Hall J, Holsinger FC, et al: Maxillary osteosarcoma associated with a dental implant: Report of a case and review of the literature regarding implant-related sarcomas. J Am Dent Assoc 139:1052, 2008
15. Schache A, Thavaraj S, Kalavrezos N: Osseointegrated implants: A potential route of entry for squamous cell carcinoma of the mandible. Br J Oral Maxillofac Surg 46:397, 2008 16. Gallego L, Junquera L, Llorente S: Oral carcinoma associated with implant-supported overdenture trauma: A case report. Dent Traumatol 25:e3, 2009 17. Gulati A, Puthussery FJ, Downie IP, et al: Squamous cell carcinoma presenting as peri-implantitis: A case report. Ann R Coll Surg Engl 91:W8, 2009 18. De Ceulaer J, Magremanne M, van Veen A, et al: Squamous cell carcinoma recurrence around dental implants. J Oral Maxillofac Surg 68:2507, 2010 19. Meijer GJ, Dieleman FJ, Berge SJ, et al: Removal of an oral squamous cell carcinoma including parts of osseointegrated implants in the marginal mandibulectomy: A case report. Oral Maxillofac Surg 14:253, 2010 20. Orhan K, Bayndr H, Aksoy S, et al: Numb chin syndrome as a manifestation of possible breast cancer metastasis around dental implants. J Craniofac Surg 22:942, 2011 21. Bhatavadekar NB: SCC in association with dental implants: An assessment of previously hypothesized carcinogenic mechanisms and a case report. J Oral Implantol 38:792, 2012 22. Javed F, Al-Askar M, Qayyum F, et al: Oral squamous cell carcinoma arising around osseointegrated dental implants. Implant Dent 21:280, 2012 23. Pfammatter C, Lindenm€ uller IH, Lugli A, et al: Metastases and primary tumors around dental implants: A literature review and case report of peri-implant pulmonary metastasis. Quintessence Int 43:563, 2012 24. Moergel M, Karbach J, Kunkel M, et al: Oral squamous cell carcinoma in the vicinity of dental implants. Clin Oral Investig 18: 277, 2014 25. Marini E, Spink MJ, Messina AM: Peri-implant primary squamous cell carcinoma: A case report with 5 years’ follow-up. J Oral Maxillofac Surg 71:322, 2013 26. Clapp C, Wheeler JC, Martof AB, et al: Oral squamous cell carcinoma in association with dental osseointegrated implants. An unusual occurrence. Arch Otolaryngol Head Neck Surg 122: 1402, 1996 27. Moxley JE, Stoelinga PJW, Blijdorp PA: Squamous cell carcinoma associated with a mandibular staple implant. J Oral Maxillofac Surg 55:1020, 1997 28. Sugimoto K-J, Shimada A, Sakurai H, et al: Primary gingival diffuse large B-cell lymphoma: A case report and a review of the literature. Int J Clin Exp Pathol 7:418, 2014
CRP 5.4.0 DTD YJOMS57152_proof 10 March 2016 5:14 pm CE AH
825 826 827 828 829 830 831 832 833 834 835 836 837 838 839 840 841 842 843 844 845 846 847 848 849 850 851 852 853 854 855 856 857 858 859 860 861 862 863 864