Received: 24 September 2019 Revised: 4 December 2019 Accepted: 17 December 2019

DOI: 10.1002/hed.26065

CLINICAL REVIEW

Postimplantation radiation therapy in head and neck

cancer patients: Literature review

Carine Koudougou MD1 | Hélios Bertin MD1,2 | Bastien Lecaplain DDS3 |

Zahi Badran DDS, PhD3 | Julie Longis MD1 | Pierre Corre MD, PhD1,4 |
Alain Hoornaert DDS, PhD2,3

1
Service de chirurgie Maxillo-faciale et
stomatologie, CHU de Nantes, 1 place
Abstract
Alexis Ricordeau, Nantes Cedex 1, France There is no recommendation regarding the timing for implant surgery in
2
Laboratoire des sarcomes osseux et patients with head and neck cancer (HNC) who require postoperative radiation
remodelage des tissus calcifiés, Unité
therapy (RT). This systematic review focused on the literature about the out-
Mixte de Recherche, Faculté de Médecine,
1 rue Gaston Veil, Nantes Cedex, France comes of implants placed during ablative surgery in patients with HNC who
3
Faculté de Chirurgie Dentaire, 1 Place underwent postoperative RT. Implants placed after radiation therapy and
Alexis Ricordeau, Nantes, France implants placed in reconstructed jaws were excluded. Four comparative studies
4
Laboratoire d'Ingénierie Ostéo-
involving 755 native mandible primary implants were analyzed. The survival
Articulaire et Dentaire (LIOAD), Faculté
de Chirurgie Dentaire, 1 Place Alexis rate with postimplantation RT was 89.6% vs 98.6% in patients with no additional
Ricordeau, Nantes, France radiation. The overall success of implant-retained overdenture in patients with
RT performed postimplantation was 67.4% vs 93.1% in patients with implant
Correspondence
Carine Koudougou, Service de chirurgie surgery that was carried out 1 year after the completion of radiation therapy.
Maxillo-faciale et stomatologie, CHU de Only five cases of osteoradionecrosis (ORN) of the jaw were reported. The out-
Nantes, 1 place Alexis Ricordeau, Nantes
Cedex 1, France.
comes for implant survival rates appear to be positive for irradiated implants.
Email: [email protected]
KEYWORDS
dental implants, head and neck cancer, implant survival, radiation therapy, radiotherapy

1 | INTRODUCTION improved.5 Furthermore, restoration of dental function

by prosthetic rehabilitation represents an important part
Curative strategies for treating head and neck cancer of reconstruction strategies.2 In addition, it contributes to
(HNC) frequently combine surgery, radiation therapy improvement of the aesthetic outcomes and quality of
(RT), and chemotherapy. Consequently, the treatment life.3,6,7 Prosthetic rehabilitation of edentulous patients
often results in alteration of the facial and oral anatomy, after oral cancer is a therapeutic challenge.8 Conven-
and it can negatively impact mandibular and maxillary tional removable prosthodontic techniques are often used
aesthetics and functions.1,2 Indeed, a large mandibular or in first intention, but there is an elevated risk of failure in
maxillary ablative surgery can impact the dentition of these altered anatomical situations.3 Furthermore, it is
patients.3 In patients requiring postoperative RT, difficult to achieve stability and retention due to the
extended dental extractions are needed in the irradiated reduction of salivary secretion and due to the impairment
area in order to prevent osteoradionecrosis (ORN) of the of chewing and swallowing. Thus, masticatory functions
jaw. Thus, a large proportion of patients become edentu- are not restored, and it is often poorly tolerated by the
lous.4 With the development and generalization of patients. Many authors and systematic reviews have
pedicle and free flaps in reconstructive strategies of the already shown good outcomes of implant surgery and
oral cavity, the quality of life of patients with HNC has dental implant-supported prosthetics in patients with

Head & Neck. 2020;1–9. wileyonlinelibrary.com/journal/hed © 2020 Wiley Periodicals, Inc. 1

2 KOUDOUGOU ET AL.

HNC. High implant survival rates and restoration of a 2.2 | Literature search
good quality of life have been reported.9-11 After facial
RT, it is now commonly thought that oral implant sur- A systematic review was conducted of the literature pub-
gery can be performed at the irradiated sites.12-17 A low lished between January 2004 and June 2019. This was
risk of implant failure has been reported for doses of less done by searching PubMed (MEDLINE) using the terms
than 50 Grays (Gy).13,18 With high doses (over 70 Gy), “dental implant,” “radiation therapy,” and “radiother-
there is a high risk of implant failure associated with a apy” in combination with the Boolean operators AND
high risk of ORN, and it is recommended that implant OR. All the abstracts retrieved were reviewed and the
surgery is avoided. With doses between 50 and 70 Gy, potentially relevant articles preselected.
implant placement does not appear to be advisable.19 In
these cases, various authors have advocated the use of
hyperbaric oxygen treatment to reduce the risk of ORN 2.3 | Inclusion criteria
and to improve the osseointegration, although there is
scant, if any, scientific evidence to back this up.20,21 • Original research articles based on:
There is currently no recommendation regarding the  clinical trials,
timing for implant surgery in patients with HNC who  case-control studies,
require postoperative RT. In most cases, implants are  cohort studies
placed after completion of the HNC treatment, with a • Involving patients with HNC who received dental
minimum of 6 months after the end of the RT.12,13,20 On implants during the ablative cancer surgery.
the other hand, some authors consider that, in addition • Patients who underwent RT after implant placement.
to the restoration of osseous and soft tissues, dental reha-
bilitation in patients with HNC can start at the same time
as the ablative surgery.22-26 In such cases, the implanta- 2.4 | Exclusion criteria
tion site has not been compromised by the radiation. This
promotes early oral rehabilitation of the patient and thus • Implants placed only after primary surgery
improvement of the quality of life. There are only a lim- • Implant placed only after RT
ited number of studies in the recent literature reporting • Minimum follow-up of 1 year after the primary
the results of primary implantation with postoperative surgery
radiation, and no systematic review has focused on this • Implants not placed in native bone (free osseous flaps)
topic. With regard to the effects of the radiation on previ- • Case reports
ously placed dental implants, the backscattering of radia- • Other literature reviews
tion results in an increased dose on the surrounding • Articles with insufficient published data
bone.27-29 However, there is no scientific evidence that
this phenomenon enhances the relative risk of ORN. In
addition, metal artifacts generated by titanium implants 3 | RESULTS
are known to decrease the accuracy of tumor delineation
and thus decrease the accuracy of dose delivery.30,31 The The PubMed database searches identified 473 potentially
aim of this systematic review was to assess the outcomes relevant articles. Of these, 140 articles were published
of implants placed during ablative surgery in patients before 2004 and thus not considered further. The remaining
with HNC who received postoperative RT. The influence 333 articles were assessed based on the abstract, and 51 arti-
of the following variables was assessed: the survival rates cles were then selected for a review of the full text.
of the implants, the local impact of RT, and the success A total of five articles that met the inclusion criteria
of prosthetic rehabilitation. were selected. Upon closer inspection, two articles publi-
shed by the same team used exactly the same cohort of
patients. We selected the article for which the data were
2 | MATERIALS AND METHODS the most detailed. Thus, we ultimately analyzed four arti-
cles (Figure 1). In three of these studies, the implants
2.1 | Focused question were placed during the ablative tumor surgery for all the
patients. The patients who received additional RT and
The main question asked in this review was: Does post- the patients with no additional RT were then compared.
operative RT significantly compromise the outcome of In one study, patients from two different head and
implant surgery performed concomitant with the primary neck oncology centers were compared. In the first cohort,
ablative surgery? the implants were placed during the ablative surgery,
KOUDOUGOU ET AL. 3

whereas in the second cohort, the implant surgery was A total of 356 implants were placed for the patients who
performed 1 year after completion of the oncological did not receive RT after the implant surgery, with an
treatment. For all the patients, the implants were placed overall survival rate of 98.6% (13 implants were lost). The
in the edentulous mandible, in the interforaminal region. implant survival rates for the individual studies ranged
The data and results are presented in Tables 1, 2, and 3. from 97.1% to 100%. There were 29 patients who under-
went implant surgery 1 year after completion of the
RT. Sixty-five implants were placed, with a survival rate
3.1 | Survival rates of 90.8%. For the patients who underwent post-
implantation RT, the reasons for loss of the implants
Implants were considered as having been lost in the fol- were: osseointegration failure for 70 implants, resection of
lowing cases: osseointegration failure, resection of a a recurrent tumor for 27 implants, and the occurrence of
recurrent tumor that included the implant(s), or the ORN for 10 implants. For the patients who did not
occurrence of ORN at the implantation site. The mean undergo RT after implant surgery, the reasons for loss of
follow-up ranged from 29.6 months to 5 years. A total of the implants were: osseointegration failure for six
755 implants were placed for the patients who underwent implants and resection of a recurrent tumor for one
implant surgery before RT, with an overall survival rate implant. For the patients who underwent implant sur-
of 89.6% (97 implants were lost). The implant survival gery, osseointegration failed with six implants.
rates for the individual studies ranged from 82% to 96.7%.

3.2 | Radiation dose

The patients who underwent postimplantation RT were

irradiated on the bed of the tumor and on the lymph
nodes with conventional doses that varied from 60 to
68 Gy in two studies and unspecified doses in two stud-
ies. The average time interval between the surgery and
the start of the RT was 6 weeks.
Schepers et al only specified the radiation dose at the
implant site, in relation to the implants lost.35 They
reported osseointegration failure of two implants that
had received a radiation dose between 20 and 40 Gy.

3.3 | The success of implant-retained

overdenture

The success rate of the prosthetic rehabilitation on

implants was evaluated based on two parameters: the
number of patients with an implant-retained overdenture
and the number of functional implants. For the patients
who underwent implant surgery before the RT, the over-
F I G U R E 1 Flow chart of the selection process [Color figure all overdenture success rate was 67.4%, with rates ranging
can be viewed at wileyonlinelibrary.com] from 34.4% to 82.8%. For the patients who did not receive

TABLE 1 General data of the selected studies

Number Follow-up
Authors Year Study type Implantation site of patients Implants (mean)
Schepers et al35 2006 Retrospective Symphyseal Mandibular area 48 139 29,6 months
25
Korfage et al 2010 Prospective Interforaminal Mandibular Area 50 195 5 years
23
Mizbah et al. 2012 Retrospective Interforaminal Mandibular area 99 314 5 years
24
Korfage et al 2014 Retrospective Interforaminal Mandibular Area 164 524 3,8 years
 4

TABLE 2 Irradiated Implants: Radiation dose, survival rate, success of the overdoverdenture

Radiation dose (Grays)

Patients with Number
Implantation Lost Survival implant-retained of functionnal
Authors Patients Implants Tumor bed site implants rate Reasons of lost implants overdenture implants
35
Schepers et al 21 (43,8%) 61 60-68 Gy 10-68 Gy 2 96,70% Osseointegration failure 15/21 (71,4%) 46/61 (75,4%)
25
Korfage et al 31 (62%) 127 Unspecified > 40 Gy 13 89,40% Osseointegration failure 9/31 (34,4%) Unspecified
Mizbah et al23 99 (36,7%) 249 60–68 Gy Unspecified 24 90,40% Osseointegration failure 82/99 (82,8%) 205/249 (82,3%)
Korfage et al24 100 (61%) 318 Unspecified Unspecified 58 82% - Osseointegration failure 81/100 (81%) Unspecified
(31 implants)
- Resection of recurrent
tumor (27 implants)
- ORN (10 implants)

Abbreviations: Gy, grays; ORN, osteoradionecrosis.

TABLE 3 Comparative groups of patients without RT or with implants placed after completion of RT

Number Lost Survival Reasons of lost Patients with implant Number of functional
Authors Patients Relation to RT of implants implants rate implants retained overdenture implants
Schepers et al35 27 (56,2%) No RT 78 0 100% / 21/27 (77,8%) 59/78 (75,6%)
25
Korfage et al 19 (38%) No RT 72 1 98,60% Osseointegration failure 11/19 (57,9%) Unspecified
23
Mizbah et al 29 Implants 1 year after 65 6 90,80% Osseointegration failure 27/29 (93,1%) 59/65 (90,8%)
completion of RT
Korfage et al24 64 (39%) No RT 206 6 97,10% Tumor (1 implant) 57/64 (89,1%) Unspecified

Abbreviation: RT, radiotherapy.

KOUDOUGOU ET AL.
KOUDOUGOU ET AL. 5

RT, the overall overdenture success rate was 74.9%, with patients who had not been irradiated. For the patients
rates ranging from 57.9% to 89.1%. who did not undergo RT after the implant surgery, the
For the patients with implant surgery that was per- overall survival rate was 98.6%. Similar results have been
formed 1 year after completion of the radiation therapy, reported in the literature for conventional implantology.39
93.1% had an implant-retained overdenture. Two studies In terms of the survival rate in relation to the timing of
only specified the number of functional implants. Of the implantation (pre- or post-RT) in this review, Mizbah
310 irradiated implants, 251 were functional, representing et al23 reported no statistically significant differences
78.8% of the total number of irradiated implants. Of the between implants placed before RT and implants placed
78 non-irradiated implants, 59 (75.6%) were functional, after RT in native mandibular bone. Similar results have
and of the 65 implants placed after the RT, 59 (90.8%) been presented by Nooh et al14 who suggested in a litera-
were functional. ture review that postimplantation RT had a slightly better
overall dental implant survival rate than preimplantation
RT, although this was not scientifically proven due to the
4 | DISCUSSION inhomogeneity of the reviewed studies.

As a result of improvements in the surgical techniques

for head and neck malignancies and advances in adju- 4.2 | Anatomical sites of implant
vant cancer therapies in recent years, the number of placement
patients going into remission has increased.
Presently, the challenge for these patients is being able In this review, all the implants were placed in the inter-
to maintain a good quality of life. Restoring oral function foraminal region on the native mandibular bone, leading
and aesthetics is, therefore, an important consideration.3,7 to more precision of the results. On the other hand, our
In this context, the French national health system findings can consequently not readily be extrapolated to
decided in 2013 to reimburse the placement of a maxi- other anatomical sites. Although a number of studies have
mum of four implants in the maxilla and a maximum of been published on implants placed during the ablative sur-
two implants in the mandible for patients with sequelae gery in the maxilla in the literature,34 these were excluded
of HNC when stabilization of a conventional prosthesis is from this study due to incomplete results. We decided to
complicated by alteration of the oral anatomy. exclude the studies with implants placed in reconstructed
Several authors have proposed guidelines for prostho- mandibles. Indeed, the reconstructed mandible appears to
dontic rehabilitation of HNC patients, based primarily on have biomechanical properties that differ from native
the cumulative dose received at the implantation site.19,32-34 mandibular bone40 and this can skew the results for sur-
There is currently no consensus regarding the ideal timing vival rates. The survival rate when implants are placed
of implant surgery. after RT has been well documented. Several studies have
In this systematic review, we sought to assess the reported a lower implant survival rate in the irradiated
validity of initiating implant-supported oral rehabilitation maxilla than in the mandible,18,21,41,42 despite the fact that
at the same time as the start of the curative treatment for the mandible is thought to be the area that is most suscep-
HNC patient. tible to ORN.33 Thus, the high survival rates in this litera-
ture review could be explained by the mandibular
placement of all of the implants in the four studies that
4.1 | Survival rates were selected. It would be interesting to undertake a com-
parative study on the behavior of implants placed during
The reported survival rates of primary implants vary from ablative surgery according to the anatomical site of the
82% in the study by Korfage et al24 to 96.7% in the study by implantation and including reconstructed jaws.
Schepers et al,35 with an overall survival rate of 89.6%. In
the study by Korfage et al, all the implants were inserted
by a number of different surgeons and residents, which 4.3 | Radiation dose
could explain their less favorable results. In the other stud-
ies, the patients were treated by a single experienced max- In this study, all the implants were placed during the pri-
illofacial surgeon and a single experienced prosthodontist. mary surgery, and the tumor bed and lymph node chain
It is reasonable to state that the results of Korfage et al bet- were subjected to RT within 6 weeks of the surgery. The
ter reflect the reality of the current practice. In concor- cumulative radiation dose at the implantation site depended
dance with the literature,21,36-38 implants were lost more on the location of the tumor and on the histopathology
frequently in the patients who underwent RT than in the results. It could, therefore, not be predicted before
6 KOUDOUGOU ET AL.

placement of the implant. Schepers et al35 reported varia- implant survival rate, to reduce the risk of ORN, and to
tion of the radiation dose at the implant site from 10 to optimize the success of the overdenture. There are cur-
68 Gy. For the 61 implants that received radiation, they rently no validated guidelines, nor is there an official con-
observed two osseointegration failures. These two implants sensus in this regard. In this review, Mizbah et al23
received radiation doses of between 20 and 40 Gy. Further- compared two protocols for implant placement: 1. A
more, 17 implants with successful osseointegration received DAS-implant group for which the placement was during
a cumulative dose >61 Gy. Therefore, when implants are the ablative primary surgery, before the RT and a P-
placed before RT, the radiation dose does not appear to cor- implant group for which the placement was during the
relate with the success of osseointegration. However, this post-therapy phase, with a minimum interval of 1 year.
hypothesis is based on a small sample of patients and it They did not find any statistically significant differences
needs to be substantiated with further scientific data. In in terms of implant survival rates between these two
terms of the effect of implant irradiation on the surrounding groups. However, in the P-implant group, 93.1% of the
bone, Korfage et al24 described five cases of ORN, rep- implants were functional whereas this figure was 82.8%
resenting 5% of the patients who underwent RT after in the DAS-implant group. Korfage et al25 reported a sur-
implantation. However, they consider that for implants vival rate of 89.4% in patients who underwent
placed before RT the presumed risk of developing ORN due postimplantation RT vs 98.6% in patients who did not
to backscattering of radiation would be lower than the risk receive RT, all of which were primary placed implants.
of developing ORN when the implants are placed in an irra- For the 31 patients who underwent RT of the implants,
diated bone, albeit without presenting any scientific proof. they reported 20 patients with overdenture success at
Backscattering radiation effects have been well documented 1 year and only 9 patients (34.4%) 5 years later. Schepers
in the literature.27-29 Ozen et al27 showed that backscatter- et al35 reported better outcomes, with 71.4% of the
ing of radiation results in an increased dose of radiation in patients who underwent postimplantation RT wearing an
the surrounding bone in front of and next to the implants, overdenture vs 77.8% of the patients who did not receive
with a range of 10%-21%. However, it has not been scientifi- RT, albeit with a mean follow-up of only 29.6 months. In
cally confirmed that there is a correlation between the the recent literature, most authors favor performing
development of ORN and radiation backscattering. Current implant surgery after completion of the primary curative
progress in radiotherapy allows accurate distribution of the treatment (surgery, RT, chemotherapy). In most situa-
radiation dose at the tumor site, and it increases the preci- tions, implants are placed starting at 1 year after the end
sion of the contouring of tumors or organs at risk. Dental of the RT,13,20 but there is still a lack of agreement
implants lead to metallic artifacts that result in a decrease regarding this matter. Claudy et al13 suggested in a sys-
of the contouring precision and a decrease in the accuracy tematic review that the placement of dental implants
of the dose calculation.30,31 Thus, it is more difficult to between 6 and 12 months post-radiotherapy was associ-
deliver an accurate radiation dose to the tumor bed. Fur- ated with a 34% higher risk of failure. Conversely, in a
thermore, deviations on a scale of a few millimeters can recent review, Zen Filho et al12 stated that the optimal
result in increased irradiation of organs at risk and they time interval between irradiation and dental implanta-
may have a significant negative impact on patient out- tion varies from 6 to 15 months. Thus, although the
comes.43 Various techniques for metal artifact reduction timing of the implant placement does not appear to result
have been described and compared.30,31,43 We did not find in different survival rates, it does appear to impact the
any studies that compared the accuracy of these techniques quality of the prosthodontic rehabilitation, which is the
with the accuracy of the delineation in patients without ultimate goal of the treatment. In these primary implant
sources of dental artifacts. Thus, it is difficult to determine cases, prosthodontic success does not appear to be corre-
to what extent a patient is not being given the best possible lated with implant survival. There is a need for more of a
chances of success of the RT with dental artifacts generated focus on the factors influencing the prosthodontic success
by titanium implants. With all these observations, whether of primary implants.
or not the risk/benefit ratio remains in favor of performing
implant surgery before RT should be a consideration.
4.5 | Economic perspective

4.4 | Timing of dental implant Any discussion of the validity of early implantation needs
placement to also consider the economic impact. Indeed, despite the
recent inclusion of implantation surgery for HNC patients
The principal aim of identifying the ideal timing of for rebates by the health system in HNC patients, the cost
implantation surgery in relation to RT is to improve the of implant-retained overdentures remains high. With a
KOUDOUGOU ET AL. 7

mean failure rate of 32.6% of implant-retained over- version of this manuscript, and agree to be accountable for
dentures for patients who undergo RT after implant sur- all aspects of work ensuring integrity and accuracy. The
gery, it needs to be considered whether this procedure is authors contributed as follows: conception and design,
indeed the most appropriate strategy. Despite this fact, C.K., and A.H.; analysis and interpretation, C.K., B.L., and
Mizbah et al23 and Schepers et al35 both agree that non- J.L.; drafting of the manuscript, C.K., H.B., and A.H.; revis-
functional primary placed implants remain less expensive ing of the manuscript, Z.B., H.B., P.C., and A.H.
than a secondary surgery. Wetzels et al found similar
results,44 although their opinion needs to be supported by ORCID
more scientific results. Hélios Bertin https://orcid.org/0000-0002-0546-079X

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