Abstract
Purpose
We aimed to evaluate the performance of hybrid bone single-photon emission computed tomography (SPECT)/computed tomography (CT) in predicting bone graft viability after maxillary or mandibular reconstructive surgery with vascularized bone grafts.
Methods
We retrospectively reviewed 46 bone planar scintigraphy and SPECT/CT images of 45 adult patients taken at 1 week (5–8 days) after maxillary or mandibular reconstructive surgery with vascularized bone grafts. By visual analysis, two nuclear medicine physicians scored the uptake degrees of each bone graft segment compared with the calvarium uptake on planar bone scintigraphy and SPECT/CT, respectively (0 = absence of uptake, 1 = less uptake, 2 = similar uptake, and 3 = more uptake). The imaging results were compared with clinical follow-up for assessing bone graft viability.
Results
During follow-up, five bone graft segments were surgically removed and confirmed as nonviable—one had a score of 0, although the other four had a score of 1–3 on planar bone scintigraphy. All five bone graft segments were scored 0 on SPECT/CT and eventually confirmed as nonviable. All other graft segments with a score of > 1 on SPECT/CT were viable and uneventful. The anatomical CT information on SPECT/CT images was helpful in discriminating bone graft uptake from adjacent bone or soft tissue uptake.
Conclusions
The absence of tracer uptake by the vascularized bone graft on bone SPECT/CT at 1 week after maxillary or mandibular reconstructive surgery can predict graft failure. Bone SPECT/CT can be used to predict vascularized bone graft viability postoperatively.
Keywords: Bone scintigraphy, Single-photon emission computed tomography, Vascularized bone graft, Maxillary or mandibular reconstruction, Graft viability
Introduction
Maxillary or mandibular reconstruction after the resection of a benign or malignant tumor, osteomyelitis, and osteoradionecrosis requires a multidisciplinary approach to optimize functional and cosmetic outcomes. Vascularized bone graft provides long-term reliability and stability and ensures a solid arch necessary to restore form and function [1]. The vascularized bone graft is considered nonviable when it loses cell viability. It can occur when the blood supply has insufficient or inadequate stabilization [2]. Therefore, postoperative monitoring of the viability of the bone graft is significant because the nonviable graft requires rapid intervention. However, vascularized bone graft monitoring in head and neck reconstructive surgery can be a major challenge. The possibilities of clinical evaluation are restricted in all kinds of “buried” grafts [3]. Clinically successful graft incorporation depends on complex biological processes, including sufficient blood supply and osteoblast vitality [4, 5]. Bone scintigraphy using 99mTc tracers, such as 99mTc-diphosphono-1,2-propanodicarboxylic acid (DPD), and 99mTc-methylene-diphosphonate, has been frequently used to monitor vascularized bone graft viability [6]. Several methods have been used to monitor bone graft viability. Radiographs are unreliable during the first few months after surgery because a 30–40% bone mineral content alteration is necessary before the changes become visible on radiographs [7]. Color duplex ultrasound is a reliable technique that can be used for the patency monitoring of vascularized bone grafts. However, its reliability is only valid for superficial anastomoses [8]. Angiography shows anastomosis patency; however, it cannot reveal microcirculation. In addition, side effects, such as spasm and thrombosis, can be hidden owing to its invasive nature [9]. Positron emission tomography has been shown to have high sensitivity in detecting the likelihood of graft viability. However, routine use is almost impracticable owing to its high cost [10]. In contrast, bone scintigraphy has been proven to be valuable because it is a noninvasive, simple, and effective postoperative assessment [3, 9]. With respect to head and neck region evaluation, single-photon emission computed tomography (SPECT) should be favored over conventional planar imaging because of the complex craniomaxillofacial region anatomy [11]. In addition to SPECT, hybrid imaging using SPECT and computed tomography (CT) provides better anatomical information of the complex craniomaxillofacial region and allows the attenuation correction of SPECT images. Therefore, SPECT/CT may be more useful for the evaluation of patients who have undergone maxillary or mandibular reconstruction surgery as it differentiates between tracer uptake by bone grafts and osteotomy stump or adjacent soft tissues. However, no studies have used bone SPECT/CT in the field of maxillofacial reconstructive surgery. Therefore, this study aimed to evaluate the performance of bone SPECT/CT in the prediction of vascularized bone graft viability after maxillary or mandibular reconstruction.
Materials and Methods
Subjects
We retrospectively reviewed the data of 59 consecutive patients who underwent maxillary or mandibular reconstruction with vascularized bone grafts between February 2014 and March 2019 at our institution to evaluate bone graft viability. Of the 59 patients, 12 who did not undergo SPECT/CT and two who had > 8 days of interval between the surgery and bone SPECT/CT were excluded. Finally, we included 45 patients (mean age, 60.7 ± 14.2 years; range 26–89 years; 27 men and 18 women) who underwent bone scintigraphy with skull SPECT/CT at approximately 1 week (5–8 days) postoperatively. This study was approved by the Institutional Review Board (IRB no. 2018-1468). The need for informed consent was waived by the IRB.
The reasons for maxilla (n = 9) or mandible (n = 36) resection in 45 patients were as follows: primary bone tumor (n = 14), metastatic tumors (n = 13), radiotherapy-induced necrosis (n = 7), bisphosphonate-related osteonecrosis of the jaw (n = 6), and osteomyelitis (n = 5). Two types of vascularized bone grafts were used—fibular free flap (FFF) and deep circumflex iliac artery flap (DCIA). In one patient, a two-stage surgery was performed to allow FFF on one side and DCIA on the other side of the mandible. Thirty-two FFF and 14 DCIA were performed. A total of 46 bone scintigraphy and SPECT/CT images of 45 patients at 1 week postoperatively were available for evaluation because one patient had undergone two-stage surgery involving the bilateral sides of the mandible, as described above. Of the 32 FFFs, 17 consisted of more than one bone segment. Moreover, 14 bone grafts consisted of two bone segments, and 3 bone grafts consisted of 3 segments. All 14 DCIAs had one bone segment. Therefore, we evaluated the 66 bone segments of 46 vascularized bone grafts on planar bone scintigraphy and SPECT/CT.
Patients were clinically followed up by the operating surgeon for a minimum of 2 months postoperatively (median, 22 months; range, 2–76 months). The nonviable grafts were clinically suspected by representative symptoms, such as covering skin changes, graft necrosis and resorption, and results of various tests during clinical follow-up. A nonviable graft was finally confirmed by the surgical removal of the graft. The patient characteristics are summarized in Table 1.
Table 1.
Patient characteristics (n = 45)
| Characteristics | Number (%) | |
|---|---|---|
| Age (mean ± SD) | 60.7 ± 14.2 years | |
| Sex | ||
| Male | 27 (60.0%) | |
| Female | 18 (40.0%) | |
| Reason for resection | ||
| Primary bone tumor | 14 (31.1%) | |
| Metastatic tumor | 13 (28.9%) | |
| Radiation-induced necrosis | 7 (15.6%) | |
| BRONJa | 6 (13.3%) | |
| Osteomyelitis | 5 (11.1%) | |
| Reconstruction location | ||
| Mandible | 36 (80.0%) | |
| Maxilla | 9 (20.0%) | |
| Flap type | ||
| FFFb | 31 (68.9%) | |
| DCIAc | 13 (28.9%) | |
| FFF + DCIA | 1 (2.2%) | |
| Number of bone segment | ||
| 3 segments | 3 (6.5%) | |
| 2 segments | 14 (30.4%) | |
| 1 segment | 29 (63.0%) | |
aBRONJ bisphosphonate-related osteonecrosis of the jaw
bFFF fibular free flap
cDCIA deep circumflex iliac artery free flap
Bone SPECT/CT Image Acquisition
The bone scintigraphy and SPECT/CT images of the head and neck regions were obtained at 3–5 h (mean, 3 h and 42 ± 30 min) after the intravenous injection of 740 MBq of 99mTc-DPD or 99mTc-hydroxymethylene-diphosphonate (99mTc-HDP). After obtaining the anterior and posterior planar images, additional regional lateral view images were also obtained in 41 (89%) of 46 planar scintigraphy images, and the subsequent SPECT/CT images were obtained. During the study period, three different dual-head gamma camera system devices were used—Precedence 16 (Philips Healthcare, Best, Netherlands) and Symbia T2 and Symbia Intevo 16 (Siemens Healthcare, Erlangen, Germany). For SPECT image acquisition, the following imaging parameters were used according to the imaging device: Precedence 16 (n = 20), 20 s per projection, 64 projections, 128 × 128 matrix; Symbia T2 (n = 6), 25 s per projection, 64 projections, 128 × 128 matrix; and Symbia Intevo 16 (n = 20), 22 s per projection, 256 × 256 matrix. The CT image acquisition parameters to correct attenuation and image fusion were as follows: helical mode at 120 kVP and 50 mAs with a 2-mm slice thickness in Precedence 16, 130 kVP and 80 mAs with a 2-mm slice thickness in Symbia T2, and 110 kVp and 40 mAs with a 1-mm slice thickness in Symbia Intevo 16. The SPECT images were reconstructed with iterative reconstruction in AutoSPECT+ software and Astonish (Philips Healthcare, Best, Netherlands) with four iterations, 16 subsets, and a Hanning filter with a cutoff frequency of 1.0 in Precedence 16; a Flash three-dimensional (3D) software (Siemens Medical Solutions, Forchheim, Germany) with four iterations, 16 subsets, and smoothing filter 6 in Symbia T2; and a Flash 3D with 24 iterations, two subsets, and smoothing filter 8 in Symbia Intevo 16.
Image Analysis
Two experienced nuclear medicine physicians independently reviewed the bone scintigraphy and SPECT/CT images without clinical information. For the bone planar scintigraphy analysis, bone graft uptake was visually scored by 4 grades in comparison with the homogenous portion of the calvarium as follows: 0 = absence of tracer uptake, 1 = less than calvarium uptake, 2 = similar to calvarium uptake, and 3 = more than calvarium uptake. Representative images are shown in Fig. 1.
Fig. 1.
Representative images of the uptake score of the bone grafts (arrows) on planar bone scintigraphy
The axial, coronal, and sagittal 3D orthogonal views of the fusion SPECT/CT images were reviewed on the dedicated workstation. Furthermore, the uptake intensity of each bone graft segment on SPECT was visually scored by 4 grades in comparison with the calvarium occipital bone, which is similar to bone planar scintigraphy. The uptake intensity of each bone segment was separately assessed if the bone graft was consisted of more than one bone segment on CT images. Representative images of each score are shown in Fig. 2. Discordant scoring between the two reviewers was resolved by consensus.
Fig. 2.
Representative images of the uptake score of the bone graft segments (arrows) on bone SPECT/CT
Results
In five patients, partial or total graft removal was necessary during the follow-up because of graft nonviability. These grafts were removed between 21, 31, 57, 116, and 129 days after reconstructive surgery. The other 40 patients showed uneventful clinical courses after reconstructive surgery.
The uptake intensity scores of 46 bone grafts on the planar bone scintigraphy of 45 patients and the incidence of subsequent graft loss according to the uptake score are summarized in Fig. 3. One patient showed the absence of tracer uptake (score 0) in the bone graft on the planar bone image; eventually, the graft was confirmed as nonviable. Nonviable grafts were also found among the bone grafts with higher score of uptakes on planar bone scintigraphy, even though the incidence decreased with increasing uptake score.
Fig. 3.
Diagram showing the uptake score of vascularized bone grafts on planar bone scintigraphy and the incidence of subsequent graft loss according to the uptake score
The uptake intensity scores of 66 bone graft segments on the bone SPECT/CT of 45 patients and the incidence of subsequent graft segment loss according to the uptake score are summarized in Fig. 4. All 61 graft segments with a score of ≥1 on SPECT/CT were viable and had an uneventful course during follow-up (Fig. 5). On SPECT/CT, five graft segments showed the absence of tracer uptake (score 0); all were confirmed as nonviable grafts on the subsequent surgery. Three graft segments with a score of 0 on SPECT/CT were scored as 2 or 3 on planar images because of the overlapping high uptake of adjacent stump end of the maxilla or mandible (Fig. 6). Table 2 shows the details of five cases with proven nonviable bone grafts. In the visual analysis of bone graft uptake on SPECT, the anatomical CT information from hybrid images was helpful in differentiating uptake by the bone graft segment with that of adjacent stump end of the maxilla or mandible or soft tissues of the surgical bed.
Fig. 4.
Diagram showing the uptake score of vascularized bone graft segments on bone SPECT/CT and the incidence of subsequent graft loss according to the uptake score
Fig. 5.
An 81-year-old woman underwent partial left mandibulectomy and reconstruction with deep circumflex iliac artery free flap because of bisphosphonate-related osteonecrosis of the jaw. The planar bone scintigraphy image (a) obtained 7 days postoperatively shows an increased uptake in the bone graft (score 3, arrow) and focal intensely increased uptake at the stumps of the left mandible. The fusion SPECT/CT image (b) and SPECT image (c) show that the focal increased uptake at the stumps of the left mandible (arrow heads) and bone graft segment (arrow) uptake are similar to calvarium uptake (score 2). She has been clinically followed up for 7 months without any complication, and the bone graft was considered viable
Fig. 6.
A 61-year-old man underwent partial left maxillectomy and reconstruction with deep circumflex iliac artery free flap because of keratoacanthoma. The planar bone scintigraphy image (a) obtained 7 days postoperatively shows that the increased uptake in the left maxillary bone graft is similar to calvarium update (score 2). However, the fusion SPECT/CT image (b) and SPECT image (c) show an increased uptake at the stumps of the left maxilla (arrow head) and soft tissue around the operation bed (arrow), although the bone graft segment area (arrow) shows the absence of tracer uptake (score 0). The graft segment was removed on postoperative day 21 and was confirmed as a nonviable osteonecrosis. Later, reoperation was performed with a fibular free flap
Table 2.
Details of the five cases with nonviable grafts
| No. | Sex/Age | Bone graft location | Flap type | Planar score | SPECT/CT score | Time of graft removal after surgery |
|---|---|---|---|---|---|---|
| 1 | M/54 | Left mandible | FFFa | 0 | 0 | 116 days |
| 2 | F/72 | Right mandible | FFF | 1 | 0 | 31 days |
| 3 | M/61 | Left maxilla | DCIAb | 2 | 0 | 21 days |
| 4 | F/77 | Right mandible | DCIA | 2 | 0 | 129 days |
| 5 | M/56 | Left mandible | DCIA | 3 | 0 | 57 days |
aFFF fibular free flap
bDCIA deep circumflex iliac artery free flap
Discussion
In this study, we evaluated the performance of bone scintigraphy and SPECT/CT in the prediction of vascularized bone graft viability after maxillary or mandibular reconstruction surgery. All graft segments showing the absence of tracer uptake on SPECT/CT images were ultimately confirmed to be nonviable. Therefore, graft failure could be predicted in the absence of tracer uptake in the bone graft on SPECT/CT images. The uptake scores on planar bone scintigraphy and SPECT/CT were mostly inconsistent in nonviable grafts. Using multiple views of planar bone scintigraphy, bone graft uptake could not be differentiated from adjacent bones or soft tissue uptake, especially shortly after surgery, and showed similar or higher uptake than that of calvarium uptake. Three-dimensional orthogonal views with axial, coronal, and sagittal planes using hybrid SPECT/CT images enabled more accurate assessment of uptake on SPECT with additional anatomical information provided by CT. If there was a bone graft without uptake on SPECT/CT, but an increased uptake was seen on planar bone scintigraphy, an intense uptake in the neighboring osteotomy stump or surrounding soft tissues masking bone graft referring to the SPECT/CT image was observed. This signifies the relevance of SPECT/CT. However, accurately differentiating both ends of the bone graft from maxillary or mandibular stump with SPECT image alone is difficult without the additional anatomical information from CT. The SPECT/CT hybrid image was useful in evaluating the graft location, whereas the SPECT image was useful in judging the range and intensity of tracer uptake.
Several studies have demonstrated the use of bone scintigraphy as a reliable tool in monitoring vascularized bone grafts [12–14]. SPECT has been recommended for more accurate tracer uptake assessment in the graft and has shown higher sensitivity in the detection of graft viability after mandibular reconstruction [3, 15–17]. The higher uptake by the bone graft than that by the cranium is usually interpreted as an evidence of bone viability and normal healing. The absence of tracer uptake in scintigraphy is associated with future complications or graft failure [3, 6, 11, 18, 19]. Thus far, no studies have used SPECT/CT hybrid imaging for bone graft viability evaluation after maxillofacial reconstruction surgery.
In our study, most SPECT/CT images showed strong uptake at the end of the bone graft and diffuse uptake across the entire graft. The grafts were considered viable as long as there was an uptake on the vascularized bone graft regardless of whether the uptake degree was high or low. Seven bone graft segments showed lower uptake than that of the calvarium uptake; however, no specific clinical events occurred during the follow-up. Vascularized bone grafts are engrafted through revascularization and graft consolidation [20]. That is, blood supply may not reach the normal bones during the early postoperative period. The vascularized bone graft may show lower uptake than the normal bone (score 1, lower than calvarium uptake) due to insufficient blood supply, although the revascularization, and healing process could develop later and graft survival could be predicted. Therefore, the discrimination between no tracer uptake (score 0) and little tracer uptake (score 1) in the bone graft is critical, and bone SPECT/CT is more advantageous than planar bone scintigraphy by removing other overlapping tissue uptakes. With respect to the anatomical information from CT, identifying the graft structure is challenging if metal artifacts are present in the teeth or facial bones. However, SPECT images are not affected by metal artifacts. Despite SPECT images were corrected attenuation by CT information in the image reconstruction process of hybrid SPECT/CT, metal artifacts could be reduced by iterative algorithms.
This study has several limitations. First, a referral bias could exist owing to the retrospective nature of our study. Of the 59 patients who underwent surgery during the study period, 12 did not undergo SPECT/CT, and as per clinician’s judgment, the patients who were expected to have a good prognosis may not have undergone SPECT/CT. Second, this single-center study has a sample size that is too small to assess viability with satisfactory statistical power and a longer clinical follow-up period may be needed, especially in cases with fewer uptakes by the bone graft than that of the calvarium. Third, three different SPECT/CT imaging devices were used, and three different image acquisition and reconstruction parameters were involved. Therefore, the difference in the quality of SPECT images may affect the qualitative visual assessment of readers. Moreover, we could not perform a quantitative analysis in this retrospective study, although the quantitative analysis may yield more reproducible results for bone viability evaluation [21]. Further prospective studies with larger number of patients and optimal SPECT/CT imaging protocol with quantitative analysis are warranted in the future.
Conclusion
The absence of tracer uptake in the vascularized bone graft on bone SPECT/CT at 1 week after reconstructive surgery can predict graft failure. Bone SPECT/CT can be used to assess vascularized bone graft viability at risk after maxillary or mandibular reconstruction.
Acknowledgment
The authors would like to thank Enago (www.enago.com) for the English language review.
Funding
There is no source of funding
Compliance with Ethical Standards
Conflict of Interest
Hyunji Kim, Koeun Lee, Sejin Ha, Eonwoo Shin, Kang-min Ahn, Jee-Ho Lee, and Jin-Sook Ryu declare that they have no conflicts of interest.
Ethical Approval
All procedures performed in this study involving human participants were in accordance with the ethical standards of the respective Institutional Research Committee and with the 1964 Helsinki Declaration and its later amendments or comparable ethical standards. Formal consent was not required for this type of study.
Informed Consent
The Institutional Review Board at our institute approved this retrospective study, and the requirement to obtain informed consent was waived.
Footnotes
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Jee-Ho Lee and Jin-Sook Ryu contributed equally as corresponding authors.
Contributor Information
Jee-Ho Lee, Email: jeehoman@naver.com.
Jin-Sook Ryu, Email: jsryu2@amc.seoul.kr.
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