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(Radiology. 1999;212:799-802.)
© RSNA, 1999

Nuclear Medicine

Primary and Recurrent Early Stage Laryngeal Cancer: Preliminary Results of 2-[Fluorine 18]fluoro-2-deoxy-D-glucose PET Imaging1

Val J. Lowe, MD, Han Kim, MD, James H. Boyd, MD, John F. Eisenbeis, MD, Frank R. Dunphy, MD and James W. Fletcher, MD

1 From the Departments of Nuclear Medicine (V.J.L., J.W.F.), Radiation Oncology (H.K.), Otolaryngology-Head and Neck Surgery (J.H.B., J.F.E.), and Hematology/Oncology (F.R.D.), PET Imaging Facility, St Louis University Health Sciences Center, 3635 Vista Ave at Grand Blvd, St Louis, MO 63110-0250. From the 1997 RSNA scientific assembly. Received April 15, 1998; revision requested May 29; final revision received December 16; accepted March 16, 1999. Address reprint requests to V.J.L. (e-mail: lowe@nucmed.slu.edu).


   Abstract
TOP
 Abstract
Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
PURPOSE: To evaluate the effectiveness of 2-[fluorine 18]fluoro-2-deoxy-D-glucose (FDG) positron emission tomography (PET) in the identification of early stage (T1–T2) primary and recurrent laryngeal cancer.

MATERIALS AND METHODS: Twelve patients with T1 or T2 laryngeal cancer underwent imaging prospectively with PET. Seven patients had new disease, and five had recurrent disease. All patients underwent imaging prior to planned therapy and tissue biopsy. PET images were evaluated by using standardized uptake ratios and visual analysis.

RESULTS: Histopathologic evidence of early stage cancer was documented in the 12 patients. One had a carcinoma in situ, nine had T1 tumors, and two had T2 tumors. Of the 12 patients, 10 had vocal cord tumors, one had a hypopharyngeal tumor, and one had a preepiglottic tumor. Eleven (92%) patients with early stage cancer had standardized uptake ratios indicative of malignancy (mean, 4.6; SD, 1.8; 95% CI, 1.2; range, 2.8–7.6). One had false-negative results (standardized uptake ratio = 2.3). Nine underwent CT, and results in the larynx were normal in seven and abnormal in two.

CONCLUSION: FDG PET can be used to identify primary and recurrent early stage laryngeal cancer. It may be useful for follow-up after therapy.

Index terms: Emission CT (ECT), comparative studies, 27.12163 • Fluorine, radioactive • Head and neck neoplasms, CT, 27.12115, 27.37 • Head and neck neoplasms, emission CT (ECT), 27.12163, 27.37 • Larynx, neoplasms, 27.37


   Introduction
TOP
 Abstract
 Introduction
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 
Early stage laryngeal cancer (T1–T2; T1, one [a] or both [b] vocal cords involved, with normal vocal cord mobility; T2, extension either above or below the vocal cords, with or without limitation of mobility, and no vocal cord fixation) can be treated with good success by using radiation therapy or surgery. Anatomic computed tomography (CT) is unable to depict the majority of early stage laryngeal lesions, and most lesions are identified with direct visualization. This difficulty in imaging is related to normal variations in the symmetry of the vocal cords, small size of the tumors, oral secretions, and movement. For these reasons, CT is not generally recommended for T1 lesions (1–3). If used, CT is more commonly performed to assess lymph node status in such patients. Moreover, clinical follow-up after therapy can be challenging. Radiation effects such as edema or scarring can make both physical examination and CT difficult.

Cancer cells have increased metabolism and rapid cell proliferation. In the 1930s, malignant cells were shown to have increased glucose metabolism (4). Their increased metabolism can, in part, be related to increased levels of glucose transport protein messenger RNA and glucose transport proteins (5). Because 2-[fluorine 18]fluoro-2-deoxy-D-glucose (FDG) is an analogue of glucose, FDG accumulates at increased rates in highly metabolic, malignant cells (6). After phosphorylation, FDG-6-phosphate does not proceed further in the metabolic pathway and for the most part remains trapped within cells, which allows for positron emission tomographic (PET) imaging. High FDG accumulation is thereby a marker of high metabolic activity.

PET can be used to accurately identify recurrent disease after therapy of advanced stage laryngeal cancer (7–9), but these results may not be applicable to early stage tumors. The small size of T1 or T2 tumors may well make PET imaging challenging in regard to these lesions. If PET can be used to identify early stage laryngeal cancer, PET may be able to provide an accurate means of assessing recurrent or residual disease. We, therefore, evaluated the ability of FDG PET to depict primary or recurrent early stage (T1–T2) laryngeal cancer in this prospective trial in patients with documented early stage disease.


   MATERIALS AND METHODS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 References
 
Patients
Twelve patients (11 men, one woman; age range, 20–77 years; mean age, 52 years ± 16 [SD]) with documented T1 or T2 laryngeal cancer were examined prospectively. Seven patients had new disease, and five had recurrent disease. Of the patients with recurrent disease, the time from the completion of initial radiation therapy until recurrence was between 5 months and 5 years (mean, 21 months). All patients underwent imaging prior to planned therapy. Tissue biopsies of all lesions were performed by means of direct laryngoscopic visualization 6–30 days before PET. CT scans were obtained in most patients (nine of 12) and were also obtained after biopsy was performed (1–27 days). All patients gave informed consent to participate in this protocol. The protocol had been approved by our institutional review board. All patients fasted before the PET study, and a serum glucose value was obtained in each patient.

PET Imaging
FDG PET imaging was performed with use of an ECAT 951/31 PET scanner (Siemens Medical Systems, Hoffman Estates, Ill). This scanner has an axial field of view of 10.8 cm that is composed of 16 bismuth germanate rings that produce 31 transaxial in-plane and cross-plane images. It has an axial resolution of 5.7 mm full width at half maximum from a point source at a 10.0-cm radius from the center and an axial resolution of 4.5 mm full width at half maximum at the center. The scanner has whole-body imaging capability.

The fluorine 18 fluoride was produced with use of an RDS 112 cyclotron (Siemens Medical Systems) that is on-site. The 18F fluoride ions were transferred to an automated system for synthesis of FDG by means of the Hamacher method. The FDG was tested for sterility, pyrogenicity, and radiochemical purity at each production run. No problems with sterility, pyrogenicity, or radiochemical purity occurred.

Transmission scans were obtained in all patients by using a germanium 68 ring source prior to the injection of FDG at 7 minutes per position. Emission images of two bed positions at 10 minutes per position to include the area from the inferior orbit to the upper lung fields were obtained 50 minutes after the intravenous injection of 370 MBq of FDG.

Transmission images were reconstructed with filtered backprojection smoothed by using a Hann filter with a cutoff frequency of 7.0 mm. Emission images were reconstructed with filtered backprojection by using a Hann filter with a cutoff frequency of 5.0 mm. Emission data were corrected for scatter, random events, and dead time losses by using the manufacturer's software.

CT Imaging
CT scans of the neck were obtained with use of a CT/i HiSpeed scanner (GE Medical Systems, Milwaukee, Wis) to include the area from the malar arch to the aortic arch. Iohexol (Omnipaque 350 [100 mL]; Nycomed Amersham, Princeton, NJ) was injected intravenously, and helical imaging was started 30 seconds thereafter with use of 5-mm collimation.

Data Analysis
PET images were evaluated by using the standardized uptake ratio as well as visual interpretation. One circular region of interest was placed on a single image over the region of greatest activity by an experienced nuclear medicine physician (V.J.L.). The regions of interest were placed in abnormalities that were visually apparent on the PET scan in the region of the larynx but that could not be explained by normal uptake. The region of interest was placed in the region of highest uptake and within the borders of the abnormality. As a check of placement and size, the region-of-interest mean activity measurement was confirmed to be about 80% of the maximum activity measurement in the region of interest (10).

Activity concentrations in megabecquerels per milliliter were measured as mean pixel values in the regions of interest. After correction for radioactive decay, the standardized uptake ratio was computed for each lesion identified on the PET scan according to the following formula: standardized uptake ratio equals the average pixel values of region-of-interest activity in megabecquerels per milliliter divided by the injected dose in megabecquerels divided by body weight in grams.

Analysis was performed without knowledge of histopathologic data and the location of the tumor. A standardized uptake ratio greater than 2.5 was considered positive for malignancy (11).

For visual interpretation, the findings considered to be positive for malignancy were focally increased FDG accumulation in the larynx clearly more intense than the background activity in the neck, asymmetry of the abnormality if bilateral, and presence on two adjacent axial image sections. These readings were performed by an experienced nuclear medicine physician (V.J.L.) without knowledge of other clinical or imaging data.

The CT scans were interpreted independently from the PET images, and the dictated impressions as reported were extracted as the results for this study. The interpreting radiologists were not blinded to clinical information. CT images that did not indicate tumor were thereafter re-reviewed by an experienced radiologist in light of the PET and surgical findings.


   RESULTS
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 References
 
Histopathologic evidence of early stage cancer was documented in the 12 patients. One patient had a carcinoma in situ, nine had T1 tumors, and two had T2 tumors. Ten patients had vocal cord tumors, one had a hypopharyngeal tumor, and one had a preepiglottic tumor. Eleven (92%) patients with early stage cancer had standardized uptake ratios indicative of malignancy (mean, 4.6; SD, 1.8; 95% CI, 1.2; range, 2.8–7.6). One patient of five with recurrent disease had false-negative results (standardized uptake ratio = 2.3). Visual interpretation yielded the same results, with the scans considered positive for tumor in 11 patients. The same patient who had the standardized uptake ratio of 2.3 had scans visually interpreted as normal. Examples of T1 and T2 tumors demonstrated at PET are shown in Figures 1 and 2.



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  		Figure 1a. (a) Axial CT and (b) axial PET scans obtained at the same level in a 55-year-old male patient with a T1a squamous cell cancer in the right vocal cord that was a new diagnosis. The CT scan was reported as normal. The PET scan demonstrates hypermetabolism (arrow) indicative of active tumor (standardized uptake ratio = 4.4).

 


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  		Figure 1b. (a) Axial CT and (b) axial PET scans obtained at the same level in a 55-year-old male patient with a T1a squamous cell cancer in the right vocal cord that was a new diagnosis. The CT scan was reported as normal. The PET scan demonstrates hypermetabolism (arrow) indicative of active tumor (standardized uptake ratio = 4.4).

 


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  		Figure 2a. (a) Axial CT and (b) axial PET scans obtained at the same level in a 58-year-old male patient with a T2 squamous cell cancer in the left anterior vocal cord that was a new diagnosis. The CT scan was reported as normal, although in retrospect, there appears to be some asymmetry of the vocal cords in the region of the PET abnormality shown in b. This region may have been thought to be a normal variation on the axial CT scan. The PET scan demonstrates hypermetabolism (arrow) indicative of active tumor (standardized uptake ratio = 7.1).

 


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  		Figure 2b. (a) Axial CT and (b) axial PET scans obtained at the same level in a 58-year-old male patient with a T2 squamous cell cancer in the left anterior vocal cord that was a new diagnosis. The CT scan was reported as normal, although in retrospect, there appears to be some asymmetry of the vocal cords in the region of the PET abnormality shown in b. This region may have been thought to be a normal variation on the axial CT scan. The PET scan demonstrates hypermetabolism (arrow) indicative of active tumor (standardized uptake ratio = 7.1).

 
Nine patients underwent CT, and the results were normal in the larynx in seven. Six of these seven patients with normal CT scans had T1 lesions, and one had a T2 lesion. Two patients had abnormal CT scans. One of these had a T1b right vocal cord tumor and had a CT scan that showed a thickened right cord. The other patient had a T2 left vocal cord lesion that was seen as a mass at CT. Both of these CT scans were in patients with new disease. Retrospective review of the CT scans that did not indicate tumor was performed in light of the histopathologic results and the PET findings. Six of the seven CT scans were available for review. On one of the CT scans in one of the six patients with recurrent disease, fullness was seen in the region of the PET abnormality (Fig 2). In one other patient with new disease, fullness of the right cord was thought to be present. In this patient, the PET scan was negative, and the patient had a left vocal cord tumor. On the four remaining CT scans, no correlative abnormality could be found.


   DISCUSSION
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
References
 
Some 20% of primary early stage laryngeal cancers will fail standard treatment. Early detection of these recurrences is difficult owing to the inherent difficulties in assessing disease with physical examination after therapy. CT does not have good accuracy in depiction of these lesions and is often used to evaluate the possibility of any neck nodal involvement. This is especially true of T1 lesions. A higher percentage of T2 lesions may be identified on CT scans, and some authors (12) advocate the use of CT for pretherapy staging of T2 lesions as some evidence has shown that CT may depict a more advanced stage.

PET imaging has been shown to be sensitive for the detection of head and neck cancer (7–9). We postulated that because there is a smaller volume of soft tissue in the neck as compared with that in the torso, and because laryngeal lesions are central in location, the optimum situation should exist for maximizing PET imaging capabilities. This should allow detection of small lesions in this area. Therefore, in this study we evaluated the ability of PET to depict small, early stage laryngeal cancer.

With this protocol, we studied primary or recurrent early stage laryngeal cancer to determine if PET could depict these lesions. Although other authors have described the use of PET to detect disease in more advanced head and neck cancer, to our knowledge, no work to date has described the use of PET in such small, early stage lesions. In the article by Bailet et al (7), only two patients had laryngeal cancer, and only one of these had early stage disease (T1N0). Anzai et al (8) described 12 patients with head and neck cancer, four of whom had laryngeal cancer, and three of these had undergone prior laryngectomy (ie, not early stage). Austin et al (9) discussed 10 patients with laryngeal cancer who had undergone an organ-salvage protocol of chemotherapy and radiation therapy and likely had stage III or IV disease. Another article (13) describes detection of recurrent laryngeal cancer by means of PET and includes T1–T4 disease.

We thought that data regarding PET detection of primary or recurrent early stage laryngeal cancer would be important. It could lead to future trials of PET in assessing recurrent early stage disease. Such trials could include performance of biopsy and be undertaken even when there may be no other indication to perform biopsy of these small lesions. Because performance of biopsy of the larynx after treatment can result in necrosis, we believed that it would be unethical to subject patients to a potentially harmful biopsy procedure without evidence to support the findings of PET in early stage disease. We, therefore, assessed the use of PET in detecting small primary or recurrent laryngeal lesions in a group that had not undergone therapy or had not undergone recent therapy. In the group studied, PET depicted 92% (11 of 12) of the lesions. One of the lesions was not detected and had a standardized uptake ratio of 2.3, which did not meet the criteria for malignancy.

In comparison, a group of nine of these patients underwent CT imaging, and CT did not depict seven of the nine lesions. Six of the seven were T1 lesions. In retrospect, one of the negative CT scans demonstrated some fullness in the area of the PET abnormality, and this was a T2 lesion (Fig 2).

These data demonstrate for the first time, to our knowledge, that primary or recurrent early stage laryngeal cancers can be detected by means of FDG PET with high sensitivity. Because no patients with benign disease were included in the study, we were not able to determine the specificity of PET for early stage cancer. One could implicate bias in the visual interpretations of the study owing to the fact that patients were referred because they all had documented cancer. For this reason, standardized uptake ratios were also used in the analysis. Further work in pretreatment and posttreatment groups that include patients with benign lesions will need to be performed to assess the accuracy of PET in distinguishing benign from malignant laryngeal disease. Our data show that such work is promising.

All patients underwent biopsy 6–30 days before the PET scans were obtained. It is possible, although we think it unlikely, that performance of biopsy without any complications may cause substantial hypermetabolism. We have subsequently obtained negative PET scans in a few patients after biopsy of the larynx, and in one patient biopsy was performed 3 days before PET. Nevertheless, hypermetabolism from recent performance of biopsy cannot be completely excluded given the methods in our study, and future studies with a healthy control group will need to be performed.

Some published data (14) on posttherapy PET scans have demonstrated substantial hypermetabolism in association with treatment-related inflammatory changes without the presence of residual tumor. Other authors (15) have described relatively few changes with radiation therapy. This issue would need to be considered in any future project concerning the accuracy of PET in assessing the larynx after therapy in cases of early stage cancer.

The findings from this study indicate that PET imaging can be used to identify primary or recurrent early stage laryngeal cancer. This may be helpful in the assessment of primary laryngeal cancer. PET imaging may aid in biopsy guidance when the initial tissue sample is negative. PET may also be useful for differentiating benign from malignant laryngeal lesions, but further work will be needed to document the accuracy of PET in distinguishing benign from malignant disease. PET likely will be unable to aid in further staging of the tumor, as soft-tissue or cartilage invasion will not be factors that PET can be used to assess.

PET may be most useful in assessing the larynx for any residual or recurrent disease after therapy in people with early stage tumors. Prior work performed at our institution has shown that posttherapy PET can be of aid in advanced stage lesions (16). More data will be needed to evaluate the utility of PET in the posttreatment period, but the present study of early stage lesions demonstrates that it has promise: FDG PET can be used to identify primary and recurrent early stage laryngeal cancer and may be useful for follow-up after therapy.


   Acknowledgments
 
The authors wish to thank Penny Yost, CNMT, Sue Paulik, CNMT, Ranajit Bera, PhD, and Rita Gentilcore, MS, of the St Louis University PET Imaging Center for their contributions in performance of the PET imaging and PET radiopharmaceutical production for this study.


   Footnotes
 
V.J.L. is on the speaker's bureau for and has received honoraria from ADAC Laboratories, CTI, GE Medical Systems, and P.E.T. Net.

Abbreviation: FDG = 2-[fluorine 18]fluoro-2-deoxy-D-glucose

Author contributions: Guarantor of integrity of entire study, V.J.L.; study concepts and design, H.K., V.J.L., J.H.B., J.F.E., F.R.D.; definition of intellectual content, H.K., V.J.L., J.H.B., J.F.E., F.R.D.; literature research, V.J.L.; clinical studies, V.J.L.; data acquisition and analysis, V.J.L.; manuscript preparation, V.J.L.; manuscript editing and review, H.K., J.H.B., J.F.E., F.R.D., J.W.F.


   References
TOP
 Abstract
 Introduction
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 References
 

  1. Thabet HM, Sessions DG, Gado MH, Gnepp DA, Harvey JE, Talaat M. Comparison of clinical evaluation and computed tomographic diagnostic accuracy for tumors of the larynx and hypopharynx. Laryngoscope 1996; 106:589-594.[Medline]
  2. Charlin B, Brazeau LL, Guerrier B, Leduc C. Assessment of laryngeal cancer: CT scan versus endoscopy. J Otolaryngol 1989; 18:283-288.[Medline]
  3. Kolbenstvedt A, Charania B, Natvig K, Tausjo J. Computed tomography in T1 carcinoma of the larynx. Acta Radiol 1989; 30:467-469.[Medline]
  4. Warburg O. The metabolism of tumors New York, NY: Smith, 1931; 129.
  5. Flier JS, Mueckler MM, Usher P, Lodish HF. Elevated levels of glucose transport and transporter messenger RNA are induced by ras or src oncogenes. Science 1987; 235:1492-1495.[Abstract/Free Full Text]
  6. Gallagher BM, Fowler JS, Gutterson NI, MacGregor RR, Wan CN, Wolf AP. Metabolic trapping as a principle of radiopharmaceutical design: some factors responsible for the biodistribution of [18F] 2-deoxy-2-fluoro-D-glucose. J Nucl Med 1978; 19:1154-1161.[Abstract/Free Full Text]
  7. Bailet JW, Sercarz JA, Abemayor E, Anzai Y, Lufkin RB, Hoh CK. The use of positron emission tomography for early detection of recurrent head and neck squamous cell carcinoma in postradiotherapy patients. Laryngoscope 1995; 105:135-139.[Medline]
  8. Anzai Y, Carroll WR, Quint DJ, et al. Recurrence of head and neck cancer after surgery or irradiation: prospective comparison of 2-deoxy-2-[F-18]fluoro-D-glucose PET and MR imaging diagnoses. Radiology 1996; 200:135-141.[Abstract/Free Full Text]
  9. Austin JR, Wong FC, Kim EE. Positron emission tomography in the detection of residual laryngeal carcinoma. Otolaryngol Head Neck Surg 1995; 113:404-407.[Medline]
  10. Lowe VJ, DeLong DM, Hoffman JM, Coleman RE. Optimum scanning protocol for FDG-PET evaluation of pulmonary malignancy. J Nucl Med 1995; 36:883-887.[Abstract/Free Full Text]
  11. Lowe VJ, Duhaylongsod FG, Patz EF, et al. Pulmonary abnormalities and PET data analysis: a retrospective study. Radiology 1997; 202:435-439.[Abstract/Free Full Text]
  12. Mukherji SK, Mancuso AA, Mendenhall W, Kotzur IM, Kubilis P. Can pretreatment CT predict local control of T2 glottic carcinomas treated with radiation therapy alone?. AJNR 1995; 16:655-662.[Abstract]
  13. Greven KM, Williams DW, Keyes JJ, McGuirt WF, Watson NJ, Case LD. Can positron emission tomography distinguish tumor recurrence from irradiation sequelae in patients treated for larynx cancer?. Cancer J Sci Am 1997; 3:353-357.[Medline]
  14. Lowe VJ, Hebert ME, Hawk TC, Anscher MS, Coleman RE. Chest wall FDG accumulation in serial FDG-PET images in patients being treated for bronchogenic carcinoma with radiation (abstr). J Nucl Med 1994; 35:76P.
  15. Rege SD, Chaiken L, Hoh CK, et al. Change induced by radiation therapy in FDG uptake in normal and malignant structures of the head and neck: quantitation with PET. Radiology 1993; 189:807-812.[Abstract/Free Full Text]
  16. Lowe V, Dunphy F, Varvares M, et al. Evaluation of chemotherapy response in patients with advanced head and neck cancer using FDG-PET. Head Neck 1997; 19:666-674.[Medline]



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