ACCURACY OF WHOLE-BODY PET AND PET-CT IN INITIAL M STAGING OF HEAD AND NECK CANCER: A META-ANALYSIS

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1 ORIGINAL ARTICLE ACCURACY OF WHOLE-BODY PET AND PET-CT IN INITIAL M STAGING OF HEAD AND NECK CANCER: A META-ANALYSIS Guo-Zeng Xu, MD, Xiao-Dong Zhu, PhD, Ming-Yao Li, MD Department of Radiation Oncology, Cancer Hospital of Guangxi Medical University, Nanning, People s Republic of China. zhuxiaodong1966@yahoo.com.cn Accepted 29 January 2010 Published online 19 May 2010 in Wiley Online Lirary (wileyonlinelibrary.com). DOI: /hed Abstract: Background. A meta-analysis was conducted to evaluate the accuracy of whole-body positron emission tomography (PET) and PET-CT in initial M staging of head and neck cancer. Methods. After a systematic review of English language studies, sensitivity, specificity, and other measures of wholebody PET and PET-CT were pooled. Summary receiver operating characteristic (SROC) curves were also used to summarize overall test performance. Results. Eight PET and 7 PET-CT studies were identified. The pooled sensitivity estimates for PET and PET-CT were (95% confidence interval [CI], ) and (95% CI, ). The pooled specificity estimates were (95% CI, ) and (95% CI, ). The Q* index estimates for PET-CT (0.9409) were not significantly higher than for PET (0.9154; p >.05). Conclusion. Whole-body PET and PET-CT have good diagnostic performance in initial M staging of head and neck cancer; although PET-CT tends to have higher accuracy than PET. VC 2010 Wiley Periodicals, Inc. Head Neck 33: 87 94, 2011 Keywords: head and neck cancer; PET; PET-CT; staging; meta-analysis Head and neck cancer is 1 of the 10 most frequently occurring cancers. 1 As many as 70% of patients with head and neck cancer present with advanced-stage disease at diagnosis. 2 Patients with head and neck cancer have a high propensity for developing distant metastasis and a second primary cancer, with reported incidence rates in the range of 6.1% to 16.3%. 3,4 Distant metastasis usually occurs late during the course of the disease, whereas a second primary cancer may be found even in patients with early-stage disease. 5 Early detection is essential for precise M staging, optimal management, and accurate comparison of protocol efficacies in patients with advanced disease. Head and neck cancers include nasopharyngeal carcinoma, cancers of the nasal cavity and paranasal Correspondence to: X.-D. Zhu VC 2010 Wiley Periodicals, Inc. sinuses, oral cancer, oropharyngeal cancer, hypopharyngeal cancer, laryngeal cancer, to name a few. The skeleton is the most frequent site of metastasis for nasopharyngeal carcinoma, accounting for 70% to 80% of patients with distant metastasis. 6 In contrast, the lung is the most frequent site in patients with other head and neck malignancies, accounting for two thirds of distant metastasis. 7 So conventional workup with chest radiography, abdominal ultrasonography, and skeletal scintigraphy is routinely performed in M staging of nasopharyngeal carcinoma. Although widely available and affordable, this combination has a sensitivity of only 32.8%. 8 The chest CT scan has been the single most important diagnostic technique in M staging of other head and neck malignancies, with a sensitivity and a specificity of 73% and 80%, respectively. 9 More sensitive whole-body imaging techniques are needed to detect distant metastasis and a second primary cancer. Whole-body positron emission tomography (PET) using 18 F-fluorodeoxyglucose has become popular in initial M staging of head and neck cancer in recent years because of its unique capability to image metabolically active lesions. 3,4,8 The integration of PET and CT is expected to provide more anatomic details and allow better correlation of the PET images, which may improve the efficacy of PET in M staging of head and neck cancer. 10 Although many studies on the value of whole-body PET and PET-CT have been done, 3,4,8,10 patient population, imaging techniques, study design, and results vary widely between studies, making it difficult to accurately assess the diagnostic value of PET and PET-CT. We performed a meta-analysis to evaluate whole-body PET and PET- CT for initial M staging of head and neck cancer, and to determine whether integrating PET with CT could improve the diagnostic accuracy of PET alone. MATERIALS AND METHODS Search Strategy and Study Selection. A comprehensive computer search for relevant articles was Whole-Body PET and PET-CT in Staging of Head and Neck Cancer HEAD & NECK DOI /hed January

2 conducted in MEDLINE, EMBASE, and the Cochrane Database of Systematic Review from January 1, 2000, to September 31, The search strategy was based on the combination of the terms (1) PET; (2) head and neck cancer, oral cancer, oropharynx cancer, hypopharynx cancer, larynx cancer, or nasopharyngeal cancer; (3) staging or distant metastasis; and (4) sensitivity, specificity, false-negative, or false-positive. Although no language restrictions were imposed initially, the full-text review and final analysis was limited to articles published in the English language. Conference abstracts and letters to the journal editors were excluded because they contained limited data. Reference lists were manually screened for additional relevant articles. Two reviewers (G.-Z.X. and M.-Y.L.) independently judged study eligibility. Disagreements were resolved by consensus. The inclusion criteria still included: (1) wholebody PET or PET-CT was used to detect distant metastasis and a second primary cancer in M staging of head and neck cancer; (2) histopathologic analysis and/or clinical and imaging follow-up were used as the reference standard; (3) only studies from which a 2 2 table could be constructed for true-positive, false-negative, false-positive, and true-negative values were included; (4) the studies were based on per patient statistic; (5) when data or subsets of data were presented in more than 1 article, the article with the most details or the most recent article was chosen; (6) the studies including at least 10 patients were selected for inclusion in the study, since very small studies may be vulnerable to selection bias; and (7) no article about patients with M 0 carcinoma by conventional imaging techniques was included. Data Extraction and Quality Assessment. Two reviewers (G.-Z.X. and M.-Y.L.) independently extracted the relevant data from each article and recorded them on a standardized form. Disagreements were resolved by consensus. Reviewers were not blinded with regard to information about the journal name, the authors, the authors affiliation, or year of publication, since this has been shown to be unnecessary. 11 In addition, for each study the following information was noted: (1) year of publication and origin; (2) sample size; (3) age distribution of study population; (4) reference standard tests; and (5) imaging details: imaging system (PET or PET-CT), methods of analysis (qualitative or quantitative or both), and number of experts interpreting the images. We assessed the methodologic quality of the studies using the quality assessment for studies of diagnostic accuracy (QUADAS) tool. 12 It is the first systematically developed evidence-based quality assessment tool to be used in systematic reviews of diagnostic accuracy studies. In addition, for each study, the following design criterias were also assessed: cross-sectional design (vs case-control design); and prospective data collection. Statistical Analysis. The analysis was based on summary receiver operating characteristic (SROC) curves. 13,14 The sensitivity and specificity for each study were used to plot SROC curves. 14,15 The degree of heterogeneity among different studies was reported using the Cochran chi-square statistic. When there was no heterogeneity observed (p >.05), a fixed-effect model was used to calculate pooled sensitivity, specificity, diagnostic odds ratio, positive likelihood ratio, and negative likelihood ratio for whole-body PET and PET-CT, respectively. In case heterogeneity was observed (p <.05), a random-effect model was applied. We also calculated SROC curves and the Q* index. (Q* index is the best statistical method to reflect the diagnostic value. It is defined by the point where sensitivity and specificity are equal, which is the point closest to the ideal top-left corner of the SROC space.) 16 A Z-test was performed to determine whether the Q* index of PET-CT was significantly different from that of PET. All analyses were performed using Meta-DiSc, version 1.4 (XI Cochrane Colloquium; Barcelona, Spain) 16 and Stata, version 9.0 (Stata Corporation, College Station, TX). RESULTS Study Selection and Description. After independent review, 29 publications dealing with whole-body fluorodeoxyglucose-pet or PET-CT for initial M staging of head andneckcancerwereconsideredtobeeligibleforinclusion in the analysis. 3,4,8,10,17 41 Of these publications, 11 articles were excluded because too little data were reported to permit construction of a 2 2tableoftruepositive, false-negative, false-positive, and true-negative values. Two articles 28,29 were excluded because the imaging data were not presented on a per patient basis but instead on a per site basis. Two articles 30,31 were excluded because they were about patients with carcinoma staged as M 0 by conventional imaging techniques. One article 32 was excluded because whole-body PET was not used. One article 33 was excluded because the data were already reported in an included article. 38 Consequently, 12 articles 3,4,8,10,34 41 met our inclusion criteria and were selected, including 7 PET-CT studies (797 patients) and 8 PET studies (795 patients). A total of 209 of 1445 eligible patients (14.4%) in the selected studies had distant metastasis or a second primary cancer. Tables 1 and 2 show the clinical characteristics and diagnostic accuracy of wholebody PET-CT and PET in the selected studies. Study Quality and Design. Seven PET 3,4,8,10,34,35,37 and 7 PET-CT 3,10,35,36,39 41 studies responded yes to 12 of 14 questions in the QUADAS quality assessment tool. And only 1 study 38 responded yes to 11 of Whole-Body PET and PET-CT in Staging of Head and Neck Cancer HEAD & NECK DOI /hed January 2011

3 Table 1. Clinical characteristics for selected studies. Study Origin No. of patients Age, y Male, % DM, or SPC*, % Execution for reference standard Thadoros, USA Histopathologic analysis or close 24 mo Chan, Taiwan Histopathologic analysis or close at least 6 mo Veit-Haibach, Germany Histopathologic analysis or close 407 d (mean) Kim, Korea Histopathologic analysis or close at least 6 mo Liu, Taiwan 300 <40y: Histopathologic analysis or close 40 60y:183 >60y:62 12 mo Gourin, USA 27 <50y: Histopathologic analysis or close >50y:22 at least 12 mo Ng, Taiwan Histopathologic analysis or close at least 12 mo Krabbe, Netherland 149 Mean: Histopathologic analysis or close at least 6 mo Ng, Taiwan Histopathologic analysis or close 12 mo Keisuke, Japan Histopathologic analysis or close at least 9 mo Ng, Taiwan Histopathologic analysis or close at least 12 mo Chua, Singapore 78 <35y: Histopathologic analysis or close * Distant metastasis or a second primary cancer y:62 >64y:10 at least 6 mo questions, in which the execution of PET interpretation was not described in sufficient detail to permit its replication (6.7% for no responses to question 8). All studies had a suboptimal design in regard to the examination with the same reference standard (100% for no responses to question 6), and the interpretation of the reference standard results without knowledge of the index test results (100% for no responses to question 11). Actually, it is impossible to perform an ideal study in clinical practice. All studies had cross-sectional design. In 4 4,8,10,34 of 8 PET studies (50.0%) and 4 10,39 41 of 7 PET-CT studies (57.1%), the study design was prospective. Diagnostic Accuracy. Figure 1 shows the forest plot of sensitivity and specificity of whole-body PET for initial M staging of head and neck cancer. The chisquare values of sensitivity, specificity, diagnostic odds ratio, positive likelihood ratio, and negative likelihood ratio were 7.12 (p ¼.417 >.05), 4.46 (p ¼.725 >.05), 2.48 (p ¼.929 >.05), 3.67 (p ¼.817 >.05), and 2.59 (p ¼.920 >.05), respectively, indicating a significant homogeneity for sensitivity, specificity, diagnostic odds ratio, positive likelihood ratio, and negative likelihood ratio between studies. The pooled sensitivity, specificity and diagnostic odds ratio, positive likelihood ratio, and negative likelihood ratio with 95% of confidence interval (CI) of whole-body PET were ( ), ( ), ( ), ( ), and ( ), respectively. Figure 2 shows the forest plot of sensitivity and specificity for whole-body PET-CT in initial M staging of head and neck cancer. The chi-square values of sensitivity, specificity, diagnostic odds ratio, positive likelihood ratio, and negative likelihood ratio were (p ¼.088 >.05), 9.18 (p ¼.164 >.05), 2.99 (p ¼.810 >.05), 5.07 (p ¼.535 >.05), and 7.93 (p ¼.243 >.05), respectively, indicating a significant homogeneity for sensitivity, specificity, diagnostic odds ratio, positive likelihood ratio, and negative likelihood ratio between studies. The pooled sensitivity, specificity, diagnostic odds ratio, positive likelihood ratio, and Whole-Body PET and PET-CT in Staging of Head and Neck Cancer HEAD & NECK DOI /hed January

4 Table 2. Results of PET and PET-CT in M staging of head and neck cancer. Study Imaging tools Method of imaging analysis No. of interpretation experts Evidence level No. of segments TP FP TN FN Thadoros, PET Qualitative 1 Ib Chan, PET Both qualitative and quantitative 1 Ib PET-CT Veit-Haibach, PET Both qualitative and quantitative 2 Ib PET-CT Kim, PET-CT Qualitative No. of Interpretation Experts:1 Ib Liu, PET Unclear 3 Ib Gourin, PET Qualitative 1 Ib Ng, PET Qualitative 3 Ib Krabbe, PET Unclear Unclear Ib Ng, PET-CT Qualitative 2 Ib Keisuke, PET-CT Qualitative 2 Ib Ng, PET-CT Qualitative 3 Ib Chua, PET Unclear 1 Ib PET-CT Abbreviations: PET, positron emission tomography; TP, true-positive; FP, false-positive; FN, false-negative; TN, true-negative. negative likelihood ratio with 95% of CI were ( ), ( ), ( ), ( ), and ( ), respectively. Unlike a traditional ROC plot that explores the effect of varying thresholds on sensitivity and specificity in a single study, each data point in the SROC plot represents a separate study. The SROC curve presents a global summary of test performance, and shows the tradeoff between sensitivity and specificity. The SROC curves and the Q* index of whole-body PET and PET- CT in initial M staging of head and neck cancer are FIGURE 1. Forest plot of sensitivity and specificity of whole-body positron emission tomography (PET) for initial M staging of head and neck cancer. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] 90 Whole-Body PET and PET-CT in Staging of Head and Neck Cancer HEAD & NECK DOI /hed January 2011

5 FIGURE 2. The forest plot of sensitivity and specificity of whole-body positron emission tomography (PET)-CT for initial M staging of head and neck cancer. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] shown in Figure 3. The Q* index estimates for PET-CT (0.9409) were not significantly higher than for PET (0.9154; Z ¼ 0.76; p >.05). DISCUSSION The presence of distant metastases is the most important predictor of patient survival in most cancers. FIGURE 3. A and B, The summary receiver operating characteristic (SROC) curves and the Q* index of whole-body positron emission tomography (PET) and PET-CT for initial M staging of head and neck cancer. [Color figure can be viewed in the online issue, which is available at wileyonlinelibrary.com.] Whole-Body PET and PET-CT in Staging of Head and Neck Cancer HEAD & NECK DOI /hed January

6 Our meta-analysis suggested that 209 (14.4%) of 1445 eligible patients in the selected studies had distant metastasis or a second primary cancer. A fast, accurate, reliable diagnostic workup before initial treatment is of the utmost importance because of its impact on treatment and prognosis. Differences in tissue tropism between metastases of nasopharyngeal carcinoma and other head and neck malignancies determine which conventional imaging techniques are recommended for their initial M staging. Although conventional workup has important limitations, it is routinely performed in M staging of nasopharyngeal carcinoma, and CT of the thorax is also not generally recommended for nasopharyngeal carcinoma because of its very low yield. 42 Whole-body PET and PET-CT were found to be more effective than conventional workup. 3,39 Because the most frequent distant-site is the lung, CT of the thorax has been the single-most important diagnostic technique in M staging of other head and neck malignancies, with a sensitivity and a specificity of 73% and 80%, respectively. 9 Liver function tests and abdominal CT scanning show low sensitivity for detection of extrapulmonary disease, with most findings being nonspecific and of questionable utility. 43,44 Whole-body PET was found to be more effective than CT of the thorax or CT of the thorax and abdomen. 4,37 In the present meta-analysis, the pooled sensitivity with 95% of CI (0.848 [ ] and [ ]) and pooled specificity (0.952 [ ] and [ ]) indicated that whole-body PET and PET-CT had a very high accuracy. The diagnostic odds ratio is a single indicator of test accuracy that combines the data from sensitivity and specificity into a single number. 45 It is the ratio of the odds of a positive test in a patient with disease relative to the odds of a positive test in a patient without disease and has a value that ranges from 0 to infinity, with higher values indicating better discriminatory test performance (ie, higher accuracy). A value of 1.0 indicates that the test does not discriminate between patients with the disorder and those without it. In the present meta-analysis, the pooled diagnostic odds ratio for whole-body PET and PET-CT was and , respectively, indicating a high level of accuracy. Because the SROC curve and the diagnostic odds ratio are not easy to interpret and use in clinical practice, 46 and because likelihood ratios are considered to be more clinically meaningful, 46,47 both positive likelihood ratio and negative likelihood ratio were calculated and served as our measures of diagnostic accuracy. Likelihood ratios of >10 or <0.1 generate large and often conclusive shifts from pretest to posttest probability (indicating high accuracy). A positive likelihood ratio value of for PET suggests that patients with distant metastasis or a second primary cancer have an approximately 17.4-fold higher chance of positive PET findings than do patients without these. A positive likelihood ratio value of for PET-CT suggests that the chance of having a true-positive PET-CT examination is approximately 16.4-fold higher in patients with distant metastasis or a second primary cancer than in patients without these. This value ( or ) is, therefore, high enough to diagnose distant metastasis or a second primary cancer. On the other hand, negative likelihood ratio for PET and PET-CT was found to be and 0.141, respectively. If the examination result of PET or PET-CT is negative, the probability that this patient has distant metastasis or a second primary cancer is 17.0% or 14.1%, respectively. These data suggest that a negative examination result of PET or PET-CT could not be used alone as a justification to rule out distant metastasis or a second primary cancer. The integration of PET and CT is expected to provide more anatomic details and allow better correlation of the PET images, which may improve the efficacy of PET in M staging of head and neck cancer. 10 In the present meta-analysis, the Q* index estimates for whole-body PET-CT and PET were and (Z ¼ 0.76; p >.05), respectively, indicating that integrating PET with CT may not obviously improve the diagnostic accuracy than PET alone. Certainly, this result may be affected by variations in patient population, imaging techniques, study design, and quality between studies. Whole-body MRI, particularly with the introduction of moving patient platforms, improved integrated surface-coil technology, and ultrafast data acquisition has become clinically feasible for the assessment of M staging of tumors. 48 Notably, 3.0T whole-body MRI and PET-CT for M staging of head and neck cancer showed similar sensitivity (77.8% vs 72.2%; p >.05), specificity (98.5% vs 97.7%; p >.05), and diagnostic capability (0.905 vs 0.878; p >.05), 40 indicating that 3.0T wholebody MRI could also be used as a first-line imaging technique for M staging of head and neck cancer. Our meta-analysis had several limitations. First, the exclusion of conference abstracts, letters to the editors, and non English-language studies may have led to publication bias. Publication bias can be tested by using funnel plots. In the present meta-analysis, funnel plot analysis was not performed because the limited number of included studies could have decreased the power of detection publication bias. Second, a wide variation in patient population, imaging techniques, study design, and quality in these selected studies may have affected the estimates of diagnostic accuracy of whole-body PET and PET-CT. This was not analyzed because the number of included studies was small. Third, the shortest following time varied widely (6 24 months) and there was no single clinical and imaging follow-up strategy. These factors may also have affected the accuracy of whole-body PET and PET-CT. In conclusion, current evidence suggests that whole-body PET-CT and PET have good diagnostic 92 Whole-Body PET and PET-CT in Staging of Head and Neck Cancer HEAD & NECK DOI /hed January 2011

7 performance in M staging of head and neck cancer; and PET-CT tends to have higher accuracy than PET. Acknowledgment. The authors thank Dr. Zhi- Yi He from the Institute of Respiratory Diseases, First Affiliated Hospital, Guangxi Medical University, Nanning, China, for critical review and correction of the manuscript. REFERENCES 1. Jemal A, Murray T, Ward E, et al. Cancer statistics, CA Cancer J Clin 2005;55: Hoffman HT, Karnell LH, Funk GF, Robinson RA, Menck HR. The National Cancer Data Base report on cancer of the head and neck. Arch Otolaryngol Head Neck Surg 1998;124: Veit-Haibach P, Luczak C, Wanke I, et al. TNM staging with FDG-PET/CT in patients with primary head and neck cancer. Eur J Nucl Med Mol Imaging 2007;34: Ng SH, Chan SC, Liao CT, et al. Distant metastases and synchronous second primary tumors in patients with newly diagnosed oropharyngeal and hypopharyngeal carcinomas: evaluation of (18)F-FDG PET and extended-field multi-detector row CT. 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8 40. Ng SH, Chan SC, Yen TC, et al. Pretreatment evaluation of distant-site status in patients with nasopharyngeal carcinoma: accuracy of whole-body MRI at 3-tesla and FDG-PET-CT. Eur Radiol [Epub ahead of print]. 41. Yoshida K, Suzuki A, Nagashima T, et al. Staging primary head and neck cancers with (18)F-FDG PET/CT: is intravenous contrast administration really necessary? Eur J Nucl Med Mol Imaging 2009;36: Leung S, Cheung H, Teo P, Lam WW. Staging computed tomography of the thorax for nasopharyngeal carcinoma. Head Neck 2000;22: de Bree R, Deurloo EE, Snow GB, Leemans CR. Screening for distant metastases in patients with head and neck cancer. Laryngoscope 2000;110(3 Pt 1): Keski-Säntti HT, Markkola AT, Mäkitie AA, Bäck LJ, Atula TS. CT of the chest and abdomen in patients with newly diagnosed head and neck squamous cell carcinoma. Head Neck 2005; 27: Glas AS, Lijmer JG, Prins MH, Bonsel GJ, Bossuyt PM. The diagnostic odds ratio: a single indicator of test performance. J Clin Epidemiol 2003;56: Deeks JJ. Systematic reviews of evaluations of diagnostic and screening tests. In: Egger M, Smith GD, Altman DG, editors. Systematic reviews in health care: meta-analysis in context. London, UK: BMJ Publishing Group, pp Jaeschke R, Guyatt G, Lijmer J. Diagnostic tests. In: Guyatt G, Rennie D, editors. Users guides to the medical literature: a manual for evidence-based clinical practice. Illinois: AMA Press; pp Lauenstein TC, Goehde SC, Herborn CU, et al. Whole-body MR imaging: evaluation of patients for metastases. Radiology 2004; 233: Whole-Body PET and PET-CT in Staging of Head and Neck Cancer HEAD & NECK DOI /hed January 2011

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