Annals of Nuclear Medicine

, Volume 23, Issue 3, pp 269–275 | Cite as

Relationship between maximum standardized uptake value (SUVmax) of lung cancer and lymph node metastasis on FDG-PET

  • Atsushi Nambu
  • Satoshi Kato
  • Yoko Sato
  • Hideto Okuwaki
  • Keiichi Nishikawa
  • Akitoshi Saito
  • Keiko Matsumoto
  • Tomoaki Ichikawa
  • Tsutomu Araki
Original Article

Abstract

Purpose

To evaluate the relationship between SUVmax of primary lung cancers on FDG-PET and lymph node metastasis.

Method and materials

The subjects were a total of consecutive 66 patients with lung cancer who were examined by FDG-PET and subsequently underwent surgery between October 2004 and January 2008. There were 41 males and 25 females, ranging in age from 45 to 83 years with an average of 68 years. The pathological subtypes of the lung cancers consisted of 49 adenocarcinomas, 11 squamous cell carcinomas, 2 adenosquamous carcinoma, 1 large cell carcinoma, 1 small cell carcinoma, 1 pleomorphic carcinoma and 1 mucoepidermoid carcinoma. We statistically compared (1) the mean SUVmax of lung cancer between the groups with and without lymph node metastasis (2) the frequency of lymph node metastasis between higher and lower SUVmax of lung cancer groups that were classified by using the median SUVmax of lung cancer, and (3) evaluated the relationship between the SUVmax of lung cancer and frequency of lymph node metastases, and (4) correlations between the SUVmax of lung cancer and number of the metastatic lymph nodes and pathological n stages.

Results

The difference in the average of the SUVmax of lung cancer between the cases with and without lymph node metastases was statistically significant (p = 0.00513). Lymph node metastasis was more frequently seen in the higher SUVmax of lung cancer group (17/33, 52%) than in the lower SUVmax of lung cancer group (7/33, 21%) with a statistically significant difference. There was no lymph node metastasis in lung cancers with an SUVmax of lung cancer less than 2.5, and lung cancers with an SUVmax of lung cancer more than 12 had a 70% frequency of lymph node metastasis. There were moderate correlations between SUVmax of lung cancer, and the number of the metastatic lymph nodes (γ = 0.404, p = 0.001) and pathological n stage (γ = 0.411, p = 0.001).

Conclusions

The likelihood of lymph node metastasis increases with an increase of the SUV of a primary lung cancer.

Keywords

SUV FDG-PET Lung cancer N-staging Lymph node 

Introduction

The evaluation of lymph node metastasis (N-staging) in patients with lung cancer is critical because it largely affects the choice of treatment; surgery is the standard treatment in limited disease while surgery is not appropriate for advanced disease. Furthermore, stereotactic radiotherapy (SRT) has been recently emerging as a new alternative treatment for lung cancer without lymph node metastasis, and yields a good local control rate and 5-year survival rate comparable to those of surgery[1, 2]. In SRT, only the lung tumor is irradiated and therefore the evaluation of lymph node metastasis is even more critical.

Fluorine-18-Fluoro-2-deoxy-D-glucose positron emission tomography (FDG-PET) has become widely used in the clinical practice of lung cancer and is already an indispensable modality for the evaluation of lymph node or distant metastasis. Many reports suggested that FDG-PET was superior to CT in accuracy of N-staging for lung cancer [3, 4, 5, 6, 7, 8, 9, 10] and therefore FDG-PET is now regarded as the most accurate imaging modality in N-staging of lung cancer. However, it has also been shown that there are a significant number of false negative and false positive findings on FDG-PET in the evaluation of lung cancer, including N-staging [10, 11, 12, 13, 14]. The major reasons of the false negative and false positive findings in N-staging are microscopic metastasis beyond the spatial resolution of FDG-PET and lymph node involvement by an underlying inflammatory disease, such as tuberculosis, or lymphadenopathy secondary to obstructive pneumonia or immune reaction due to the presence of lung tumor [10, 11, 12, 13, 14]. The ability of FDG-PET by direct assessment of each lymph node station is inherently limited and, therefore, we needed another approach to achieve a better accuracy of N-staging of lung cancer.

Standardized uptake value (SUVmax) is a well-known measure indicating the disease activity or the aggressiveness of tumor [15, 16, 17, 18]. We thought that if SUV correlates with the likelihood of lymph node metastasis, the accuracy of N-staging in lung cancer might be improved by considering the SUVmax of the lung cancer into the interpretations of FDG-PET. Thus, our purpose in this study was to evaluate the relationship between SUVmax of lung cancer on FDG-PET and lymph node metastasis.

Materials and methods

Study population

Our institutional review board does not require its approval for a retrospective study obtained with routine clinical data. Patient informed consent was not required either.

The subjects were a total of consecutive 66 patients with lung cancer who were examined by FDG-PET and subsequently underwent surgery between October 2004 and January 2008. There were 41 males and 25 females, ranging in age from 45 to 83 years old with an average of 68 years. The pathological subtypes of the lung cancers consisted of 49 adenocarcinomas, 11 squamous cell carcinomas, 2 adenosquamous carcinoma, 1 large cell carcinoma, 1 small cell carcinoma, 1 pleomorphic carcinoma and 1 mucoepidermoid carcinoma.

Methods of FDG-PET

FDG-PET was carried out with Biograph LSO DUO (Siemens, Germany) in all cases within one month before the surgery. This was an integrated PET/CT machine. All patients fasted for at least 6 h before FDG-PET. After confirmation of a normal blood glucose level (less than 150 mg/dl) in peripheral blood, the patients received an intravenous injection of 3.0 MBq/kg of FDG and thereafter rested for 60 min before the scan.

The CT scan in PET/CT was performed from the head to the pelvis with the following scan parameters: electric current of 200–300 mA, peak voltage of 120–140 kv, x-ray tube rotation time of 0.5 s, a slice pitch of 9, and slice thickness of 2.5 mm. No contrast material was used. Immediately after this CT scan, PET was performed with the same field of view. The acquisition time for PET was 2 min per table position. The CT data were converted from 512 × 512 matrixes to 128 × 128 matrixes to match the PET data, by which the images of both examinations could be fused. PET data were reconstructed with an ordered subsets expectation maximization algorithm and attenuation correction was done with the CT data. Coregistered scans were displayed by e-soft-PET software (Siemens, Germany).

SUVmax of the primary tumor was calculated by the following formula in all cases.
$$ {\text{SUVmax}} = {\text{maximum tissue concentration}}({\text{MBq}}/{\text{g}})/[{\text{injected dose (MBq)}}/{\text{body weight (g)}}] $$

The maximum tissue concentration was represented by the counts per second of the voxel showing the maximum radioactivity in the volume of interest encompassing the tumor divided by the volume (milliliters).

Methods of surgery and pathological examination

The surgical methods generally consisted of lobectomy of the affected lobe and lymph node dissection of the ipsilateral pulmonary hilum and mediastinum. The pathological investigations of the resected lymph nodes were done at one section of their central portions. The presence or absence of lymph node metastasis was determined by the pathologists in our institution. We used the results that were described on the medical records as the standard of reference.

Methods of the evaluations and data analysis

We statistically compared (1) the mean SUVmax of lung cancer between the groups with and without lymph node metastases (2) the frequency of lymph node metastasis between higher and lower SUVmax of lung cancer groups that were classified by using the median SUVmax, and (3) evaluated the relationships between the SUVmax of lung cancer and frequencies of lymph node metastasis, and (4) correlations between the SUVmax of lung cancer and number of the metastatic lymph nodes and pathological n stages. Additionally, we investigated the relationship between SUVmax of lung cancer and the pathological subtype. Statistical analysis was done using SPSS software Ver.16. The difference in the mean SUVmax was compared using unpaired t-test. The difference in the frequency of lymph node metastasis was compared using Fisher’s exact test. Spearman’s rank correlation coefficient was used to evaluate the correlations. A p value less than 0.05 was considered significant.

Sensitivity, specificity and accuracy in N-staging of FDG-PET were also calculated on a per-patient basis. We retrospectively evaluated the lymph node stations that were surgically dissected for the presence or absence of lymph node metastasis using the criterion that the SUVmax of 2.5 or more was considered metastatic. The CT scans in the PET/CT were used to localize each lymph node station. The pathological results were used as the standard of reference. These results were compared with those when the criteria for lymph node metastasis were modified by using the SUVmax of the lung cancers.

Results

The extent of lymph node metastasis

Lymph node metastasis was pathologically proven in 24 of 66 cases (36%), consisting of 14 n1 cases (hilar or intrapulmonary lymph node metastasis) and 10 n2 cases (ipsilateral mediastinal lymph node metastasis with or without hilar or intrapulmonary lymph node metastasis).

Range of SUVmax

The SUVmax ranged from 0.37 to 28.41 with an average of 6.17. The median was 4.83, which was the average between two middle values, 4.75 and 4.91. Thus, the lower SUV group ranged from 0.37 to 4.75 and the higher SUV group ranged from 4.91 to 28.41.

Comparison of the mean SUVmax between the groups with and without lymph node metastases

In cases with lymph node metastases, the SUVmax ranged from 2.58 to 21.10 with an average of 8.70. In cases without lymph node metastasis, the SUVmax ranged from 0.37 to 28.41 with an average of 4.72. The difference in the average of the SUVmax between the cases with and without lymph node metastasis was statistically significant (p = 0.00513) (Fig. 1).
Fig. 1

Scattergram of SUVmax of lung cancer in the groups with and without lymph node metastasis. There is considerable overlap in SUVmax between the groups with and without lymph node metastasis. However, in the group with lymph node metastasis, no case shows an SUVmax less than 2.5

The frequency of lymph node metastasis between higher and lower SUV groups

The frequencies of lymph node metastasis were 21% (7/33) in the lower SUV group and 52% (17/33) in the higher SUV group. The difference was statistically significant (p = 0.02) (Table 1).
Table 1

Frequency of lymph node metastasis in the higher and lower SUVmax of lung cancer groupa

 

Lower SUVmax of lung cancer group (n = 33)

Higher SUVmax of lung cancer group (n = 33)

Metastasis positive

7 (21)b

17 (52)

Metastasis negative

26 (79)

16 (48)

The difference of frequency of lymph node metastasis between the lower and higher SUV max of lung cancer groups is statistically significant (p < 0.05, Fisher’s exact test)

aThese two groups were divided by the median SUVmax of lung cancer

bNumbers in the parentheses are percentages

Relationship between the SUVmax and frequency of lymph node metastasis

There was no lymph node metastasis in cases with a SUVmax less than 2.5 (0/20) (Fig. 2), whereas cases with a SUVmax 12 or more had lymph node metastasis in 70%(7/10) (Fig. 3). The remaining cases with a SUV ranging from 2.5 or more to less than 12 had lymph node metastasis in 47% (17/36) (Table 2).
Fig. 2

An 82-year-old male with lung adenocarcinoma with mixed subtypes (bronchioloalveolar carcinoma + papillary type), a case with low SUVmax of the lung cancer and increased accumulation of FDG into a lymph node station. a Thin-section CT shows a focal area of ground-glass opacity with a solid area in the left lower lobe. b A fusion image of PET-CT at the level of the tumor shows faint accumulation of FDG into the tumor. The SUVmax was 1.54. c A fusion image of PET-CT through the subaortic region shows an increased accumulation of the left tracheobronchial lymph node. The SUVmax of the lymph node was 2.58. According to the criterion of our institution, this lymph node was judged to be metastatic. However, given the low SUVmax of the lung cancer, this patient is unlikely to have lymph node metastasis. This lymph node was confirmed to be negative for metastasis on the pathological examination

Fig. 3

A 73-year-old male with pleomorphic carcinoma, a case with high SUVmax of the lung cancer and no increased accumulation of FDG into the lymph node stations. a Enhanced CT with mediastinal window through the level of the lung cancer shows an inhomogeneously enhanced mass at the subpleural region of the right lower lobe (asterisk). A triangular soft tissue density is also seen at the region between the right middle and lower bronchus (arrow). b A fusion image of PET-CT through the tumor demonstrates a strong accumulation of the lung cancer with an SUVmax of 17.48. The SUVmax of the right hilar lymph node was 1.28 (arrow), which was judged to be negative for metastasis. However, given the high SUVmax of the lung cancer, this patient is more likely to have lymph node metastasis although we cannot know which lymph node station is affected. This pulmonary hilar lymph node was positive for metastasis on the pathological examination

Table 2

Relationship between SUV max of lung cancer and frequency of lymph node metastasis

Range of SUV max of lung cancer

Frequency of lymph node metastasis

2.5>

0/20 (0)a

2.5≦, 12>

17/36 (47)

12≦

7/10 (70)

aNumbers in the parentheses are percentages

Correlations between the SUVmaxs and, number of the metastatic lymph nodes and pathological n stages

There were moderate correlations between SUVmax, and the number of lymph node metastasis (γ = 0.404, p = 0.001) and pathological n stage (γ = 0.411, p = 0.001) (Figs. 4, 5).
Fig. 4

Correlation between the SUVmax of lung cancer and number of metastatic lymph nodes

Fig. 5

Correlation between the SUVmax of lung cancer and pathological n stage

Relationship between SUVmax of lung cancer and the pathological subtype

The frequencies of lymph node metastasis were 31% (15/49) in adenocarcinoma (8 n1 cases and 7 n2 cases), 27% (3/11) in squamous cell carcinoma (2 n1 cases and 1 n2 case), 100% (2/2) in adenosquamous carcinoma (1 n1 case and 1 n2 case), 100% (1/1) in pleomorphic carcinoma (n1), 100% (1/1) in small cell carcinoma (n1), 100% (1/1) in large cell carcinoma (n2) and 100% (1/1) in mucoepidermoid carcinoma (n1). There was no statistically significant difference in the frequency of lymph node metastasis between adenocarcinoma and squamous cell carcinoma (p = 0.827).

SUVmax ranged from 0.37 to 28.41 with a mean of 5.03 in adenocarcinoma and from 2.46 to 19.08 with a mean of 9.39 in squamous cell carcinoma. The difference in mean SUVmax was statistically significant (p = 0.019).

The data in the lung cancers other than adenocarcinoma and squamous cell carcinoma were not calculated because the number of cases was too small for the statistical analysis.

Sensitivity, specificity and accuracy of N-staging on FDG-PET on a per-patient basis

When the SUVmax of 2.5 or more was used as the criterion of the presence of lymph node metastasis at each lymph node station, sensitivity, specificity and accuracy were 57, 80 and 68%, respectively. If we devised the criteria of lymph node metastasis, incorporating the SUVmax of the primary tumors, as follows; when the SUVmax of the primary tumor was less than 2.5, lymph node metastasis was considered absent disregarding the SUVmax of each lymph node station and when the SUVmax of the primary tumor was more than 12, lymph node metastasis was considered present disregarding the SUVmax of each lymph node station, and only when the SUVmax of the primary tumor ranged from 2.5 to 12, the presence of lymph node metastasis was evaluated for each lymph node station using the cutoff SUVmax of 2.5, sensitivity, specificity and accuracy became 67, 76 and 73%, respectively.

Discussion

Our results demonstrated that the likelihood of lymph node metastasis increases with increase of SUVmax of the primary tumor. When the SUVmax of the primary lung cancer is greater than 12, the probability of lymph node metastasis is high, reaching 70%, irrespective of the degree of FDG accumulation into the lymph node stations. This finding would allow us to more sensitively predict the presence of lymph node metastases, including microscopic ones that cannot be detected by a direct evaluation of the lymph node stations. The presence of microscopic lymph node metastasis is especially problematic when SRT is contemplated, where only the lung tumor is irradiated [1, 2]. It is noncontroversial that the post-SRT patients with microscopic lymph node metastases are at higher risk for lymph node recurrence. We may say that the patients with lung cancers showing high SUVmax constitute a high risk group for lymph node recurrence. Therefore, close follow-up with special attention to the lymph nodes is required in these patients after SRT. However, there was no upper threshold of SUVmax of the lung cancers, above which lymph node metastasis was always present. Thus, even when a lung cancer shows high SUVmax exceeding 10 or 20, the presence of lymph node metastasis is still inconclusive based on the evaluation of the SUVmax of the primary tumor. Therefore, a high SUVmax of the lung cancer should not be used as an exclusion criterion of SRT.

On the other hand, the lung cancers with an SUVmax less than 2.5 are unlikely to cause lymph node metastases. Therefore, if there is strong accumulation in the lymph node stations in lung cancers with an SUVmax less than 2.5, we should consider false positive finding first before we judge them to be metastatic. We should not preclude surgery or SRT in patients with lung cancers having an SUVmax less than 2.5 only because of strong accumulation of FDG into the lymph node stations.

Higashi et al. [15] documented in a multicenter study that the incidence of lymphatic vessel invasion and lymph node metastasis in non-small cell lung cancer depended on 18F-FDG uptake and concluded that 18F-FDG by the primary tumor is a strong predictor of lymphatic vessel invasion and lymph node metastasis. Our results are consistent with their observations. In their study, however, SUV was not used for the evaluation because of differences in the PET methodology in each institution and instead a 3-point visual scoring system (low, moderate or high grade) was employed. Although this method of evaluation is convenient and is applicable to other institutions that employ different methods of examination, the classification is relatively rough and not suitable for determination of the presence or absence of a threshold that would be practically useful in N-staging. In fact, 5.9% of the patients had lymph node metastasis even in the low 18F-FDG uptake group in their study. In our study, owing to having employed SUVmax we were able to find the possible presence of a lower threshold and absence of an upper threshold.

It has been also shown that the SUV of lung cancer correlates with the prognosis [17, 18]. Worsening of prognosis in lung cancers with a high SUV may be partly due to an increase of lymph node metastasis as demonstrated in our study. We have also shown that there are moderate correlations between SUVmax, and the number of lymph node metastases and pathological n stage. These results suggest that the extent of lymphatic spread of lung cancer increases with SUVmax. Ohtsuka et al. [17] concluded that SUV could be used for determining an indication of postoperative adjuvant chemotherapy. Similarly, the patients with lung cancers having a high SUVmax might be the candidates for postoperative radiotherapy to the mediastinum because the lymphatic spread beyond the extent of lymph node dissection is more likely to occur in this population.

When the criteria for lymph node metastasis were modified by the SUVmax of the primary cancers, the sensitivity together with accuracy were slightly higher than those by the cutoff value of 2.5 alone. The increase of sensitivity was due to the classification of cases with cancers having high SUVmax and microscopic lymph node metastases (i.e. negative in direct assessment of the lymph node station) as positive for lymph node metastasis. Unfortunately, specificity was mildly decreased due to the classification of cases with cancers having high SUVmax but no lymph node metastasis as positive for lymph node metastases. Although the cases with a cancer having an SUVmax less than 2.5 and lymph node stations having an SUVmax greater than 2.5 that was judged metastatic in direct assessment of the lymph node station could contribute to increasing specificity, there was only one such case in our study. This may be because lung cancer with a low SUV is less likely to cause obstructive pneumonia, which is one of the major causes of false positive lymphadenopathy. However, as the presence of underlying diseases such as old tuberculosis, which may demonstrate high SUVmax in the lymph node stations, is not associated with the SUVmax of lung cancer, consideration of SUVmax of lung cancer could potentially contribute to eliminating false positive lymph nodes.

Although we believe that this approach in the interpretation of FDG-PET is useful in improving accuracy of the evaluation of lymph node metastasis in lung cancer, our modification was retrospective and biased. Further investigation will be necessary to establish a definitively better method of FDG-PET interpretation in the evaluation of lymph node metastasis in lung cancer.

Mean SUVmax of lung cancer was significantly lower in adenocarcinoma than in squamous cell carcinoma. However, the frequency of lymph node metastasis was almost the same between the two pathological subtypes. These results suggest that adenocarcinoma is more likely to metastasize to lymph nodes than squamous cell carcinoma when the SUVmax is equal. Pathological subtype might be another significant factor that affects the likelihood of lymph node metastasis.

There are limitations to the present study. First, the number of the patients was too small to make a definitive conclusion regarding the threshold of SUVmax of the primary tumor, below which lymph node metastasis does not occur. Additionally, SUV can vary among machines depending on the methods of calculation. Therefore, our data could not be simply applied to other institutions. Second, our study population consisted only of patients who underwent surgery, while patients who were inoperable due to advanced stage by clinical evaluations, refused surgery or preferred SRT had been excluded from this study. This might have resulted in selection bias. Third, the pathological specimens of the resected lymph nodes were of one section at their central portion although it was a standard method in the pathological evaluation of surgical specimens. There could have been hidden cancer foci in other areas of lymph nodes, which may have affected the results of this study. Nevertheless, we clearly documented that the likelihood of lymph node metastasis correlates with the SUVmax of the primary lung cancer. This finding would be helpful in the evaluation of N-staging of lung cancer and in the management of the patients who have undergone SRT.

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Copyright information

© The Japanese Society of Nuclear Medicine 2009

Authors and Affiliations

  • Atsushi Nambu
    • 1
  • Satoshi Kato
    • 1
  • Yoko Sato
    • 2
  • Hideto Okuwaki
    • 3
  • Keiichi Nishikawa
    • 4
  • Akitoshi Saito
    • 5
  • Keiko Matsumoto
    • 6
  • Tomoaki Ichikawa
    • 1
  • Tsutomu Araki
    • 1
  1. 1.Department of RadiologyUniversity of YamanashiYamanashiJapan
  2. 2.Department of RadiologyKofu Neuro Surgical HospitalYamanashiJapan
  3. 3.Second Department of SurgeryUniversity of YamanashiYamanashiJapan
  4. 4.Second Department of Internal MedicineUniversity of YamanashiYamanashiJapan
  5. 5.Department of RadiologyYamanashi Prefectural HospitalYamanashiJapan
  6. 6.Department of RadiologyKobe University Graduate School of MedicineHyogoJapan

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