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 »  Abstract
 » Introduction
 » Subjects and Methods
 » Results
 » Discussion
 » Conclusion
 » Acknowledgment
 »  References
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ORIGINAL ARTICLE
Year : 2017  |  Volume : 54  |  Issue : 1  |  Page : 333-339
 

Tumor characteristics and metabolic quantification in carcinoma breast: An institutional experience


Department of Nuclear Medicine, Army Hospital (Research and Referral), New Delhi, India

Date of Web Publication1-Dec-2017

Correspondence Address:
Dr. A Jain
Department of Nuclear Medicine, Army Hospital (Research and Referral), New Delhi
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijc.IJC_121_17

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 » Abstract 

BACKGROUND: In India, carcinoma breast is the most common cancer among urban women population and second most common cancer after carcinoma cervix in rural areas. One in 22 women in India develops carcinoma of the breast in their lifetime. Fluorine-18-fluoro-2-deoxy-D-glucose (18F-FDG) uptake in breast cancer usually indicates the degree of tumor metabolism and hence can predict its behavior and prognosis. On the other hand, the estrogen receptor (ER), progesterone receptor (PR), and human epidermal growth factor receptor-2 (HER-2) or neu state of breast cancer is a biomarker that provides important prognostic information in addition to predicting response to therapy. AIMS: The main objective of this study is to assess whether a correlation exists between 18F-FDG uptake in untreated cases of breast cancer, their receptor status (ER, PR, and HER-2 or neu), tumor histology, and tumor size. SUBJECTS AND METHODS: Sixty consecutive female patients, with biopsy-proven primary breast cancer, were enrolled in this prospective study for whom 18F-FDG positron emission tomography-computed tomography scan was done in the Department of Nuclear Medicine. Results obtained were analyzed using appropriate statistical tests (t-test and Pearson Chi-square tests), and interpretation was made with 95% confidence level. RESULTS: In our series, a positive correlation between tumor size, high tumor grade, and standardized uptake value (SUV) was found. Tumors with positive receptor status for estrogen, progesterone, and HER-2/neu receptors had statistically insignificant lower maximum SUV (SUVmax) values than their negative counterparts. Triple-negative breast tumors (ER−, PR−, and no overexpression of HER-2/neu) are currently a subject of major interest because of their aggressiveness, poor prognosis, and lack of targeted therapy. Based on receptor status when the SUVmaxof the group with triple-negative receptor status (ER−/PR−/HER-2/neu−) was compared to rest of the patient group, it was seen that patients with negative receptor status had significantly higher mean SUVmaxvalues. CONCLUSIONS: We have inferred that in patients with breast cancer, various biological parameters such as tumor size, grade, histology, and hormonal receptor status have different impact on tumor metabolic activity.


Keywords: Carcinoma breast, fluorine-18-fluoro-2-deoxy-D-glucose-positron emission tomography-computed tomography, maximum standardized uptake value, receptor status, tumor characteristics


How to cite this article:
Dubey I P, Jain A, Chauhan M S, Kumar R, Agarwal S, Kishore B, Vishnoi M G, Paliwal D, John A R, Kumar N, Sharma A, Pandit A G. Tumor characteristics and metabolic quantification in carcinoma breast: An institutional experience. Indian J Cancer 2017;54:333-9

How to cite this URL:
Dubey I P, Jain A, Chauhan M S, Kumar R, Agarwal S, Kishore B, Vishnoi M G, Paliwal D, John A R, Kumar N, Sharma A, Pandit A G. Tumor characteristics and metabolic quantification in carcinoma breast: An institutional experience. Indian J Cancer [serial online] 2017 [cited 2020 Apr 5];54:333-9. Available from: http://www.indianjcancer.com/text.asp?2017/54/1/333/219534



 » Introduction Top


Breast cancer is commonly occurring female cancer in the world with an age-standardized incidence rate (ASR) of 39.0/100,000, which is more than double that of the second ranked cancer (cervical cancer ASR = 15.2/100,000).[1],[2] Breast cancer accounts for 23% of all newly occurring cancers in women worldwide and represents 13.7% of all cancer deaths.[1] It is the most frequent cause of cancer death in these regions (280,000 deaths in developing countries) of the world.[1] Although incidence rates are higher in the Western countries, the disability-adjusted life years show the highest burden for breast cancer in middle-income countries (3,144,000 vs. 1,856,000 in high-income and 1,626,000 in low-income countries), where there are increasing incidence rates and a higher proportion with late stage of disease at diagnosis.[3] Male breast cancer is rare compared to female breast cancer and has a different etiology as well as epidemiology.[4]

In India, it is the most common cancer among urban women population and second most common cancer after carcinoma cervix in rural areas. One in 22 women in India develops carcinoma of the breast in their lifetime.[5]

Invasive ductal carcinoma is the most common histological type (70%–80%), followed by invasive lobular carcinoma (6%–10%) and medullary carcinoma (~3%).[6] Invasive breast cancer may present as a single, multifocal (if tumors are growing in the same quadrant of the breast), and as multicentric (if detected in different quadrants). Patients with locally advanced disease, i.e., tumors with direct extension to chest wall or skin (Stage T4); advanced nodal disease (fixed axillary nodes, involvement of ipsilateral supraclavicular, infraclavicular, or internal mammary nodes); and inflammatory carcinomas have dismal prognosis because majority of the patients develop distant metastases despite appropriate therapy.

Existing guidelines and recommendations on carcinoma breast include history and physical examination, bilateral mammogram ultrasound and optional breast magnetic resonance imaging (MRI), pathology review, and determination of estrogen/progesterone receptors (PRs), nuclear grade, and human epidermal growth factor receptor-2 (HER-2)/neu status. To detect distant metastases, chest radiography, abdominal ultrasound, and bone scintigraphy with plain bone radiographs (if necessary) are carried out as the standard of care. Additional imaging procedures to assess suspicious findings include computed tomography (CT) and MRI.

Developments in integrated modalities incorporating morphological imaging and functional imaging in the form of positron emission tomography-CT (PET-CT) and single photon emission CT-CT have brought a paradigm shift in cancer management. In the past few years, these modalities have been subjected to critical evaluation, both with regard to utility as well as cost-effectiveness. Health technology assessment initiatives by several countries have led to evidence-based evaluation of this technology. PET using 2-(fluorine-18) fluoro-2-deoxy-D-glucose (18F-FDG-PET) visualizes the increased glucose consumption by the malignant tissue, thus providing the functional-metabolic information regarding cancer deposits and for differentiating benign from malignant tissue with high accuracy. FDG-PET lacks precise anatomical localization and morphological characterization of metastases which is overcome using combined PET/CT scanners.

Breast cancer is curable with early diagnosis and optimal treatment. Among various tests for predicting response to treatment, determination of estrogen receptor (ER) and PR in tumor cells is essential for appropriate hormone therapy. The HER-2 or neu receptor has been introduced as another predictive and prognostic marker. Determination of this receptor is useful for selecting patients with advanced breast cancer for treatment with therapeutic antibodies such as trastuzumab.[3]


 » Subjects and Methods Top


18F-FDG uptake in breast cancer usually indicates the degree of tumor metabolism and hence can predict its behavior and prognosis. On the other hand, the ER, PR, and HER-2 or neu state of breast cancer is a biomarker that provides important prognostic information in addition to predicting response to therapy. The main objective of this study is to assess the correlations between 18F-FDG uptake of primary breast cancer lesions and predictive and prognostic factors such as receptor status (estrogen, progesterone, HER-2 or neu, tumor histology, and tumor size).

Army Hospital (Research and Referral), Delhi Cantt, New Delhi, India, is a tertiary care hospital looking after the health care of all the three wings of armed forces. Patients of primary carcinoma breast for pretreatment evaluation, referred from the Oncology Department, were included in the study. Sixty consecutive patients, all adult females (median age, 51 years; range, 25–77 years), both indoor and outpatient department cases referred from all parts of India were enrolled in this prospective study. These patients were diagnosed with biopsy-proven primary breast cancer, and in the Department of Nuclear Medicine, they were examined by 18F-FDG PET-CT. This prospective project was designed to assess whether a correlation exists between 18F-FDG uptake in untreated cases of breast cancer and their receptor status (ER, PR, and HER-2 or neu), tumor histology, and tumor size.

Patient's age, sex, and demography were obtained from history. The tumor tissue was analyzed for ER, PR, and HER-2/neu state using standardized immunohistochemical techniques. Tumor size and maximum standardized uptake value (SUVmax) were obtained from PET/CT scan (Siemens, Biograph 2). Two nuclear medicine physicians had interpreted the PET/CT data independently. FDG uptake (SUVmax) in primary breast cancer was correlated with various parameters such as age, tumor histology, tumor grade, tumor size, and hormonal receptor status (estrogen, progesterone, and HER-2 or neu). Results obtained were analyzed using appropriate statistical tests (t-test and Pearson Chi-square tests), and interpretation was made with 95% confidence level.


 » Results Top


Study was carried out at Army Hospital (Research and Referral), New Delhi, from January 2012 to April 2014. A total of sixty consecutive patients were enrolled with histologically proven carcinoma breast and FDG PET CT done [Table 1] and [Figure 1].
Figure 1: SUV- standardized uptake value, IDC- Infiltrating ductal carcinoma, DCIS- Ductal carcinoma in situ

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Table 1: Histological subtypes of breast cancer in study

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Age

Age group distribution is shown in [Table 2].
Table 2: Age distribution in study population

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Tumor grades

There were sixty patients enrolled for the study, of which all were females. Among the sixty patients enrolled for the study, distribution as per the various grades of tumor is as given in [Table 3].
Table 3: Grades of tumor in study population

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Hormonal receptor profile

Positive or negative receptor status of all sixty patients is as depicted in [Figure 2]. Triple- negative receptor status is a special identity, known for its poor prognosis; hence it has been analyzed separately as shown in [Figure 3].
Figure 2: ER=Estrogen receptor, PR=Progesterone receptor; HER-2=Human epidermal growth factor receptor-2

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Figure 3: Triple neg- ER, PR, Her-2 all three negative

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Comparison of maximum standardized uptake value with progesterone receptor status

Progesterone receptor status of sixty available patients was assessed [Table 4]. When the PR receptor status was compared with the mean SUVmax obtained for the tumor post-PET scan, it was seen that 38 patients whose tumor was negative for the mentioned receptors had a mean SUVmax of 12.29 ± 7.83, and the 37 patients who were positive for the receptor status had a mean SUVmax of 11.16 ± 6.94, respectively. On comparison between the two groups, it was found that there was no significant difference in SUVmax of these groups (P = 0.58), i.e., PR status does not influence FDG uptake significantly [Figure 4].
Figure 4: SUV- standardized uptake value, PR=Progesterone receptor

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Table 4: Significance of PR status in study population

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Comparison of maximum standardized uptake values with estrogen receptor status

ER status of sixty available patients was assessed [Table 5] and [Figure 5]. When the ER receptor status was compared with the mean SUVmax values obtained for the tumor post-PET scan, it was seen that 31 patients whose tumor was negative for the mentioned receptors had a mean SUVmax of 12.27 ± 8.25 and the 29 patients who were positive for the receptor status had a mean SUVmax of 10.39 ± 6.35, respectively. On comparison between the two groups, it was found that there was no significant difference in SUVmax of these groups (P = 0.137), i.e., ER status does not influence FDG uptake significantly.
Figure 5: SUV- standardized uptake value, ER= Estrogen receptor

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Table 5: Significance of ER status in study population

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Comparison of maximum standardized uptake values with human epidermal growth factor receptor-2 neu receptor status

HER-2 neu receptor status of sixty available patients was assessed [Table 6] and [Figure 6]. When the receptor status was compared with the mean SUVmax values obtained for the tumor post-PET scan, it was seen that 29 patients whose tumor was negative for the mentioned receptors had a mean SUVmax of 14.11 ± 8.94 and the 31 patients who were positive for the receptor status had a mean SUVmax of 9.79 ± 5.10, respectively. On comparison between the two groups, patients who had negative receptor status had statistically significant higher SUVmax values compared to those who were receptor positive (P = 0.024).
Figure 6: SUV- standardized uptake value, HER-2=Human epidermal growth factor receptor-2

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Table 6: Significance of Her-2 neu receptor status in study population

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Comparison of maximum standardized uptake values with size of tumor

When SUVmax values of various tumor stages [Table 7] and [Figure 7] were compared, it was detected that the tumor size had significant positive influence on FDG uptake.
Figure 7: SUV- standardized uptake value

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Table 7: Significance of tumor size in study population

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Comparison of maximum standardized uptake values with grade of tumor

During comparison of different SUVmax values for tumors with different grades [Table 8] and [Figure 8], it was detected that tumors with higher grade showed a trend toward higher SUVmax values and the results were statistically significant (P = 0.007).
Figure 8: l&ll, III - tumor grades, SUV- standardized uptake value

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Table 8: Significance of tumor grade in study population

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Correlation of various prognostic markers (hormonal receptors) with maximum standardized uptake values

All the patients enrolled in the study were divided into two groups based on their hormonal receptor status [Table 9]. In one group (n = 19), the patients were negative for PR/ER and HER-2 neu receptor status. In the other group comprising 41 patients, all other combinations were taken except triple-negative receptor status. When SUVmax was compared among these two groups, it was seen that patients with negative receptor status had significantly higher mean SUVmax values (14.70 ± 9.24 vs. 10.57 ± 6.20, P = 0.046).
Table 9: Significance of triple negative hormonal receptors status in study population

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 » Discussion Top


We enrolled sixty patients of which all were females. These patients were studied for the tumor histology, tumor grade, and conventional hormone receptor status, i.e., ER/PR and HER-2/neu. The staging and grading of the tumor was available as per the standard criteria.

Of the sixty patients whose tumor staging and grading was available as per the histological criteria, SUVmax values showed a statistically significant correlation. Variable factors have been considered important for predicting and forecasting prognosis in breast cancer patients including the state of ER, PR, and HER-2/neu in the excised tumor. The results from these biologic measurements are of pivotal importance for the management of breast cancer patients. Multiple expert panels, including those of the American Society of Clinical Oncology, the National Academy of Clinical Biochemistry (United States), the National Institutes of Health, the European Group on Tumor Markers, and the European Society of Mastology, have recommended that ER and PR be assayed on all primary breast cancers because of the striking differences between the responses of steroid receptor positive and negative breast cancers to hormone therapy.[6] Furthermore, in advanced breast cancer, the state of tumors with regard to ER and PR is of great importance before adjuvant endocrine treatment is initiated.[7] HER-2/neu is a member of subclass 1 of the superfamily of receptor tyrosine kinases.

An important finding is that the SUV was dependent on tumor size, with increased uptake seen with increase in size [Table 7] and [Figure 9]. Our findings are in agreement with Kumar et al., who found a lower SUV in small tumors. Our findings did not match with those of Favier et al., who found no influence of tumor size on baseline SUV.[8] Here, it is worth emphasizing that in patients with larger tumor size, tumor grade was also on higher side. This finding may have some impact on increased uptake in large size tumors.
Figure 9: Triple neg- ER, PR, Her-2 all three negative

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Tumor grade is a major predictive factor in breast carcinoma. In our series, a positive correlation between high tumor grade and SUV was found (SUV 13.46 for Grade 3 vs. 6.15 for Grades 1 + 2 tumors; P = 0.007). Tumors with more aggressive stage/grade had higher SUVmax values. This finding is in agreement with previous reports.[6],[8],[9],[10],[11],[12],[13] Grade is a composite parameter. Favier et al. found a significant influence of nuclear pleomorphism and number of mitoses but not of architectural differentiation.[8]

Breast cancer patients with tumors that are ER+ and/or PR+ have lower risks of mortality after their diagnosis compared to women with ER− and/or PR− disease.[1],[2],[3],[4],[5],[6] Clinical trials have also shown that the survival advantage for women with hormone receptor-positive tumors is enhanced by treatment with adjuvant hormonal and/or chemotherapeutic regimens.[6],[14],[15],[16],[17],[18],[19],[20],[21] A recent study by Grann et al. which also used data collected from the SEER program reported that joint ER/PR status was an independent predictor of outcome in a large cohort of women with breast carcinoma.[22] SUVmax values obtained on PET-CT scan in all sixty patients were compared with hormonal receptor status of the tumor. Tumors with positive receptor status for ERs had statistically insignificant lower SUVmax values than their negative counterparts (10.39 ± 6.35 vs. 11.16 ± 6.94, P = 0.137) on PET scan. There have been contradictory reports on steroid hormone receptor status and 18F-FDG uptake. Some studies showed no correlation between hormone receptor status and SUV.[23],[24],[25],[26],[27],[28] However, others showed higher SUV in ER− tumors.[29],[30],[31] Few other studies such as Crowe et al. investigated the correlation between preoperative 18F-FDG uptake by a tumor and the postoperative ER and PR states of the tumor in 28 patients.[32] However, no correlation has been reported between the degree of 18F-FDG uptake and the ER or PR content of the lesions in these studies.[33] However, this finding is discordant with the study done by Groheux et al., who found that ER state alone had a significant effect on 18F-FDG uptake in this malignancy. ER− lesions had a significantly higher SUVmax than did ER+ lesions.[34]

When we analyzed the FDG uptake with PR status, it was found that PR+ tumors had statistically insignificant lower SUVmax values than PR− tumors (11.16 ± 6.94 vs. 12.29 ± 7.83, P = 0.58). The results from this study were concordant with the one done by Kramer and Osborne in a study of 36 patients found no significant association with SUV and PR status.[21] The study by Groheux et al. could document a significantly higher 18F-FDG uptake in PR− tumors than in PR+ tumors (P = 0.003) which does not match with our results.[34]

HER-2 neu receptor status of sixty available patients was assessed. When the receptor status was compared with the mean SUVmax values obtained, it was seen that 29 patients whose tumor was negative for the mentioned receptors had a mean SUVmax of 14.11 ± 8.94 and patients who were positive for the receptor status had a mean SUVmax of 10.39 ± 6.35, respectively. On comparison between the two groups, patients who had negative receptor status had statistically significant higher SUVmax values compared to those who were receptor positive (P = 0.024). This finding is in contrast with the fact that oncoprotein HER-2 neu overexpression is a well-known factor of tumor aggressiveness and poor prognosis. The results from this study were concordant with the one done by Ueda et al., who found a significant relationship between 18F-FDG uptake and HER-2/neu oncogene expression.[35] In the study by Groheux et al., no significant influence of HER-2/neu overexpression on SUV was found. Our findings suggest that HER-2/neu has major influence on glycolytic pathways.[34]

Triple-negative breast tumors (ER−, PR−, and no overexpression of HER-2/neu) are currently a subject of major interest because of their aggressiveness, poor prognosis, and lack of targeted therapy. In their molecular portrait, most triple-negative tumors are of “the basal-like” molecular subtype. Based on receptor status when the SUVmax of the group with triple-negative receptor status (ER−/PR−/HER-2 neu−) was compared to rest of the patient group, it was seen that patients with negative receptor status had significantly higher mean (14.70 ± 9.24 vs. 10.57 ± 6.20 P = 0.046) SUVmax values. The results from this study were concordant with the one done by Ohara et al.[36] In their study, SUVmax ranged from 0.8 to 22.1, and the mean SUVmax in the triple-negative subtype was 6.32, which was considerably higher than of the value of 3.75 for all patients. This finding was also reported by Basu et al.[37]

More studies need to be carried out to understand the relationship between glucose metabolism and hormonal receptor status of breast cancer.


 » Conclusion Top


We have inferred that in patients with breast cancer, various biological parameters such as tumor size, grade, histology, and hormonal receptor status have different impact on tumor metabolic activity.

Based on the data described here, it was found that ER -ve lesions have slightly higher SUVmax than do ER +ve lesions, but it is insignificant to derive any conclusion. Same relationship exists between PR - ve and PR +ve tumors. The results clearly demonstrated that the degree of 18F-FDG uptake (expressed as SUVmax) of breast cancer lesions with HER-2 or neu -ve status is significantly higher than HER-2 or neu +ve tumors.

Triple negative receptor status had significantly higher SUV max than rest of the tumor status. SUVmax in a primary site might be used for the new clinical trial about adjuvant chemotherapy such as adding new drugs.

Tumors with histological subtype, invasive or infiltrative ductal carcinoma (IDC) are found to have higher SUVmax than ductal carcinoma in situ (DCIS) and lobular carcinomas. Grade III tumors had significantly higher SUVmax than grade 1 & II tumors. Sizes of the tumor also have a positive correlation with the SUVmax; higher values are found with increasing size of tumor.

Limitations of our study are its small size and the fact that triple negative breast cancer has poor prognosis, could have been further correlated with follow up PET/CT scan after 2-3 cycles of neoadjuvant chemotherapy. It can predict the response to therapy and efficacy of the particular regime. A study should be performed to validate these findings with interim PET used as a surrogate marker in clinical trials involving novel therapeutic strategies. A long term follow up can also establish the fact whether SUVmax of breast cancer lesions can serve as an independent prognostic factor. Therefore, prospective studies on new FDG-PET/CT-based imaging algorithms in breast cancer patients are highly desirable.


 » Acknowledgment Top


The authors would like to thank the Department of Oncology, Army Hospital (Research and Referral), Delhi Cantt, 110010.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

 
 » References Top

1.
Ferlay J, Bray F, Pisani P, et al. GLOBOCAN 2000: cancer incidence, mortality and prevalence worldwide, version 1.0. IARC Cancer Base No. 5. Lyon: IARC, 2001.  Back to cited text no. 1
    
2.
Ferlay J SH, Bray F, Forman D, Mathers C and Parkin DM. GLOBOCAN 2008 vl.2, Cancer Incidence and Mortality Worldwide: IARC Cancer Base No. 10. [Internet], 2010; Available from: http://Elobocan.iarc.fr. [cited 2011 Oct 25].  Back to cited text no. 2
    
3.
Organization WH. The global burden of disease: 2004 update: Department of Health Statistics and Informatics; 2008. Report No.: ISBN 978b 9 4 156 3710.  Back to cited text no. 3
    
4.
Schottenfield DaF, Jr., Joseph F., editor. Cancer Epidemiology and Prevention, Second Edition. Second ed. New York: Oxford University Press; 1996.  Back to cited text no. 4
    
5.
Murthy NS, Chaudhry K, Nadayil D, Agarwal UK, Saxena S. Changing trends in incidence of breast cancer: Indian scenario. Indian J Cancer 2009;46:73-4.  Back to cited text no. 5
[PUBMED]  [Full text]  
6.
Duffy MJ. Predictive markers in breast and other cancers: A review. Clin Chem 2005;51:494-503.  Back to cited text no. 6
[PUBMED]    
7.
Bardou VJ, Arpino G, Elledge RM, Osborne CK, Clark GM. Progesterone receptor status significantly improves outcome prediction over estrogen receptor status alone for adjuvant endocrine therapy in two large breast cancer databases. J Clin Oncol 2003;21:1973-9.  Back to cited text no. 7
[PUBMED]    
8.
Favier L, Berriolo-Riedinger A, Coudert B, Touzery C, Riedinger J, Toubeau M,et al. Predicative value of [18F]-FDG PET scan for pathological complete response to neoadjuvant chemotherapy in breast cancer. J Clin Oncol 2007:505.  Back to cited text no. 8
    
9.
Nixon AJ, Neuberg D, Hayes DF, Gelman R, Connolly JL, Schnitt S, et al. Relationship of patient age to pathologic features of the tumor and prognosis for patients with stage I or II breast cancer. J Clin Oncol 1994;12:888-94.  Back to cited text no. 9
[PUBMED]    
10.
Albain KS, Allred DC, Clark GM. Breast cancer outcome and predictors of outcome: Are there age differentials? J Natl Cancer Inst Monogr 1994;16:35-42.  Back to cited text no. 10
    
11.
Diab SG, Elledge RM, Clark GM. Tumor characteristics and clinical outcome of elderly women with breast cancer. J Natl Cancer Inst 2001;93:65-6  Back to cited text no. 11
    
12.
Turner RR, Chu KU, Qi K, Botnick LE, Hansen NM, Glass EC, et al. Pathologic features associated with nonsentinel lymph node metastases in patients with metastatic breast carcinoma in a sentinel lymph node. Cancer 2000;89:574-81.  Back to cited text no. 12
[PUBMED]    
13.
Rosen PP, Groshen S, Saigo PE, Kinne DW, Hellman S. Pathological prognostic factors in stage I (T1N0M0) and stage II (T1N1M0) breast carcinoma: A study of 644 patients with median follow-up of 18 years. J Clin Oncol 1989;7:1239-51.  Back to cited text no. 13
[PUBMED]    
14.
Powe JE. Positron emission tomography (PET) scanning in breast cancer. Br J Radiol 1997;70:668-70.  Back to cited text no. 14
[PUBMED]    
15.
Rostom AY, Powe J, Kandil A, Ezzat A, Bakheet S, el-Khwsky F, et al. Positron emission tomography in breast cancer: A clinicopathological correlation of results. Br J Radiol 1999;72:1064-8.  Back to cited text no. 15
[PUBMED]    
16.
American Cancer Society. Cancer Facts and Figures 2007. Atlanta: American Cancer Society; 2007.  Back to cited text no. 16
    
17.
Rosen PP, Groshen S, Kinne DW. Prognosis in T2N0M0 stage I breast carcinoma: A 20-year follow-up study. J Clin Oncol 1991;9:1650-61.  Back to cited text no. 17
[PUBMED]    
18.
Tubiana M, Koscielny S. The natural history of breast cancer: Implications for a screening strategy. Int J Radiat Oncol Biol Phys 1990;19:1117-20.  Back to cited text no. 18
[PUBMED]    
19.
Mankoff DA, Eubank WB. Current and future use of positron emission tomography (PET) in breast cancer. J Mammary Gland Biol Neoplasia 2006;11:125-36.  Back to cited text no. 19
[PUBMED]    
20.
Smith RA, Guisti R. The epidemiology of breast cancer. In: Basset LW, Jackson VP, eds. Diagnosis of diseases of the breast. Philadelphia: Saunders;1996:293-316.  Back to cited text no. 20
    
21.
Kramer R, Osborne CK. Evaluation of patients for metastasis prior to primary therapy. In: Harris JR, Lippman ME, Morrow M, Osborne CK, eds. Diseases of the breast, 3rd ed. Philadelphia: Lippincott Williams & Wilkins, 2004:670.  Back to cited text no. 21
    
22.
Grann VR, Troxel AB, Zojwalla NJ, Jacobson JS, Hershman D, Neugut AI. Hormone receptor status and survival in a population-based cohort of patients with breast carcinoma. Cancer 2005;103:2241-51.  Back to cited text no. 22
[PUBMED]    
23.
Dehdashti F, Mortimer JE, Siegel BA, Griffeth LK, Bonasera TJ, Fusselman MJ, et al. Positron tomographic assessment of estrogen receptors in breast cancer: Comparison with FDG-PET and in vitro receptor assays. J Nucl Med 1995;36:1766-74.  Back to cited text no. 23
[PUBMED]    
24.
Crippa F, Seregni E, Agresti R, Chiesa C, Pascali C, Bogni A, et al. Association between [18F] fluorodeoxyglucose uptake and postoperative histopathology, hormone receptor status, thymidine labelling index and p53 in primary breast cancer: A preliminary observation. Eur J Nucl Med 1998;25:1429-34.  Back to cited text no. 24
[PUBMED]    
25.
Avril N, Menzel M, Dose J, Schelling M, Weber W, Jänicke F, et al. Glucose metabolism of breast cancer assessed by 18F-FDG PET: Histologic and immunohistochemical tissue analysis. J Nucl Med 2001;42:9-16.  Back to cited text no. 25
    
26.
Buck A, Schirrmeister H, Kühn T, Shen C, Kalker T, Kotzerke J, et al. FDG uptake in breast cancer: Correlation with biological and clinical prognostic parameters. Eur J Nucl Med Mol Imaging 2002;29:1317-23.  Back to cited text no. 26
    
27.
Kumar R, Chauhan A, Zhuang H, Chandra P, Schnall M, Alavi A. Clinicopathologic factors associated with false negative FDG-PET in primary breast cancer. Breast Cancer Res Treat 2006;98:267-74.  Back to cited text no. 27
[PUBMED]    
28.
Shimoda W, Hayashi M, Murakami K, Oyama T, Sunagawa M. The relationship between FDG uptake in PET scans and biological behavior in breast cancer. Breast Cancer 2007;14:260-8.  Back to cited text no. 28
[PUBMED]    
29.
Gil-Rendo A, Martínez-Regueira F, Zornoza G, García-Velloso MJ, Beorlegui C, Rodriguez-Spiteri N. Association between [18F] fluorodeoxyglucose uptake and prognostic parameters in breast cancer. Br J Surg 2009;96:166-70.  Back to cited text no. 29
    
30.
Mavi A, Cermik TF, Urhan M, Puskulcu H, Basu S, Yu JQ, et al. The effects of estrogen, progesterone, and C-erbB-2 receptor states on 18F-FDG uptake of primary breast cancer lesions. J Nucl Med 2007;48:1266-72.  Back to cited text no. 30
[PUBMED]    
31.
Osborne JR, Port E, Gonen M, Doane A, Yeung H, Gerald W, et al. 18F-FDG PET of locally invasive breast cancer and association of estrogen receptor status with standardized uptake value: Microarray and immunohistochemical analysis. J Nucl Med 2010;51:543-50.  Back to cited text no. 31
[PUBMED]    
32.
Crowe JP Jr., Adler LP, Shenk RR, Sunshine J. Positron emission tomography and breast masses: Comparison with clinical, mammographic, and pathological findings. Ann Surg Oncol 1994;1:132-40.  Back to cited text no. 32
    
33.
Eubank WB, Mankoff DA. Evolving role of positron emission tomography in breast cancer imaging. Semin Nucl Med 2005;35:84-99.  Back to cited text no. 33
[PUBMED]    
34.
Groheux D, Giacchetti S, Moretti JL, Porcher R, Espié M, Lehmann-Che J, et al. Correlation of high 18F-FDG uptake to clinical, pathological and biological prognostic factors in breast cancer. Eur J Nucl Med Mol Imaging 2011;38:426-35.  Back to cited text no. 34
    
35.
Ueda S, Tsuda H, Asakawa H, Shigekawa T, Fukatsu K, Kondo N, et al. Clinicopathological and prognostic relevance of uptake level using 18F-fluorodeoxyglucose positron emission tomography/computed tomography fusion imaging (18F-FDG PET/CT) in primary breast cancer. Jpn J Clin Oncol 2008;38:250-8.  Back to cited text no. 35
[PUBMED]    
36.
Ohara M, Shigematsu H, Tsutani Y, Emi A, Masumoto N, Ozaki S, et al. Role of FDG-PET/CT in evaluating surgical outcomes of operable breast cancer: Usefulness for malignant grade of triple- negative breast cancer. Breast, 2013;22:958-963.  Back to cited text no. 36
[PUBMED]    
37.
Basu S, Chen W, Tchou J, Mavi A, Cermik T, Czerniecki B, et al. Comparison of triple-negative and estrogen receptor-positive/progesterone receptor-positive/HER2-negative breast carcinoma using quantitative fluorine-18 fluorodeoxyglucose/positron emission tomography imaging parameters: A potentially useful method for disease characterization. Cancer 2008;112:995-1000.  Back to cited text no. 37
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    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4], [Figure 5], [Figure 6], [Figure 7], [Figure 8], [Figure 9]
 
 
    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6], [Table 7], [Table 8], [Table 9]

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