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Detection of Clinically Unexpected Malignant and Premalignant Tumors with Whole-Body FDG PET: Histopathologic Comparison¹

¹ From the Department of Radiology, Division of Nuclear Medicine, Hackensack University Medical Center, 30 Prospect Ave, Hackensack, NJ 07601. Received December 12, 2002; revision requested February 20, 2003; final revision received July 11; accepted August 6. Address correspondence to H.A. (e-mail: hagress@humed.com).

	ABSTRACT

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
PURPOSE: To determine the clinical importance and malignant potential of unexpected abnormal foci of hypermetabolism at fluorodeoxyglucose (FDG) positron emission tomography (PET) performed for evaluation of malignancy.

MATERIALS AND METHODS: A total of 1,750 FDG PET scans were obtained to evaluate a variety of known or suspected malignancies. Each scan was evaluated for abnormal unexpected hypermetabolism based on unusual location (ie, foci that did not conform to the usual distribution of metastases given the primary tumor for which the PET scan was requested) and discrete focal nature of an abnormality. Unexpected findings were followed by pathologic confirmation and were considered clinically important if the final pathologic diagnosis was cancerous, precancerous, or noncancerous but had the potential for local destruction or systemic physiologic effects.

RESULTS: On the basis of the normal spread pattern of the primary lesion, 58 abnormal unexpected foci of hypermetabolism were identified in 53 patients. Forty-five of these abnormalities were followed up with computed tomography (CT), magnetic resonance imaging, and/or mammography, and 42 had subsequent tissue confirmation at endoscopic, CT-guided, or surgical biopsy. Of 42 histopathologically confirmed abnormalities, 30 (71%) were either malignant or premalignant tumors that differed from the cancer for which the patient was originally scanned. Nine other suspicious abnormal foci proved benign and three represented false-positive findings, with no abnormal findings at endoscopy. Three of nine nonmalignant lesions were considered clinically important because of the potential for local destruction and/or systemic effects.

CONCLUSION: The identification of unexpected foci of hypermetabolism at whole-body FDG PET may signal the presence of tumors that are unrelated to the neoplasm for which the patient was scanned. Findings of this study emphasize the need for follow-up of these abnormalities because the majority represent either malignant or premalignant neoplasms, which were not clinically apparent.

© RSNA, 2003

Index terms: Neoplasms, PET, **.12163² • Positron emission tomography (PET), comparative studies

	INTRODUCTION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Whole-body positron emission tomography (PET) with fluorine 18 fluorodeoxyglucose (FDG) has been used successfully and with increasing frequency in the evaluation and clinical management of an expanding number of neoplasms (1–8). This encompasses initial staging, restaging of recurrence, and monitoring therapy in oncology patients, as well as evaluation of solitary pulmonary nodules (SPNs) (4) and identification of carcinomas of unknown primary origin (9). In the oncology patient, FDG PET has frequently been shown to be more accurate than computed tomography (CT) (1–11) in depicting unexpected foci of metastases or recurrent tumors that either were not seen or were difficult to observe on CT scans.

In addition, during a routine interpretation of FDG PET scans, abnormal incidental foci of hypermetabolism may be identified that are unlikely to be related to the neoplasm for which the patient was being scanned. These areas of increased activity are in unusual locations relative to the common metastatic spread of individual cancers, as well as to the many normal physiologic variants of FDG distribution (12,13). The purpose of this study was to determine the clinical importance and malignant potential of unexpected abnormal foci of hypermetabolism seen on FDG PET scans obtained for the evaluation of malignancy.

	MATERIALS AND METHODS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Patient Population
A total of 1,750 patients underwent FDG PET from November 2000 to July 2002 to evaluate a variety of known or suspected malignancies, including lung cancer, colon cancer, lymphoma, melanoma, breast cancer, esophageal cancer, head and neck cancer, neuroblastoma, and SPNs. All scans were initial for each patient. Follow-up PET scans were not included in the study because none demonstrated unexpected findings that were not already present on the initial scan. This study was submitted to our institutional review board, which determined that the study was exempt from institutional review board approval. The study did not require patient informed consent.

FDG PET Examinations
Patients were instructed to halt exercise for 48 hours prior to FDG PET scanning (to minimize muscle uptake) and to eat a high-protein low-carbohydrate meal as the last meal prior to scanning (to decrease cardiac activity) (14). They then drank 24–32 ounces of water and otherwise fasted for 4–6 hours prior to the injection of FDG.

Whole-body dedicated 32-detector ring PET (ECAT Exact HR+; CTI/Siemens, Knoxville, Tenn) was performed, with transverse spatial resolution of 4.6-mm full width half maximum and a 1.0- and 15.5-cm transverse field of view. Scanning began 45–60 minutes after intravenous injection of 370–555 MBq (10–15 mCi) of FDG. Emission data were processed with iterative reconstruction ordered-subset expectation maximization. Attenuation correction was performed with segmented filtered back projection. Emission and transmission image acquisition times per bed position were 5 minutes (300 seconds) and 3 minutes (180 seconds), respectively. Six bed positions were typically used for our patients. Images were evaluated on a monitor (Sun Microsystems, Palo Alto, Calif) in transverse, coronal, and sagittal planes, as well as in a rotational projection display.

FDG PET Image Interpretation
Foci of expected hypermetabolic activity included the primary site of the disease being evaluated, expected sites of lymphangitic or hematogenous spread for a specific malignancy (eg, lung cancer with liver or adrenal or bone metastases), tumor recurrence, and normal physiologic variants. Metastases from an already known primary malignancy that were not seen at prior imaging such as CT scanning were frequently identified (eg, bone metastases seen at PET but not at CT). However, these were not included in this study because they were considered to be potentially expected in a patient with a known cancer.

Determination of abnormal unexpected hypermetabolism was based on an unusual location (which did not conform to the usual distribution of metastases, given the primary tumor for which the PET scan was requested) and discrete focal nature of the abnormality. In the colon, discrete foci were considered abnormal if the FDG uptake was greater than that in the liver or if it represented the only area of colonic uptake. Subtle lesions were frequently demonstrated best with rotational projection display. This was particularly true within the colon, where focal abnormalities were more conspicuous relative to the more diffuse physiologic metabolic activity. An abnormality was considered unexpected if it represented a single discrete isolated focus, distant from a known primary lesion, and there was no other evidence of metastatic disease. For example, although lung cancer may metastasize to the colon, it would be unusual for this to occur with no other evidence of metastatic disease in the mediastinum, hila, liver, adrenal glands, or osseous structures.

Review of prior CT findings, with the PET abnormality used as a guide, was also valuable in identifying previously overlooked anatomic lesions. Although the PET scans were individually interpreted by any one of four experienced radiologists, all scans not initially interpreted by the first author (H.A.) were retrospectively reviewed (420 of 1,750) within 2 weeks of scanning by the first author, who had 25 years of experience in nuclear medicine scan interpretation and 3 years of PET experience by completion of the study.

Image Correlation and Follow-up
PET scans were correlated not only with the patient’s most recent CT scans but also with clinical history and relevant therapy. A registry of patient follow-up information was updated on a daily basis by using spreadsheet software (Excel; Microsoft, Redmond, Wash) and digital image archiving, which included referring physician data, patient diagnosis, unexpected findings, follow-up imaging, and pathologic results.

Follow-up studies and procedures, which were recommended by the PET interpreter, included targeted CT, magnetic resonance (MR) imaging, mammography, endoscopy, and image-guided or surgical biopsy. In addition to the transcribed report, the referring physicians were contacted by the interpreting physician by telephone at the time of the interpretation and approximately 1 month later. Further follow-up calls by the interpreting physician were continued until either a definitive diagnosis was made or it was determined that confirmation could not be obtained. Diagnoses were considered final only after a histopathologic confirmation with biopsy or surgical excision.

Confirmed unexpected findings were considered clinically important by the referring and interpreting physicians if the final pathologic diagnosis was cancerous or precancerous with the potential to produce either localized symptoms or metastases. Nonmalignant lesions were considered clinically important if they had the potential for local destructive changes or systemic effects for which the referring physician would institute specific treatment.

	RESULTS

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
In this series of 1,750 FDG PET scans, 58 unexpected abnormal foci of hypermetabolism were identified in 53 patients (Fig 1). Thirteen of these unexpected foci could not be pathologically confirmed because of patient refusal for further studies or biopsy, poor clinical condition of the patient, or loss of patient to follow-up. Of the 45 foci that were further evaluated, 42 in 37 patients had histopathologic confirmation. Three had follow-up CT confirmation of an unexpected mass, but the patients refused biopsy. In this subgroup, there were 26 men with an age range of 57–87 years (mean, 73 years) and 11 women with an age range of 46–86 years (mean, 65 years). Our results are based on the 42 confirmed cases.

View larger version (38K): [in this window] [in a new window] [Download PPT slide]   Figure 1. Flowchart shows results of the unexpected FDG PET findings.

View larger version (110K): [in this window] [in a new window] [Download PPT slide]   Figure 2a. New right lung mass in a 73-year-old woman with a history of breast cancer. (a) Coronal (left) and sagittal (right) attenuation-corrected PET scans show positive hypermetabolic focus corresponding to the lung mass (upper arrow) and an unexpected intense rectal focus (lower arrow). (b) Transverse CT scans were reported as not depicting a mass, and the patient was asymptomatic relative to the presence of a rectal mass (black arrow), which occupies the entire bowel lumen, posterior to the bladder (white arrow) and uterine cervix (dotted arrow). (c) Transverse attenuation-corrected PET scan shows intense rectal focus (lower arrow) posterior to the bladder (upper arrow). (d) Colonoscopy and biopsy revealed 4-cm tubular villous adenoma (arrow). Resected lung mass was pulmonary adenocarcinoma.

View larger version (69K): [in this window] [in a new window] [Download PPT slide]   Figure 2b. New right lung mass in a 73-year-old woman with a history of breast cancer. (a) Coronal (left) and sagittal (right) attenuation-corrected PET scans show positive hypermetabolic focus corresponding to the lung mass (upper arrow) and an unexpected intense rectal focus (lower arrow). (b) Transverse CT scans were reported as not depicting a mass, and the patient was asymptomatic relative to the presence of a rectal mass (black arrow), which occupies the entire bowel lumen, posterior to the bladder (white arrow) and uterine cervix (dotted arrow). (c) Transverse attenuation-corrected PET scan shows intense rectal focus (lower arrow) posterior to the bladder (upper arrow). (d) Colonoscopy and biopsy revealed 4-cm tubular villous adenoma (arrow). Resected lung mass was pulmonary adenocarcinoma.

View larger version (74K): [in this window] [in a new window] [Download PPT slide]   Figure 2c. New right lung mass in a 73-year-old woman with a history of breast cancer. (a) Coronal (left) and sagittal (right) attenuation-corrected PET scans show positive hypermetabolic focus corresponding to the lung mass (upper arrow) and an unexpected intense rectal focus (lower arrow). (b) Transverse CT scans were reported as not depicting a mass, and the patient was asymptomatic relative to the presence of a rectal mass (black arrow), which occupies the entire bowel lumen, posterior to the bladder (white arrow) and uterine cervix (dotted arrow). (c) Transverse attenuation-corrected PET scan shows intense rectal focus (lower arrow) posterior to the bladder (upper arrow). (d) Colonoscopy and biopsy revealed 4-cm tubular villous adenoma (arrow). Resected lung mass was pulmonary adenocarcinoma.

View larger version (158K): [in this window] [in a new window] [Download PPT slide]   Figure 2d. New right lung mass in a 73-year-old woman with a history of breast cancer. (a) Coronal (left) and sagittal (right) attenuation-corrected PET scans show positive hypermetabolic focus corresponding to the lung mass (upper arrow) and an unexpected intense rectal focus (lower arrow). (b) Transverse CT scans were reported as not depicting a mass, and the patient was asymptomatic relative to the presence of a rectal mass (black arrow), which occupies the entire bowel lumen, posterior to the bladder (white arrow) and uterine cervix (dotted arrow). (c) Transverse attenuation-corrected PET scan shows intense rectal focus (lower arrow) posterior to the bladder (upper arrow). (d) Colonoscopy and biopsy revealed 4-cm tubular villous adenoma (arrow). Resected lung mass was pulmonary adenocarcinoma.

View larger version (126K): [in this window] [in a new window] [Download PPT slide]   Figure 3a. Right lower lobe SPN in a 66-year-old woman. (a) Coronal non-attenuation-corrected PET scans show hypermetabolic SPN (large arrow) and clinically unsuspected focus in the left breast (small arrow). Both abnormal foci were most conspicuous on the non-attenuation-corrected images. Frequently, small pulmonary and/or superficial nonpulmonary lesions were more easily identified on non-attenuation-corrected images. (b) Transverse CT scan (in retrospect) shows a masslike area of high attenuation in the left breast (arrow). Initial mammogram obtained at another institution was interpreted as negative. (c) Follow-up spot magnification compression mammogram shows a mass (arrow). Invasive ductal carcinoma was detected at ultrasonography (US)-guided biopsy. Surgical excision of the lung lesion revealed carcinoid tumor.

View larger version (96K): [in this window] [in a new window] [Download PPT slide]   Figure 3b. Right lower lobe SPN in a 66-year-old woman. (a) Coronal non-attenuation-corrected PET scans show hypermetabolic SPN (large arrow) and clinically unsuspected focus in the left breast (small arrow). Both abnormal foci were most conspicuous on the non-attenuation-corrected images. Frequently, small pulmonary and/or superficial nonpulmonary lesions were more easily identified on non-attenuation-corrected images. (b) Transverse CT scan (in retrospect) shows a masslike area of high attenuation in the left breast (arrow). Initial mammogram obtained at another institution was interpreted as negative. (c) Follow-up spot magnification compression mammogram shows a mass (arrow). Invasive ductal carcinoma was detected at ultrasonography (US)-guided biopsy. Surgical excision of the lung lesion revealed carcinoid tumor.

View larger version (76K): [in this window] [in a new window] [Download PPT slide]   Figure 3c. Right lower lobe SPN in a 66-year-old woman. (a) Coronal non-attenuation-corrected PET scans show hypermetabolic SPN (large arrow) and clinically unsuspected focus in the left breast (small arrow). Both abnormal foci were most conspicuous on the non-attenuation-corrected images. Frequently, small pulmonary and/or superficial nonpulmonary lesions were more easily identified on non-attenuation-corrected images. (b) Transverse CT scan (in retrospect) shows a masslike area of high attenuation in the left breast (arrow). Initial mammogram obtained at another institution was interpreted as negative. (c) Follow-up spot magnification compression mammogram shows a mass (arrow). Invasive ductal carcinoma was detected at ultrasonography (US)-guided biopsy. Surgical excision of the lung lesion revealed carcinoid tumor.

View larger version (66K): [in this window] [in a new window] [Download PPT slide]   Figure 4a. Scans in a 68-year-old woman with prior treatment for breast cancer. (a) Follow-up coronal attenuation-corrected PET scan shows unexpected asymptomatic uterine hypermetabolic focus (upper arrow) above the bladder (lower arrow). (b) Top: Transverse attenuation-corrected PET scan shows intrauterine focus (solid arrow) and the left ureter (dotted arrow), which is a normal variant. Bottom: Follow-up transverse T2-weighted turbo spin-echo MR image shows an endometrial mass (solid arrow) and the left ureter (dotted arrow). Endometrial adenocarcinoma was found at biopsy and was treated with hysterectomy (no evidence of tumor spread at surgery). (Reprinted, with permission, from reference 15.)

View larger version (120K): [in this window] [in a new window] [Download PPT slide]   Figure 4b. Scans in a 68-year-old woman with prior treatment for breast cancer. (a) Follow-up coronal attenuation-corrected PET scan shows unexpected asymptomatic uterine hypermetabolic focus (upper arrow) above the bladder (lower arrow). (b) Top: Transverse attenuation-corrected PET scan shows intrauterine focus (solid arrow) and the left ureter (dotted arrow), which is a normal variant. Bottom: Follow-up transverse T2-weighted turbo spin-echo MR image shows an endometrial mass (solid arrow) and the left ureter (dotted arrow). Endometrial adenocarcinoma was found at biopsy and was treated with hysterectomy (no evidence of tumor spread at surgery). (Reprinted, with permission, from reference 15.)

Three of the nine benign abnormalities were believed to be clinically important and were not suspected by the referring physicians. Each of these cases resulted in surgical or medical treatment that was not considered prior to FDG PET.

One asymptomatic patient with an SPN had asymmetric peripheral incidental gallbladder uptake (Fig 5). Follow-up MR imaging demonstrated cholelithiasis and inflammation of the liver adjacent to the gallbladder. At surgery, inflammatory changes of acute and chronic cholecystitis were discovered, with extensive adhesions involving the gallbladder, adjacent colon, and stomach. This patient was most likely asymptomatic because of diabetes and associated insensitivity to pain. The second patient, who had malignant melanoma of the face, demonstrated an incidental FDG focus in the right knee. Follow-up MR imaging and surgery yielded a pigmented villonodular synovitis. Although the patient had no symptoms relative to the knee, this finding was believed to be clinically important because of the potential for growth and adjacent bone destruction. In the third patient, who had intense diffuse thyroid hypermetabolism, Hashimoto thyroiditis was diagnosed only after endocrine evaluation, which was recommended in the PET scan report. The patient had markedly elevated levels of antithyroid antibodies, was clinically hypothyroid, and subsequently received thyroid hormonal replacement therapy. Of the 42 confirmed unexpected findings, 33 (30 malignant and premalignant and three benign) were clinically important.

View larger version (40K): [in this window] [in a new window] [Download PPT slide]   Figure 5. Right lower lobe SPN in a 72-year-old asymptomatic man with diabetes, which was negative at FDG PET. Coronal (top) and transverse (bottom) attenuation-corrected PET scans show unexpected asymmetric hypermetabolic focus in the periphery of the gallbladder (arrow). Follow-up MR images (not shown) demonstrated cholelithiasis and inflammation of the liver adjacent to gallbladder. Acute and chronic cholecystitis with inflammation and adhesions to adjacent bowel and stomach was discovered at surgery.

Lack of clinical symptoms related to the incidental lesions was common in our study. Twenty-three (92%) of the 25 patients with unexpected tumors were asymptomatic. In retrospect, one patient with colon cancer admitted having occasional mild blood streaking in the stool but had never informed her physician. One other patient with laryngeal cancer discovered at FDG PET previously underwent evaluation for hoarseness, which included direct laryngoscopy and yielded no evidence of malignancy.

The average interval between PET scan interpretation and tissue confirmation was 6.4 weeks (range, approximately 2–15 weeks), and it was not uncommon to require multiple follow-up telephone communications (after the 1st month) to perform follow-up examinations and/or obtain tissue confirmation.

	DISCUSSION

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 
Findings of several studies have shown that whole-body PET imaging may identify unexpected foci of hypermetabolism within the colon, many of which have clinical relevance. Tatlidil et al (16) retrospectively reviewed the correlation between FDG uptake on PET scans and colonoscopic and/or histopathologic findings among patients without a known history of colorectal carcinoma. They described multiple patterns of abnormal colonic FDG uptake and the need to perform follow-up endoscopy when high nodular uptake is seen in the colon.

Yasuda et al (17) studied the detection of colonic adenomas, which they considered precursors of colon cancer, in 110 patients with both PET and colonoscopy. They demonstrated that PET findings were positive in 24% of 59 adenomas found at endoscopy and in 90% of all adenomas 1.3 cm or larger.

Zhuang et al (18) identified five unsuspected colon cancers in a retrospective analysis of FDG PET scans in 197 patients evaluated for SPN. Yasuda et al (19) identified three asymptomatic colon carcinomas with PET in a study of 1,872 individuals. Multiple case reports have demonstrated FDG PET uptake in other incidental neoplasms, including thyroid (20,21), endometrial (22), and breast (23,24) carcinoma.

Yasuda et al (25) retrospectively evaluated the role of PET as part of an overall screening program in asymptomatic patients in Japan. The study utilized modalities such as CT, MR imaging, US, and PET, as well as laboratory tests and physical examination results. In an updated follow-up study, Ide et al (26) reported detection of 115 (2.0%) cancers in 5,716 patients. Approximately one-half of these cancers were not identified at FDG PET, but 63 were positive at PET (1.1% of the population studied).

In addition to the identification of incidental findings on FDG PET scans, several additional observations became apparent during the follow-up phase of this study. In that the referring physician (frequently, a subspecialty consultant) is mainly focused on the evaluation of the patient’s primary disease, the need for follow-up of incidental PET findings may be a relatively low priority. A major component of this study involved personal communication with the referring physicians to emphasize the potential for unanticipated malignancy and the subsequent need for follow-up studies and/or tissue sampling. This was especially true in that the majority of patients with malignant and premalignant findings were asymptomatic, even in retrospect.

We also found that follow-up imaging findings were most definitive when correlated directly with the PET images and could be misinterpreted if correlated with the PET report only. In the future, the co-registered fused imaging of combined PET/CT units (or other co-registration software packages) would seem to provide a useful method of immediate correlation and could possibly decrease the number of necessary follow-up imaging studies prior to biopsy.

In our study, we found that when colonoscopy was required, it was also helpful to review the PET scan with the endoscopist prior to the procedure for better localization of lesions.

It is also apparent that correlation with anatomic imaging, with PET as a guide, is extremely useful for identifying previously undetected subtle lesions on prior CT scans and to therefore determine the sites for biopsy without necessitating further imaging. This is due to the frequent increased target to background ratio of many foci positive at PET relative to the more subtle anatomic CT abnormalities. For example, many small colonic lesions were difficult, if not impossible, to see on CT scans secondary to surrounding feces, whereas they were frequently easily identifiable on FDG PET scans. In this regard, knowledge of the many normal physiologic variants in FDG distribution (12,13,16) was important to limit the number of false-positive results.

In conclusion, the identification of incidental foci of abnormal hypermetabolism on FDG PET scans frequently signals the presence of unsuspected subclinical tumors, which differ from the indicated reason for which the patient was initially scanned. This study emphasizes the importance of follow-up of these incidental findings, preferably to the point of tissue confirmation, as 71% of the histopathologically confirmed foci represented either malignant or premalignant neoplasms, the majority of which were asymptomatic.

Findings of this study emphasize the added value of PET as a whole-body imaging technique, which provided important information above and beyond that for which the scan was ordered. In many cases, this is because whole-body PET may depict more of the body than would another imaging modality, which is limited to smaller body segments.

It should be noted that the results of this study might not be applicable to the general population, because our specific study group consisted of patients who either had or were suspected of having a malignancy. The study is limited to the evaluation and follow-up of abnormalities positive at FDG PET and therefore does not provide information relative to the frequency of false-negative malignancies. Also, we were unable to perform histopathologic follow-up in 16 patients.

The reported findings demonstrate an increasing role of the radiologist and nuclear medicine physician in patient treatment and care. The observations demonstrate the ability of FDG PET to depict early malignancies; although the incidence is relatively low in our particular patient population, it does suggest the potential role in the evaluation of very high-risk individuals (eg, patients with a very strong family history of cancer or positive genetic screening results). This is presently limited because of the high cost of PET imaging and the lack of information regarding the cost/benefit analysis of PET for screening in this setting, and further studies are necessary.

	ACKNOWLEDGMENTS

 
The authors express their appreciation and thanks to Michael Petrenko, ARRT(R)(N), Gordon Tellefsen, BS, RT(N), Jorge Nuviola, AAS, RT, Paul Lizotte, RT, David Panush, MD, Patrick J. Toth, MD, Andrew Osiason, MD, Robert L. Krugman, MD, the Hackensack Radiology Group for their technical and clinical support, and Charles P. Weber, MA, for his support and editorial comments.

	FOOTNOTES

 
²_**. Multiple body systems

Abbreviations: FDG = fluorodeoxyglucose, SPN = solitary pulmonary nodule

Author contributions: Guarantor of integrity of entire study, H.A.; study concepts and design, H.A.; literature research, H.A., B.C.; clinical studies, H.A.; data acquisition, H.A.; data analysis/interpretation, H.A., B.C.; statistical analysis, H.A., B.C.; manuscript preparation, definition of intellectual content, editing, revision/review, and final version approval, H.A., B.C.

	REFERENCES

TOP ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS DISCUSSION REFERENCES

 

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