Noninvasive Detection of Clinically Occult Lymph-Node Metastases in Prostate Cancer
Mukesh G. Harisinghani, M.D., Jelle Barentsz, M.D., Ph.D., Peter F. Hahn, M.D., Ph.D., Willem M. Deserno, M.D., Shahin Tabatabaei, M.D., Christine Hulsbergen van de Kaa, M.D., Ph.D., Jean de la Rosette, M.D., Ph.D., and Ralph Weissleder, M.D., Ph.D.
Background Accurate detection of lymph-node metastases in prostatecancer is an essential component of the approach to treatment.We investigated whether highly lymphotropic superparamagneticnanoparticles, which gain access to lymph nodes by means ofinterstitial–lymphatic fluid transport, could be usedin conjunction with high-resolution magnetic resonance imaging(MRI) to reveal small nodal metastases.
Methods Eighty patients with presurgical clinical stage T1,T2, or T3 prostate cancer who underwent surgical lymph-noderesection or biopsy were enrolled. All patients were examinedby MRI before and 24 hours after the intravenous administrationof lymphotropic superparamagnetic nanoparticles (2.6 mg of ironper kilogram of body weight). The imaging results were correlatedwith histopathological findings.
Results Of the 334 lymph nodes that underwent resection or biopsy,63 (18.9 percent) from 33 patients (41 percent) had histopathologicallydetected metastases. Of these 63 nodes, 45 (71.4 percent) didnot fulfill the usual imaging criteria for malignancy. MRI withlymphotropic superparamagnetic nanoparticles correctly identifiedall patients with nodal metastases, and a node-by-node analysishad a significantly higher sensitivity than conventional MRI(90.5 percent vs. 35.4 percent, P<0.001) or nomograms.
Conclusions High-resolution MRI with magnetic nanoparticlesallows the detection of small and otherwise undetectable lymph-nodemetastases in patients with prostate cancer.
In 2001, about 198,000 new cases of prostate cancer were diagnosedin the United States and 31,500 men died of the disease.1 Thenatural history and aggressiveness of the disease vary widely,and the means to identify men with clinically occult lymph-nodemetastases is greatly needed.2,3,4,5,6,7,8 The adverse prognosticimplications of lymph-node metastases have been widely established.9,10
Magnetic resonance imaging (MRI) provides images with excellentanatomical detail and soft-tissue contrast but is relativelyinsensitive for the detection of lymph-node metastases.11 However,the results of MRI can be improved by using different imagingagents and acquisition techniques.12,13,14 In particular, theuse of lymphotropic superparamagnetic nanoparticles holds considerablepromise.15,16,17,18 As shown in Figure 1, these nanoparticleshave a monocrystalline, inverse spinel, superparamagnetic ironoxide core, contain a dense packing of dextrans to prolong theirtime in circulation, and are avidly taken up by lymph nodesin animals16 and humans.19 The nanoparticles are slowly extravasatedfrom the vascular into the interstitial space, from which theyare transported to lymph nodes by way of lymphatic vessels (Figure 1).16 Within the lymph nodes, lymphotropic superparamagneticnanoparticles are internalized by macrophages, and these intracellulariron-containing particles cause changes in magnetic propertiesdetectable by MRI.20
Figure 1. Electron Micrograph of Hexagonal Lymphotropic Superparamagnetic Nanoparticles (Panels A and B), Molecular Model of Surface-Bound 10-kD Dextrans and Packing of Iron Oxide Crystals (Panels C and D), and Mechanism of Action of Lymphotropic Superparamagnetic Nanoparticles (Panel E).
The model lymphotropic superparamagnetic nanoparticles shown here measure 2 to 3 nm on average (Panels A and B). The mean overall particle size of the 10-kD dextrans is 28 nm (Panels C and D). In Panel E, the systemically injected long-circulating particles gain access to the interstitium and are drained through lymphatic vessels. Disturbances in lymph flow or in nodal architecture caused by metastases lead to abnormal patterns of accumulation of lymphotropic superparamagnetic nanoparticles, which are detectable by MRI.
We investigated whether lymphotropic superparamagnetic nanoparticlescan be used in conjunction with MRI to detect metastatic tumorin local and distant lymph nodes in humans, as they have beenused in mouse models.20 We were particularly interested in casesin which metastases had not caused an increase in the size ofthe lymph node (clinically occult disease). We prospectivelydetermined the accuracy of the method in 334 lymph nodes in80 patients with biopsy-proven prostate cancer who subsequentlyunderwent resection of the tumor or pelvic lymph nodes (or both)or a targeted lymph-node biopsy.
Methods
Patients
Patients with a resectable prostate cancer as determined byconventional imaging methods, digital rectal examination, anultrasound-guided sextant core biopsy, and measurement of serumprostate-specific antigen levels were enrolled in this studyaccording to established surgical practice.21,22 All patientshad stage T1, T2, or T3 prostate cancer before surgical intervention.The first cohort consisted of 40 patients who were treated atMassachusetts General Hospital in Boston between 1999 and 2002.The second cohort consisted of 40 patients who were treatedat the University Medical Center in Nijmegen, the Netherlands,between 1999 and 2001. All 80 men gave informed written consentand completed the study. The studies were approved by the medicalethics committees of the respective hospitals.
Lymphotropic Superparamagnetic Nanoparticles
The lymphotropic superparamagnetic nanoparticle used in thisstudy was a monocrystalline iron oxide (Combidex, Advanced Magnetics,in the United States and Sinerem, Guerbet, in the Netherlands;Combidex and Sinerem are identical).23 The lyophilized ironoxide was reconstituted in normal saline and injected at a doseof 2.6 mg of iron per kilogram of body weight over a periodof 15 to 30 minutes. Five patients reported low back pain duringthe infusion, which disappeared after the infusion was temporarilystopped; the pain did not recur when the infusion was resumed.All patients received the full dose and completed the entirestudy.
Magnetic Resonance Imaging
MRI was performed at 1.5 T with the use of state-of-the-artimaging systems (Magnetom Vision, Siemens, in the 40 patientsin the Netherlands and Horizon, GE Medical Systems, in the 40patients in the United States) and pelvic phased-array coils.Images of the pelvis, extending from the pubic symphysis tothe level of aortic bifurcation, were obtained before and 24hours after the intravenous administration of lymphotropic superparamagneticnanoparticles. Details of the pulse sequences are given in Supplementary Appendix 1(available with the full text of this article athttp://www.nejm.org). The images were evaluated at workstationsin a blinded fashion by two experienced readers and analyzedas described below.
Image Analysis
On conventional MRI, lymph nodes were classified as malignantif the short-axis diameter was elongated and exceeded 10 mmor was rounded and exceeded 8 mm, according to standard criteria.24On MRI with lymphotropic superparamagnetic nanoparticles, nodeswere considered malignant when one of the following three criteriawere present: a decrease in signal intensity of less than 30percent on T2-weighted fast spin–echo or gradient-echosequences after the administration of lymphotropic superparamagneticnanoparticles; a heterogeneous signal (giving the entire nodea mottled appearance), discrete focal defects (isolated islandsof high signal intensity), or both; and nodes with a centralarea of hyperintensity (excluding a fatty hilum) but a peripheraldecrease in signal intensity. The signal-to-noise ratios oflymph nodes were determined by manually marking regions of interestover lymph nodes on different scans and pulse sequences. A receiver-operating-characteristic(ROC) curve analysis was also performed by two readers who wereunaware of the patients' serum prostate-specific antigen level,clinical stage, or Gleason score. The diagnostic standard washistopathological evaluation of each lymph node. Three-dimensionalreconstructions of the pelvic anatomy were also obtained (AdvantageWindows version 3.1, GE Medical Systems) in a subgroup of 40patients to aid in the approach to surgery and radiotherapy.
Surgery
Open resections were performed in 60 patients, and 15 patientsunderwent a laparoscopic resection. In five patients, the presenceor absence of nodal metastases in specific lymph nodes was ascertainedby computed-tomography–guided biopsy and no surgery wasperformed. Open and laparoscopic dissection of pelvic lymphnodes consisted of a generally accepted resection of left andright obturator lymph nodes and included more extensive explorationin nine patients because of suggestive findings on imaging.To ensure optimal correlation, the surgeon was given a schematicdrawing or a three-dimensional rendering identifying all thelymph nodes in relation to the iliac vessels. Resected nodeswere placed on a grid identifying their location and orientationand then sent for histopathological analysis. Multiple sectionsof all of the resected lymph nodes were stained with hematoxylinand eosin, and the slides were reviewed by at least two pathologistswho had no knowledge of the MRI findings. The histopathologicalresults for each lymph node were catalogued for subsequent comparisonwith MRI findings.
Statistical Analysis
The statistical significance of the sensitivities and specificitiesof conventional MRI and MRI with lymphotropic superparamagneticnanoparticles was calculated with the use of McNemar's test,and a two-tailed P value of less than 0.001 was considered toindicate statistical significance. For comparison among thegroups, Fisher's exact test was used, with a P value of lessthan 0.001 considered to indicate statistical significance.Accuracy was defined as the percentage of all patients or lymphnodes in which MRI with lymphotropic superparamagnetic nanoparticlescorrectly predicted the presence or absence of metastatic tumor,calculated with the following equation: (true positive + truenegative) ÷ (true positive + true negative + false positive+ false negative).
For the ROC analysis, the readers were asked to assign one offive confidence levels to each node. The readers had no knowledgeof the correct histopathological diagnosis. A binomial ROC curvewas fitted to the confidence rating assigned by each observerwith a maximum likelihood estimation.25 The diagnostic accuracyof MRI studies before and after the administration of lymphotropicsuperparamagnetic nanoparticles as determined by each observerwas evaluated by calculating the area under the ROC curve. Interobserveragreement with respect to the evaluation of both MRI studieswas assessed with use of the kappa statistic.26
The likelihood of lymph-node metastases on the basis of a nomogramwas calculated with the use of established criteria: low riskwas defined by an incidence of nodal metastases of less than4 percent if the serum prostate-specific antigen level was lessthan 10 ng per milliliter, the Gleason score was less than 6,and stage T1 prostate cancer was present; intermediate riskwas defined by 18 percent incidence of nodal metastases if theserum prostate-specific antigen level was 10 to 20 ng per milliliter,the Gleason score was 6 or 7, and stage T1 prostate cancer waspresent; and high risk was defined by a very high but variableincidence of nodal metastases if the serum prostate-specificantigen level exceeded 20 ng per milliliter, the Gleason scoreexceeded 7, and stage T2 or greater prostate cancer was present.27,28Statistical analysis was carried out with the use of SAS software.
Results
Characteristics of the Patients
A total of 80 patients with pathologically proven prostate cancerwere enrolled in the study (Table 1), and a total of 334 lymphnodes with direct MRI–histologic correlations were evaluated.Of the 334 lymph nodes, 271 were benign (81.1 percent) and 63lymph nodes (18.9 percent) — from 33 patients (41 percent)— contained microscopically detectable metastases. Ofthese 63 nodes, 17 measured less than 5 mm, 28 were 5 to 10mm, and 18 exceeded 10 mm. Overall, 71.4 percent of the malignantnodes did not fulfill the traditional imaging criteria for malignancy(more than 10 mm if elongated or more than 8 mm if rounded).
Table 1. Characteristics of the 80 Patients in the Study.
Diagnosis
Figure 2 shows representative examples of retroperitoneal imagesfrom three patients. In normal lymph nodes, the signal intensitydecreased homogeneously after the administration of lymphotropicsuperparamagnetic nanoparticles, indicating normal deliveryof the nanoparticles to the lymph nodes and normal uptake ofthe particles by nodal macrophages. In lymph nodes containingmetastases, there was either a limited decrease in signal intensityor discrete focal defects within the node owing to replacementof nodal architecture by tumor deposits. In the representativeexample shown in Figure 2G, Figure 2H, and Figure 2I, MRI withlymphotropic superparamagnetic nanoparticles facilitated thedetection of 2-mm metastases in retroperitoneal nodes. Figure 3Ashows a three-dimensional rendering of normal (green) andmetastatic (red) lymph nodes superimposed onto vascular mapsderived from the same imaging sequence. In this rendering, therelation of individual nodes to vascular landmarks can be established.This example also illustrates how readily malignant iliac nodescan be distinguished from adjacent benign nodes on MRI afterthe administration of lymphotropic superparamagnetic nanoparticles(Figure 3C) but not before (Figure 3B).
Figure 2. MRI Nodal Abnormalities in Three Patients with Prostate Cancer.
As compared with conventional MRI (Panel A), MRI obtained 24 hours after the administration of lymphotropic superparamagnetic nanoparticles (Panel B) shows a homogeneous decrease in signal intensity due to the accumulation of lymphotropic superparamagnetic nanoparticles in a normal lymph node in the left iliac region (arrow). Panel C shows the corresponding histologic findings (hematoxylin and eosin, x125). Conventional MRI shows a high signal intensity in an unenlarged iliac lymph node completely replaced by tumor (arrow in Panel D). Nodal signal intensity remains high (arrow in Panel E). Panel F shows the corresponding histologic findings (hematoxylin and eosin, x200). Conventional MRI shows high signal intensity in a retroperitoneal node with micrometastases (arrow in Panel G). MRI with lymphotropic superparamagnetic nanoparticles demonstrates two hyperintense foci (arrows in Panel H) within the node, corresponding to 2-mm metastases. Corresponding histologic analysis confirms the presence of adenocarcinoma within the node (Panel I, hematoxylin and eosin, x200).
Panel A shows a three-dimensional reconstruction of the prostate, iliac vessels, and metastatic (red) and nonmetastatic (green) lymph nodes, to assist in the planning of surgery and radiotherapy. There is a malignant node (thick arrow) immediately adjacent to the normal node (thin arrow) posteromedial to the iliac vessels. In Panel B, conventional MRI shows that the signal intensity is identical in the two nodes (arrows). In Panel C, MRI with lymphotropic superparamagnetic nanoparticles shows that the signal in the normal node is decreased (thick arrow) but that it is high in the metastatic node (thin arrow). In Panel D, abdominal CT fails to differentiate between the two lymph nodes (arrows). In Panel E, histopathological examination of the malignant lymph node reveals sheaths of carcinoma cells (hematoxylin and eosin, x200).
Sensitivity
Table 2 summarizes the quantitative analysis of all patientson the basis of objective changes in the signal intensity ofMRI. On MRI with lymphotropic superparamagnetic nanoparticles,the signal-to-noise ratios of normal nodes decreased from amean (±SD) of 192±24 to 69.7±16 on T2-weightedsequences, and the decrease was homogeneous across lymph nodes.Objective signs such as a limited decrease in signal intensity(P<0.001), the presence of hyperintense foci within nodes(P<0.001), or a mottled appearance on gradient-echo images(P<0.001) were all highly specific for nodal metastases.On a patient-by-patient analysis (Table 2), MRI with lymphotropicsuperparamagnetic nanoparticles correctly identified all patientswith metastases (100 percent sensitivity). Among patients freeof lymph-node metastases, MRI with lymphotropic superparamagneticnanoparticles provided the correct diagnosis in 96 percent.MRI with lymphotropic superparamagnetic nanoparticles was alsomore accurate than conventional MRI with respect to publishedand validated nomograms for predicting lymph-node metastases.27,28In the low-risk group of 12 patients, 1 had nodal metastases(true incidence, 8 percent; estimated risk, less than 4 percent).In the intermediate-risk group, 15 of 48 patients had nodalmetastases (true incidence, 31 percent; estimated risk, 18 percent),and in the high-risk group, 17 of 20 patients had metastases(true incidence, 85 percent).
Table 2. Sensitivity, Specificity, Accuracy, and Positive and Negative Predictive Values of MRI Alone and MRI with Lymphotropic Superparamagnetic Nanoparticles.
On a node-by-node basis, the overall sensitivity of MRI withlymphotropic superparamagnetic nanoparticles was 90.5 percentand was significantly higher (P<0.001) than that of conventionalMRI (sensitivity, 35.4 percent). Similarly, the administrationof lymphotropic superparamagnetic nanoparticles improved thediagnostic specificity from 90.4 percent to 97.8 percent. Forlymph nodes with a diameter of 5 to 10 mm on the short axis,which would be considered normal on conventional MRI, the sensitivityof MRI with lymphotropic superparamagnetic nanoparticles was96.4 percent. In all nine of the patients in whom the lattermethod suggested the presence of metastases in lymph nodes notclassically considered to be candidates for resection and whounderwent more extensive exploration, metastases were histologicallyconfirmed at distant sites. The false positive nodes were alllarger than 10 mm and showed reactive hyperplasia on staining,which most likely resulted in heterogeneous uptake of lymphotropicsuperparamagnetic nanoparticles. All false negative nodes hada short-axis diameter of less than 5 mm, which is probably belowthe current detection threshold of MRI. ROC analysis indicatedthat the areas under the curve were significantly higher forMRI with lymphotropic superparamagnetic nanoparticles than forconventional MRI (0.975 vs. 0.756, P<0.001).
Discussion
A sensitive and reliable means of detecting lymph-node metastasesin men with prostate cancer is important because patients withtruly local disease have the options of radical prostatectomy,watchful waiting, and radiotherapy.2,5 In men with locally advancedor metastatic disease, however, adjuvant androgen-deprivationtherapy with radiation is the mainstay of management.3,4,29
We found that lymph-node metastases can be accurately diagnosedby high-resolution MRI with lymphotropic superparamagnetic nanoparticlesbut not by conventional MRI. On a patient-by-patient basis,the addition of lymphotropic superparamagnetic nanoparticlesincreased the sensitivity of MRI from 45.4 percent to 100 percent,with a specificity of 95.7 percent. These results confirm earlierwork in animal models20 and preliminary observations in patientswith other types of cancer.19,30,31,32,33 Unexpectedly, evenvery small metastases — less than 2 mm in diameter —were occasionally identified within normal-sized lymph nodes.Such microscopic tumor deposits are below the threshold of detectionof any other imaging technique. For comparison, the limit ofdetection of tumor deposits in the pelvis on positron-emissiontomography is often 6 to 10 mm.34
Dissection of pelvic lymph nodes is the diagnostic standardfor detecting metastatic prostate cancer in iliac lymph nodesand is therefore performed with either an open or a laparoscopictechnique in most patients deemed candidates for surgery. Thisapproach, however, has several limitations. First, the areaof surgical exploration is limited to groups within the externaliliac obturator nodes, but so-called skip metastases to theinternal and common iliac nodes are not uncommon and go undetectedwith the use of this method. Nine examples of this phenomenonwere encountered in the 80 patients we studied. Second, therates of morbidity and complications of 4 to 5 percent withthis invasive technique are not negligible. Third, dissectionof pelvic lymph nodes is expensive and requires hospitalization.On average, the cost per metastasis diagnosed in patients witha low risk of postsurgical complications is approximately $43,600.Fourth, it is typically a one-time procedure performed at thebeginning of cancer treatment.35 Although these aspects of costand outcome of MRI with lymphotropic superparamagnetic nanoparticleswill have to be studied in larger, prospective clinical trials,this approach could provide clinical and cost benefits.
The routine imaging protocols used in this study are readilyavailable at most MRI centers. We found that the adapted three-dimensionalreconstruction techniques were of particular help in displayingand analyzing the massive amount of high-resolution data. Withthem, it is feasible to show both normal and abnormal lymphnodes and their location with respect to important surgicallandmarks such as vessels, obturator nerves, and ureters inthree dimensions.
Supported in part by departmental funds from both institutionsto defray imaging costs and by a grant from the National CancerInstitute (RO1CA59649, to Dr. Weissleder). The experimentalimaging agent was supplied to the investigators at no cost.
We are indebted to Alex F. Althausen, M.D., W. Scott McDougal,M.D., Francis J. McGovern, M.D., Donald S. Kaufman, M.D., DouglasM. Dahl, M.D., Chin Lee Wu, M.D., Mansi A. Saksena, M.D., JamesJ. Perumpillichira, M.D., Katharina Marten, M.D., James H. Thrall,M.D., Jack Wittenberg, M.D., and Peter R. Mueller, M.D. (allat Massachusetts General Hospital), and R.J.F. Laheij, Ph.D.(University Medical Center, Nijmegen), for facilitating theperformance of the trial; to Elkan F. Halpern, Ph.D. (MassachusettsGeneral Hospital), for help with the statistical analysis; andto Scott Gazelle, M.D., Ph.D., and Lee Josephson, Ph.D. (bothat Massachusetts General Hospital), for many helpful discussions.
Source Information
From Massachusetts General Hospital and Harvard Medical School, Boston (M.G.H., P.F.H., S.T., R.W.); and University Medical Center, Nijmegen, the Netherlands (J.B., W.M.D., C.H.K., J.R.). Drs. Harisinghani and Barentsz contributed equally to the article.
Address reprint requests to Dr. Weissleder at the Center for Molecular Imaging Research, Department of Radiology, Massachusetts General Hospital, Bldg. 149, 13th St., Rm. 5403, Charlestown, MA 02129-2060, or at weissleder{at}helix.mgh.harvard.edu.
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Korosoglou, G., Shah, S., Vonken, E.-J., Gilson, W. D., Schar, M., Tang, L., Kraitchman, D. L., Boston, R. C., Sosnovik, D. E., Weiss, R. G., Weissleder, R., Stuber, M.
(2008). Off-Resonance Angiography: A New Method to Depict Vessels--Phantom and Rabbit Studies. Radiology
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Mease, R. C., Dusich, C. L., Foss, C. A., Ravert, H. T., Dannals, R. F., Seidel, J., Prideaux, A., Fox, J. J., Sgouros, G., Kozikowski, A. P., Pomper, M. G.
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Guillem, J. G., Diaz-Gonzalez, J. A., Minsky, B. D., Valentini, V., Jeong, S.-Y., Rodriguez-Bigas, M. A., Coco, C., Leon, R., Hernandez-Lizoain, J. L., Aristu, J. J., Riedel, E. R., Nitti, D., Wong, W. D., Pucciarelli, S.
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Persigehl, T., Bieker, R., Matuszewski, L., Wall, A., Kessler, T., Kooijman, H., Meier, N., Ebert, W., Berdel, W. E., Heindel, W., Mesters, R. M., Bremer, C.
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Sosnovik, D. E., Nahrendorf, M., Deliolanis, N., Novikov, M., Aikawa, E., Josephson, L., Rosenzweig, A., Weissleder, R., Ntziachristos, V.
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Speight, J. L., Roach, M. III
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(2006). Cervical Lymph Node Metastases: MR Imaging of Gadofluorine M and Monocrystalline Iron Oxide Nanoparticle-47 in a Rabbit Model of Head and Neck Cancer. Radiology
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Zhu, J., Zhou, L., XingWu, F.
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Redston, M., Compton, C. C., Miedema, B. W., Niedzwiecki, D., Dowell, J. M., Jewell, S. D., Fleshman, J. M., Bem, J., Mayer, R. J., Bertagnolli, M. M.
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Deserno, W. M. L. L. G., Harisinghani, M. G., Taupitz, M., Jager, G. J., Witjes, J. A., Mulders, P. F., Hulsbergen van de Kaa, C. A., Kaufmann, D., Barentsz, J. O.
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(2004). Nanotechnology and Medicine. Radiology
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A correction has been published: N Engl J Med 2003;349(10):1010.
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