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Nuclear Magnetic Resonance Studies of Several Experimental and Human Malignant Tumors

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Nuclear Magnetic Resonance Studies of Several Experimental and Human Malignant Tumors [CANCER RESEARCH 33, 2156-2160, September 1973J Nuclear Magnetic Resonance Studies of Several Experimental and Human Malignant Tumors Donald P. i' James S. Economou, Leon C. Parks, Joseph C. Eggleston, Leon A. Saryan,2 and Jeffrey 1. Czeisler3 Departments ofPathologv (J. C. E.J and Physiological Chemistry [D. P. H., L. A. S., J. L. C.] and Division of Transplantation Surgery [J. S. E., L. C. P.]. The Johns Hopkins University School ofMedicine, Baltimore, Maryland 21205 SUMMARY induced fibrosarcoma produced in this laboratory were studied. All were transplantable solid tumors produced by Several animal and human malignant tumors were cx s.c. trocar injection. Control tissues were obtained from amined by nuclear magnetic resonance spectrometry. When normal animals of each of the mouse strains used. Four compared with normal tissue, the spin-lattice (T) magnetic human malignant tumors, 3 with normal tissue controls, relaxation times were longer for all tumors except one were obtained from the Division of Surgical Pathology. human sample. Comparable results were obtained for T1 They include an adenocarcinoma of the lung, a squamous measurements of cultured tumor cells. Possible mechanisms carcinoma of the renal pelvis, an adenocarcinoma of the for this effect are reviewed briefly and its potential in cancer colon, and stromatosis involving pelvic soft tissue. Samples diagnosis is discussed. of these tissues were excised from the surgically resected specimens and gently tamped into cellulose nitrate sample INTRODUCTION tubes. Four mouse tumors, maintained in standard culture Measurements of spin-lattice (T1) and spin-spin (T2) media (minimal essential medium, 20% fetal calf sera, magnetic relaxation times of the protons of tissue water antibiotics, North American Biologicals, Winnipeg, M ani were reported by Damadian (4) and subsequently by others toba. Canada), were also examined. Control tissues were (7, 10, 15) to discriminate between normal and malignant not available. tissue. The relaxation times T1 and T2 are time constants Specimens were packed into Beckman cellulose nitrate that describe the exponential return to equilibrium of the centrifuge tubes Y@inchin diameter and l-3@inch long for T1 nuclear magnetism of the water protons in directions measurement. Spin-lattice (T) magnetic relaxation times parallel or perpendicular, respectively, to the applied mag were measured using the null method (2) on a pulsed NMR4 netic field (12). spectrometer operating at 24 M Hz. Replicate measure When compared to normal tissues, malignant tumors ments were made as indicated in the tables. On a single have longer relaxation times. The physical nature of this specimen the T1 values were reproducible to about ±5%. phenomenon and its biological significance are poorly Readings were made at ambient temperature. understood. Measurements were unaffected when tissues were kept in This report presents spin-lattice (T1) relaxation times for airtight plastic tubes at room temperature for up to 12 hr. In 9 mouse tumors, 4 human malignant tumors, and assorted instances when measurements were not made immediately normal tissues. It is the most extensive study to date of after excision, the samples were kept in airtight tubes on ice animal experimental tumors. Measurements were also for less than 4 hr. Samples kept cold in this way before obtained for malignant cells maintained in culture. Possible measurement were allowed to equilibrate to room tempera clinical applications of this phenomenon and its underlying ture before being placed in the spectrometer. Relaxation physical mechanism are discussed. times did not vary with sample packing or orientation of the sample in the probe. Representative samples of all tumors and the human MATERIALS AND METHODS control tissues were fixed in 10% formalin and imbedded in paraffin. Hematoxylin- and eosin-stained sections, cut at 6 Eight mouse tumors obtained from The Jackson Labora zm were examined by light microscopy. tory, Bar Harbour, Maine, and a methylcholanthrene 1 Recipient of a career development award from the NIH. To whom RESULTS requests for reprints should be addressed, at Department of Physiological Chemistry, Wood Basic Science Building, The Johns Hopkins University TI relaxation times for the transplantable mouse tumors School of Medicine, 725 N. Wolfe Street, Baltimore, Md. 21205. 2 Recipient of a predoctoral traineeship from the NIH. and control tissues are presented in Tables I to 3. The T1's 3 Recipient of a postdoctoral fellowship from the NIH. Received January 22. 1973; accepted May 29, 1973. ‘Theabbreviation used is: NMR, nuclear magnetic resonance. 2156 CANCER RESEARCH VOL. 33 Downloaded from cancerres.aacrjournals.org on September 29, 2021. © 1973 American Association for Cancer Research. NMR Studies of Malignant Tumors Table I Spin-lattice relaxation times for transplantable mouse tumors From each of 3 mice, as many as 3 different samples of each tumor type were measured, depending on the amount of tumor tissue available.JacksonT1 (msec)Mouse IIIMouseLabora IMouse 11Mouse no.Tumor no.Sample no.Sample toriesSample 3AdenocarcinomaC57BL/6JBW10232822typestrainCode no.1 2 31 2 31 2 787Anaplastic 815 808791 772 808805 778 654FibrosarcomaC57BL/6JOurcarcinomaA/i15091 A670 673 661637662 749LymphosarcomaC3H/HEJ6C3HED803 lab 625 640596 605731 725 oratory621 847MelanomaC57BL/6JB16695 815 668Prepuptial 690 741746 730 760660 681 tumorC57BL/6JESR586758675RhabdomyosarcomaCE/JBWIOI39705gland 749Round 702 693720 693 679738 745 627Spindlecell tumorA/JC1300593 635 696681 633 cellcarcinomaA/iSal681 628 649681 660 682687 685 693 Table 2 measured, except in cases where the tumor size was too Spin-lattice relaxation times for normal mouse tissue, strain C57BL/6J small to provide 3 specimens. In Table 2, a study of 10 Two samples of liver and I sample each of4 other tissues are presented. control mice of the C57BL/6J strain showed that for 60 T1 (msec)Skeletal normal tissue samples no control Ti overlapped with any tumor TL . In Table 3, it is shown that individual normal specimens from other mouse strains have values comparable MouseBrain1 Liver Kidney Spleen muscle to those for the C57BL/6J mice. The data seem sufficient to support the principal conclusion that the T1 of the various 292,291 351 444 454 483 normal mouse tissues examined do not overlap with the 2 229,238 284 333 386 465 3 259,261 286 312 378 456 values for any of the tumors examined. The difference 4 251,269 284 337 352 480 between relaxation times of normal and malignant tissues 5 246,252 284 316 396 461 holds on a statistical as well as an individual basis. For 6 285,277 242 416 415 478 comparison, T1 values for 4 mousetumors grown in tissue 7 239,252 259 358 513 8 295,307 319 338 448 506 culture were obtained as shown in Table 4. That the 9 287,287 318 368 464 470 phenomenon of T1 elevation for tumors is a characteristic of 520Av.10 301,301 316 432 454 the cancer cell and not merely a function of cell packing or extracellular material is suggested by the observation (Table 271 ±24 294 ±3022Table 366 ±48 411 ±40 483 ± 4) of elevated T1 values for malignant cells maintained in tissue culture. Control cultured cells were not available. The 3 T1 values observed for the cultured tumor cells are above the Spin-lattice relaxation times for normaltissueT1 mouse range observed for normal tissues and are comparable to the (msec)C57BL/6J corresponding in vivo tumors. A spleen from a lymphosarcoma-bearing mouse, grossly A/i CE/J thought to be normal, registered a high T1 of 612 msec. mouseBrainTissue type mouse mouse Subsequent microscopic examination revealed partial in volvement of the splenic tissue by lymphosarcoma cells as 526 508 518 well as scattered large bizarre cells interpreted as atypical Lung 491 500 482 Heart 490 476 482 megak a ryocytes. Liver 263 283 296 Histological examination of representative samples of the Spleen 458 433 399 9 mouse tumors used in this study was performed in an Kidney 370 314 286 attempt to correlate T1valueswith morphological features. Skeletal muscle 471 415 372 The percentage of each tissue sample uninvolved by tumor Small intestine 255 357 Tail 218 207 216 was noted, as was the extent of necrosis within each tumor. Skin 199 186 194 In addition, semiquantitative comparisons of cell size, Ribs and muscle 421 390 nuclear-cytoplasmic ratio and number of mitotic figures Testis 205 were made, as well as a subjective determination of the degree of cytoplasmic differentiation of each tumor. ranged from 593 to 847 msec for the 9 tumor types studied None of the features evaluated could be correlated with and from 186 to 526 msec. for the various control tissues. the degree of elevation of the T1 values. However, the T1 For the tumor data (Table 1), as many as 3 different determinations and the morphological evaluations for each samples of each tumor type from each of 3 mice were tumor were performed on adjacent samples oftissue, not on SEPTEMBER 1973 2157 Downloaded from cancerres.aacrjournals.org on September 29, 2021. © 1973 American Association for Cancer Research. Hol!is, Economou, Parks. Eggleston, Saryan, Czeisler Table 4 1.165 sec compared to 0.776 sec for normal lung. Details of Spin-lattice relaxation times of mouse tumors maintained in standard the individual measurements are not available to us at culture media present. It may be significant, however, that the uninvolved (msec)MouseCode host lung that we examined could not be considered as Cultured tissue normal and showed focal atelectasis and inflammation as sampje(msec)HepatomaC57L/JBW7756600MelanomaC57BL/6JBl6620FibrosarcomaC57BL/6JOur (pellet)T1 no.T1 well as other abnormalities as described in “Results.―This raises the possibility that abnormal states other than cancer might produce elevated T1 values, an eventuality which laboratory619AnaplasticA/J15091 could have profound consequences in any serious considera A697carcinoma tion of NMR as a diagnostic tool.
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