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Hi, two years ago, my father was diagnosed with CREST Syndrome as well as with Overlap Syndrome.
This year my father got really ill. He suffered from two episodes of oesophageal bleeding ; in the course of the last bleed, he nearly died. Since then oesophageal varices continued to develop and new varices were found last week.
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Appeal from the Circuit Court of McLean County; the Hon.
Luther H. Dearborn, Judge, presiding.
On August 9, 1977, the plaintiff, Shirley Sears, filed a complaint in the circuit court of McLean County alleging that (1) the defendant, Julie Rutishauser, negligently operated her automobile, and (2) as a direct and proximate cause of the defendant's negligent acts the plaintiff sustained permanent personal injuries. Following a jury trial, the trial court entered a judgment against the defendant on June 24, 1982, awarding the plaintiff $40,000 in damages. The defendant appeals. We affirm.
On appeal, the defendant maintains that (1) the trial court erred in refusing to allow the defendant to cross-examine one of the plaintiff's treating physicians about the number and frequency of patient referrals which that physician had received from plaintiff's counsel, (2) the trial court erred in allowing plaintiff to introduce into evidence certain cross-examination testimony which allegedly was beyond the scope of the defendant's direct examination, and (3) the closing rebuttal argument of plaintiff's counsel was so prejudicial as to deny the defendant her right to a fair trial.
Because no question is raised concerning the sufficiency of proof, we discuss the evidence only briefly. The plaintiff testified at trial that at approximately 8:15 a.m. on February 14, 1977, she was proceeding eastbound on Vernon Avenue, a four-lane street in Normal. Noting that the roads were slippery because of a recent snowfall, the plaintiff drove in the lane next to the curb at a speed of approximately 15 miles per hour. Immediately prior to the accident, the plaintiff observed the defendant's vehicle traveling westbound on Vernon Avenue and estimated its speed at 40 miles per hour. As the defendant's vehicle drew near it went into a skid, spun around into the eastbound lane, and the right rear portion of the defendant's vehicle struck the left fender and hood of the plaintiff's vehicle while both vehicles were still moving.
The defendant's testimony concerning the circumstances surrounding the accident was substantially similar to that of the plaintiff. However, the defendant did state that after her vehicle hit a patch of ice, crossed the center line and came to rest against the south curb of Vernon Avenue, she had been stopped for less than five seconds when plaintiff's vehicle struck the rear of defendant's vehicle. The defendant also stated that she had been traveling at a rate of 25 miles per hour immediately before she encountered the patch of ice.
The plaintiff testified that following the accident she developed pain and stiffness in her neck and in the right top portion of her body. As to her symptoms at the time of trial, the plaintiff stated that (1) her right hand and arm felt as though they were asleep and she had a loss of strength in that arm, and (2) she was unable to raise her right hand or arm above her head and her neck was stiff and painful.
During the approximately five-year period between the automobile accident and the jury trial, the plaintiff was treated by various doctors. At trial, the plaintiff relied primarily on the testimony of three of those doctors. Dr. John Wright testified that, in his opinion, the plaintiff had an acute cervical strain with contractures and disuse changes caused by the automobile accident. In his evidence deposition, Dr. Hugh McMenamin stated that the plaintiff had cervical radiculitis and shoulder encapsulitus, or frozen shoulder. Dr. Donald Rumer, the plaintiff's treating physician at the time of the trial, stated that (1) the plaintiff had thoracic outlet syndrome, and (2) the plaintiff's permanent injuries were among the worst he had ever treated.
The defendant introduced the testimony of Dr. Rieber Hovde, the plaintiff's family doctor at the time of the accident. Dr. Hovde testified that (1) the plaintiff had osteoarthritis which had existed prior to the automobile accident, (2) her injuries resulting from the accident were minor, (3) she had only a slight loss of motion in her neck which was both psychological and physiological in nature, and (4) she did not have thoracic outlet syndrome.
Prior to trial, the defendant filed a motion in limine requesting that the trial court prohibit the plaintiff from offering the testimony of Dr. Rumer, unless the doctor personally appeared at trial and produced the files of all the patients he had treated in the preceding four years on referral from attorney Jerome Mirza. Although Mr. Mirza was not trial counsel, his firm was representing plaintiff. During a hearing on this motion, the defendant argued that she should be allowed to introduce evidence concerning the number and frequency of client referrals from Mr. Mirza to Dr. Rumer in order to question Dr. Rumer's credibility by showing bias and interest on his part in testifying for the plaintiff, who had also been referred to Dr. Rumer by Mr. Mirza. Relying on the case of Davis v. Gulf, Mobile & Ohio R.R. Co. (1971), 130 Ill. App.2d 988, 272 N.E.2d 240, the trial court determined that Dr. Rumer could be asked whether he had received other referrals from Mr. Mirza, but he could not be asked about the number or frequency of those referrals.
The defendant argues that the trial court erred in refusing to allow Dr. Rumer to be cross-examined concerning the number and frequency of patient referrals which he had received from Mr. Mirza. The defendant points out that (1) the plaintiff's expert, Dr. Rumer, and the defendant's expert, Dr. Hovde, disagreed as to the cause and extent of the plaintiff's injuries, and (2) this conflict between the experts made the credibility of Dr. Rumer and Dr. Hovde an important consideration.
The Davis case is the only Illinois case dealing with the issue of whether a party's treating physician may be cross-examined concerning the frequency of referrals he has received from the party's counsel. Although the final form of the Davis opinion is disputed, the court clearly held that no error resulted merely because the trial court permitted such cross-examination. The court indicated that whether to permit the cross-examination was a matter of discretion for the trial court. Analogy was drawn to McMahon v. Chicago City Ry. Co. (1909), 239 Ill. 334, 88 N.E. 223, where the court held that a similar discretion existed concerning the frequency with which a physician had testified for the various street car lines of Chicago. In McMahon, the trial court had exercised its discretion by allowing the cross-examination. Courts> in other States have held that allowance of cross-examination of a physician as to the frequency of referrals to him by the opposing party's counsel was not error. See Wilson v. Stilwill (1981), 411 Mich. 587, 309 N.W.2d 898, and Ager v. Baltimore Transit Co. (1957), 213 Md. 414, 132 A.2d 469.
We also note that Professors Cleary and Graham state in section 705.2 of their treatise that:
"Inquiry into compensation [of expert witnesses] is a matter of right. [Citation.] Prior employment by the same party may be brought out [McMahon], as well as referrals from the same attorney [Davis]; but refusal to permit questions as to a consistent pattern of testifying for parties with similar interests in other cases has been sustained. Chicago & Eastern Illinois R.R. Co. v. Schmitz (1904), 211 Ill. 446, 71 N.E. 1050. In the latter situation, if the showing is sufficient to cast substantial doubt on the good faith and integrity of the witness, the inquiry would seem in principle to be allowable within the discretion of the trial judge, despite the risk of collateral issues." E. Cleary & M. Graham, Handbook of Illinois Evidence sec. 705.2, at 385 (3d ed. 1979).
We conclude that the issue of whether to allow cross-examination of an expert medical witness concerning the frequency of his patient referrals from a party's attorney is within the discretion of the trial court. However, in this case, the issue involves matters collateral to the question of the extent of the party's injury. Here, defendant's offer of proof indicated that Dr. Rumer was uncertain as to the frequency of the referrals. Defense counsel's request for Dr. Rumer's records indicated that lengthy questioning might be necessary if the matter was pursued. The trial court seemed to be under the impression that because of the precedent of Davis it "probably" could not properly permit the cross-examination. However, the court's remarks permit the inference that it would not have permitted the cross-examination even if it had discretion. The court's ruling was not error.
The defendant's next contention concerns the introduction of Dr. Hugh McMenamin's testimony which was relied upon by the plaintiff at trial. This testimony consisted of portions of Dr. McMenamin's cross-examination by plaintiff during an evidence deposition taken by defendant. The defendant maintains that (1) this cross-examination exceeded the scope of the direct examination conducted by defense counsel in taking the evidence deposition, and (2) the procedure used allowed the plaintiff to present Dr. McMenamin's entire course of treatment of the plaintiff through the use of leading questions.
Defense counsel's direct examination of Dr. McMenamin, which dealt primarily with his opinion concerning the use of two drugs prescribed by Dr. Rumer for the plaintiff, included the following questions:
"Q. Did you feel that when you saw this woman and treated her that there would be any guarantee that this particular drug of Prednisone would give any significant relief to her?"
"Q. Now, as far as Prednisone, would you use that in reference to the treatment of a woman with the complaints that she told you about?"
"Q. Isn't it true that unless you are absolutely up against the wall, that you wouldn't use Butazolidin in reference to your treatment of this woman?"
The scope of cross-examination is an issue which lies largely within the discretion of the trial court. (Biel v. Wolff (1970), 126 Ill. App.2d 209, 261 N.E.2d 474.) In propounding the foregoing questions to Dr. McMenamin, defense counsel was delving into the treatment prescribed by Dr. McMenamin for the plaintiff. The trial court did not abuse its discretion in ruling that the plaintiff's cross-examination of Dr. McMenamin concerning the details of that treatment did not exceed the scope of the direct examination.
Finally, we consider defendant's assertion that plaintiff's rebuttal closing argument was so prejudicial as to deny her a fair trial. Plaintiff's counsel said defense counsel had "just plain misstated" certain matters, that doing so was "inexcusable," and that the number of times he had done so was such that "it could not have been unintentional." Plaintiff's counsel also asserted that defense counsel (1) stated things that were inaccurate, (2) "twisted" things in a way which "just [was not] true," (3) threw "mud," (4) did not tell the truth in summarizing the testimony of a physician, and (5) insulted the jury by changing the testimony as often as he did. Near the conclusion of his argument, plaintiff's counsel stated:
"I am depending on the twelve of you to have remembered that testimony and not let this man get away with changing that testimony in closing argument."
Defendant argues that the foregoing comments (1) made a direct appeal to the passion and prejudice of the jury, (2) branded defense counsel as a liar, (3) told the jury that the lies were an insult to them, and (4) requested the jury to punish defendant for these lies. In support of these contentions the defendant relies primarily on Manninger v. Chicago & Northwestern Transportation Co. (1978), 64 Ill. App.3d 719, 381 N.E.2d 383, Cecil v. Gibson (1976), 37 Ill. App.3d 710, 346 N.E.2d 448, and Paulsen v. Gateway Transportation Co. (1969), 114 Ill. App.2d 241, 252 N.E.2d 406.
In Manninger, plaintiff's counsel during his closing argument asserted that defense counsel had prepared the testimony for the defense witnesses and told them what to say in order to defeat plaintiff's claim. The appellate court concluded that this closing argument accused defense counsel of subornation of perjury and suppression and distortion of evidence and deprived the defendant of a fair trial.
In Cecil, defense counsel in his closing argument referred to plaintiffs' counsel as a "slick attorney from Chicago" and a "slick hiredhand" and claimed that plaintiffs' counsel "manufactured" evidence, had a "wild imagination," and was not worthy of the jury's trust. (Cecil v. Gibson (1976), 37 Ill. App.3d 710, 711, 346 N.E.2d 448, 449.) The appellate court determined that defense counsel's closing argument was grossly prejudicial and denied the plaintiffs their right to a fair trial.
In Paulsen, plaintiff's counsel during his closing argument referred to defense counsel as "this man who plays fast and loose with the facts in this case." Plaintiff's counsel also stated:
"`[Defense counsel] is trying to change the facts by trickery, he is trying to change the situation, he is trying to color the facts, to distort the facts and take them out of context.
But I'm up to his gimmicks, I'm up to his tricks.'" (Paulsen v. Gateway Transportation Co. (1969), 114 Ill. App.2d 241, 245, 252 N.E.2d 406, 408.)
The Paulsen court condemned these remarks and others as having no application to the factual issues of the case and reversed the judgment for the plaintiff. The court stated that the argument was "an unwarranted characterization of defendant's counsel and a successful effort to belittle, impugn and ridicule him and thus deprive the defendant of fair treatment by the jury." 114 Ill. App.2d 241, 247, 252 N.E.2d 406, 409.
Plaintiff's counsel in Paulsen also accused defense counsel of torturing the plaintiff by asking her if she should have a myelogram and stated that the defendant had put her in the hospital by its negligent conduct and then wanted to "`* * * subject her to this horrifying, terrible ordeal of another jab with the needle into her back * * *.'" 114 Ill. App.2d 241, 246, 252 N.E.2d 406, 409.
Here, unlike in Manninger and Cecil, plaintiff's argument contained no accusations of perjury, suppression of evidence, or creation of "manufactured" evidence. This case is more like Paulsen in that the argument complained of the accuracy with which opposing counsel recited the evidence and stated that opposing counsel had misstated the evidence intentionally. However, here plaintiff's counsel did not accuse the defense of wishing to torture the plaintiff.
Counsel may, of course, dispute the accuracy of opposing counsel's interpretation of the evidence and may also comment upon the extent of the inaccuracies. No exact line can be drawn as to how far, beyond that point, one's argument may go in criticizing opposing counsel's accuracy. In the heat of trial where each counsel has ridiculed the other's argument, accusations are often made which would have been better left unsaid. Such was the case here when plaintiff's counsel stated that defense counsel "did not tell the truth" and made other comments implying that he had lied. However, considering the vigorous nature of the arguments on both sides and the fact that the size of the verdict did not indicate prejudice against defendant, we hold that plaintiff's argument did not deprive defendant of a fair trial. We need not consider whether defendant waived error in plaintiff's argument by failing to object or to demand rulings on the objections that were made. No reversible error occurred.
For the foregoing reasons we affirm the judgment entered by the circuit court of McLean County.
MILLS, J., concurs.
PRESIDING JUSTICE WEBBER, concurring in part and dissenting in part:
I agree with my learned colleagues that no error occurred in the treatment of Dr. McMenamin's testimony; however, I differ seriously with them on the matters concerning the cross-examination of Dr. Rumer and the rebuttal argument of plaintiff's counsel.
The handling of expert witnesses and their cross-examination may be summed up in the old adage, "Whose bread I eat, his song I sing." One need only scan the professional journals to observe that experts are for hire in the market place on an almost illimitable number of "specialties." In this era of complex technology and with a litigation explosion of geometric proportions, especially in the fields of products liability and malpractice, these persons are essential for the jury's understanding of the subject matter of lawsuits. However, the corollary to this proposition is that they are hired partisans and in judging their testimony the jury is entitled to know whence they came. This is especially true when, as in the instant case, the duel of the experts is one-on-one. It would be a rare case today when the expert witness is the saintly country doctor or the kindly county surveyor, known to the whole community including the jury.
It then follows that the widest latitude should be allowed in presenting anything, including relationships with the parties or their counsel, which might affect the credibility of the witness.
I do not read Davis with quite the same aplomb as does the majority. A close inspection of that opinion reveals that much of what was said in it was irrelevant to the precise problem presented. Moreover, the text as set forth in the official reports (Davis v. Gulf, Mobile & Ohio R.R. Co. (1971), 130 Ill. App.2d 988) is not the final one. The records in the office of the Clerk of the Fifth Appellate District show that the opinion was revised upon denial of rehearing and the revised opinion was filed June 22, 1971. The final version is correctly reported at 272 N.E.2d 240.
In Davis the defendant in cross-examination sought to undermine the credibility of a medical witness by showing that he had referrals from plaintiff's counsel. Ten individuals were apparently mentioned who either had had, or then had, suits against railroads and were represented by plaintiff's counsel. In eight of the 10 the doctor remembered the patient or the patient's name but did not know who had referred him, and in two cases did not remember the patient. In only one case out of seven did the doctor remember testifying against a railroad. In this state of the record "both counsel made reference to the fact that plaintiff's attorney had sent the plaintiff to consult Dr. Deyton. There was no testimony of the witnesses to support this statement of both counsel." (Emphasis added.) (272 N.E.2d 240, 243.) "Defendant offered no evidence to support the inference of bias which the specific inquiries raised by suggestion of counsel that each had been referred by plaintiff's counsel." 272 N.E.2d 240, 243-44.
In lieu of headnote 1 in the Official Reports (130 Ill. App.2d 988, 992) the following appears at 272 N.E.2d 240, 244-45:
"In the present case the Doctor was not asked whether he testified only for plaintiffs on cross-examination, but stated that he had received referrals from plaintiffs' counsel but could not state how many nor whether they could be described as frequent. The Doctor's admission that he had received referrals from plaintiffs' counsel raised an inference of bias, and it was the Doctor's subsequent evasive answers concerning the frequency that allowed the court to exercise its discretion as to whether specific cases should be shown in this particular case. However, the evidence elicited did not support the suggestions that any of the 10 individual cases had been referred by plaintiff's counsel, and defendant offered no evidence that any of those 10 had been referred by plaintiff's counsel. In Chicago City Ry. Co. v. Smith, 226 Ill. 178 at page 187, 80 N.E. 716, at page 720, the Court stated:
`Conceding appellants right of cross-examination to discover the motives, feelings and prejudices of a witness, still we are not inclined to hold that there was any error committed in refusing to allow the cross-examination to be extended to other cases having no connection with the case then being tried.'
In C. & E.I. Railroad v. Schmitz, 211 Ill. 446, 72 N.E. 150, the Court stated:
`It was also sought by the Appellants to show by direct examination of certain witnesses that the physician in question was interested as a medical man in a large number of personal injury suits against corporations. This class of testimony the trial court refused to admit. Cross-examination upon independent cases of the same character, and about the same time as the principal case, is not allowed.'
From the authorities cited herein, we conclude that under ordinary circumstances, having shown the relationship between the Doctor and plaintiff's counsel there is no proper basis for going into specific cases, and to do so would be reversible error, however, under the circumstances here present, permitting interrogation with respect to specific cases without the defendant then offering evidence of the relationship in those specific cases was error, but under the circumstances here present, not reversible error."
From these excerpts it is apparent that the real problem in Davis was not the legitimacy of the cross-examination which produced nothing of value, but the fact that argument was made based on assumptions not established in the record.
The problem in the instant case is that defendant was prevented by the trial court from making a record. Prior to trial, the defendant filed a motion in limine requesting that the trial court prohibit the plaintiff from offering the testimony of Dr. Rumer, unless the doctor personally appeared at trial and produced the files of all the patients he had treated in the preceding four years on referral from plaintiff's attorney. During a hearing on this motion, the defendant argued that she should be allowed to introduce evidence concerning the number and frequency of client referrals to Dr. Rumer in order to question Dr. Rumer's credibility and show bias and interest on his part in testifying for the plaintiff who had also been referred to Dr. Rumer by her counsel. The defendant noted that Dr. Rumer would not be asked to disclose the names of his other patients or identify them in any way, but that the files were necessary for cross-examination about the frequency and number of referrals from plaintiff's counsel.
The court granted the defendant's motion in limine in part and denied it in part. The trial court ruled that because of a prior stipulation between the parties, Dr. Rumer had to testify in person rather than by evidence deposition. However, the trial court refused to require the doctor to produce records of other patients who had been referred to him by Mr. Mirza. In the opinion of the court, the doctor could be asked whether he had received other referrals from plaintiff's attorney but he would not be asked about the number or frequency of those referrals.
Defendant was thus denied an opportunity to lay the foundation for showing the bias of Dr. Rumer. The motion was renewed at the close of Rumer's direct examination and again denied by the trial court, relying on Davis. As an offer of proof, defendant was compelled to use a deposition made by Rumer who was singularly evasive on the subject.
In my judgment Davis does not stand for the proposition that inquiry is forfended into a relationship between an expert witness and counsel; it stands only for the familiar doctrine that matters not in evidence cannot be argued to the jury. The Davis court appeared distracted in its gratuitous discussion of the former.
The older authorities cited in Davis, i.e., Handy, McMahon, Plambeck, belong to an earlier, simpler age. They need reexamination. In my judgment the Michigan and Maryland cases mentioned in the principal opinion, Wilson and Ager, together with the statement of Cleary & Graham, indicate the modern rule. In Wilson it is said:
"An expert witness's experience testifying in court may influence the manner in which he or she testifies. The same is true for experience in evaluating cases which may come to court. It is thus proper to bring out on cross-examination the number of times a witness testifies in court, or is involved in particular types of cases.
A showing of a pattern of testimony for a particular attorney in past cases raises a possible inference that the witness has testified in such a manner that he would be hired in future cases." 411 Mich. 587, 599-600, 309 N.W.2d 898, 902.
To the same effect is a statement by the Ager court:
"This Court has held on many occasions that evidence tending to establish possible interest, bias or prejudice on the part of a witness is admissible as an aid in testing the weight and credit to be afforded his testimony. A situation, almost identical to the one in this case, arose in the Supreme Court of Missouri in the case of Lammert v. Wells, 321 Mo. 952, 13 S.W.2d 547. That Court held that the evidence tended to show the relation existing between the witness and the attorney, and was proper for the consideration of the jury as showing possible interest or bias." 213 Md. 414, 427-28, 132 A.2d 469, 476-77.
In my judgment the proper rule is that while some discretion must be left with the trial court in order to prevent abuse, that discretion is limited. The question should never be settled on a motion in limine. If doubt exists, an offer of proof should be taken from the witness himself. If the party seeking to impugn the testimony of the expert makes a prima facie showing of the relationship, he should then be permitted to present the matter to the jury under the usual and normal rules of cross-examination. The fact that this might be lengthy is no reason for denying the party his opportunity to attack the credibility of the expert. It is just one of the facts of modern legal life.
The trial court in this case was in error on this issue and I would reverse for a new trial on that basis alone.
As to the rebuttal argument, it is true that it did not rise to the level of the invective hurled by John Randolph against Henry Clay, "So brilliant, yet so corrupt, which, like a rotten mackerel by moonlight, shines and stinks." Nonetheless, in my judgment it exceeded the bounds of propriety. If there is a dispute over the meaning of evidence or inferences to be drawn therefrom, that can be so stated without subtly, or otherwise, vilifying opposing counsel. Such conduct belongs to the days when court was a form of theater and I hope that those days died with the Scopes trial.
I would reverse and remand for a new trial.
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A fast and quantitative 2D high-resolution magic angle spinning (HR-MAS) total correlation spectroscopy (TOCSY) experiment was developed to resolve and quantify the choline- and ethanolamine-containing metabolites in human prostate tissues in ≈1 hr prior to pathologic analysis. At a 40-ms mixing time, magnetization transfer efficiency constants were empirically determined in solution and used to calculate metabolite concentrations in tissue. Phosphocholine (PC) was observed in 11/15 (73%) cancer tissues but only 6/32 (19%) benign tissues. PC was significantly higher (0.39 ± 0.40 mmol/kg vs. 0.02 ± 0.07 mmol/kg, z = 3.5), while ethanolamine (Eth) was significantly lower in cancer versus benign prostate tissues (1.0 ± 0.8 mmol/kg vs. 2.3 ± 1.9 mmol/kg, z = 3.3). Glycerophosphocholine (GPC) (0.57± 0.87 mmol/kg vs. 0.29± 0.26 mmol/kg, z = 1.2), phosphoethanolamine (PE) (4.4± 2.2 mmol/kg vs. 3.4± 2.6 mmol/kg, z = 1.4), and glycerophosphoethanolamine (GPE) (0.54± 0.82 mmol/kg vs. 0.15± 0.15 mmol/kg, z = 1.8) were higher in cancer versus benign prostate tissues. The ratios of PC/GPC (3.5± 4.5 vs. 0.32± 1.4, z = 2.6), PC/PE (0.08± 0.08 vs. 0.01± 0.03, z = 3.5), PE/Eth (16± 22 vs. 2.2± 2.0, z = 2.4), and GPE/Eth (0.41± 0.51 vs. 0.06± 0.06, z = 2.6) were also significantly higher in cancer versus benign tissues. All samples were pathologically interpretable following HR-MAS analysis; however, degradation experiments showed that PC, GPC, PE, and GPE decreased 7.7± 2.2%, while Cho+mI and Eth increased 18% in 1 hr at 1°C and a 2250 Hz spin rate.
The choline- (Cho) and ethanolamine (Eth)-containing metabolites are major cytosolic precursors and degradation products of phospholipid membrane assembly and catabolism (1). There is currently much interest in correlating the individual Cho- and Eth-containing metabolites with cancer presence, aggressiveness, and therapeutic response because of the information they contain about cellular proliferation, apoptosis, and the activity of key enzymes (2-7). Historically, 31P spectroscopy has been used both in vitro (8-12) and in vivo (13-15) to resolve the phosphomonoesters (phosphocholine [PC] and phosphoethanolamine [PE]) and phosphodiesters (glycerophosphocholine [GPC] and glycerophosphoethanolamine [GPE]). 1H spectroscopy has mainly focused on detection of the choline head group singlets of free Cho, PC, and GPC (16-18), which give rise to a composite choline peak at ≈3.2 ppm in vivo (19). Although Cho, PC, and GPC can be resolved from each other in extracts, they cannot typically be resolved from each other in intact prostate tissue at 11.7T, and free ethanolamine (Eth), PE, GPE, glucose, taurine, and myo-inositol (mI) also co-resonate in this highly overlapping region (17).
Total correlation spectroscopy (TOCSY) (20) is a powerful 2D NMR experiment which has previously been used in HR-MAS studies of cultured melanoma cells (21) and intact prostate (22), liver (23,24), brain (25), and kidney (26) tissues. In TOCSY, an isotropic mixing pulse is used to transfer magnetization between protons within a spin system such that, depending on the duration of the mixing time, correlations can be observed between protons that are several bonds apart. One advantage of TOCSY over conventional correlation spectroscopy (COSY) is that the cross-peak multiplets have an absorption phase rather than dispersive phase character. Consequently, TOCSY can be used quantitatively provided the magnetization transfer (MT) efficiency is known for the specific metabolites under investigation at the mixing time being used (27). Recent studies have demonstrated that TOCSY can be used to resolve and quantify the sidechain CH2-CH2 cross-peaks of several Cho- and Eth-containing metabolites, including PC, GPC, Eth, PE, and GPE (21,22). For the Cho and Eth metabolites, the sidechain methylene protons give rise to a single cross-peak on each side of the diagonal, which simplifies their quantification compared to more complicated spin systems (e.g., myo-inositol).
Previous studies have also demonstrated that rotor synchronization, in which the duration of the isotropic mixing pulses are matched to the reciprocal of the spin rate, is crucial for TOCSY experiments under HR-MAS conditions (22,28). Because of their insensitivity to RF (B1) imperfections, adiabatic mixing pulses (e.g., WURST) have also been shown to improve the signal-to-noise ratio (S/N) of TOCSY cross-peaks compared to conventional hard pulse mixing schemes (e.g., MLEV-17) (22,29). In tissue studies the time typically allowed for 2D frequency encoding (≥3 to 5 hr) can severely degrade the metabolic and pathologic integrity of the tissue and compromise subsequent genetic and/or proteomic analyses (17). In this study, a rotor synchronized adiabatic TOCSY experiment was optimized for the quantitative detection of Cho and Eth metabolites in ≈1 hr and then applied to benign and malignant postsurgical prostate tissues prior to pathologic analysis of the same tissues.
Choline chloride (Cho), phosphocholine chloride calcium salt tetrahydrate (PC), L-α-glycerophosphorylcholine cadmium chloride complex (GPC), ethanolamine hydrochloride (Eth), O-phosphorylethanolamine (PE), deuterium oxide (D2O), and 1.0 mL vials of deuterium oxide (99.9% atom D) containing 0.75% 3-(trimethylsilyl)propionic-2,2,3,3-d4 acid (D2O+TSP) were purchased from Sigma-Aldrich (St. Louis, MO). Glycerophosphoethanolamine hydrate (GPE) was a kind gift from Euticals S.p.A. (Lodi, Italy). Stock solutions of Cho, PC, GPC, Eth, PE, and GPE were prepared in 1× phosphate-buffered saline and used to optimize the data acquisition parameters and determine MT efficiency constants (KMT) in order to calculate metabolite concentrations in tissue. Samples were analyzed individually and as a mixture of all six metabolites. For solution studies, 3.0 μL of D2O+TSP was pipetted into the bottom of a tared rotor and weighed to 0.01 mg. The balance was tared again and then the solution samples were pipetted into the rotor and weighed.
Forty-seven postsurgical prostate tissues were harvested from 22 patients (mean age: 60 ± 13 years), placed in cryogenic vials, and stored at -80°C until use. Samples were analyzed using custom-designed 20 and 30 μL leak-proof zirconium rotors, which contained an oblate spheroid-shaped sample chamber to facilitate shimming and an airtight screw top plug to prevent leakage (17). 3.0 μL of D2O+TSP was pipetted into the bottom of a tared rotor and weighed to 0.01 mg. Tissue cores were then excised from the surgical specimens using a 3.5 mm biopsy punch (Sklar Instruments, West Chester, PA). The balance was tared again and the tissues were weighed to 0.01 mg (mean = 17.36 ± 3.71 mg), then slowly inserted into the rotor. Finally, the top screw was carefully inserted to avoid air bubbles, tightened, and then the rotor was placed in the spectrometer for analysis.
Data were acquired at 11.7T (500 MHz for 1H), 1°C, and a 2250 Hz spin rate using a Varian INOVA spectrometer equipped with a 4-mm gHX nanoprobe (Varian, Palo Alto, CA). Prior to beginning each 2D experiment a quantitative 1D "presat" spectrum was acquired with a 2-sec presaturation delay, 2-sec acquisition time (TR = 4 sec for tissue, 6 sec for solutions), and 128 transients (17). TOCSY data were acquired using a rotor synchronized WURST-8 adiabatic mixing scheme flanked by two sets of ≈1.8 ms trim pulses (22). Both the adiabatic and trim pulses were rotor synchronized by setting the pulse lengths equal to the reciprocal of the spin rate (0.444 ms). Solution data were acquired with a repetition time (TR) = 2.04 sec (presaturation delay = 1.5 sec, mixing time [tm] = 40 ms [39.96 ms exactly], acquisition time [AT] = 0.50 sec); steady-state pulses (SS) = 4 (first increment only); number of transients per increment (NT) = 24; number of points (NP) = 4096 (complex) and spectral width = 20,000 Hz in the direct dimension (F2); number of increments (Ni) = 64 (complex) and spectral width = 6000 Hz in the indirect dimension (F1); total time = 1.77 hr.
The experiment time was then optimized for tissue studies by determining the minimum TR and NT needed to achieve adequate S/N, and the minimum Ni needed to resolve the metabolites of interest. For TOCSY, the total experiment time = TR × NT × Ni, where TR is the sum of the combined presaturation and relaxation delay, the average evolution time, tm, and AT. The TR was minimized by determining the power level and duration of presaturation needed to adequately suppress the water signal to the level of the other metabolites, the evolution time was fixed, the optimal tm was previously determined to be 40 ms (39.96 ms exactly) (22), and AT was minimized based on the loss of signal in the free induction decay (FID). For a sample mass ≥10 mg, the following parameters provided optimal water presaturation, S/N, and resolution in a total experiment time of 1.08 hr: TR = 1.24 sec (presaturation delay = 1.0 sec, tm = 40 ms, AT = 0.20 sec); SS = 4 (first increment only); NT = 24; NP = 4096 (complex) and spectral width = 20,000 Hz in F2; Ni = 64 (complex) and spectral width = 6000 Hz in F1. Finally, data were acquired in interleaved mode and phase sensitive using the States et al. method (30). For the 47 tissue samples the total time for sample preparation, shimming, and 1D and 2D data acquisition was <1.5 hr per sample. To investigate the degradation of Cho- and Eth-containing metabolites over time, serial TOCSY experiments were performed on three additional samples for 8 hr at 1°C using the same parameters as for the ≈1-hr experiment.
Data were processed offline using ACD/Labs 1D and 2D NMR processor v. 9 (ACD/Labs, Toronto). One-dimensional spectra were processed and quantified using Lorentzian-Gaussian peak fitting as previously described (17). TOCSY data were processed using 4×N linear prediction in F1, zerofilled to 4K (F2) and 1K (F1) complex points, apodized using a Gaussian function and Fourier transformed in both dimensions. TOCSY spectra were then phased by displaying slices containing cross-peaks near the beginning, middle, and end of the spectrum in F2 and then F1. Zero- and first-order phase corrections were applied in each dimension and then to the entire 2D matrix. Finally, the spectra were frequency-referenced to TSP at 0.0 ppm.
The cross-peaks above the diagonal were used for quantitation because they contained less environmental or "t1" noise than the cross-peaks below the diagonal (21). Specifically, artifacts arising from the Cho, PC, and GPC singlet diagonal peaks (3.20-3.24 ppm) overlap the Eth cross-peaks below the diagonal, but have no effect on the cross-peaks above the diagonal. Metabolic changes were evaluated by comparing ratios of metabolites to one another and by estimating metabolite concentrations using the diagonal peak of TSP as an internal quantitation reference. Metabolite cross-peaks and the TSP diagonal peak were volume integrated by setting a threshold at 0.05% of each cross-peak's maximum intensity, below which the data were considered to be in the noise. The cross-peak volumes above the threshold were then numerically integrated and exported to an Excel spreadsheet. Metabolite cross-peak to TSP diagonal peak ratios were then calculated and corrected for MT efficiency based on the phantom data as follows. In the 1D spectra of the phantom solutions (n = 3), the downfield metabolite multiplets of Cho (4.07 ppm), PC (4.21 ppm), GPC (4.33 ppm), Eth (3.81 ppm), PE (4.02 ppm), GPE (4.12 ppm), and the TSP singlet (0.00 ppm) were quantified as previously described (17). Empirical MT efficiency constants (KMT) were then calculated by equating the 2D metabolite cross-peak volume (Vmet) to TSP diagonal peak volume (VTSP) ratios to the corresponding 1D metabolite peak area (Amet) to TSP (ATSP) peak area ratios:
KMT was calculated for each metabolite and averaged across the three phantom datasets. Note that normalization factors for the respective numbers of protons are not needed since they would appear on both sides of the equation and thus cancel out. For tissue spectra, metabolite concentrations (mmol/kg wet weight) were then calculated based on the masses of tissue and D2O+TSP in the rotor, and the TSP and metabolite cross-peak volumes using the following equation:
where 0.75% was treated as a constant.
Following HR-MAS, samples were immediately frozen in optimal cutting temperature (OCT) compound and were then sectioned and stained with hematoxylin and eosin (H&E) as previously described (17). Slides were reviewed by two pathologists who determined the percentage of benign glandular, benign stroma, inflammation, and the percentage and grade of prostate cancer. Pathology readings were then recorded into a database and averaged for both readers. For statistical comparisons, prostate cancer tissues were compared to benign tissues, regardless of relative glandular and stromal composition.
Statistical analyses were performed using SAS statistical analysis software (SAS Institute, Cary, NC). Metabolite concentrations (mmol/kg) were statistically compared between benign and malignant prostate tissues using Z statistics for paired data:
where xh and xc are the mean metabolite values for benign and cancer tissues, σh and σc are the standard deviations of benign and cancer metabolite concentrations, respectively, ρhc is the correlation between the paired values, and nh, nc, and nhc represent the numbers of benign, cancer, and paired samples, respectively. The Z score of greater than 1.96 was considered significant to 5% and 2.58 was considered significant to 1%.
Figure 1 illustrates the problem of spectral overlap in one-dimensional 1H HR-MAS spectra of prostate tissue. Figure 1a shows a 1H HR-MAS spectrum of a phantom solution containing 1.8 mM Cho, PC, GPC, Eth, PE, and GPE, which has been scaled up to emphasize the sidechain CH2-CH2 resonances. Figure 1b shows a 1H HR-MAS spectrum of benign predominantly glandular prostate tissue, and Fig. 1c shows a 1H HR-MAS spectrum of Gleason 3+4 prostate cancer tissue. As shown in the phantom spectrum, the Cho and Eth sidechain methylene resonances are well separated in frequency such that they can be resolved by 2D spectroscopy. Also note that GPC and GPE contain additional resonances due to the glyceryl (CH2-CH-CH2) protons in the regions from 3.59-3.71 and 3.85-3.98 ppm. In tissue (Fig. 1b,c), the multiple resonances of lactate, myo-inositol, taurine, and polyamines dominate those of Cho (4.07 and 3.55 ppm), GPE (4.12 and 3.30 ppm), and Eth (3.15 ppm). In the cancer spectrum shown in Fig. 1c, there is a visually apparent increase in the Cho (3.21 ppm), PC (3.23 ppm), and GPC (3.24 ppm) head group singlets; however, these metabolites cannot be resolved from each other in tissue and PE (3.22 ppm) co-resonates in this highly overlapping region. Furthermore, the remaining Cho and Eth methylene signals (e.g., GPC, PC, PE, and Eth) are difficult to distinguish from the baseline due to low signal intensity and spectral broadness (Fig. 1b,c).
Figure 2 shows the upper diagonal CH2-CH2 region of the 2D TOCSY spectra obtained on the same (Fig. 2a) phantom solution, (Fig. 2b) benign predominantly glandular, and (Fig. 2c) Gleason 3+4 prostate cancer tissue samples shown in Fig. 1. The Cho, PC, GPC, Eth, PE, and GPE cross-peaks are identified and their relative concentrations are reflected by the number of contour levels as in a topographic map. The corresponding 1D spectral regions are shown above and to the left of the 2D plots and representative histopathologic sections (H&E, 10× magnification) are shown in insets in Fig. 2b,c. Based on the phantom data acquired at tm = 40 ms, the MT efficiency constants (KMT) for each metabolite were: Cho (71 ± 1%), PC (54 ± 1%), GPC (46 ± 1%), Eth (79 ± 0%), PE (61 ± 1%), and GPE (50 ± 0%). Consistent with previously reported chemical shift values (21), the Cho and Eth cross-peaks were observed in tissue at: Cho (3.55×4.07 ppm); PC (3.62×4.17 ppm); GPC (3.71×4.33 ppm); Eth (3.14×3.82 ppm); PE (3.23×3.99 ppm); and GPE (3.30×4.12 ppm); however, note that the frequencies observed in tissue differ slightly from those observed in solution. The Cho cross-peak co-resonates with myo-inositol and is therefore labeled as Cho+mI in tissue. On visual inspection, PC was observed in 11/15 (73%) cancer tissues but only 6/32 (19%) benign tissues. Ethanolamine and PE were observed in all benign tissues and 14/15 (93%) cancer tissues, but the spectra in which Eth and PE were not observed were from different patients. GPE was observed in 28/32 (87%) benign tissues and 12/15 (80%) cancer tissues. GPC was observed in all cancer tissues and 30/32 (94%) benign tissues. In two benign tissues from different patients, PC, GPC, and GPE were not observed.
Table 1A summarizes the individual Cho and Eth metabolite concentrations observed in benign and malignant prostate tissues. The PC concentration was significantly higher in malignant versus benign prostate tissues, while the Eth concentration was significantly lower in malignant versus benign prostate tissues. GPC, PE, and GPE concentrations were all higher in cancer versus benign prostate tissues, but the differences were not statistically significant. Note that PE and Eth had the highest concentrations of all metabolites, GPC and GPE had similar concentrations, and PC concentrations were the lowest in both benign and cancer tissues. Several metabolite ratios were also calculated and are summarized in Table 1B. Ratios were calculated for each spectrum and then averaged across all cases; data were excluded when the value in the denominator was zero. PC/GPC, PC/PE, PE/Eth, and GPE/Eth ratios were all significantly higher in malignant versus benign prostate tissues. Figure 3 shows the overlap of Cho and Eth metabolite ratios in benign versus prostate cancer tissues and dashed lines indicate the metabolite ratios above which all samples were malignant, i.e., specificity = 100%. Positive cutoff ratios, sensitivities, and specificities that yielded minimum false positives and false negatives and represented the best compromise between sensitivity and specificity were: PC/GPC >0, sensitivity = 73%, specificity = 81%; PC/PE >0, sensitivity = 73%, specificity = 81%; PE/Eth >4.0, sensitivity = 50%, specificity = 77%; and GPE/Eth >0.1, sensitivity = 64%, specificity = 81%.
At pathologic evaluation, 32 samples were benign and 15 contained prostate cancer (Gleason score: 3+3 [n = 9]; 3+4 [n = 3]; 4+4 [n = 1]; and 4+5 [n = 2]) with a surface area of at least 20%. Benign samples contained an average of 40 ± 16% glandular tissue (range: 10-70%) and 60 ± 16% stroma (range: 30-90%). Malignant samples contained an average of 53 ± 26% cancer (range: 20-100%), 16 ± 13% glandular tissue (range: 0-50%), and 31 ± 21% stroma (range: 0-65%). In every case, both pathologists could interpret the slides, indicating that the duration of time in the spectrometer (<1.5 hr) did not compromise the pathologic integrity of the samples. Figure 4 shows the mean percent change in Cho and Eth metabolites over 8 hr at 1°C and a 2250 Hz spin rate. For this experiment, samples were chosen that contained high levels of PC+GPC in the 1D spectrum. During the course of a 1-hr TOCSY experiment, PC and GPC decreased by an average of 8.9% and 8.6%, respectively, while Cho+mI increased by 12%; PE and GPE decreased by 8.9% and 4.5%, respectively, while Eth increased by 24%. However, over the course of 8 hr, PC, GPC, PE, and GPE levels decreased even more dramatically, while the combined Cho+mI and Eth cross-peaks increased by nearly 150 and 300%, respectively. This indicates that HR-MAS spectroscopy data should be acquired as quickly and efficiently as possible to preserve the integrity of the tissue for subsequent analysis.
The purpose of this study was to develop a fast and quantitative 2D HR-MAS TOCSY experiment to resolve and quantify the individual Cho- and Eth-containing metabolites in postsurgical prostate tissues prior to pathologic analysis of the same tissues. A nominal ≈ 1-hr acquisition time was chosen to preserve the metabolic and pathologic integrity of the tissue and to make the experiment feasible for routine use in a high-throughput environment. To achieve this goal, a rotor synchronized WURST-8 adiabatic mixing scheme was optimized to obtain the necessary S/N and resolution in the shortest possible time and this combination was previously shown to provide up to 10 times greater S/N in tissue compared to conventional isotropic mixing pulses (MLEV-17) (22). Magnetization transfer efficiency constants (KMT) were determined empirically using phantom solutions containing Cho, PC, GPC, Eth, PE, and GPE and then used to calculate the corresponding metabolite concentrations in prostate tissue based on the cross-peak to TSP diagonal peak volumes, and the masses of tissue and TSP in the rotor. At a 40 ms mixing time the calculated magnetization transfer efficiencies for each metabolite decreased from Cho (71 ± 1%) to PC (54 ± 1%) to GPC (46 ± 1%), and from Eth (79 ± 0%) to PE (61 ± 1%) to GPE (50 ± 0%). These data indicate that MT has a substantial influence on the cross-peak volumes of different metabolites, and this information should be taken into account when quantifying the data.
Consistent with previous in vivo (14) 31P MRS studies of prostate cancer patients, and in vitro (8,10) 31P MRS studies of prostate cancer tissue and xenograft extracts, higher concentrations of phosphomonoesters (PC and PE) were observed in prostate cancer versus benign prostate tissues. Note, however, that the increase in PE was not significant in prostate cancer samples in this study. The current results are also consistent with previous in vivo 1H MRSI (31) and ex vivo HR-MAS spectroscopy (16,17) studies that demonstrated an overall increase in Cho-containing metabolites in prostate cancer versus benign prostate tissues, and suggest that the Eth-containing metabolites, particularly PE, are major contributors to the in vivo "choline" region. Based on the data in Table 1, and assuming that free Cho concentrations are similar to PC and GPC concentrations in prostate cancer tissue, the total area of Eth-containing metabolites could be almost as much as the total area of Cho-containing metabolites, after correcting for the respective number of protons (2 vs. 9). However, it must be noted that other metabolites including taurine, myo-inositol, glucose, creatine, and polyamines also contribute to the in vivo Cho region, and that the intensity of the Eth metabolites observed in vivo is reduced due to J-modulation and T2 effects. TOCSY could potentially be used to resolve the Cho and Eth metabolites in vivo, and a localized 1D TOCSY sequence has recently been applied to the brain (32).
The dramatic increase in PC concentration in prostate cancer observed in this study is also consistent with many previous studies involving prostate (18), breast (5,33), and other cancers (1,2,13). Specifically, PC was observed in 11/15 (73%) cancer tissues but only 6/32 (19%) benign tissues and PC increased from 0.02 ± 0.07 to 0.39 ± 0.40 mmol/kg or ≈19 fold between benign and cancer tissues. GPC concentrations also increased between benign and cancer tissues; however, the difference was not as dramatic (≈2-fold) as that observed for PC and did not reach statistical significance. Nonetheless, the PC/GPC ratio was over 10 times greater in cancer than benign prostate tissues. These findings are in agreement with those of Ackerstaff et al. (18), who reported that both PC and GPC are elevated in human prostatic epithelial cells after malignant transformation. PC/PE, PE/Eth, and GPE/Eth ratios were also significantly higher in prostate cancer versus benign tissues. As shown in Fig. 3, there was considerable overlap of individual metabolite ratios; however, good sensitivity and specificity values were obtained with a minimum number of false-positives and false-negatives. Ongoing studies involve determining whether there are grade-dependent changes in the concentrations and metabolite ratios of phospholipid intermediates in a larger patient cohort.
One limitation of the current study is the unknown state of metabolic degradation encountered when working with postsurgical tissues and that caused by the freeze-thaw process. To solve this problem, studies are under way using biopsy tissues, which can be harvested and frozen in seconds and therefore provide a much better metabolic snapshot of in vivo metabolism than surgical tissues. However, the degradation experiments performed in this study indicate that, even at 1°C, PC, GPC, PE, and GPE decompose to form free Cho and Eth, and over several hours, breakdown of phospholipid membranes contributes to the continuing increase in Cho and Eth metabolites. These observations are consistent with a previous 1D HR-MAS study from our group, which showed a temperature-dependent decrease in the combined GPC+PC peak and a concomitant increase in the free choline peak over 12 hr. While the mechanisms for the degradation of the phosphorylated Cho and Eth derivatives into their free bases are not completely understood, several Kennedy cycle enzymes including phospholipases could be biologically active at 1°C or upregulated under ischemic conditions. Additionally, sheer mechanical degradation could occur due to the fast spinning rates used for HR-MAS. Therefore, in order to preserve the integrity of the tissue, the HR-MAS data should be acquired at 1°C and as fast and efficiently as possible. While slower spinning 1D HR-MAS spectroscopy has been shown to preserve prostate tissue histology (34), no slower spinning 2D HR-MAS TOCSY experiments have been reported to date. The development of a quantitative slower spinning TOCSY experiment would be technically challenging but is worthy of future investigation. Under the conditions used in the current study we have shown that the Cho and Eth metabolites can be resolved and quantified in a reasonable amount of time and that the same tissues can be interpreted pathologically following HR-MAS analysis.
A potential source of error in this study arises from the choice of TR. Although the T1s of the Cho and Eth sidechain protons cannot be determined in tissue due to spectral overlap and low signal intensity, they are assumed to be similar to each other and to that of taurine, which has a T1 of ≈600 ms at 1°C and 11.7T (17). As in 1D NMR, a TR ≈1.25 × T1 provides the maximum S/N during signal averaging in 2D NMR and is quantitative when the T1s of the metabolites of interest are similar. Therefore, the repetition time of 1.24 sec used in this study is a reasonable compromise between maximizing S/N and the time needed to presaturate the water signal. Another potential source of error arises because a solution was used to calibrate the magnetization transfer efficiency. For small molecules in solution, T1 ≈ T2, and the primary difference is due to magnetic field inhomogeneity (T2*). As the correlation time (τc) increases, T1 and T2 both decrease and then diverge from each other. Excluding citrate and polyamines, the T1 relaxation times of prostate metabolites are ≈1.5 to 3 times T2 at 11.7 T and 1°C (17). Since 1/T1 < 1/T1ρ ) 1/T2, concentration errors due to differences in T2 between solution and tissue samples are estimated to be 10% or less at a mixing time of 40 ms.
There are other approaches that could be used to resolve and quantify the Cho and Eth metabolites in tissue. Conventional COSY can be applied quantitatively and the magnitude mode cross-peaks are linearly proportional to concentration. However, TOCSY provides better sensitivity than COSY because of the net magnetization transfer and lengthening of T1ρ provided by isotropic mixing and because COSY cross-peak multiplets have both absorptive and dispersive components, which partially cancel each other. Therefore, COSY would not be practical in a 1-hr setting (35). Payne et al. (36) recently demonstrated the feasibility of 31P HR-MAS spectroscopy of intact tissues. Although 31P MRS provides complementary and additional information to 1H MRS, 31P sensitivity is critically dependent on coil design and, therefore, a dedicated probe designed for 31P detection may be necessary. Additionally, 31P requires faster spin rates than 1H under HR-MAS conditions to overcome broadening due to increased chemical shift anisotropy. Therefore, 31P may be impractical for delicate samples such as biopsies, which typically weigh less than 10 mg and are ≈1 mm thick. Loening et al. (37) recently described a 31P edited 1H MRS sequence to quantify the concentrations of Cho, PC, and GPC in biological samples and demonstrated its utility in human brain tumor extracts; however, this technique has not yet been applied in tissue.
A fast and quantitative 2D high-resolution magic angle spinning (HR-MAS) total correlation spectroscopy (TOCSY) technique was developed that can be used to resolve and quantify the choline- and ethanolamine-containing metabolites in human prostate tissues in ≈1 hr prior to pathologic analysis of the same tissues. Phosphocholine concentrations were significantly higher, while Eth concentrations were significantly lower in cancer versus benign prostate tissues. PC/GPC, PC/PE, PE/Eth, and GPE/Eth ratios were also significantly higher in cancer versus benign prostate tissues.
The authors thank Drs. Eriks Kupce, Daina Avizonis, and Bao Nguyen of Varian Instruments (Palo Alto, CA) for valuable discussions and continued support of this research.
Grant sponsor: National Institutes of Health; Grant numbers: K01 CA096618, R01 CA102751; Grant sponsor: American Cancer Society; Grant number: RSG-05-241-01-CCE; Grant sponsor: University of California Discovery Grant; Grant number: ITL-BIO04-10148.
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Testing Promotions through Email Marketing
Ryan Allis
Ryan Allis is the CEO and co-founder of iContact, a leading on-demand email marketing service. As CEO, he's managed iContact from its start in July 2003 to its current size with more than 90 employees and 25,000 customers worldwide. In 2005, Ryan was named by BusinessWeek as one of the "Top 25 Entrepreneurs Under 25." Ryan is also the author book Zero to One Million: How I Built a Company To $1 Million in Sales and How You Can Too, published by McGraw-Hill. As an email marketing expert, Ryan will provide guidance in his blog posts on how to enhance and improve your online marketing campaigns.
Latest posts by Ryan Allis (see all)
- Creating Email Campaigns to Measure Your Website's Performance - October 29, 2014
- Email Marketing Review - November 21, 2008
- Segmenting Email Campaigns: What Criteria Should You Use - November 18, 2008
The end of the year can be a challenging yet promising time for Email Marketers trying to get the attention of prospective customers. During the holiday season, consumers are slammed with large email volume from a variety of vendors. To cut through the noise, you should consider using effective promotions within your email campaigns.
Many Email Marketers fail to recognize when preparing their email campaigns is the importance of testing messages before they are sent out. Sending out your promotional emails to a small group of people is a great way to understand what really drives your message. Even more, your test audience can give you substantial feedback that can greatly impact the effectiveness of your messages.
Another reason to test your promotions through email marketing is because it can dramatically affect your other communication channels. By sending out well crafted emails and tracking the results, you can save both time and money before investing in other marketing materials, such as direct mail.
Thanks for reading. I will be back soon to discuss more tips on email marketing.
Ryan Allis


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Check in from 3:00 PM / Check out prior to 11:00 AM
Holiday Inn Express & Suites Shreveport: Find photos, reviews, information, amenities and compare prices for 2 stars hotels in Shreveport, United States.
Holiday Inn Express & Suites Shreveport offers a comfortable setting while in Shreveport. It provides a swimming pool and an outdoor pool.
Hotel description
There are a range of facilities at Holiday Inn Express Hotel & Suites Bert Kouns Shreveport on offer to guests, such as meeting rooms, an executive floor and a gym. Wi-Fi is also provided.
The rooms are air conditioned and include tea and coffee making facilities, wireless internet access and movies-on-demand. Cable/satellite channels, a microwave and a shower are also provided.
A satisfying breakfast is available for purchase, and there are numerous cafés and eateries close by. Those looking for after-dinner entertainment can enjoy the on-site casino.
Shreveport Regional Airport is within a 20-minute car ride of the hotel, as are Centenary College of Louisiana, the Strand Theater Shreveport and Cathedral of St. John Berchmans. Louisiana State University in Shreveport is a quick drive away.
Hotel features
Pet Friendly, Disabled Access, Air Conditioned, Cable / Satellite TV, In Room Movies, Coffee / Tea Maker, Microwave, Hair Dryer, TV, Disabled Accessible Rooms, Shower
Business Center, Dry Cleaning, Conference Room(s), Safe-Deposit Box, Meeting Rooms, Laundry service, Shops, Desk
Fitness Room/Gym, Swimming pool, Bath / Hot Tub, Casino, Pool Outdoor
High-speed Internet, Internet Connection (wireless)
Executive Floor, Souvenirs/Gift Shop
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Users who viewed Holiday Inn Express & Suites Shreveport also viewed these 2 stars Shreveport hotels:
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Super 8 Shreveport
4911 Monkhouse Drive, Shreveport
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text:
The Old Religion
David Mamet. The Old Religion.
New York: The Free Press, 1997. 194 pp. Cloth $24.00
With The Old Religion, David Mamet offers his interpretation of the famous Leo Frank case. Briefly, a thirteen-year-old girl was molested and killed in Atlanta, Georgia in April 1913. Suspects were numerous, but in the end, Leo Frank, a Jewish manager for the National Pencil Factory, a Jewish owned and operated company, was charged with the murder. The case received national attention, and still stands as one of the best examples of American bigotry in our history. After an extremely problematic trial during which the jury's hatred of Jews overrode their usual distaste for African-Americans, Frank was found guilty of murder. Many, including the governor, believed that the verdict was inaccurate, so Frank was not executed following the trial. Instead, while serving a life sentence, he was lynched and castrated by an irate mob. Frank was officially cleared of any wrongdoing in 1986.
Mamet's representation of the case is not straightforward, so those who are unfamiliar with it will find the novel confusing. Part of the difficulty stems from Mamet's decision to tell the tale through the often-fragmented thoughts of Frank. For those familiar with the case, this strategy offers compelling insights into the mind of the unjustly accused. Frank, for example, attempts to reconcile his own fragile faith and Judaic teachings with the injustice of his situation. And through Mamet's retelling, it is not difficult to see how the crime against Frank foreshadows the brutalities of the Holocaust in order to illustrate the depths of American anti-Semitism. However, Mamet does not illustrate the issue too simplistically; even Frank's prison rabbi thinks that he is guilty of the crime.
One of the most disturbing aspects of the novel is Mamet's treatment of the female victim, Mary Phagan. Her age is never mentioned, and in a passage presumably constructed to create sympathy for Frank, Mamet indicates that Frank could not have done anything to Phagan because she was too physically repulsive to Frank. At moments like this, the novel reads like a sequel to Mamet's controversial play Oleanna, in which a young male professor loses his chance at tenure as a result of a female student's accusations of sexual harassment. In this case, however, the female never has the opportunity to interrupt.
Mamet makes the case more provocative, too, by his focus on the American economy and its burgeoning consumerism. Frank, for instance, ponders the means by which advertising works on its audiences: "Advertising must appeal, as is its essential nature, to the fear that one is to be excluded. It must both awaken and suggest how to allay this fear" (48). In addition to depicting Frank as a contemplative and philosophical character, such musings reflect Frank's own position as a Jew, an outsider, in a Christian culture. More interesting still is Mamet's implication that what Frank could have used most was not a better lawyer but a more astute public relations representative. In a subtle, macabre, and ironic conclusion, Mamet reminds us that Frank became an object on the consumer marketplace--a photograph of his lynching and castration were reproduced on a postcard, and it was "sold for many years in stores throughout the South" (194).
Ohio Dominican College


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"Since it is a Taj property nothing was left unturned. Rooms were impeccable Quality was ...." - Tejas ShahRead more reviews >>
Taj Coromandel (A Taj Hotel)
Nungambakkam, Chennai, Tamil Nadu - 600 034
Taj Coromandel (A Taj Hotel), Chennai - Location on Map
Taj Coromandel (A Taj Hotel), chennai
Taj Coromandel (A Taj Hotel), Chennai - Overview
Conveniently located in the commercial hub of Chennai the Taj Coromandel is a rich fusion of South-Indian cues & European elegance. It maintains a total of 212 guest rooms that are luxuriously stylish and enviously comfortable. There are three distinctive specialty restaurants, namely Prego, an Italian restaurant; Golden Dragon, the Signature Chinese restaurant & Southern Spice for Southern cuisine. Guests can live-it-up at Chipstead, the Bar & can indulge on the wide variety of single malts & Cognacs.
Other amenities include a rejuvenating dip in the pool, workout session at the fitness club, the business travelers can avail of eight conference rooms, including a ballroom and a boardroom. The gourmets can enjoy a sumptuous meal at Southern Spice or relax at Match Point, a 24 hrs coffee shop. For recreation, the guests can also try the outdoor activities like golf, tennis and swimming.
Check-in time : From 02:00 pm
Check-out time : Until 12:00 pm
Taj Coromandel (A Taj Hotel)Guest Reviews based on 2 reviews
of our customers recommend this hotel
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Taj Coromandel (A Taj Hotel), Chennai - Amenities
- 24-Hour Front Desk
- 24-Hour Security
- Babysitting or child care
- Beauty Parlour
- Business center
- Coffee shop or cafe
- Conference Room
- Conventions
- Front desk
- Gym
- Internet Access
- Kids Pool
- LCD / Projector
- Laundry facilities
- Lift
- Lounge
- Newspaper
- Restaurant
- Room service
- Swimming pool
- Telephone
- Travel counter
- Wake up service/Alarm clock
- Wedding services


text:
"It is wise to keep us seniors informed about the services or products you offer! How would we know about you unless you tell us, and the best way to tell us is with an ad in Today's Senior Magazine, our favorite senior resource guide"
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PO Box 6456, Eureka, CA 95502
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Your ads show us "life does still go on". Bye and thanks for brightening my day."
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text:
Alaskan Malamute Breeders near Milton Keynes, Buckinghamshire
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Displaying 1 - 6 of 6 Alaskan Malamute Breeders near MK9
24 Miles Arcticbear Alaskan Malamutes Eric Allen Chesham Bucks
30 Miles Sireniki Natalie Joannou Wisbech Cambridgeshire
33 Miles Eskanno Mr & Mrs G J Gensale Huntingdon Cambs
Sockeye Alaskan Malamutes
Diane Jackson
Kingston Bagpuize
Current Health Tests
36 Miles
I have owned and worked Alaskan Malamutes for 10 years and live in Oxfordshire with my current pack of Goose and Be Bop. They are very much the centre of things here and life revolves around them. Firstly they are my pets but they love to work and are consistently successful in all disciplines including sprint racing, trekking, back packing and weight pull. When not working both of them achieve considerable success in the show ring. They are true all rounders with beautiful temperaments and are fantastic representatives of the breed.
48 Miles Shane & Lydia Jenkins New Haw Surrey
49 Miles Snowtrails Bill & Jill Robins Ely Cambs.
Displaying 1 - 6 of 6 Alaskan Malamute Breeders near MK9


text:
Friend's Email:
Subject: I have found a DVD that I think you would enjoy
|Barney Please Thank You
Actor: Barney
UR 2010 1hr 5min
Join Barney & Friends? as they learn the importance of being kind and courteous to others. When Baby Bop? forgets to say "please? and "thank you", Barney realizes it?s time for a lesson on how magic words can make other pe... more »
Larger Image
|Actor: Barney
Studio: Lyons / Hit Ent.
Format: DVD - Color,Full Screen - Closed-captioned,Dubbed
DVD Release Date: 01/05/2010
Release Year: 2010
Run Time: 1hr 5min
Screens: Color,Full Screen
Number of Discs: 1
SwapaDVD Credits: 1
Total Copies: 0
Members Wishing: 0
MPAA Rating: Unrated
Languages: English, Spanish
|Barney - Best Manners
Invitation To Fun
UR 2003 0hr 50min
|Barney Night Before Christmas - The Movie
UR 2008 0hr 57min
|Barney Furry Friends
UR 2010 1hr 2min
|Barney Let's Go To the Farm
NR 2005 0hr 50min
|Pirates of the Caribbean - The Curse of the Black Pearl
Two-Disc Collector's Edition
Director: Gore Verbinski
PG-13 2003 2hr 23min
|Ghosts of Girlfriends Past
Director: Mark Waters
PG-13 2009 1hr 40min
|The Good Girl
Director: Miguel Arteta
R 2003 1hr 33min
|Barbie of Swan Lake
Director: Owen Hurley
NR 2003 1hr 21min
|Sesame Street - Learning About Letters
Directors: Jim Henson, Jim Martin, Randall Balsmeyer, Victor DiNapoli, Diego, Ken
UR 2004 1hr 0min
Two-Disc Special Edition
R 2005 2hr 51min
|Barbie and the Magic of Pegasus
Director: Greg Richardson
NR 2005 1hr 23min
|The Wiggles - Wiggledancing
Live in the USA
Director: Paul Field
UR 2006 1hr 18min
|The Ninth Gate
Director: Roman Polanski
R 2007 2hr 13min


text:
Chevy trucks for sale in pa for sale on US's largest classifieds sites (308 results)
2000 Chevrolet S-10 Pickup Truck
2000 Chevrolet S-10 pickup truck. This S-10 is in excellent condition it was originally from Florida and has been garage kept the last seven years and not driven in the winter. The only known mechanical issue is a slight oil pan seepage , A/C compressor was replaced this past summer with new GM com
1950 Chevy Truck 3100
Very RARE Find! 3100 Chevy Short bed Truck, She Has Never Been in an accident. No Signs of Body Filler, This is a Rust Free Truck inside and Out Truck and Will make a Good Daily Driver. Tire Tread is 95% Breaks 95% Clutch 90% Truck Runs, Drives and Stops Just Like New with it's Original L
2007 Chevrolet Silverado 1500 LTZ Z71 Loaded
2007 Chevrolet 1500 HD LTZ Z71 4x4 Crew Vortec MAX Sunroof Heated Leather Navigation Lift Wheels Tires Etc.Truck is in Great Condition, Very Comfortable, and Looks Great with the Brand New Lift, Rims and Tires. Only has 159k which is nothing for the 6.0 Vortec Max Motor and is good to go for many y
1978 Chevrolet C-10 STEP SIDE
Brand new build Full Frame Off, Under 500 easy miles on this truck, driven only to local car meets. All Brand new Steel Body and cab, 3 inch chopped roof. New glass front and rear, new lexan on doors. Front tilt steel hood with 4" cowl, fiberglass bumper, custom phantom
1966 Chevrolet C-10
1951 Chevrolet Other Pickups 3100 truck
1952 Chevrolet 3100
1952 Chevrolet truck sitting on a 2000 S-10 Extreme Chassis. 350 Engine. Turbo 350 transmission. Suicide Doors. Power steering, power disc brakes. Ratchet shifter in floor. Battery has been relocated to the bed. New side glasses and vent glass assemblies with new window felts and window chann
1945 Chevrolet Other Pickups truck
1945 chevy 1/2 ton pickup. Great war model pickup to restore or drive the way it is ! Truck runs great and has a very smooth sounding 216 engine. We drive this truck often on short trips. Tranny , brakes , engine , all work great . This 1945 war y
Year: 1945, Make: Chevrolet, Model: Other Pickups
1949 Chevrolet Other Pickups
1949 Chevrolet Pick up. This was a frame off restoration almost 4 years ago. Since then its been driven about 10k miles. This is an absolute beauty! This thing turns heads every where it goes. Under the hood is the original straight 6 which was rebuilt a couple thousand miles ago. It is mated to a
Year: 1949, Make: Chevrolet, Model: Other Pickups
1965 Chevrolet C-10 truck
1949 Chevrolet Other Pickups truck
1989 Camaro front clip and rear end. 1989 Camaro 350 Engine and 700R4 Transmission Disk brake all around Paint is about 5 years old. (It has few scratches, one large one on rear fender) Wood is about 1 year old. 90% done. Runs and Drives. Currently registere
Year: 1949, Make: Chevrolet, Model: Other Pickups
1962 Chevrolet Other Pickups truck
1962 Chevy short bed is a life-long dry Oklahoma pickup and is straight as a string. I purchased it from the second owner from new and he had it the last 38 years, he bought it in 1977. He kept it in a shed on his property after having it painted two years ago. The truck is sold minus the orig. eng
1957 Chevrolet Bel Air/150
The body of the Truck is solid and rust free. The door pockets, cab corners, floors, fenders, flares, firewall, everything is solid. It was repainted professionally in a single stage Black which shines out exceptionally well. She does have a few minor scratches in areas but overall, she looks great
2008 Chevy Silverado crew cab 4x4 PA TRUCK
Chevy s10 4x4 truck
1997 chevy P30 diesel /great for food truck /reduced
Year: 2001, Make: Chevrolet


text:
Young and Gay
Under 26?
Want to meet new people?
Want to talk about stuff relating to your sexuality?
If you answer "yes" to the above, then Young & Gay is the right workshop for you!
Young & Gay offers a fun, interactive and supportive environment for you to meet new people and discuss topics relating to sexuality, sex and sexual health. We talk about coming out, self-esteem, homophobia, HIV/AIDS, STIs, relationships and the gay community.
Follow Young & Gay on Facebook: www.facebook.com/youngandgay.
Some feedback from recent participants:
"This is a fantastic workshop that has been really impactful and valuable. Keep it going! :)."
"I've gained lots of self-growth and self-love, as well as lots of knowledge on HIV - I will recommend Young & Gay to others - too valuable!"
"Young & Gay is very helpful and every gay young person should participate in it."
Next Workshop
The next Young & Gay workshop will be held on:
Date: 29 October – 3 December (every Saturday for 6 weeks)
Time: 10AM to 1 PM
Location: VAC, 6 Claremont St, South Yarra
To register for this workshop contact (03) 9865 6700 or email@example.com or fill out the form below
Other Peer Education Workshops:
Primary links
- Home
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text:
Prices, promotions, styles and availability may vary by store and online.
Action - Over Under
Gauge - 20 Ga.
Chamber - 3"
Barrel Length - 26"
Weight - 5.8 Lbs.
The Beretta Gold Pigeon over-and-under shotguns are a perfect blend of beauty and performance, the meticulous detail of their appearance mirrored by their flawless performance in the field. It features deep relief engravings depicting hunting scenes on the side plates and rich English scrolls decorate the receiver. All metallic parts are coated in Beretta's special nickel-based finish for corrosion resistance. The stock and Schnabel forend are either matte lacquer finished or oil finished to bring out the high quality grain of the wood. The fine checkering, embedded oval plate for initials, gold single-selective trigger, and rubber recoil pad give these guns a touch of elegance. This shotgun includes a single bead sight and modified and cylinder chokes. Its wood, metal, and bore are all in good condition.


text:
Mouse wheel for scroll only - disable middle button paste
this wiki
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created 2003 · complexity basic · author Girish Gajwani · version 6.0
I have had a problem when using the mousewheel for scrolling. I occasionally press the wheel and it pastes text in the clipboard's "*" register at the place where the scroll wheel was pressed accidentally. This has been a constant irritation.
The workaround is documented at :help <MiddleMouse>, which includes the following information.
If you have a scrollwheel and often accidentally paste text, you can use these mappings to disable the pasting with the middle mouse button:
:map <MiddleMouse> <Nop> :imap <MiddleMouse> <Nop>
To revert to the original setting for middle button click:
:unmap <MiddleMouse> :iunmap <MiddleMouse>
While at it, take care also of 2-MiddleMouse, 3-MiddleMouse and (oh, humanity!) 4-MiddleMouse (that's for middle double clicks and triple and ...).
Alternatively, instead of simply ignoring it, make it the same as a left click with:
noremap <MiddleMouse> <LeftMouse>
Also with noremap!, and the whole 2-,3-,etc. list above.
These tips are helpful in stopping an accidental *single* click, but two or more clicks in same location (such as the button being pressed on by a book) will still cause a paste to occur. Anyone know why?
The solution is to add the following as well, to handle double-click, triple-click, and quadruple-click:
:map <2-MiddleMouse> <Nop> :imap <2-MiddleMouse> <Nop> :map <3-MiddleMouse> <Nop> :imap <3-MiddleMouse> <Nop> :map <4-MiddleMouse> <Nop> :imap <4-MiddleMouse> <Nop>
I find it easier to hold down the Ctrl key since I have nothing mapped to Ctrl-Middle. And then the middle mouse button still works according to my creaky old X-windows-originated intuitions.


text:
Catherine did a brilliant job of capturing the love and excitement my husband felt after becoming engaged! We had a lovely, fun and relaxed shoot at South Bank and took some incredible pictures of us as a couple that all our family and friends agree are so "us". To this ..
Whitedress Productions followed up with my enquiry straight away, and were extremely professional in their manner. They were really proficient at gathering a detailed brief about my needs and objectives for the project. On the day of filming they cleverly dealt with my camera-s..
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