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John W. Gofman, M.D., Ph.D., Professor Emeritus of Molecular &
Cell Biology, University of California at Berkeley.
Egan O'Connor, Executive Director and Editor, CNR.
Part 1 More Good than Harm, or Vice Versa?
Recently, the benefit of certain x-ray screening procedures has been openly challenged, especially by some radiologists.
Can the benefit possibly be challenged? Haven't we heard testimonials again and again from patients who say, "My life was saved by that screening, which discovered a cancer that otherwise could have killed me!"
And haven't most of us seen or heard advertisements for whole-body CT or EBCT screening (both procedures use x-rays), promising to reveal whether we have a health problem of which we are unaware?
One recent advertisement for such scans asserts that, for heart attack, cancer, and stroke, "Early detection makes all the difference . . . The full body scan and virtual colonoscopy are simple life-saving examinations that only take minutes but can save your life! Every Body Benefits" (San Francisco Chronicle, April 10, 2002, p.A11).
Can "every body" benefit from various x-ray screening tests? If enough people are screened, inevitably some miseries and some premature cancer and noncancer deaths are prevented --- in those particular individuals (a) where the discovered problem really would have become nasty, and (b) where such evolution could have been prevented in the same individuals by early treatment. (Available treatments which work for some individuals do not necessarily work for others.)
The Chance of Personal Benefit, Personal Harm
The fact that some people do benefit from various x-ray screening tests certainly does not guarantee that individuals who consent to (or insist upon) getting screened are likely to receive more personal benefit than personal harm.
The older you are, the more abnormalities you have accumulated. When they are detected by x-ray screening, you are very likely to face a host of additional procedures which are not risk-free (e.g., more x-rays, biopsies, surgeries, etc.) --- quite possibly to care for abnormalities which would never have caused you any trouble.
Responsible health professionals are finally asking: Do some sorts of screening policies cause more harm than good? Because the potential benefits have been so widely promoted, this document concentrates on providing more information about the likelihood of harms.
Part 2 Screening vs. Diagnostic Procedures
At the outset, it is important to make the distinction between screening and diagnostic procedures.
Screening procedures are employed to look periodically at symptom-free people in certain categories for some undetected disease --- for example, screening women over age 40 or 50 for breast cancer, or adults past a certain age for colon cancer, or men past age 50 for prostate cancer, or smokers and former smokers for lung cancer.
"Screening is the systematic testing of asymptomatic individuals for pre-clinical disease," states Robert J. Stanley, radiologist and past president of the American Roentgen Ray Society, in a deeply thoughtful article entitled, "Inherent Dangers in Radiologic Screening" (Stanley 2001). "Pre-clinical" refers to the phase of a disease between its genuine onset and manifestation of its signs and symptoms.
Although screening detects rather than prevents disease, its goal is to detect treatable problems while treatment will have its maximum benefit. The widespread assumption in medicine is that the earlier the treatment begins for most diseases, the more effective the treatment will be. The assumption has been particularly difficult to confirm with respect to many major cancers.
"We bring it [screening] to healthy people, and those who test positive become sick people, the subjects of medical intervention. We need to be awfully careful," warns Dr. Steven Goodman, associate professor of pediatrics and epidemiology at Johns Hopkins Medical School (in Kolata 2002, p.D4).
By contrast with screening procedures, diagnostic procedures are careful examinations of people who already have some suspicious signs (objective) or symptoms (subjective) of a potential problem --- e.g., cancer.
Part 3 Why Benefits of Screening Are Not Self-Evident
The difficulty, in establishing that cancer-screening which results in early treatment does more good than harm, is intimately tied to the difficulty in telling an early genuine cancer from an abnormality which is harmless.
"On the basis of animal models, my predisposition is to believe that early diagnosis is a good thing . . . Early diagnosis works in animals . . . Early diagnosis makes sense if you are diagnosing a true cancer," says Dr. Larry Norton, breast cancer specialist at the Memorial Sloan-Kettering Cancer Center, and president of the American Society for Clinical Oncology (in Kolata 2002, p.D4).
"True Cancer" --- the Key Phrase.
"True cancer" is a phrase which should interest everyone who contemplates having cancer-screening. Cancer has been defined in several ways. One attempt (in King 1990, p.46): "A class of diseases of animals characterized by uncontrolled cellular growth." Another try (in NAS 1990, p.392): "A malignant tumor of potentially unlimited growth, capable of invading surrounding tissue or spreading to other parts of the body by metastasis." In addition, there are "distributed" non-tumorous cancers (e.g., blood cancers).
A tumor is a mass of new tissue which persists and grows independently of its surrounding structures, and which has no physiologic use.
A neoplasm is "any new and abnormal growth, such as a tumor; neoplastic disease refers to any disease that forms tumors, whether malignant or benign" (NAS 1990, p.395).
"In situ cancer" is one which is still located in its original place. Then is it really cancer? The disagreement among experts is reflected in Dr. Stanley's statement that in situ cancers are "lesions of questionable malignancy" (Stanley p.991). Cancer biologists have had a saying: "Cancer is what cancer does. If it kills you, it was a malignancy."
Cancer Therapy for Non-Cancers.
The earlier the detection of an abnormality, the greater is the chance that treatment is directed at a lesion which would never become a malignancy and is not a true cancer. And this means that some resulting rises in apparent cure-rates of early cancers could be largely unreal.
How common is cancer therapy for non-cancers? No one knows. "Overdiagnosis exists in virtually every [class of] cancer," says Dr. Otis Brawley, professor of medical oncology and epidemiology of the Winship Cancer Institute at Emory University (in Kolata 2002, p.D4).
Longer Survival Times for True Cancers?
In this section, let us assume that screening does result in treatment of only genuine early cancers. The benefit of various treatments is most usually judged by an increase in survival time after diagnosis. "Unfortunately, increasing the [frequency of] five-year survival has little or nothing to do with proving that a disease is curable," says Dr. Stanley (2001, p.990).
Many experts have made the same point: Even a treatment which delivers no biological benefit, to patients having early cancer, will produce an increase in average survival time after diagnosis, whenever screening causes the diagnosis to occur earlier than it otherwise would.
"Damn Difficult!" Being Slow to Blame
In medical school over fifty years ago, one of my (jwg) professors warned everyone, "In medicine, it's damn difficult to prove anything about anything!" He was right. It is no criticism of anyone, when we or others point to the persisting difficulties in telling a true early cancer from an abnormality which needs no treatment, and in establishing how often your early treatment would be a benefit and how often it would be a harm.
Part 4 Breast Cancer: X-Ray Screening
Most readers will be aware of the raging debate, in professional and mass media, over whether mammography does more good than harm (e.g., in The Lancet, Jan. 8, 2000 + Oct. 20, 2001 + Feb. 2, 2002 + Mar. 16, 2002 + New York Times, Dec. 9, 2001 + Apr. 9, 2002 + AARP Bulletin, Apr. 2002).
We think the existing evidence is not solid about the probability of any personal benefit. And probability is the key issue, when an individual tries to weigh the chance of personal benefit versus personal harm. The probabilities related to harms are not solid, either. Estimates vary.
The Probability of Radiation Harm
Using the assumptions that the mean glandular dose to the breast per 2-view exam is 0.2 rad (0.2 centi-gray or cGy), that a woman starting at age 50 accumulates 15 mammograms, and that 3.7 is the incidence to mortality ratio, we estimated that the likelihood of a fatal mammogram-induced breast-cancer is roughly 1 chance in 500 (Gofman 1996: pp.180-81 for incidence, adjusted for fatality, pp.279-80).
But the upper limit of "permissible" dose per exam has been 0.6 rad. For individuals receiving 0.6 rad per exam, the dose and the risks would be three-fold higher. And the risks would also be variably higher for women who (unknown to them) have inherited certain genetic mutations (e.g., in the AT gene or in other DNA) which make x-ray-induced damage less likely to be correctly repaired.
Even so, it is reasonable to think that, from annual screening, your chance of not developing a mammogram-induced fatal breast cancer greatly exceeds the chance that you will.
The Probability of False-Positives
The radiation risk is just one consideration. There are others. There is the harm of false-positive results from the screening. False-positives are results which suggest the possibility of disease in a person for whom the possibility is not confirmed by repeated or other tests --- or by subsequent diagnosis of clinical disease.
How likely are false-positive mammograms in the USA? In 1998, the New England Journal of Medicine published a study, based on the HMO records of 4,319 women who received mammograms between 1983 and 1993 (Elmore 1998). The resulting estimates are (p.1092): For women having mammographies at age 50 or older, the cumulative risk of false-positives after five screening mammograms is 24%, and after ten exams, 47%. For younger women (age 40-49), the risks are, respectively, 30% and 56%. Such studies have stimulated progress on computer-assisted interpretation of mammograms, aimed at reducing such very high rates.
The findings above were supported by a separate study published in the Journal of the National Cancer Institute (Christiansen 2000). This study looked additionally at how the false-positive rate varied with the number of breast-cancer risk factors a woman has. "By the ninth mammogram, the risk [of a false-positive result] can be as low as 5% for women with low-risk variables and as high as 100% for women with multiple high-risk factors."
The harm from false-positives is not limited to anxiety. The harms can include unnecessary additional exposure to x-rays at higher doses. And biopsies. Indeed, some percutaneous biopsies are guided by additional x-rays.
The Probability of Unnecessary Treatment
More worrisome than a false-positive, whose result is corrected later, is an "overdiagnosis" --- followed by harmful treatment (surgery, radiation therapy, and or chemotherapy) for a non-cancer.
No one knows how much overdiagnosis occurs as a result of mammography. The issue concerns Dr. Barnett Kramer, director of disease prevention at the National Institutes of Health (NIH), who has studied the numbers from 1983 to 1998. His conclusion is described by Ms. Kolata (2002, p.D5) as follows:
If screening worked perfectly, every breast cancer found early "would correspond to one fewer cancer found later. That, he said, did not happen. Mammography, instead, has resulted in a huge new population of women with early stage cancer but without a corresponding decline in the numbers of women with advanced cancer."
Perhaps future evidence will be able to settle the question: Does the USA recently have a large increase in the number of genuine breast cancers --- detected and successfully treated, or do we have a large number of non-cancers which are mistakenly identified as cancers and treated "successfully"? What is more likely?
The external pressure on women to have periodic mammograms has been intense. But considering the uncertainty that mammograms will deliver more personal benefit than harm, "Rational women can make the decision not to have a mammogram, and no one should castigate them for doing that," says Russell Harris, M.D., of the University of North Carolina Medical School and member of a National Cancer Institute advisory board (in Greider 2002, p.15).
Part 5 Lung Cancer: X-Ray Screening
For smokers and former smokers, how often does x-ray screening, by "low-dose" spiral CT (computed tomography) for asymptomatic lung cancer, deliver a benefit?
Earlier Detection Not Yet a Benefit
CT may succeed in finding small lung cancers missed by conventional x-rays, but "there is no evidence to date that earlier detection leads to better patient outcomes," according to a very thoughtful analysis about screening by Thomas H. Lee, M.D., and Troyen A. Brennan, M.D., of the Harvard Medical School, in the New England Journal of Medicine (NEJM), Feb. 14, 2002 (Lee 2002, p.530).
Regarding lung cancer, they cite a recent study (Patz 2000-a) showing similar outcomes for patients diagnosed with 3-cm masses and with nodules less than 1 cm (less than 10 mm). "The reason may be that small tumors, such as 5-mm nodules, probably do not truly represent early disease; by the time tumors are visible on CT imaging, their potential to metastasize has already been realized. Research suggests that metastases may occur when lesions are just 1 to 2 mm in diameter --- well before they are detectable by any current method" (Lee 2002, p.530).
The Probability and Danger of False Positives
Patz reports the high rate of false-positives when 1,520 current or former smokers were screened at the Mayo Clinic by low-dose spiral CT (Patz 2000-b). According to Lee & Brennan, "15 cases of lung cancer were diagnosed, of which 60% were in early stages. However, 51 percent of all patients had at least one nodule and required follow-up with either additional CT examinations or invasive procedures" (Lee 2002, p.530).
That cohort of 1,520 people continues to receive an annual CT screen of the lungs and abdomen. According to Stephen Swenson, M.D., head of radiology at the Mayo Clinic, by now (the study's fourth year) the screenings have detected 44 lung cancers, and also 2,900 lung nodules.
"Ninety-nine percent of lung nodules are benign," said Dr. Swensen, according to Ridgely Ochs (Ochs 2002, p.D7). Now we quote Mr. Ochs: "Each nodule requires a biopsy --- an invasive, painful, and costly procedure. It can also be deadly. Studies have found that about 4% of surgeries taking out lung nodules result in death, Swensen said." And Swensen added, "We could realistically be doing more harm than good."
The Society of Thoracic Radiology has issued a "consensus statement" on screening for lung cancer by low-dose helical CT (at www.thoracicrad.org). It recommends against mass screening until and unless its benefits to patients are validated by appropriate trials.
Meanwhile, a Japanese study of spiral CT screening for early lung cancer reports similar rates of lesions in people who never smoked as in smokers, even though ten times more smokers than nonsmokers die from lung cancer (Kolata p.D4). Dr. Barnett Kramer, of the NIH, points out that such screening procedures are probably finding many lesions that are "not dangerous" (in Kolata, p.D4).
The Estimated Radiation Dose
The chest CT for cancer screening is estimated to deliver an entrance dose (skin dose) of about 0.2 to 0.4 rad (centi-gray), according to Drs. Edward L. Nickoloff and Philip O. Anderson, both of the radiology department at Columbia University (Nickoloff 2001, p.286).
Part 6 Colon Cancer: X-Ray Screening
Currently, screening for colon cancer is done mostly by endoscopy (no radiation). However, for people who find cleansing of the colon and insertion of the endoscope unappealing, "virtual colonoscopy" seems very much more attractive.
Virtual colonoscopy is the popular name for CT colonography, an x-ray procedure which also requires cleansing of the colon, but eliminates deep penetration by any tube. Still, a rectal tube is required to insert air, in order to distend and unfold the walls of the colon.
"Helical CT scanning is performed in a single breath-hold . . . Acquisition [of images] is repeated with the patient in the prone position to redistribute the gas into previously collapsed segments," according to Dr. Joseph T. Ferrucci, of the radiology department at Boston University School of Medicine (Ferrucci 2001, p.977).
The three-dimensional (3-D) images available from virtual colonoscopy can simulate what is viewed during conventional colonscopy --- although the 3-D capability is usually reserved for only the colonic areas where the two-dimensional rendition suggests the need for additional inspection (Ferrucci p.977).
Should Every Polyp Be Removed?
Virtual colonoscopy is in its early stages. Today, "polyps greater than 1.0 cm are detected with sensitivity and specificity approaching 90%, with sensitivity falling to 50% for polyps at the 5-mm level," according to Dr. Ferrucci (p.978). Polyps are "a mucosal elevation or protuberance, not necessarily a precancerous neoplasm" (Ferrucci p.982).
Again, the issue arises: Would it be beneficial or harmful to have all the smaller polyps detected and removed?
According to Dr. Ferrucci (p.980), when polyp size is less than 5 mm, "hyperplastic polyps are far more prevalent than tubular adenomas . . .Overlooking them [hyperplastic polyps], however, is of no clinical importance, because they are not precancerous, and removing them at colonoscopy, now a widespread practice, conveys no benefit." He seems unusually certain. He continues (p.980):
"One area of concern, nevertheless, is the true `flat adenoma,' which, although uncommon, may exhibit a more aggressive biologic behavior, evolving into invasive cancer more rapidly. Imaging flat adenomas could pose problems for CT colonography, but no published results are yet available." (Adenoma = a tumor, usually benign, of glandular structure or glandular origin.)
The Probability of Overtreatment
Again, the treatment of countless harmless lesions is the issue. According to Dr. Ferrucci (p.982): "Colonic polyps are common after age 50 (50% of adults), increasing even more in prevalence with advancing age. However, only about 3% of all adenomas ever become malignant. The likelihood of any given polyp being malignant . . . is closely related to size, because only 1% of adenomas less than 1 cm will harbor invasive cancer . . . More than 70% of all discovered polyps are less than 1 cm."
The Radiation Dose
"The prospect of population screening by CT requires careful consideration of radiation dose, especially with the dissemination of multi-detector CT and its potential for [upward] `dose creep'," warns Dr. Ferrucci (p.984).
He reports estimated radiation doses of 0.187 rad (cGy) for women and 0.285 rad for men when "low dose protocols" were devised, using tube currents of only 50-70 milli-amps (p.984). "Although image noise and beam hardening are theoretic disadvantages of the lower dose [75% lower than for a standard abdominal-pelvic CT examination], in practice they do not appear to interfere with clinical interpretation" (p.984). He concludes his discussion of radiation dose:
"Finally, as the relative clinical insignificance of polyps smaller than the 0.5 cm [ 5 mm ] threshold becomes understood . . . there might be less reluctance to sacrifice spatial resolution for lower dose."
But, until there are better ways to tell genuine cancer threats from harmless lesions, American physicians in our litigious society may worry about their legal liability for choosing a technique which "misses" small lesions . . . and for recommending against treating every detected abnormality.
Part 7 Incidental Findings: Adrenal and Kidney Tumors
"Incidentalomas" are tumors which show up incidentally when people have a CT procedure (or an MRI) for some other medical reason.
According to Gina Kolata (2002, p.D4), adrenal-gland tumors of unknown significance "began turning up in increasing numbers" during such procedures. She reports, "Medical specialists do not know whether they should be removed or left alone, but they do know that lethal adrenal cancers are far too rare for many of those tiny tumors to be dangerous."
The inability to distinguish dangerous from harmless is acknowledged for renal (kidney) growths, too. "The prevalence of small cortical lesions at autopsy suggests that many proliferations of renal cortical epithelium lack the capacity to develop into clinical cancer. However, the search for a means to distinguish those lesions that have the potential to progress and those that do not has been unsuccessful" (Bostwick 1997).
What might be the ratio between harmless and fatal lesions? Dr. Stanley (2001, p.989) points out that "Only 1% of the adult (US) population develops potentially lethal renal cancer. However, if the detection threshold is lowered to the serial sectioning level (2-3 mm) and histology remains the gold standard [for diagnosis], 22% of the screened population could be said to have pathologically proven renal cell carcinoma."
Part 8 Entire Body: X-Ray Screening
A full-body CT scan usually includes the neck (starting at the thyroid gland) and then the whole area through the pelvis.
According to Fred A. Mettler, M.D., chair of radiology at the Univ. of New Mexico, it does not easily detect breast, prostate, ovarian, cervical, or endometrial cancers (in Ochs 2002, p.D7). But it does detect various lesions which, after additional tests, may be called cancer.
According to Anouk Stein, M.D., radiologist at one of the commercial facilities offering the test, it also spots emphysema, calcium in the coronary arteries, aneurysms, and spinal problems (in Ochs, p.D7).
Heart Examinations: Calcium Deposition
The benefit of measuring the amount of calcium deposited in the coronary arteries is not well established. According to Dr. Thomas H. Lee, a cardiologist, there are some data suggesting that asymptomatic persons with greater calcification have an increased chance of heart attacks and other coronary events, but "the role of electron beam CT as a screening test or a tool to guide therapy remains unclear" (Lee 2002, p.529).
Division within the Radiology Profession
The advocates of whole-body CT screening are generally radiologists who say that it may save your life. And it may (see Part 1). The issue is: What is the probability of true benefits vs. the probabilty of true harms? Someday, there may be enough credible statistical and biological knowledge to answer the question, but not now.
The full-body screening procedure was introduced about two years ago. On September 27, 2000, the Board of Chancellors of the American College of Radiology (ACR) approved the following statement:
"The ACR, at this time, does not believe there is sufficient scientific evidence to justify recommending total body computed tomographic (CT) screening for patients with no symptoms or a family history suggesting disease. To date, there is no evidence that total body CT screening is cost effective or is effective in prolonging life. In addition, the ACR is concerned that this procedure will lead to the discovery of numerous findings that will not ultimately affect patients' health, but will result in increased patient anxiety, unnecessary follow-up examinations and treatments and wasted expense. ACR will continue to monitor scientific studies concerning this procedure."
In Febrary 2002, Lee & Brennan wrote (Lee, p.530): "There are no rigorous published data on the use of CT scanning of the entire body to screen for cancers . . . The most obvious weakness of these screening programs is that they do not use oral or intravenous contrast medium, thereby compromising the ability of CT scans to detect small tumors in organs such as the liver, pancreas, and kidneys . . . False positive findings are also common, with the detection of cysts and other benign lesions that can only be evaluated through other tests or invasive procedures."
In March 2002, Dirk Sostman, M.D., head of radiology at Weill Medical College of Cornell University, told Ridgely Ochs (Ochs, p.D7): "People say, `Look, we save lives; we discover disease' . . . The thing they don't talk about is the prevalence of abnormalities. It's extremely high and most are benign . . ."
Dr. Stephen Swensen, the Mayo Clinic's chief of radiology, told Mr. Ochs (p.D6), "I guess the core question is: Has anyone proved it is effective? Do we save lives? And if we are unclear about that, are we doing more harm than good?"
The Full-Body Radiation Dose
Besides false-positives and overtreatment, another overt concern is the extra radiation exposure, estimated to be about 1.75 rads (centi-gray) absorbed internal dose per whole-body procedure by a radiologist, Fred Mettler, M.D., (in Ochs, p.D7).
If Dr. Mettler's estimate is correct, we calculate that the radiation dose per procedure would be equivalent to the extra radiation from well over 1,000 commercial 5-hour airplane trips from coast to coast, USA. And the additional radiation doses from repeated screenings cannot be swept under the rug. After all, when you consent to (or insist upon) a screening procedure, the reason is to find disease early --- which requires frequent repetitions of the search.
"We do have a concern that people are getting irradiated without good reason," said Thomas B. Shope, Ph.D. to Mr. Ochs (p.D6). Dr. Shope is a leading figure at the U.S. Food and Drug Administration's Center for Devices and Radiological Health.
We certainly share that worry. Our recent research indicates that accumulated exposure to medical radiation is a necessary co-actor in causing over half of the fatal cases both of cancer and coronary artery disease in the USA (Gofman 1999). Every additional x-ray dose counts in the accumulating risk. Therefore, off-setting benefits need to be real.
The Menace of Future Lawsuits?
The risk of x-ray-induced cancer, caused by full-body CT screening tests for early cancer, troubles some radiologists. For instance, Nickoloff & Alderson wrote (Nickoloff 2001, p.287):
"The likelihood of false-positive findings that might lead to further CT or other procedures enhances the possibility for repeated exposures. At least asymptomatic patients who undergo such procedures should receive written and verbal information about the estimated increase in cancer risks associated with the procedure that they are undergoing to reduce their cancer risk." And:
"Such information and documentation of the patient's full knowledge also should help avoid unnecessary legal confrontations in the future should such patients develop cancer. Given that the latency time for cancer induction in the dose ranges used in CT is calculated to be 10-30 years, policies need to be adopted now to avoid problems in the future."
In our legal system, physicians may now be at risk both for recommending certain x-ray screening tests, and for not recommending them.
Who Pays for Full-Body CT Scans?
Presently, individuals send themselves to commercial facilities and spend their own money for the full-body CT screening (in the range of $850). Don't people have a right to purchase information about their own bodies? Lee & Brennan confront this issue (Lee, p.530-31):
". . . there are financial consequences [from screening] that affect the rest of the health care system. The most obvious of these consequences are the costs associated with the follow-up of false positive results . . . These costs include not only those of additional tests and procedures that are likely to be covered by the patient's health insurance, but also the costs resulting from complications of those interventions." [False-positive results raise the cost of health insurance for everyone.] "Care provided to one patient will most likely affect the care available to other patients."
Part 9 The Ethical Issues, and Thinking about Extremes
Lee & Brennan (Lee, p.531) have raised additional ethical issues, particularly about physician-ordered screening tests. Their opinion:
"The proliferation of [screening] tests that lack a scientific basis is an issue that must be addressed by the profession, not left to the discretion of the individual physician . . . A good case can be made that professional ethics prohibits providing unproven diagnostic screening tests, even if there is substantial demand from patients. Rather, physicians should be instructing patients that such tests are unnecessary and [physicians should be] using their energy for the appropriate development of evidence regarding the efficacy of these tests."
With respect to cancer, we are confident that the new tools of molecular biology will be able to tell early malignancies from harmless lesions far better in the future than now.
Meanwhile, we agree with a warning from Prof. Bradley Efron, statistician and health policy expert at Stanford University. He warns (here we quote Ms. Kolata's summary, p.D4) that the value of a screening test has to be in doubt if "the number of lives saved is miniscule compared with the number of people who are harmed by overdiagnosis, by unnecessary treatments, [and] by treatments that could have been delayed with no ill effects." Then Ms. Kolata quotes Prof. Efron directly:
"The people who say `We're saving lives' [by screening] are undoubtedly right . . . But the question is, what's the cost? We could save even more lives if all men had their prostates removed at age 50 and if all women had their breasts removed at age 50."
# # # # #
- Bostwick 1997 (David G. + John N. Eble), Urologic Surgical Pathology. ISBN 0801675030.
- Christiansen 2000 (Cindy L. et al), "Predicting the Cumulative Risk of False-Positive Mammograms," J. Natl. Cancer Inst. 92: 1657-66.
- Elmore 1998 (Joann G. et al), "Ten-Year Risk of False Positive Screening Mammograms and Clinical Breast Examinations," New Engl. J. Med. 338: 1089-96.
- Ferrucci 2001 (Joseph T.), "Colon Cancer Screening with Virtual Colonoscopy," Amer. J. Roentgenology 177: 975-988.
- Gofman 1996 (John W.), Preventing Breast Cancer. ISBN 932682960
- Gofman 1999 (John W.), Radiation from Medical Procedures in the Pathogenesis of Cancer and Ischemic Heart Disease. ISBN 0932682979.
- Greider 2002 (Linda), "Mammogram Quandary: Women Find No Easy Answers in Screening Debate," AARP Bulletin 43 (Apr): 14-15.
- King 1990 (Robert C. + Wm. D. Stansfield), A Dictionary of Genetics, 4th Ed. ISBN 0195063716.
- Kolata 2002 (Gina), "Test Proves Fruitless, Fueling New Debate on Cancer Screening," New York Times, Science Times, Apr. 9, 2002, pp.D1+D4.
- Lee 2002 (Thomas H. + Troyen A. Brennan), "Direct-to-Consumer Marketing of High-Technology Screening Tests," (Sounding Board), New Engl. J. Med 346: 529-531.
- NAS 1990 (Natl Acad. of Sciences Advisory Com'tee on Biological Effects of Ionizing Radiation), Health Effects of Exposure to Low Levels of Ionizing Radiation, ISBN 0309039959.
- Nickoloff 2001 (Edward L. + Philip O. Alderson), "Radiation Exposures to Patients from CT: Reality, Public Perception, and Policy," (Commentary), Amer. J. Roentgenology 177: 285-87.
- Ochs 2002 (Ridgely), "A Diagnostic Tool, with Complications: Supporters Tout the Full-Body CT Scan . . .," Newsday, March 19, 2002, pp.D6-D7.
- Patz 2000-a (E.F., Jr. et al), "Correlation of Tumor Size and Survival in Patients with Stage 1A Non-Small Cell Lung Cancer," Chest 117: 1568-71.
- Patz 2000-b (E.F., Jr. et al), "Screening for Lung Cancer," New Engl. J. Med. 343: 1627-33.
- Stanley 2001 (Robert J.), "Inherent Dangers in Radiologic Screening," Amer. J. of Roentgenology 177 (Nov): 989-992.
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