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Original Article

A Look-Back Investigation of Patients of an HIV-Infected Physician — Public Health Implications

Richard N. Danila, Ph.D., M.P.H., Kristine L. MacDonald, M.D., M.P.H., Frank S. Rhame, M.D., Michael E. Moen, M.P.H., Dorothy O. Reier, B.S.N., M.P.H., Joan C. LeTourneau, M.P.H., Mary K. Sheehan, R.N., M.P.H., Joann Armstrong, R.N., B.A., Mitchell E. Bender, M.D., Michael T. Osterholm, Ph.D., M.P.H., and the Investigation Team*

N Engl J Med 1991; 325:1406-1411November 14, 1991

Abstract
Abstract

Background

Transmission of the human immunodeficiency virus (HIV) to five patients receiving care from an HIV-infected dentist in Florida has recently been reported. Current data indicate that the risk of HIV transmission from health care workers to patients is extremely low. Despite this low risk, programs to notify patients of past exposure to an HIV-infected health care worker are being conducted with increasing frequency.

Methods

We recently conducted an investigation of all the patients cared for by an HIV-infected family physician during a period when he had severe dermatitis caused by Mycobacterium marinum on his hands and forearms. After reviewing the patients' records, we notified 336 patients who had undergone one or more procedures (digital examination of a body cavity or vaginal delivery) placing them at potentially increased risk of HIV infection. The patients were offered tests for HIV infection and counseling.

Results

Of the 336 patients, 325 (97 percent) had negative tests for HIV antibody, 3 (1 percent) refused testing, 1 (<1 percent) died of a cause unrelated to HIV infection before notification, and the HIV-antibody status of 7 (2 percent) remained unknown. The direct and indirect public health costs of this investigation were approximately $130,000.

Conclusions

The results of this investigation raise important questions about the risk of HIV transmission from health care workers to patients and the usefulness of HIV look-back programs, particularly in the light of recently published recommendations from the Centers for Disease Control. We propose that before a look-back investigation is undertaken, there should be a clearly identifiable risk of transmission of the infection, substantially higher than the risk requiring limitation of an HIV-infected health care worker's practice prospectively. (N Engl J Med 1991; 325:1406–11.)

Media in This Article

Figure 1 M. marinum Infection of the Right Hand, September 1990.
Table 1Medical Procedures Performed by the Physician That Resulted in the Notification of Patients.
Article

TRANSMISSION of the human immunodeficiency virus (HIV) to health care workers caring for HIV-infected patients has been well documented.1 The possibility of such transmission to patients receiving care from an HIV-infected health care worker was hypothesized before it was first reported, on the basis of experience with the transmission of the hepatitis B virus from health care workers to patients.2 , 3 To date, there has been only one documented report of HIV transmission from an infected health care worker to patients.4 In that case, five patients became infected with HIV after receiving care from an HIV-infected dentist; the mechanism of transmission remains unclear.4 5 6 Current data indicate that the risk of HIV transmission from health care workers to patients is so low that it cannot be measured accurately; nonetheless, the potential for such transmission raises complex medical, ethical, legal, and social issues that have major public health implications.

Guidelines addressing these issues have been developed by a variety of professional organizations.7 8 9 10 11 12 13 14 15 16 On July 12, 1991, the Centers for Disease Control (CDC) recommended that HIV-infected health care workers should not perform exposure-prone procedures unless they have sought counsel from a review panel of experts and have been advised under what circumstances they may be allowed to perform such procedures.16 The CDC recommendations are the only published guidelines that also address the issue of notifying patients cared for in the past by an HIV-infected health care worker. The recommendations state that such efforts should be considered on a case-by-case basis.

During the summer of 1991, there was widespread news coverage about the potential for HIV transmission from HIV-infected health care workers to patients. Because of the increasing awareness of this issue, more than 30 HIV-infected health care workers in the United States were identified publicly by institutions, news organizations, or public health agencies between June 1 and July 31, 1991 (Minnesota Department of Health: unpublished data). This contrasts with the 12 investigations of health care workers (6 published and 6 unpublished) conducted before June 1991.4 5 6 , 17 18 19 20 21 22 23

Both formal and informal look-back investigations have been initiated for the patients of these health care workers. In a formal investigation, patients are systematically notified by an institution or public health agency, and provision is made for coordinated HIV-antibody testing. In an informal investigation, an HIV-infected health care worker is identified publicly by an institution, public health agency, or news organization, but there is no systematic program of patient notification and testing. Given that more than 7000 health care workers in the United States have the acquired immunodeficiency syndrome (AIDS) and an additional unknown number have HIV infection, the potential for a dramatic increase in the number of investigations involving notification is substantial.

In May 1991, the Minnesota Department of Health conducted a formal look-back investigation of patients cared for by an HIV-infected family physician who had extensive dermatitis caused by Mycobacterium marinum on his hands and forearms. The results of the investigation offer a framework for discussing the public health implications of conducting such investigations.

Case Report

A 39-year-old male physician was well until March 1989, when seborrhea and a papular eruption developed on his face, hands, arms, and trunk. In January 1989, he had begun a voluntary weight-loss program; during the next 10 months he lost 26 percent of his body weight. In 1990 he was seen by a dermatologist who made a clinical diagnosis of vitiligo on the legs and in the perianal and pubic areas, and one of alopecia areata and folliculitis of the scalp. Skin biopsies were not performed. Subsequently, the physician had fatigue and chronic diarrhea. In June 1990, he noted a nodular skin lesion on the dorsum of his right hand. During the next several months additional nodules developed on this hand, as well as on the dorsum of the left hand and on the right arm, left thigh, and left foot. After minor trauma, or spontaneously in the case of nodules on extensor surfaces, the larger nodules produced serous fluid for up to a day and then formed scabs. Occasionally, after more severe trauma, the nodules bled.

In September 1990, the physician was evaluated by another dermatologist, who noted violaceous papules, pustule-like lesions, and nodules on the dorsum of the fingers and hands, the right forearm, and the right leg (Fig. 1Figure 1 M. marinum Infection of the Right Hand, September 1990.). An HIV-antibody test on September 12 was positive. A chest roentgenogram was interpreted as normal. The CD4 T-lymphocyte count was 0.03 × 109 per liter. A skin biopsy on September 12 revealed epithelial hyperplasia, foci of lymphocytes, and a superficial bandlike infiltrate in the dermis composed of histiocytes, many of which were in an epithelioid configuration (i.e., granulomas), and neutrophils. A Fite stain revealed multiple acid-fast bacilli. Culture yielded a mycobacterium species that was identified at the Tuberculosis Laboratory of the Minnesota Department of Health as M. marinum. Therapy with zidovudine (100 mg five times per day), doxycycline (100 mg twice per day), isoniazid (300 mg once per day), and rifampin (600 mg once per day) was instituted in September 1990. In November, minocycline (100 mg twice per day) was substituted for the previous antimycobacterial regimen.

Beginning in October 1990, the skin lesions and constitutional symptoms gradually improved. The last episode of serous or bloody drainage from any of the nodular lesions occurred in December 1990. By the end of February 1991, the nodular areas had become macular, and no excoriated areas were present.

In 1986, the physician had tested negative for hepatitis B surface antigen and positive for hepatitis B surface and core antibody.

Methods

Background

The Minnesota Department of Health received an AIDS case report about this physician in September 1990. The Minnesota Board of Medical Examiners, a separate state agency with the legal authority to license and discipline physicians, also received a report about this physician from another physician. On October 19, 1990, representatives of the Board of Medical Examiners met with the physician, and he agreed to cease performing invasive procedures and to wear two pairs of gloves during any potential direct contact with patients until he was further instructed. After additional review of the case that included consultation with national experts, the Board of Medical Examiners requested in May 1991 that the Minnesota Department of Health conduct an epidemiologic investigation of the patients seen by this physician. At that time, the department notified the physician of its plans to conduct a look-back investigation of his patients; he agreed to cooperate fully.

This physician was a family practitioner who practiced in two private clinics and a hospital in the Minneapolis—St. Paul metropolitan area. He saw approximately 90 to 100 patients each week and assisted in approximately 60 vaginal deliveries annually, occasionally performing episiotomies. He did not perform cesarean sections but did care for infants immediately after delivery by cesarean section. He conducted limited types of minor surgery, such as excising moles and suturing lacerations in an outpatient setting.

Period of Risk and Procedures Involving Potential Risk

Although this physician did not generally perform the types of invasive procedures that would be most likely to expose patients to his blood, the severe dermatitis of his hand was considered to be an unusual feature that may have placed his patients at increased risk of acquiring HIV infection. Thus, we defined a procedure involving increased risk as one in which the physician's gloved or ungloved hand or finger was placed inside a patient's body cavity during the time when the dermatitis was present on his hands and could potentially have leaked serous fluid. This at-risk period, determined by interviewing the physician and his dermatologists and reviewing his medical records, was defined as lasting from May 1990 through February 1991. To ensure complete inclusiveness, this interval was defined to include approximately three weeks before the onset of the skin lesions and another three weeks after their resolution. The procedures involving increased risk included vaginal and rectal examinations, oral examinations with the physician's finger inside the mouth, and vaginal deliveries with or without episiotomy. Newborn infants were considered to have been exposed during delivery. Suturing of minor lacerations, excision of moles, and circumcisions were excluded from the list of risky procedures, because contact between the gloved hand and open tissue was considered extremely unlikely.

The physician reported wearing examination gloves during the at-risk period (with double-gloving after October 19, 1990) whenever he touched mucous membranes. He used vinyl and latex examination gloves equally, depending on their availability. He did not document or recall any needle sticks, other percutaneous injuries, or other incidents that might have exposed patients to his blood.

Review of Records and Notification of Patients

The records for all patients seen during the at-risk period were reviewed by nurses on the investigation team. These records included 3291 clinic and hospital records for 1382 patients, identified by a review of clinic appointment books and hospital admission logs. Three hundred thirty-six patients were considered to have been potentially exposed to HIV. Letters signed by the physician were sent to these patients by both certified and first-class mail, notifying them of their risk and recommending HIV-antibody counseling and testing. The patients were directed to call an unpublished telephone number at the Minnesota Department of Health to receive additional information. A second telephone number was made public, for use by the general public and by the patients of this physician who had been determined not to be at risk.

Free counseling and testing for HIV antibody were offered to the at-risk patients in clinics established for this purpose at the University of Minnesota Hospital and Clinics HIV Clinic under contract with the Department of Health. Counseling was provided by health care professionals specializing in HIV disease and AIDS who received additional training specific to this situation. Clinical information and demographic data were collected for each patient during the clinic visits. For 43 patients, the most recent potential exposure had occurred after December 31, 1990, less than six months before the date of their HIV-antibody test. However, they were not encouraged to be retested after six months, as is recommended to health care workers who have needle sticks.1 This recommendation was made because at the time of the procedure the physician was wearing double gloves and his dermatitis was resolving; presumably, both factors decreased the risk of transmission substantially. Department of Health staff members provided follow-up to nine institutionalized patients, and all at-risk patients living out of state were reimbursed for the cost of testing.

Specimens of blood from the patients were initially tested for HIV by enzyme immunoassay. Repeatedly reactive specimens were then tested by the Western blot assay, a recombinant immunoblot assay (RIBA-HIV216, Chiron), a synthetic-peptide solid-phase enzyme immunoassay (GENIE HIV-1 and HIV-2, Genetic Systems), polymerase chain reaction, and viral culture.24 25 26 27 A specimen of the physician's peripheral-blood mononuclear cells was stored, and arrangements were made to compare the nucleic acid sequences of his HIV with isolates from any HIV-infected patients.

AIDS and HIV infection are reportable conditions in Minnesota regardless of the patient's clinical status, and the Minnesota Department of Health conducts active surveillance for these conditions. The list of patients at risk was cross-checked against the AIDS/HIV registries. Finally, we determined the number of hours spent by the department's staff and the costs of the record review, notification process, and the counseling and testing clinic.

Results

Of the 336 patients, 77 were male (23 percent), and 259 were female (77 percent). Thirty-eight (11 percent) were less than 1 year old at the time of their initial exposure, 24 (7 percent) were 1 through 19 years old, 231 (69 percent) were 20 through 49 years old, 42 (12 percent) were 50 or older, and the age of 1 patient (<1 percent) was undetermined. The patients underwent a total of 742 medical procedures that were considered to involve potential risk (Table 1Table 1Medical Procedures Performed by the Physician That Resulted in the Notification of Patients.). One hundred eighty patients (54 percent) underwent one such procedure during the at-risk period; 90 (27 percent), two procedures; 11 (3 percent), three procedures; 12 (4 percent), four procedures; 5 (1 percent), five procedures; 8 (2 percent), six procedures; 18 (5 percent), seven procedures; and 12 (4 percent), eight or more procedures. Table 2Table 2Patients Treated by the Physician during the At-Risk Period, According to Earliest Date of Potential Exposure.* shows the number and type of procedures performed according to the timing of the exposure. Over two thirds of the patients were seen in the first exposure period, when the physician's hand lesions were the most severe and he was using only one pair of gloves.

All the patients (or their parents) received the letters sent to them, and all either contacted Minnesota Department of Health staff members or were contacted by them. Three hundred twenty-five patients (97 percent) were tested, three (1 percent) refused testing, one (<1 percent) died of a cause unrelated to HIV infection before notification, and the HIV-antibody status of seven (2 percent) remained unknown. Of those tested, 308 were tested at the clinic sponsored by the Minnesota Department of Health, and 17 were tested by private physicians. Copies of the test results were obtained for 7 of these 17 patients, and the results were obtained verbally from the other 10. Serum samples from 324 patients were initially nonreactive on enzyme immunoassay, and 1 was weakly reactive on repeated testing. Follow-up Western blot tests of the latter specimen using both in-house and licensed test kits were indeterminate, with a moderately reactive band in the p24 region and an atypical, weakly reactive band in the p66 region. The specimen was subsequently negative for antibody to HIV-1 and HIV-2 by the synthetic-peptide solid-phase enzyme immunoassay, negative for HIV-1 antibody by the recombinant immunoblot assay, and negative for HIV-1 by the polymerase chain reaction and by viral culture. None of the 336 patients were matched with the 2723 persons listed in the AIDS/HIV registries of the Minnesota Department of Health.

No M. marinum infections were documented in the incisions or wounds of 28 patients who required suturing during the at-risk period. In addition, none reported tenderness, persistent drainage, or redness that required evaluation by a physician at the site of an incision or wound.

The direct and indirect economic costs for public health of this look-back investigation are shown in Table 3Table 3Estimated Direct and Indirect Costs Incurred by the Minnesota Department of Health for the Look-Back Investigation, as of August 1, 1991.. The highest cost was that of the salary and benefits for the departmental personnel who reviewed the medical records, compiled the list of potentially exposed patients, staffed the telephone bank to counsel patients and the general public, and responded to inquiries from news organizations. Fifty-seven staff members were directly involved in this effort, for more than 4200 person-hours. Other costs were those of HIV-antibody—test counseling, laboratory testing, legal fees, postal fees, and the installation and leasing of additional telephone lines to handle the volume of calls. Costs to the Board of Medical Examiners, the physician, or the clinics or hospital where the physician practiced were not determined.

Discussion

Published guidelines specify that health care workers with exudative dermatitis should refrain from direct contact with patients and from handling equipment used in direct patient care until the condition resolves fully.1 , 7 8 9 , 11 , 16 This proscription is recommended regardless of the health care worker's HIV-infection status. According to standard infection-control policies, the physician we have described should not have had direct contact with patients during the time of his severe hand dermatitis. This incident underscores the need to reinforce standard infection-control policies in clinical settings.

Although the physician wore single or double gloves, their usefulness in preventing HIV transmission is unclear. Several studies have documented that surgical gloves often have microscopic tears before or during use. The extent of leakage depends on the type of glove (sterile or nonsterile, latex or vinyl) and on the testing procedure used to measure leakage.28 29 30 31 32 33 Presumably, the risk of HIV transmission was substantially decreased during the time the physician wore double gloves. One study of surgical personnel found that the outer glove decreased the rates of perforation of the inner glove and of cutaneous blood exposure by 60 to 80 percent; presumably, there would be a similar reduction in the risk of HIV transmission from the health care worker to a patient.34

Six investigations of HIV-infected health care workers have been published in the medical literature to date. One involved the transmission of HIV by a Florida dentist to five patients.4 5 6 In another study, 616 patients of a surgeon who died of AIDS were tested; 1 was HIV-antibody—positive.17 This person had used illicit drugs intravenously and had a medical history suggesting that he was already infected with HIV at the time of his surgery. Two additional studies involved the follow-up testing of 75 and 76 patients of HIV-infected surgeons; none were HIV-positive.18 , 19 In another study, the names of 400 former patients of a surgeon with AIDS were compared with the names in Florida's AIDS registry; no matches were found.20 , 21 In the sixth study, no HIV infections were found among 143 former patients of an HIV-infected dental student.22

The lack of HIV transmission in the patients we studied is encouraging, given the severity of the physician's dermatitis and the presence of serous fluids potentially containing HIV. However, this and similar look-back investigations are limited in their ability to demonstrate transmission, because of the relatively small number of patients studied, the probability of a low risk of transmission in a given procedure, and the potential for clustering of cases of HIV transmission in association with a single practitioner rather than random infrequent transmission by all HIV-infected health care workers.

The public health cost to the Minnesota Department of Health of this formal look-back investigation equaled one third of the entire annual budget for statewide AIDS and HIV surveillance. This amount does not include the costs borne by the Board of Medical Examiners, the physician and the clinics where he worked, or the hospital. More important, all other major efforts of the department's Acute Disease Epidemiology Section to promote disease prevention and control were delayed for approximately six weeks as staff resources were diverted. Additional costs would have been incurred if any HIV-infected patients had been found. Extensive counseling and further testing would then have been required, including nucleotide sequencing of HIV isolates from the physician and the patient.

Although it was not directly assessed in this investigation, most persons expressed extreme anxiety and fear after receiving their notification letters. An indirect measure of this reaction is that more than 90 percent of the tests requested were carried out in the first four days of the clinic. In addition, the Minnesota Department of Health received approximately 1300 telephone calls in the 10 days after the initial announcement of the investigation.

Our experience raises questions about the value of look-back investigations. In some instances, such investigations were performed because there was a substantial risk of transmission of disease to patients; in other instances, they were performed in the absence of increased risk because of concern for the patients' right to know or because of concern for legal liability. Look-back investigations may also be conducted in order to collect data to define the risk of HIV transmission in these settings more fully.

A number of questions need to be considered before a look-back investigation is started for public health reasons. Did the health care worker perform procedures that potentially placed patients at increased risk? Is there evidence of egregious violation of infection-control practices that would increase the likelihood of HIV transmission? Did the health care worker have other conditions, such as dermatitis of the hand or a bleeding disorder, that could increase the risk of transmission? Is it known when the health care worker first became infected with HIV? Is an HIV isolate available from the health care worker that can later be used to determine whether a patient's HIV isolate is related? What is the expected prevalence of HIV, independently of any health care worker—associated transmission, in the population of patients who would be tested? If the health care worker is still living, is he or she cooperative? What effect will it have on the health care worker, his or her family, the patients involved, and the general public?

Since June 1991, look-back investigations have been conducted with growing frequency. Because society has increasingly demanded governmental action to guarantee virtually a zero risk, with little regard to the expenditures required and the impossibility of achieving a zero risk, we believe there will continue to be widespread public support for these investigations.35 Our experience in Minnesota supports this conclusion.

In addition, further support for look-back investigations may be inferred from the CDC guidelines issued on July 12.16 A logical extension of these guidelines is that if prospective restrictions are to be placed on a health care worker's practice, then there should also be retrospective notification of patients. The CDC guidelines do not provide criteria for initiating lookback investigations.

Since these investigations are very costly, involving the diversion of extensive monetary and staff resources, and the likelihood of identifying HIV-infected patients is extremely small, the usefulness of such investigations for the public health is likely to be minimal. For this reason, we propose that routine notification of patients who have undergone exposure-prone invasive procedures should not be considered a standard public health practice. Rather, we believe that look-back investigations should be undertaken in only three situations. First, they should be initiated when there is evidence of HIV transmission to a patient as a result of a procedure performed by a health care worker. Second, selective look-back investigations should be considered when there is evidence of egregious violation of standard infection-control practices (such as the presence of exudative dermatitis) during the time the health care worker was probably infected with HIV. Third, because of the need for additional data to define the risk of HIV transmission from health care workers to patients, carefully designed studies to collect information may be considered when appropriate oversight by an institutional review board has been obtained and the necessary resources are available.

Before the practice of an HIV-infected health care worker is limited prospectively, the risk of transmitting the virus to patients should be very high, given the extremely low likelihood of such transmission in normal circumstances. Before a look-back investigation is conducted, the risk should be clearly identifiable and substantially higher.

*The members of the Investigation Team are listed in the Appendix.

We are indebted to Charles Schable, M.S., David Bell, M.D., Mary Chamberland, M.D., M.P.H., and James Curran, M.D., M.P.H., of the CDC; to William Schaffner, M.D., of the Departments of Preventive Medicine and Medicine, Vanderbilt University School of Medicine; to the entire staff and the board members of the Minnesota Board of Medical Examiners; and to Jan Wiehle, Chris Heininger, Teresa Jacques, Mary Pavek, and Tina Klein for assistance in the preparation of the manuscript.

Source Information

From the Acute Disease Epidemiology Section and the AIDS/STD Prevention Services Section, Division of Disease Prevention and Control, Minnesota Department of Health (R.N.D., K.L.M., M.E.M., D.O.R., J.C.L., M.K.S., M.T.O.), and the University of Minnesota Hospital and Clinic (F.S.R., J.A.), both in Minneapolis; and Dermatology Specialist, Edina. Minn. (M.E.B.). Address reprint requests to Dr. Danila at the Acute Disease Epidemiology Section, Minnesota Department of Health, 717 SE Delaware St., P.O. Box 9441, Minneapolis, MN 55440.

Appendix

The following institutions and persons were members of the Investigation Team: Minnesota Department of Health — Bruce Brandwick, Debra Burns, M.A., John Clare, M.S., Kris Ehresmann, M.P.H., Buddy Ferguson, Jan Forfang, M.P.H., Mary Jo Fritz, Linda Gabriel, Anne Gamble, Daniel Geshrick, M.P.H., Craig Hedberg, M.S., Margaret Higgins, Robert Hiller, M.S., Teresa Hilmer, M.P.H., Jill Isensee, M.P.H., Jean Jacobs, Kim Jeppesen, M.S., Janice Johnson, M.P.H., C.I.C., Maribel Kain, M.A., Janet Keysser, M.A., M.B.A., Jack Korlath, M.P.H., Therese Lauer, Aggie Leitheiser, M.P.H., Joe Mariotti, Marlene Marschall, M.A., Claudia Miller, Kathy Miller, Chris Moore, Steve Moore, M.P.H., Anne Murrill, Fraser Nelson, Roy Nelson, M.S., R.H.Ed., Cheryl Norton, Gary Novotny, M.A., Andrea Carroll O'Brian, M.H.P., Mary Jo O'Brien, M.R.C., Jeanne Pfeiffer, M.P.H., C.I.C., Lynne Pierson, Terry Ristinen, Steve Schletty, John Soler, M.P.H., Don Stiepan, M.P.H., Sue Turner, M.S., Karen White, M.P.H., Stella Whitney-West, Carol O'Boyle Williams, M.S., C.I.C., and Elizabeth Wilson Lopp; Minnesota Attorney General's Office, St. Paul —Terrance O'Brien, J.D.; University of Minnesota, Minneapolis — Ann Alger, Jocelyn Archer, Judy Bergh, Gloria Bonnickson, Priscilla Bormann, Linda Brandt, Bev Chase, Joan Debelak, Bev Dorsey, M.P.H., Kristin Grage, Brian Goodroad, Pam Hagen, Judy Kind, Suzanne Kinn, M.S.W., Shannon Lorbiecki, M.H.A., JoAnn Lucid, M.A., Myra Maki, Holly Melroe, M.S.N., Anne Moore, M.A., Diane Olson, Marge Page, Chris Peterson, Susan Pollock, Sue Reany, Renee St. Jacques, Karen Sprangers, Chuck Sieber, and Mary Ellen Wells, M.A., M.H.A.; American Red Cross Blood Services, St. Paul Region — Robert Bowman, M.D., and William Kline, M.S.

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Citing Articles (10)

Citing Articles

  1. 1

    (2009) HIV and AIDS in the Workplace. Journal of Occupational and Environmental Medicine 51:2, 243-250
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  2. 2

    Gillian D. Sanders, Robert F. Nease, Douglas K. Owens. (2001) Publishing web-based guidelines using interactive decision models. Journal of Evaluation in Clinical Practice 7:2, 175-189
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  3. 3

    Stanley H. Weiss. (1997) RISKS AND ISSUES FOR THE HEALTH CARE WORKER IN THE HUMAN IMMUNODEFICIENCY VIRUS ERA. Medical Clinics of North America 81:2, 555-575
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  4. 4

    Esteban, Juan I., Gómez, Jordi, Martell, María, Cabot, Beatriz, Quer, Josep, Camps, Joan, González, Antonio, Otero, Teresa, Moya, Andrés, Esteban, Rafael, Guardia, Jaime, . (1996) Transmission of Hepatitis C Virus by a Cardiac Surgeon. New England Journal of Medicine 334:9, 555-561
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  5. 5

    W K Mariner. (1995) AIDS phobia, public health warnings, and lawsuits: deterring harm or rewarding ignorance?. American Journal of Public Health 85:11, 1562-1568
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  6. 6

    Margaret E. Hansen. (1994) Bloodborne pathogens: Occupational risk and infection control in radiology. Emergency Radiology 1:2, 89-92
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  7. 7

    Margaret E. Hanson, Donald D. McIntire, George L. Miller, Helen C. Redman. (1994) Use of universal precautions in interventional radiology: Results of a national survey. American Journal of Infection Control 22:1, 1-5
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  8. 8

    David M. Bell, Craig N. Shapiro, Barbara F. Gooch. (1993) Preventing HIV Transmission to Patients during Invasive Procedures. Journal of Public Health Dentistry 53:3, 170-173
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  9. 9

    Margaret E. Hansen, George L. Miller III, Helen C. Redman, Donald D. Mclntire. (1993) HIV and Interventional Radiology: A National Survey of Physician Attitudes and Behaviors. Journal of Vascular and Interventional Radiology 4:2, 229-236
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  10. 10

    (1992) Risk of HIV transmission during dental treatment. The Lancet 340:8830, 1259-1260
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