- Email: [email protected]
Back to basics in management of Clostridium difficile infections
COMMENTARY
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and density in healthy women during breastfeeding and after weaning. Osteoporosis Int 1996; 6: 153–59. Prentice A, Jarjou LM, Cole TJ, Stirling DM, Dibba B, FairweatherTait S. Calcium requirements of lactating Gambian mothers effects of a calcium supplement on breast milk calcium concentration, maternal bone mineral content, and urinary calcium excretion. Am J Clin Nutr 1995; 62: 58–67. Cross NA, Hillman LS, Allen SH, Krause GF, Vieira NE. Calcium homeostasis and bone metabolism during pregnancy, lactation, and postweaning: a longitudinal study. Am J Clin Nutr 1995; 61: 514–23. Prentice A, Jarjou LM, Stirling DM, Buffenstein R, Fairweather-Tait S. Biochemical markers of calcium and bone metabolism during 18 months of lactation in Gambian women accustomed to a low calcium intake and in those consuming a calcium supplement. J Clin Endocrinol Metab 1998; 83: 1059–66. Yamaga A, Taga M, Minaguchi H, Sato K. Changes in bone mass as determined by ultrasound and biochemical markers of bone turnover during pregnancy and puerperium: a longitudinal study. J Clin Endocrinol Metab 1996; 81: 752–56. Gulson BL, Jameson CW, Mahaffey KR, Mizon KJ, Korsh MJ, Vimpani G. Pregnancy increases mobilization of lead from maternal skeleton. J Lab Clin Med 1997; 130: 51–62. Kent GN, Price RI, Gutterigge DH, et al. The efficiency of intestinal calcium absorption is increased in late pregnancy but not established lactation. Calcified Tissue Int 1991; 48: 293–95. Kalkwarf KJ, Specker BL, Bianchi DC, Ranz J, Ho M. The effect of calcium supplementation on bone density during lactation and after weaning. N Engl J Med 1997; 337: 523–28. Lepre F, Grill V, Ho P, Martin T. Hypercalcaemia in pregnancy and lactation associated with parathyroid-hormone related protein. N Engl J Med 1993; 328: 666–67. Sowers MF, Hollis BW, Shapiro B, et al. Elevated parathroid hormone-related peptide associated with lactation and bone density loss. JAMA 1996; 276: 549–54. Liel Y, Atar D, Ohana N. Pregnancy-associated osteoporosis: preliminary densitometric evidence of extremely rapid recovery of bone mineral density. South Med J 1998; 91: 33–35. Tuppurainen M, Kroger H, Honkanen R, et al. Risks of perimenopausal fractures—a prospective population-based study. Acta Obstet Gynecol Scand 1995; 7: 624–28. Abrams SA. Bone turnover during lactation—can calcium supplementation make a difference? J Clin Endocrinol Metab 1998; 83: 1056–58.
Back to basics in management of Clostridium difficile infections Over the 20 years since Clostridium difficile was first associated with pseudomembranous colitis and antibiotic-associated diarrhoea, much has been learnt about the epidemiology and treatment of this infection. Most classes of antibiotics have now been associated with the development of C-difficile-associated disease (CDAD), although some, such as the cephalosporins and clindamycin, have been implicated to a greater extent than others1—for example, the aminoglycosides or quinolones. Contamination of the environment and persistence of the spores have been demonstrated and implicated in cross-infection.2 Large outbreaks of CDAD have occurred,3 and in some units C difficile has become endemic. In response to these problems guidelines for the prevention and management of C difficile infection have been issued, such as those of the UK Department of Health issued in 1994.4 Yet problems remain. The numbers of C difficile infections continue to rise, although this trend may in part be due to improved detection and reporting. C difficile is now the commonest cause of diarrhoea in the elderly and is associated with substantial morbidity and mortality. The financial burden to hospitals is also large and increasing.5 A particular problem is recurrence of symptoms after successful treatment of initial C difficile infections. Because these recurrences are thought to be “relapses” and therefore treatment failures, various complex treatment regimens are prescribed. These
THE LANCET • Vol 352 • August 15, 1998
regimens include combinations of metronidazole or vancomycin with rifampicin or fusidic acid, tapering or pulsed courses of vancomycin, and biotherapy with Saccharomyces boulardii or Lactobacillus sp. Recently, by random amplified polymorphic DNA typing of C difficile strains from patients with recurrence of symptoms after initial response to treatment, M H Wilcox and colleagues6 confirmed the findings of smaller studies that more than 50% of the recurrences of symptoms were due to reinfection rather than to relapse. Although this study was of C difficile infections in one hospital, which may not be wholly representative of others, the high number of reinfections demonstrated suggests that reinfection may be much commoner than previously thought. Therefore patients with recurrence of diarrhoea after successful therapy are quite likely to have acquired infection due to a new strain of C difficile, which is purely a failure of infection control, not of treatment. In clinical practice there must be a return to basics. Handwashing remains an essential infection-control measure. Isolation of symptomatic patients is advisable but lack of side-rooms commonly results in “cohorting” of patients, a practice that may lead to reinfection from other members of the cohort or from a heavily contaminated ward. Ward cleaning, with targeted, increased cleaning during outbreaks of C difficile infection, is therefore another basic essential that ideally should be intensified. Although proof is lacking, cuts in cleaning budgets may increase the burden of hospitalacquired infection. Implementation and effective policing of antibiotic policies can, in theory, reduce unnecessary antibiotic prescriptions and thus lower the selective pressure that favours C difficile, but they may be difficult to achieve.7 Changing of antibiotic policies to reduce the use of cephalosporins or clindamycin may be a more successful measure.8,9 At Southmead Hospital a change of antibiotic policy for the treatment of community-acquired pneumonia from defuroxime with or without a macrolide to a combination of benzylpenicillin plus ciprofloxacin with or without a macrolide has substantially reduced nosocomial acquisition of C difficile and the number of bed days occupied by infected patients. This reduction in incidence has been maintained for 2 years since the policy change. Treatment of symptomatic recurrences of CDAD due to reinfection need not be any different from the primary treatment of C difficile infection. However, without typing of strains, differentiation between relapse and reinfection is impossible. Perhaps more important is the improvement, during initial therapy, of the patients’ colonisation resistance to further infection with C difficile, perhaps by the prophylactic use of biotherapies. However, this approach may be controversial.
E M Jones, *A P MacGowan Depar tment of Medical Microbiology, Southmead Hospital, Bristol BS10 5NB, UK 1
2
3
4
Impallomeni M, Galletly NP, Wort SJ, Starr JM, Rogers TR. Increased risk of diarrhoea caused by Clostridium difficile in elderly patients receiving cefotaxime. BMJ 1995; 311: 1345–46. Malamou-Ladas H, O’Farrell S, Nash JQ, Tabaqchali S. Isolation of Clostridium difficile from patients and the environment of hospital wards. J Clin Pathol 1983; 36: 88–92. Cartmill TDI, Panigrahi H, Worsley MA, McCann DC, Nice CE, Keith E. Management and control of a large outbreak of diarrhoea due to Clostridium difficile. J Hosp Infect 1994; 27: 1–15. Department of Health/Public Health Laboratory Service Joint
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COMMENTARY
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Working Group. The prevention and management of Clostridium difficile infection, 1994. Wilcox MH, Cunniffe JG, Trundle C, Redpath C. Financial burden of hospital-acquired Clostridium difficile infection. J Hosp Infect 1996; 34: 23–30. Wilcox MH, Fawley WN, Settle CD, Davidson A. Recurrence of symptoms in Clostridium difficile infection—relapse or reinfection? J Hosp Infect 1998; 38: 93–100. Jones EM, Kirkpatrick BL, Feeney R, Reeves DS, MacGowan AP. Hospital-acquired Clostridium difficile diarrhoea. Lancet 1997; 349: 1176–177. McNulty C, Logan M, Donald IP, et al. Successful control of Clostridium difficile infection in an elderly care unit through use of a restrictive antibiotic policy. J Antimicrob Chemother 1997; 40: 707–11. Climo MW, Israel DS, Wong ES, Williams D, Coudron P, Markowitz SM. Hospital-wide restriction of clindamycin; effect on the incidence of Clostridium difficile. Ann Intern Med 1998; 128: 989–95.
Prospects for improvement in physicians’ communication skills and in prevention of HIV infection Although certain features of HIV and its life-cycle have worked to its advantage in chillingly effective ways, behavioural factors have also helped greatly to promote the global extension of the pandemic of HIV infection. Public-health measures to stem the transmission of this infection by influencing behaviour are challenging because the transmission is effected largely by individual private acts that have important social consequences. A complicating factor is that some of these behaviours may be illegal (eg, injecting drug use) or socially unacceptable in some cultural contexts (eg, homosexuality). Some of the behaviours are also socially valued (eg, childbearing). Moreover, HIV-prevention efforts have been limited by social acceptability (eg, condom use and contraception). Despite these difficulties, a good physician-patient relationship in routine clinical care should should contribute substantially to risk reduction and hence the prevention of this infection. In the USA most individuals visit a physician at least twice a year. Although many physicians may think that they counsel their patients about HIV risk effectively,1 it has been shown that even the most experienced clinicians sometimes exhibit discomfort or difficulty when discussing sexuality and substance-use behaviours with their patients.1,2 A national survey of physicians in the USA1 found that fewer than 1% of visits to primary-care physicians involved counselling or advice about HIV transmission.1 Another study2 found, in a convenience sample of physicians in outpatient practice in Rochester, New York, that physicians did not elicit adequate information for determination of patients’ risk status in nearly three-quarters of all encounters, which were videotaped and reviewed by both physicians and patients. Much of the difficulty physicians experienced in this context was attributed to their own emotional discomfort with these issues, or to financial disincentives against indepth counselling of patients during routine clinic visits. The same study found, as have other studies,1 that patients expressed an interest in discussing HIV with their physicians, and expected that their physicians would broach the topic with them. Another study,3 this time from the UK and of senior oncologists, has found that the oncologists expressed discomfort or a perceived lack of expertise in communicating with patients and families about difficult clinical issues in the context of life-threatening illness. The oncologists then underwent a brief communications506
skills training course consisting of a combination of didactic teaching, structured feedback, videotape review of interviews with standardised patients, and small-group discussion. Immediately after the course, confidence ratings for key communication areas improved significantly. Importantly, these changes were sustained in 95% of physicians at 3 months of follow-up. These encouraging findings suggest that a focused measure to improve communications skills for clinicians might be expected to have an important potential impact on discussions between doctor and patient on HIV-risk behaviour. Other reports also suggest that problem-based teaching methods can help address difficult attitudinal and communication issues more appropriately than can traditional didactic methods alone.1 The findings of another recent study4 also support the need for improving physicians’ communication skills: a survey of HIV-infected patients in outpatient HIV clinics in Boston, Massachusetts, and Providence, Rhode Island, found that 40% of patients had not informed their primary sexual partners of their HIV infection, and slightly more than half of these had used condoms less than half the time.4 This finding was consistent with those of other studies, in which, despite making some effort to modify behaviour, a significant minority of HIV-infected patients continued to engage in unsafe sexual or drug-use behaviours.5-7 Thus, it is fair to surmise that many physicians interacting daily with patients who are at potentially high risk of HIV transmission or reacquisition are not taking the opportunity to promote behaviour change, whether for primary prevention or for the prevention of further transmission from those already infected. On a global scale, it will not be changes in physician consultations that will contribute in a significant way to the slowing and eventual retreat of the HIV epidemic, but rather an effective vaccine against HIV, improvements in the social and economic status of women in developing countries, prevention and treatment of drug addiction, and more systematic treatment and prevention of sexually transmitted diseases in high-risk populations. However, caregivers should not avoid or overlook opportunities to help patients protect themselves against disease, especially when some of the communication barriers are due to their own emotional discomfort or lack of expertise in discussing sensitive issues. Peter A Selwyn AIDS Program, Yale School of Medicine, New Haven, CT 06510, USA 1
2
3
4 5
6
7
Makadon HJ, Silin JG. Prevention of HIV infection in primary care: current practices, future possibilities. Ann Intern Med 1998; 123: 715–19. Epstein RM, Morse DS, Frankel RM, Frarey L, Anderson K, Beckham HB. Awkward moments in patient-physician communication about HIV risk. Ann Intern Med 1998; 128: 435–42. Fallowfield L, Lipkin M, Hall A. Teaching senior oncologists communication skills: results from phase I of a comprehensive longitudinal program in the United Kingdom. J Clin Oncol 1998; 16: 1961–68. Stein MD, Freedberg KA, Sullivan LM, et al. Sexual ethics: disclosure of HIV-positive status to partners. Arch Intern Med 1998; 158: 253–57. Lemp GF, Hirozawa AM, Givertz D, et al. Seroprevalence of HIV and risk behaviours among young homosexual and bisexual men. JAMA 1994: 272: 449–54. McKusker J, Bigelow C, Frost R, Hindin R, Vickers-Lahti M, Zorn M. The relationship of HIV status and HIV risky behavior with readiness for treatment. Drug Alcohol Depend 1994; 34: 129–38. Metsch LR, McCoy CB, Lai S, Miles C. Continuing risk behaviors among HIV seropositive chronic drug users in Miami, Florida. AIDS Behavior 1998; 2: 161–69.
THE LANCET • Vol 352 • August 15, 1998
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and density in healthy women during breastfeeding and after weaning. Osteoporosis Int 1996; 6: 153–59. Prentice A, Jarjou LM, Cole TJ, Stirling DM, Dibba B, FairweatherTait S. Calcium requirements of lactating Gambian mothers effects of a calcium supplement on breast milk calcium concentration, maternal bone mineral content, and urinary calcium excretion. Am J Clin Nutr 1995; 62: 58–67. Cross NA, Hillman LS, Allen SH, Krause GF, Vieira NE. Calcium homeostasis and bone metabolism during pregnancy, lactation, and postweaning: a longitudinal study. Am J Clin Nutr 1995; 61: 514–23. Prentice A, Jarjou LM, Stirling DM, Buffenstein R, Fairweather-Tait S. Biochemical markers of calcium and bone metabolism during 18 months of lactation in Gambian women accustomed to a low calcium intake and in those consuming a calcium supplement. J Clin Endocrinol Metab 1998; 83: 1059–66. Yamaga A, Taga M, Minaguchi H, Sato K. Changes in bone mass as determined by ultrasound and biochemical markers of bone turnover during pregnancy and puerperium: a longitudinal study. J Clin Endocrinol Metab 1996; 81: 752–56. Gulson BL, Jameson CW, Mahaffey KR, Mizon KJ, Korsh MJ, Vimpani G. Pregnancy increases mobilization of lead from maternal skeleton. J Lab Clin Med 1997; 130: 51–62. Kent GN, Price RI, Gutterigge DH, et al. The efficiency of intestinal calcium absorption is increased in late pregnancy but not established lactation. Calcified Tissue Int 1991; 48: 293–95. Kalkwarf KJ, Specker BL, Bianchi DC, Ranz J, Ho M. The effect of calcium supplementation on bone density during lactation and after weaning. N Engl J Med 1997; 337: 523–28. Lepre F, Grill V, Ho P, Martin T. Hypercalcaemia in pregnancy and lactation associated with parathyroid-hormone related protein. N Engl J Med 1993; 328: 666–67. Sowers MF, Hollis BW, Shapiro B, et al. Elevated parathroid hormone-related peptide associated with lactation and bone density loss. JAMA 1996; 276: 549–54. Liel Y, Atar D, Ohana N. Pregnancy-associated osteoporosis: preliminary densitometric evidence of extremely rapid recovery of bone mineral density. South Med J 1998; 91: 33–35. Tuppurainen M, Kroger H, Honkanen R, et al. Risks of perimenopausal fractures—a prospective population-based study. Acta Obstet Gynecol Scand 1995; 7: 624–28. Abrams SA. Bone turnover during lactation—can calcium supplementation make a difference? J Clin Endocrinol Metab 1998; 83: 1056–58.
Back to basics in management of Clostridium difficile infections Over the 20 years since Clostridium difficile was first associated with pseudomembranous colitis and antibiotic-associated diarrhoea, much has been learnt about the epidemiology and treatment of this infection. Most classes of antibiotics have now been associated with the development of C-difficile-associated disease (CDAD), although some, such as the cephalosporins and clindamycin, have been implicated to a greater extent than others1—for example, the aminoglycosides or quinolones. Contamination of the environment and persistence of the spores have been demonstrated and implicated in cross-infection.2 Large outbreaks of CDAD have occurred,3 and in some units C difficile has become endemic. In response to these problems guidelines for the prevention and management of C difficile infection have been issued, such as those of the UK Department of Health issued in 1994.4 Yet problems remain. The numbers of C difficile infections continue to rise, although this trend may in part be due to improved detection and reporting. C difficile is now the commonest cause of diarrhoea in the elderly and is associated with substantial morbidity and mortality. The financial burden to hospitals is also large and increasing.5 A particular problem is recurrence of symptoms after successful treatment of initial C difficile infections. Because these recurrences are thought to be “relapses” and therefore treatment failures, various complex treatment regimens are prescribed. These
THE LANCET • Vol 352 • August 15, 1998
regimens include combinations of metronidazole or vancomycin with rifampicin or fusidic acid, tapering or pulsed courses of vancomycin, and biotherapy with Saccharomyces boulardii or Lactobacillus sp. Recently, by random amplified polymorphic DNA typing of C difficile strains from patients with recurrence of symptoms after initial response to treatment, M H Wilcox and colleagues6 confirmed the findings of smaller studies that more than 50% of the recurrences of symptoms were due to reinfection rather than to relapse. Although this study was of C difficile infections in one hospital, which may not be wholly representative of others, the high number of reinfections demonstrated suggests that reinfection may be much commoner than previously thought. Therefore patients with recurrence of diarrhoea after successful therapy are quite likely to have acquired infection due to a new strain of C difficile, which is purely a failure of infection control, not of treatment. In clinical practice there must be a return to basics. Handwashing remains an essential infection-control measure. Isolation of symptomatic patients is advisable but lack of side-rooms commonly results in “cohorting” of patients, a practice that may lead to reinfection from other members of the cohort or from a heavily contaminated ward. Ward cleaning, with targeted, increased cleaning during outbreaks of C difficile infection, is therefore another basic essential that ideally should be intensified. Although proof is lacking, cuts in cleaning budgets may increase the burden of hospitalacquired infection. Implementation and effective policing of antibiotic policies can, in theory, reduce unnecessary antibiotic prescriptions and thus lower the selective pressure that favours C difficile, but they may be difficult to achieve.7 Changing of antibiotic policies to reduce the use of cephalosporins or clindamycin may be a more successful measure.8,9 At Southmead Hospital a change of antibiotic policy for the treatment of community-acquired pneumonia from defuroxime with or without a macrolide to a combination of benzylpenicillin plus ciprofloxacin with or without a macrolide has substantially reduced nosocomial acquisition of C difficile and the number of bed days occupied by infected patients. This reduction in incidence has been maintained for 2 years since the policy change. Treatment of symptomatic recurrences of CDAD due to reinfection need not be any different from the primary treatment of C difficile infection. However, without typing of strains, differentiation between relapse and reinfection is impossible. Perhaps more important is the improvement, during initial therapy, of the patients’ colonisation resistance to further infection with C difficile, perhaps by the prophylactic use of biotherapies. However, this approach may be controversial.
E M Jones, *A P MacGowan Depar tment of Medical Microbiology, Southmead Hospital, Bristol BS10 5NB, UK 1
2
3
4
Impallomeni M, Galletly NP, Wort SJ, Starr JM, Rogers TR. Increased risk of diarrhoea caused by Clostridium difficile in elderly patients receiving cefotaxime. BMJ 1995; 311: 1345–46. Malamou-Ladas H, O’Farrell S, Nash JQ, Tabaqchali S. Isolation of Clostridium difficile from patients and the environment of hospital wards. J Clin Pathol 1983; 36: 88–92. Cartmill TDI, Panigrahi H, Worsley MA, McCann DC, Nice CE, Keith E. Management and control of a large outbreak of diarrhoea due to Clostridium difficile. J Hosp Infect 1994; 27: 1–15. Department of Health/Public Health Laboratory Service Joint
505
COMMENTARY
5
6
7
8
9
Working Group. The prevention and management of Clostridium difficile infection, 1994. Wilcox MH, Cunniffe JG, Trundle C, Redpath C. Financial burden of hospital-acquired Clostridium difficile infection. J Hosp Infect 1996; 34: 23–30. Wilcox MH, Fawley WN, Settle CD, Davidson A. Recurrence of symptoms in Clostridium difficile infection—relapse or reinfection? J Hosp Infect 1998; 38: 93–100. Jones EM, Kirkpatrick BL, Feeney R, Reeves DS, MacGowan AP. Hospital-acquired Clostridium difficile diarrhoea. Lancet 1997; 349: 1176–177. McNulty C, Logan M, Donald IP, et al. Successful control of Clostridium difficile infection in an elderly care unit through use of a restrictive antibiotic policy. J Antimicrob Chemother 1997; 40: 707–11. Climo MW, Israel DS, Wong ES, Williams D, Coudron P, Markowitz SM. Hospital-wide restriction of clindamycin; effect on the incidence of Clostridium difficile. Ann Intern Med 1998; 128: 989–95.
Prospects for improvement in physicians’ communication skills and in prevention of HIV infection Although certain features of HIV and its life-cycle have worked to its advantage in chillingly effective ways, behavioural factors have also helped greatly to promote the global extension of the pandemic of HIV infection. Public-health measures to stem the transmission of this infection by influencing behaviour are challenging because the transmission is effected largely by individual private acts that have important social consequences. A complicating factor is that some of these behaviours may be illegal (eg, injecting drug use) or socially unacceptable in some cultural contexts (eg, homosexuality). Some of the behaviours are also socially valued (eg, childbearing). Moreover, HIV-prevention efforts have been limited by social acceptability (eg, condom use and contraception). Despite these difficulties, a good physician-patient relationship in routine clinical care should should contribute substantially to risk reduction and hence the prevention of this infection. In the USA most individuals visit a physician at least twice a year. Although many physicians may think that they counsel their patients about HIV risk effectively,1 it has been shown that even the most experienced clinicians sometimes exhibit discomfort or difficulty when discussing sexuality and substance-use behaviours with their patients.1,2 A national survey of physicians in the USA1 found that fewer than 1% of visits to primary-care physicians involved counselling or advice about HIV transmission.1 Another study2 found, in a convenience sample of physicians in outpatient practice in Rochester, New York, that physicians did not elicit adequate information for determination of patients’ risk status in nearly three-quarters of all encounters, which were videotaped and reviewed by both physicians and patients. Much of the difficulty physicians experienced in this context was attributed to their own emotional discomfort with these issues, or to financial disincentives against indepth counselling of patients during routine clinic visits. The same study found, as have other studies,1 that patients expressed an interest in discussing HIV with their physicians, and expected that their physicians would broach the topic with them. Another study,3 this time from the UK and of senior oncologists, has found that the oncologists expressed discomfort or a perceived lack of expertise in communicating with patients and families about difficult clinical issues in the context of life-threatening illness. The oncologists then underwent a brief communications506
skills training course consisting of a combination of didactic teaching, structured feedback, videotape review of interviews with standardised patients, and small-group discussion. Immediately after the course, confidence ratings for key communication areas improved significantly. Importantly, these changes were sustained in 95% of physicians at 3 months of follow-up. These encouraging findings suggest that a focused measure to improve communications skills for clinicians might be expected to have an important potential impact on discussions between doctor and patient on HIV-risk behaviour. Other reports also suggest that problem-based teaching methods can help address difficult attitudinal and communication issues more appropriately than can traditional didactic methods alone.1 The findings of another recent study4 also support the need for improving physicians’ communication skills: a survey of HIV-infected patients in outpatient HIV clinics in Boston, Massachusetts, and Providence, Rhode Island, found that 40% of patients had not informed their primary sexual partners of their HIV infection, and slightly more than half of these had used condoms less than half the time.4 This finding was consistent with those of other studies, in which, despite making some effort to modify behaviour, a significant minority of HIV-infected patients continued to engage in unsafe sexual or drug-use behaviours.5-7 Thus, it is fair to surmise that many physicians interacting daily with patients who are at potentially high risk of HIV transmission or reacquisition are not taking the opportunity to promote behaviour change, whether for primary prevention or for the prevention of further transmission from those already infected. On a global scale, it will not be changes in physician consultations that will contribute in a significant way to the slowing and eventual retreat of the HIV epidemic, but rather an effective vaccine against HIV, improvements in the social and economic status of women in developing countries, prevention and treatment of drug addiction, and more systematic treatment and prevention of sexually transmitted diseases in high-risk populations. However, caregivers should not avoid or overlook opportunities to help patients protect themselves against disease, especially when some of the communication barriers are due to their own emotional discomfort or lack of expertise in discussing sensitive issues. Peter A Selwyn AIDS Program, Yale School of Medicine, New Haven, CT 06510, USA 1
2
3
4 5
6
7
Makadon HJ, Silin JG. Prevention of HIV infection in primary care: current practices, future possibilities. Ann Intern Med 1998; 123: 715–19. Epstein RM, Morse DS, Frankel RM, Frarey L, Anderson K, Beckham HB. Awkward moments in patient-physician communication about HIV risk. Ann Intern Med 1998; 128: 435–42. Fallowfield L, Lipkin M, Hall A. Teaching senior oncologists communication skills: results from phase I of a comprehensive longitudinal program in the United Kingdom. J Clin Oncol 1998; 16: 1961–68. Stein MD, Freedberg KA, Sullivan LM, et al. Sexual ethics: disclosure of HIV-positive status to partners. Arch Intern Med 1998; 158: 253–57. Lemp GF, Hirozawa AM, Givertz D, et al. Seroprevalence of HIV and risk behaviours among young homosexual and bisexual men. JAMA 1994: 272: 449–54. McKusker J, Bigelow C, Frost R, Hindin R, Vickers-Lahti M, Zorn M. The relationship of HIV status and HIV risky behavior with readiness for treatment. Drug Alcohol Depend 1994; 34: 129–38. Metsch LR, McCoy CB, Lai S, Miles C. Continuing risk behaviors among HIV seropositive chronic drug users in Miami, Florida. AIDS Behavior 1998; 2: 161–69.
THE LANCET • Vol 352 • August 15, 1998