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Microbiological services for a transplantation service
Clinical Microbiology Newsletter October 15, 1995
Vol. 17, No. 20
Microbiological Services for a Transplantation Service Edward. R. Bannister, Ph.D. Dallas County Health Department Dallas, TX 75207-2710
The microbiological services necessary to support a successful transplant service have changed drastically over the last 10 to 15 yr. Infections in these patients have increased sufficiently so that they are one of the most important problems occurring after transplant surgery in addition to the medical and surgical problems related to organ rejection. The number and types of transplants taking place has increased to the extent that the microbiology laboratory has found it necessary to increase services and improve turnaround time. In addition to the major medical centers where transplantation procedures are performed, the community hospital or extended-care facilities and their physicians may be called upon to help manage the care of these patients after they return home. The most common types of transplants being performed today are kidney, liver, heart, lung, heart-lung, and bone marrow. Of these, lung and heart-
Table 1. Factors contributing to clinical infection after transplantation a Type of organ tTansplanted Underlying medical condition at time of transplant Level of immunosuppression Tune after transplant Age of patient Rejection of graft aFrom ref, 5.
CMNEEJ 17(20)153-160,1995
lung have been the slowest to develop. Pancreas and small bowel procedures are still in the early stages of development but most certainly will develop rapidly. As with any major surgery, risk factors are associated with this procedure. Table 1 summarizes some of the risk factors associated with infections in transplant patients.
Etiology of T r a n s p l a n t Infections In general, the largest number of infections occur during the first 4 mo after transplant, and the majority of these occur in the first 3 too. The infecting microorganism can either be exogenous or endogenous (1). Given the diversity of sources of microorganisms that may cause infections in transplant patients, the types of infections are also diverse and the type of transplant a patient has undergone predisposes them to certain infections, as shown in Table 2. It also appears that the type of immunosuppressive agent used plays a role in the microorganism involved in the patient's infection (2). Many microorganisms can be involved in a patient's infection even though the major sites of infection appear to be limited. Table 3 lists a few of these organisms by category. This table is by no means a complete listing of the etiologic agents that have been implicated in these infections, and it is apparent that the microbiology laboratory must or should be competent in many areas if it is to support an active transplant service regardless of the type of transplant involved. To be sure, as surgical techniques are improved and new information is gained about controlling Elsevier
rejection, more institutions will consider offering transplant services for organs not considered even a few years ago. It is also important to note that patients with some types of transplants are more susceptible to certain infectious agents than others, as summarized in Table 4. Viral infections are a unique problem for all transplant patients and 40 to 50% of them develop some form of symptomatic viral infection. Only a few viruses are responsible; the most important ones are in the herpes virus group, which includes cytomegalovirus (CMV), herpes simplex virus (HSV) types 1, and 2, varicella-zoster virus (VZV), and Epstein-Barr virus (EBV)
In This Issue Microbiological Services for a Transplantation Service . . . . . . . . .
153
Should the laboratory offer anything different or unique to support an organ transplant program?
Nosocomially Acquired Bacteremia Caused by Serratia plymuthica . . . . . . . . . . . . . . . . . . . . . . .
156
A case report
Fatal Nocardia asteroides Bacteremia in a Cirrhotic and Human Immunodeficiency Virus-Infected Patient . . . . . . . . . . . . . . . . . . 157 A case report
Helicobacter cinaedi Bacteremia
in an Asymptomati¢ Patient with Human Immunodeficiency Virus Infection . . . . . . . . . . . . . . . . . . . . . . 159 A case report 0196- 4399/95/$0.00 + 09.50
Table 2. Type of transplant and most common infection site a Type Site Kidney Urinary tract Heart Pulmonary, intrathoracic Liver Abdominal, gastrointestinal Heart-lung Pulmonary Bone-marrow Blood, soft tissue Pancreas Wound Small bowel Blood aFrom refs. 6-11.
(3). Adenoviruses are a particular problem for bone-marrow transplant patients and in one study (4), 4.9% of patients were positive for adenovirus by culture. Parasitic infections have mostly been eliminated in bone marrow transplant patients because of the prophylactic measures that must be taken (4). Specimens for C u l t u r e The type of transplant and the site of infection dictates the required specimen necessary to isolate and identify the infectious agent. For bacterial infections, the primary site of infection in a symptomatic patient will determine what specimen to collect. For example, in kidney transplant patients, urinary tract infections are the most common; thus, collection of urine sample in asymptomatic patent would be most useful. In other transplants and in kidney too, development of bacteremia is a common occurrence and can indicate a serious bacterial infections located at another site ( lung, abdomen, gastrointestinal, etc). It is also recognized that cultures for certain viruses may be helpful in managing these patients. Routine cultures are probably not necessary but periodic cultures of throat, mine, and buffy coat for cytomegalo- and herpes simplex viruses may be useful in managing patients who have undergone heart, heart and lung, liver, or bone-marrow transplants. Kidney transplant patients rarely develop viral infections, and thus cultures are probably not necessary in this
group. It may be very useful prior to the transplant to obtain a serum sample that can be tested after the procedure if problems develop. In this instance studies for herpes, human immunodeficiency, and hepatitis B virus and Legioneila and Toxoplasma IgG antibody will be very useful. In some instances it may be important to check for CMV and HSV every 2 to 4 wk for up to 3 mo after transplantation. On occasion ifa patient develops fever, it could be helpful to know if virus is being shed at that time (1). A tuberculin skin test performed prior to transplant would also be beneficial (1). Table 5 presents data collected from the Pittsburgh experience during the first year after transplantation. It illustrates the number and percentage of patients with bacterial, CMV, and fungal infections by anatomic site. The number of infections was high in most all transplants except renal and none of these died from their infection. It does appear that when infection develops in transplant patients, no one group of microorganisms can be excluded and careful attention must be paid to the clinical signs and symptoms to easily identify the infectious agent. P r o c e d u r e s to Offer It is apparent from the above discussion of infections in transplant patients that the microbiology laboratory is a very important adjunct to the transplant team. Before a transplant service is started in any hospital, the microbiol-
ogy laboratory should be consulted conceming what tests to offer, what new tests they may able to offer, and how rapidly some of the results can be obtained. The type of transplant that is going to be performed will dictate to a certain degree the type of laboratory services needed by the transplant team. It appears that the laboratory would have to offer expert services in bacteriology, virology, mycology, and parasitology, the four major subgroups of a clinical microbiology laboratory. Other than some special virology laboratory services as mentioned above, the standard microbiology services should be available. Consideration could be given to offering predetermined batteries of tests dependent on the needs of the transplant service or providing special transplant microbiology services in a Table 3. Common microorganisms found in infections in transplant patients a
Bacteria gram-negative enterics Pseudornonas spp. Legionella spp. Anaerobes Staphylococcus spp. Streptococcus spp. Haernophilus influenzae Listeria monocytogenes Mycoplasma hominis Fungi Candida spp. Aspergillus spp. Cryptococcus spp. Viruses
Herpes simplex, types 1 and 2 Cytomegalovirus Varicella-zoster virus Epstein-Barr virus Parasites Pneumocystis carinii Toxoplasma gondii aFrom ref. 1.
NOTE: No responsibility is assumed by the Publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. No suggested test or procedure should be carried out unless, in the reader's judgment, its risk is justified. Because of rapid advances in medical sciences, we recommend that the independent verification of diagnoses and drag dosages should be made. Discussions, views, and recommendations as to medical procedures, choice of drugs, and drag dosages are the responsibility of the authors.
Clinical Microbiology Newslctt¢r (ISSN 1069-417X) is issued twice monthly in one indexed volume per year by Elsevier Science Inc., 655 Avenue of the Americas, New York, NY 113010. Subscription price per year: $175.00 including postage and handling in the United States, Canada, and Mexico. Add $59.00 for postage in the rest of the wodd. Second-class postage paid at New York, NY and at additional mailing offices. Postmaster. Send address changes to Clinical Microbiology Newsletter, Elsevier Science Inc., 655 Avenue of the Americas, New York, NY 10010.
154
0196-4399/95/$0.00 + 09.50
© 1995 Elsevier Science Inc.
Clinical Microbiology Newsletter 17:19,1995
Table 4. Type of transplant and most common infectious agents a Transplantedorgan Infectious agent Kidney Heart, lung, heart-lung Liver Pancreas Bone marrow aFrom refs. 11-16
Grana-negative enterics Gram-negative enterics, staphylococci, Legionella Bacterial, fungal B acteriai Bacterial, fungal
Table 5. Number and percentage of types of infection during the first year after transplanta
Transplant
N
Patients with bacteremia (%)
Patients with symptomatic CMV (%)
Kidney Heart Heart-lung Liver
64 119 31 101
5 13 19 23
8 16 39 22
dedicated area of the laboratory. This approach would minimize costs and also limit the repeated handling of specimens if numerous tests are requested. Facilities for serologic should also be available. This service may or not be a part of the microbiology laboratory but is of vital importance if the transplant service is to be successful. Knowledge o f nosocomial infections rates of specific organisms and their antibiotic susceptibility patterns is also important. The infection control department in the hospital can be of great service when it comes to determining the primary nosocomial pathogens and considering what tests to offer for their detection. Rapid turnaround times of results are also critical for a successful transplantation program. Microscopic procedures with Gram, acid-fast, and immunofluoreseence staining can all be used to provide rapid, same-day, direct detection for many infectious agents. Another concern is the community hospital where certain patients go if an infection occurs after they return home. These institutions should be able to provide minimal bacteriologic, fungal, and serologic testing services. Alternatively, specimens should be referred to a larger laboratory with an expected rapid turnaround time on results.
Conclusion In summary, the microbiology laboClinical Microbiology Newsletter 17:19,1995
Patients with invasive fungal infections (%) 0 8 23 16
ratory must become an integral part of any transplant service. Communication must begin before the transplant begins and continue during the entire time that the service is offered at that institution. Changes in test methods, levels of service, and turnaround times are all important aspects of an evolving transplant service and the laboratory must be willing to work with the transplant team if it is to be successful. Just as important is that the transplant team seek the counsel of the microbiology staff before on setting up new programs. References 1. Ho, M., and J.S. Dummer. 1995. Infections in transplant recipients, p. 27092717. In G.L. Mandel, J.E. Bennett, and R. Dolin (eds), Principles and practices of infectious diseases, vol. 2. Churchill Livingston, New York. 2. Starzl, T.E., et al. 1983. The ColoradoPittsburgh cadaveric renal transplantation study on cyclosporine. Transpl. Proc. 15:2459-2468. 3. Ho, M. 1977. Virus infections after transplantation in man. Arch. Virol. 36:259--267. 4. Shields, A.F., et al. 1985. Adenovirus infection in patients undergoing bone marrow transplantations. N. Engl. J. Med. 312:529-533. 5. Ho, M. 1987. Infection and organ transplantation, p. 49-60. In Gelman, S (ed.), Anesthesia and organ transplantation. W.B. Saunders, Philadelphia.
© 1995 Elsevier Science Inc.
6.
Ho, M., et al. 1983. Infections in kidney, heart, and liver transplant recipients on cyclosporine. Transplant. Proc. 125:2768-2772.
7.
Dummer, J.S. 1988. Infectious complications of transplantation, p. 163-179. In Brest, A.N. (ed), Cardiovascular clinics.
8.
Kusne, S., et al. 1988. Infections after liver transplantation. An analysis of 101 consecutive cases. Medicine 67:132-143.
9.
Villablanca, J.G., et al. 1990. The clinical spectrum of infections with viridans streptococci in bone marrow transplant patients. Bone Marrow Transplant 6:387-393.
10. Ozaki, C.F., et al. 1992. Surgical complications in solitary and combined pancreas-kidney transplantation. Am. J. Surg. 164:546-551. 11. Todo, S., et al. 1992. Cadaveric small bowel and small bowel-liver transplantation in humans. Transplantation 53:369-376. 12. Myerowitz, R.L., A.A. Medeiros, and T.F. O'Brien. 1972. Bacterial infection in renal homotransplant recipients: a study of fifty-three bacteremic episodes. Am J. Med. 53:308-314. 13. Brooks, R.G., et al. 1985. Infectious complications in heart-lung transplant recipients Am. J. Med. 79: 412--422. 14. Paya, C.V., et al. 1989. Incidence, distribution and outcome of episodes of infections in 100 orthotopic liver transplantations. Mayo Clin. Proc. 64:555-564. 15. George, D.L., et al. 1991. Bacterial infections as a complication of liver transplantation: epidemiology and risk factors. Rev. Infect. Dis.13:387-396. 16. Hesse, U.J., et al 1985. Intra-abdominal infections in pancreas transplant recipients. Ann. Surg. 203:153-162. 17. Dummcr, J.S. 1990. Infectious complications of heart-lung transplantation. In DK.C. Cooper and D. Novitsky (eds), The transplantation and replacement of thoracic organs. Kluwer Academic Publishers, Lancastcr, U.K. 18. Singh, N., et al. 1988. Infections with cytomegalovirus and other herpes viruses in 121 liver transplant recipients: transmission by donated organ and the effect of OKT3 antibodies. J. Infect. Dis 158:124-131.
0196-4399/95/$0.fl0 + 09.50
155
Vol. 17, No. 20
Microbiological Services for a Transplantation Service Edward. R. Bannister, Ph.D. Dallas County Health Department Dallas, TX 75207-2710
The microbiological services necessary to support a successful transplant service have changed drastically over the last 10 to 15 yr. Infections in these patients have increased sufficiently so that they are one of the most important problems occurring after transplant surgery in addition to the medical and surgical problems related to organ rejection. The number and types of transplants taking place has increased to the extent that the microbiology laboratory has found it necessary to increase services and improve turnaround time. In addition to the major medical centers where transplantation procedures are performed, the community hospital or extended-care facilities and their physicians may be called upon to help manage the care of these patients after they return home. The most common types of transplants being performed today are kidney, liver, heart, lung, heart-lung, and bone marrow. Of these, lung and heart-
Table 1. Factors contributing to clinical infection after transplantation a Type of organ tTansplanted Underlying medical condition at time of transplant Level of immunosuppression Tune after transplant Age of patient Rejection of graft aFrom ref, 5.
CMNEEJ 17(20)153-160,1995
lung have been the slowest to develop. Pancreas and small bowel procedures are still in the early stages of development but most certainly will develop rapidly. As with any major surgery, risk factors are associated with this procedure. Table 1 summarizes some of the risk factors associated with infections in transplant patients.
Etiology of T r a n s p l a n t Infections In general, the largest number of infections occur during the first 4 mo after transplant, and the majority of these occur in the first 3 too. The infecting microorganism can either be exogenous or endogenous (1). Given the diversity of sources of microorganisms that may cause infections in transplant patients, the types of infections are also diverse and the type of transplant a patient has undergone predisposes them to certain infections, as shown in Table 2. It also appears that the type of immunosuppressive agent used plays a role in the microorganism involved in the patient's infection (2). Many microorganisms can be involved in a patient's infection even though the major sites of infection appear to be limited. Table 3 lists a few of these organisms by category. This table is by no means a complete listing of the etiologic agents that have been implicated in these infections, and it is apparent that the microbiology laboratory must or should be competent in many areas if it is to support an active transplant service regardless of the type of transplant involved. To be sure, as surgical techniques are improved and new information is gained about controlling Elsevier
rejection, more institutions will consider offering transplant services for organs not considered even a few years ago. It is also important to note that patients with some types of transplants are more susceptible to certain infectious agents than others, as summarized in Table 4. Viral infections are a unique problem for all transplant patients and 40 to 50% of them develop some form of symptomatic viral infection. Only a few viruses are responsible; the most important ones are in the herpes virus group, which includes cytomegalovirus (CMV), herpes simplex virus (HSV) types 1, and 2, varicella-zoster virus (VZV), and Epstein-Barr virus (EBV)
In This Issue Microbiological Services for a Transplantation Service . . . . . . . . .
153
Should the laboratory offer anything different or unique to support an organ transplant program?
Nosocomially Acquired Bacteremia Caused by Serratia plymuthica . . . . . . . . . . . . . . . . . . . . . . .
156
A case report
Fatal Nocardia asteroides Bacteremia in a Cirrhotic and Human Immunodeficiency Virus-Infected Patient . . . . . . . . . . . . . . . . . . 157 A case report
Helicobacter cinaedi Bacteremia
in an Asymptomati¢ Patient with Human Immunodeficiency Virus Infection . . . . . . . . . . . . . . . . . . . . . . 159 A case report 0196- 4399/95/$0.00 + 09.50
Table 2. Type of transplant and most common infection site a Type Site Kidney Urinary tract Heart Pulmonary, intrathoracic Liver Abdominal, gastrointestinal Heart-lung Pulmonary Bone-marrow Blood, soft tissue Pancreas Wound Small bowel Blood aFrom refs. 6-11.
(3). Adenoviruses are a particular problem for bone-marrow transplant patients and in one study (4), 4.9% of patients were positive for adenovirus by culture. Parasitic infections have mostly been eliminated in bone marrow transplant patients because of the prophylactic measures that must be taken (4). Specimens for C u l t u r e The type of transplant and the site of infection dictates the required specimen necessary to isolate and identify the infectious agent. For bacterial infections, the primary site of infection in a symptomatic patient will determine what specimen to collect. For example, in kidney transplant patients, urinary tract infections are the most common; thus, collection of urine sample in asymptomatic patent would be most useful. In other transplants and in kidney too, development of bacteremia is a common occurrence and can indicate a serious bacterial infections located at another site ( lung, abdomen, gastrointestinal, etc). It is also recognized that cultures for certain viruses may be helpful in managing these patients. Routine cultures are probably not necessary but periodic cultures of throat, mine, and buffy coat for cytomegalo- and herpes simplex viruses may be useful in managing patients who have undergone heart, heart and lung, liver, or bone-marrow transplants. Kidney transplant patients rarely develop viral infections, and thus cultures are probably not necessary in this
group. It may be very useful prior to the transplant to obtain a serum sample that can be tested after the procedure if problems develop. In this instance studies for herpes, human immunodeficiency, and hepatitis B virus and Legioneila and Toxoplasma IgG antibody will be very useful. In some instances it may be important to check for CMV and HSV every 2 to 4 wk for up to 3 mo after transplantation. On occasion ifa patient develops fever, it could be helpful to know if virus is being shed at that time (1). A tuberculin skin test performed prior to transplant would also be beneficial (1). Table 5 presents data collected from the Pittsburgh experience during the first year after transplantation. It illustrates the number and percentage of patients with bacterial, CMV, and fungal infections by anatomic site. The number of infections was high in most all transplants except renal and none of these died from their infection. It does appear that when infection develops in transplant patients, no one group of microorganisms can be excluded and careful attention must be paid to the clinical signs and symptoms to easily identify the infectious agent. P r o c e d u r e s to Offer It is apparent from the above discussion of infections in transplant patients that the microbiology laboratory is a very important adjunct to the transplant team. Before a transplant service is started in any hospital, the microbiol-
ogy laboratory should be consulted conceming what tests to offer, what new tests they may able to offer, and how rapidly some of the results can be obtained. The type of transplant that is going to be performed will dictate to a certain degree the type of laboratory services needed by the transplant team. It appears that the laboratory would have to offer expert services in bacteriology, virology, mycology, and parasitology, the four major subgroups of a clinical microbiology laboratory. Other than some special virology laboratory services as mentioned above, the standard microbiology services should be available. Consideration could be given to offering predetermined batteries of tests dependent on the needs of the transplant service or providing special transplant microbiology services in a Table 3. Common microorganisms found in infections in transplant patients a
Bacteria gram-negative enterics Pseudornonas spp. Legionella spp. Anaerobes Staphylococcus spp. Streptococcus spp. Haernophilus influenzae Listeria monocytogenes Mycoplasma hominis Fungi Candida spp. Aspergillus spp. Cryptococcus spp. Viruses
Herpes simplex, types 1 and 2 Cytomegalovirus Varicella-zoster virus Epstein-Barr virus Parasites Pneumocystis carinii Toxoplasma gondii aFrom ref. 1.
NOTE: No responsibility is assumed by the Publisher for any injury and/or damage to persons or property as a matter of products liability, negligence or otherwise, or from any use or operation of any methods, products, instructions or ideas contained in the material herein. No suggested test or procedure should be carried out unless, in the reader's judgment, its risk is justified. Because of rapid advances in medical sciences, we recommend that the independent verification of diagnoses and drag dosages should be made. Discussions, views, and recommendations as to medical procedures, choice of drugs, and drag dosages are the responsibility of the authors.
Clinical Microbiology Newslctt¢r (ISSN 1069-417X) is issued twice monthly in one indexed volume per year by Elsevier Science Inc., 655 Avenue of the Americas, New York, NY 113010. Subscription price per year: $175.00 including postage and handling in the United States, Canada, and Mexico. Add $59.00 for postage in the rest of the wodd. Second-class postage paid at New York, NY and at additional mailing offices. Postmaster. Send address changes to Clinical Microbiology Newsletter, Elsevier Science Inc., 655 Avenue of the Americas, New York, NY 10010.
154
0196-4399/95/$0.00 + 09.50
© 1995 Elsevier Science Inc.
Clinical Microbiology Newsletter 17:19,1995
Table 4. Type of transplant and most common infectious agents a Transplantedorgan Infectious agent Kidney Heart, lung, heart-lung Liver Pancreas Bone marrow aFrom refs. 11-16
Grana-negative enterics Gram-negative enterics, staphylococci, Legionella Bacterial, fungal B acteriai Bacterial, fungal
Table 5. Number and percentage of types of infection during the first year after transplanta
Transplant
N
Patients with bacteremia (%)
Patients with symptomatic CMV (%)
Kidney Heart Heart-lung Liver
64 119 31 101
5 13 19 23
8 16 39 22
dedicated area of the laboratory. This approach would minimize costs and also limit the repeated handling of specimens if numerous tests are requested. Facilities for serologic should also be available. This service may or not be a part of the microbiology laboratory but is of vital importance if the transplant service is to be successful. Knowledge o f nosocomial infections rates of specific organisms and their antibiotic susceptibility patterns is also important. The infection control department in the hospital can be of great service when it comes to determining the primary nosocomial pathogens and considering what tests to offer for their detection. Rapid turnaround times of results are also critical for a successful transplantation program. Microscopic procedures with Gram, acid-fast, and immunofluoreseence staining can all be used to provide rapid, same-day, direct detection for many infectious agents. Another concern is the community hospital where certain patients go if an infection occurs after they return home. These institutions should be able to provide minimal bacteriologic, fungal, and serologic testing services. Alternatively, specimens should be referred to a larger laboratory with an expected rapid turnaround time on results.
Conclusion In summary, the microbiology laboClinical Microbiology Newsletter 17:19,1995
Patients with invasive fungal infections (%) 0 8 23 16
ratory must become an integral part of any transplant service. Communication must begin before the transplant begins and continue during the entire time that the service is offered at that institution. Changes in test methods, levels of service, and turnaround times are all important aspects of an evolving transplant service and the laboratory must be willing to work with the transplant team if it is to be successful. Just as important is that the transplant team seek the counsel of the microbiology staff before on setting up new programs. References 1. Ho, M., and J.S. Dummer. 1995. Infections in transplant recipients, p. 27092717. In G.L. Mandel, J.E. Bennett, and R. Dolin (eds), Principles and practices of infectious diseases, vol. 2. Churchill Livingston, New York. 2. Starzl, T.E., et al. 1983. The ColoradoPittsburgh cadaveric renal transplantation study on cyclosporine. Transpl. Proc. 15:2459-2468. 3. Ho, M. 1977. Virus infections after transplantation in man. Arch. Virol. 36:259--267. 4. Shields, A.F., et al. 1985. Adenovirus infection in patients undergoing bone marrow transplantations. N. Engl. J. Med. 312:529-533. 5. Ho, M. 1987. Infection and organ transplantation, p. 49-60. In Gelman, S (ed.), Anesthesia and organ transplantation. W.B. Saunders, Philadelphia.
© 1995 Elsevier Science Inc.
6.
Ho, M., et al. 1983. Infections in kidney, heart, and liver transplant recipients on cyclosporine. Transplant. Proc. 125:2768-2772.
7.
Dummer, J.S. 1988. Infectious complications of transplantation, p. 163-179. In Brest, A.N. (ed), Cardiovascular clinics.
8.
Kusne, S., et al. 1988. Infections after liver transplantation. An analysis of 101 consecutive cases. Medicine 67:132-143.
9.
Villablanca, J.G., et al. 1990. The clinical spectrum of infections with viridans streptococci in bone marrow transplant patients. Bone Marrow Transplant 6:387-393.
10. Ozaki, C.F., et al. 1992. Surgical complications in solitary and combined pancreas-kidney transplantation. Am. J. Surg. 164:546-551. 11. Todo, S., et al. 1992. Cadaveric small bowel and small bowel-liver transplantation in humans. Transplantation 53:369-376. 12. Myerowitz, R.L., A.A. Medeiros, and T.F. O'Brien. 1972. Bacterial infection in renal homotransplant recipients: a study of fifty-three bacteremic episodes. Am J. Med. 53:308-314. 13. Brooks, R.G., et al. 1985. Infectious complications in heart-lung transplant recipients Am. J. Med. 79: 412--422. 14. Paya, C.V., et al. 1989. Incidence, distribution and outcome of episodes of infections in 100 orthotopic liver transplantations. Mayo Clin. Proc. 64:555-564. 15. George, D.L., et al. 1991. Bacterial infections as a complication of liver transplantation: epidemiology and risk factors. Rev. Infect. Dis.13:387-396. 16. Hesse, U.J., et al 1985. Intra-abdominal infections in pancreas transplant recipients. Ann. Surg. 203:153-162. 17. Dummcr, J.S. 1990. Infectious complications of heart-lung transplantation. In DK.C. Cooper and D. Novitsky (eds), The transplantation and replacement of thoracic organs. Kluwer Academic Publishers, Lancastcr, U.K. 18. Singh, N., et al. 1988. Infections with cytomegalovirus and other herpes viruses in 121 liver transplant recipients: transmission by donated organ and the effect of OKT3 antibodies. J. Infect. Dis 158:124-131.
0196-4399/95/$0.fl0 + 09.50
155