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Opportunistic Infections—Coming to the Limits of Immunosuppression?

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Opportunistic Infections—Coming to the Limits of Immunosuppression? Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press Opportunistic Infections—Coming to the Limits of Immunosuppression? Jay A. Fishman Transplant Infectious Disease and Compromised Host Program, Infectious Disease Division, MGH Transplantation Center, Harvard Medical School, Massachusetts General Hospital, Boston, Massachusetts 02114 Correspondence: jfi[email protected] Possible etiologies of infection in the solid organ recipient are diverse, ranging from common bacterial and viral pathogens to opportunistic pathogens that cause invasive disease only in immunocompromised hosts. The recognition of infectious syndromes in this population is limited by alterations in the clinical manifestations by immunosuppression. The risk of serious infections in the organ transplant patient is determined by the interaction between the patients’ recent and distant epidemiological exposures and all factors that contribute to the patient’s net state of immune suppression. This risk is altered byantimicrobial prophylaxis and changes in immunosuppressive therapies. In addition to the direct effects of infection, opportunistic infections, and the microbiome mayadversely shape the host immune respons- es with diminished graft and patient survivals. Antimicrobial therapies are more complex than in the normal host with a significant incidence of drug toxicity and a propensity for drug interactions with the immunosuppressive agents used to maintain graft function. Rapid and specific microbiologic diagnosis is essential. Newer microbiologic assays have improved the diagnosis and management of opportunistic infections. These tools coupled with assays that assess immune responses to infection and to graft antigens may allow optimization of man- agement for graft recipients in the future. f one were to design an experiment to study servations regarding infection in transplanta- Ithe effects of infection following organ trans- tion include: www.perspectivesinmedicine.org plantation, it is unlikely that one would use as subjects an outbred population with multiple, 1. The risk for infection is related to the nature severe comorbidities, uncontrolled infectious and intensity of immunosuppression and exposures, and a wide variety of regimens for the infectious exposures of the organ recip- immunosuppression undergoing major surgery ient and donor (Fishman and Rubin 1998; with implantation of organs from an equally Fishman et al. 2007). An understanding of diverse donor pool. Nonetheless, as regimens the relationship between the intensity of for immunosuppression have “stabilized,” some immunosuppression and infectious risk al- general observations can be made based on this lows the development of effective prophy- ongoing “experiment.” Important clinical ob- lactic strategies. Editors: Laurence A. Turka and Kathryn J. Wood Additional Perspectives on Transplantation available at www.perspectivesinmedicine.org Copyright # 2013 Cold Spring Harbor Laboratory Press; all rights reserved; doi: 10.1101/cshperspect.a015669 Cite this article as Cold Spring Harb Perspect Med 2013;3:a015669 1 Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press J.A. Fishman 2. Recognition of infection is more difficult 1. The epidemiologic exposures of both the pa- in transplant recipients than in individuals tient and the organ donor including those with normal immune function given dimin- unrecognized by the patient or distant in ished signs and symptoms of infection and time (Rubin et al. 1981; Fishman and Rubin the array of noninfectious etiologies of fever 1998). (e.g., graft rejection, drug toxicity) (Fishman 2. The patient’s “net state of immunosuppres- and Rubin 1998; Fishman 2007). Nonspecif- sion” including all factors contributing to ic signs and symptoms must be appreciated. the risk for infection (Table 1) (Fishman and 3. Infection progresses rapidly in the immuno- Rubin 1998). compromised host. Thus, the prevention of These factors are conceptual assessments infection is essential. Confronted with infec- similar to measuring the area under the curve tion, early and effective therapy is required. of a formula relating epidemiology and im- 4. The spectrum of potential pathogens is mune function. At higher levels of immuno- broad; multiple pathogens may be present suppression, infection occurs at lower levels at the same time (e.g., virus and molds). of infectious “exposure” or with organisms of Rapid and specific diagnoses are needed to lower levels of native virulence. With lower guide antimicrobial therapies and to limit levels of immunosuppression, infection is less avoidable drug interactions and toxicities. common, drug toxicities are less frequent, but Rapid and improved microbiologic assays graft rejection more prevalent. Specific immune have greatly improved care. Surgical debride- deficits (genetic or acquired) and specific im- ment and invasive diagnostic procedures are munosuppressive regimens predispose to infec- often required. tion with specific classes of organisms (e.g., T-lymphocyte depletion activates latent cyto- 5. There are no currently available assays that megalovirus [CMV] and allows viral replica- can determine an optimal immunosuppres- tion to occur while corticosteroids predispose sive regimen while avoiding infection. to Pneumocystis and other fungal infections) The nature of the clinical transplantation (Table 2) (Issa and Fishman 2009). Successful experiment has tended to obscure the impact prophylaxis reduces the burden of organisms of diverse infections on immune functions in- or protects against invasive infection (e.g., bac- cluding tolerance induction and graft rejection. teremia) and allows more intensive immuno- Recent studies in animal models have empha- suppression. As a result, preventative strat- sized the importance of the microbiome, infec- egies must be adapted to immunosuppression www.perspectivesinmedicine.org tious exposures, and the innate immune system and to the individual’s risk factors for infec- in determining aspects of immune function in- tion. cluding the development of T-cell specificity and function, the risk for subsequent infections, EPIDEMIOLOGY and, to a degree, graft and patient survival (Fig. 1) (Selin et al. 1994; Yewdell and Bennink Epidemiologic exposures can be divided in- 1999; Adams et al. 2003a; Chong and Alegre to four categories: donor-derived (often un- 2012). This review focuses on more recent con- known exposures), recipient-derived infec- cepts in the impact of infection in solid organ tions and colonization, endemic community- transplantation. derived infections, and healthcare institu- tion-derived pathogens. The importance of an otherwise unimportant organism on the RISK FOR INFECTION AND THE TIMELINE skin of a transplant recipient is magnified in OF INFECTION the face of surgery, devitalized tissues, hema- The risk for infection in an individual trans- toma or fluid collections, and immunosup- plant recipient is determined by two factors: pression. 2 Cite this article as Cold Spring Harb Perspect Med 2013;3:a015669 Downloaded from http://perspectivesinmedicine.cshlp.org/ on September 24, 2021 - Published by Cold Spring Harbor Laboratory Press Infections in Organ Tranplantation Timeline of posttransplant infections Time of transplantation <4 Weeks 1–12 Months >12 Months Common infections in solid organ transplant recipients Infections of complex surgical patients Opportunistic Community-acquired • Line infection infections pneumonia • Wound infection • Pneumocystis jirovecii * • Aspiration • Cytomegalovirus* Urinary tract • Anastamotic leaks • Epstein–Barr virus* infections • Graft ischemia • Other Herpesviruses* • Clostridium difficile colitis • Nocardia species* Late opportunistic • Listeria monocytogenes* infections Antimicrobial-resistant species • Hepatitis B virus* • Molds and Cryptococcus • Methicillin-resistant Staphylococcus aureus (MRSA) • Hepatitis C virus • Nocardia species • Extended-spectrum β-lactamase (ESβL) Gram-negative bacilli • Toxoplasma gondii * • Rhodococcus species • Vancomycin-resistant Enterococcus (VRE) • Strongyloides stercoralis * • Candida species (non-albicans) • Leishmania species Late viral • Trypanosoma cruzi * • CMV (colitis/retinitis) Donor-derived (known and unknown pathogens) • Mycobacterium tuberculosis • Hepatitis (HBV, HCV) • Herpes simplex virus (HSV) • Community-acquired • HSV encephalitis • Lymphocytic choriomeningitis virus (LCMV) respiratory viruses • Community acquired • Rabies • BK polyomavirus • JC polyomavirus leading • West Nile virus • Clostridium difficile to progressive multifocal • Cryptococcus neoformans leukoencephalopathy (PML) Recipient-derived (latent or colonized) • Skin cancer • Aspergillus Anastamotic • Posttransplant lymphoproliferative disorder • Pseudomonas complications (PTLD) • Strongyloides • Trypanosoma cruzi *Many infections prevented by appropriate prophylaxis Sources of infection www.perspectivesinmedicine.org Donor or recipient Nosocomial, technical, Activation of latent Community acquired derived donor/recipient infections, relapsed, residual, opportunistic infections Figure 1. The timeline of infections following organ transplantation. The risk for infection following organ transplantation follows a standard pattern with routine immunosuppression and infectious exposures. The potential pathogens for which the risk is modified by prophylaxis, including vaccinations and antimicrobial
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