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The Antimicrobial Stewardship Program: Keeper of the S. aureus bacteremia Checklist Manifesto

Staphylococcus aureus bacteremia (SAB) is a serious and sometimes devastating infection. There are established guidelines for optimal management, and more recently, numerous studies have shown the benefits of Infectious Diseases consultation, including improving guideline-adherent management, and reducing hospital stays, 30-day readmissions, and in-hospital mortality. Pharmacist-driven initiatives embedded within the Antimicrobial Stewardship Program (ASP) have also been shown to improve quality of care for patients with SAB.

In this study, Remtulla et al. described the impact of combining unsolicited prospective audit and feedback (PAF) a standardized SAB bundle on SAB management. ASP pharmacists used the SAB bundle once per patient, to make PAF recommendations to teams whose patients developed SAB. The SAB patients were identified to the ASP by twice-daily microbiology laboratory emails, only during normal business hours on non-holiday weekdays. The SAB checklist recommendations included ID consultation, repeat blood cultures, empiric therapy recommendation (vancomycin unless MSSA known), echocardiogram, duration of therapy guidance, and source control recommendations.

In their analysis of 199 patients, PAF recommendations were accepted at a rate of 92.6%, and 44% of the recommendations were for ID consultation. SAB bundle adherence increased from 29.0% to 72.8% (p<0.001) in the intervention group, with statistically significant (p<0.001) increases in ID consultation (56.5% vs 93.4%), guideline-adherent therapy (83.9% vs 99.3%), echocardiography (72.6% vs 95.6%), and duration of therapy (87.0% vs 100%). Reductions in 30 day readmission and 30 day mortality rates were not statistically significant, likely owing to the small study size.

Implementation of this SAB bundle seemed to augment the impact of ID consultation, because even in the intervention groups without ID consultation, the adherence to the bundle elements approached that of the pre-intervention groups with ID consultation.

This is yet another study demonstrating the ease of implementation of checklists/bundles for improving quality of patient care. Other studies have shown that automatic ID consultation for SAB can lead to better patient outcomes. However, the resources needed for automatic consultation may not be available to all hospitals, and this study provides another pharmacist-driven protocol that can also improve outcomes. Further improvements in an approach like this should include a mechanism for weekend/holiday notification in the absence of pharmacist presence, or inclusion of rapid diagnostic testing such as detection of mecA gene to facilitate earlier definitive treatment during uncovered periods.

 

Citation: Shahileen Remtulla, Karen Zurek, Carlos Cervera, Cristina Hernandez, Mao-Cheng Lee, Holly L Hoang, Impact of an Unsolicited, Standardized Form–Based Antimicrobial Stewardship Intervention to Improve Guideline Adherence in the Management of Staphylococcus aureus Bacteremia, Open Forum Infectious Diseases, Volume 6, Issue 4, April 2019, ofz098, https://doi.org/10.1093/ofid/ofz098


 

Bryan Alexander, PharmD on Why I Love ID

Why I love ID:

I love academic medicine; working jointly with an interdisciplinary team of experts to sort out the most complex clinical cases excites me. There is no place in the region that fulfills each of the aspects of that statement better than Nebraska Medicine.

While more and more of the practice of medicine necessarily moves to the long-term management of chronic disease states, infectious disease is one area where we are routinely able to cure a patient’s medical condition and appreciate the satisfaction that can bring for them. Also, the pathogen-host-antimicrobial interaction is fascinating and unique in medicine from a pharmacotherapy perspective. Drug therapy can be complicated enough in other areas without the host and its associated resistance mechanisms further complicating things, which makes being an ID pharmacist very intellectually rewarding. Finally, microbes are some of the most diverse, important, and fascinating entities on our planet. There’s always so much more to appreciate and learn (or re-learn!).

I also love:

I’ve always loved music, but developed an particular appreciation for opera in high school, which I was able to foster while living in Chicago and Baltimore/D.C. during my university years. I then lived away from a city without access to live performances for about a decade and had two small children. Now having moved here and with children that are a bit older (7 and 4), my wife and I have been excited to attend Opera Omaha and share more aspects of our love for music with them.

 


 

When you see CRE: Add Equal Parts Antimicrobial Stewardship and Infection Control

The following was previously posted by Dr. Marcelin to SHEA Journal Club published online in April 2019.

Dealing with carbapenem resistant organisms presents both an antimicrobial stewardship and infection control problem. Richter et al. aimed to predict risk factors for carbapenem resistance among Gram-negative rods (CR-GNR). The authors were particularly interested in whether differences exist in risk factors for development of ertapenem-resistance (ER-GNR), versus resistance to antipseudomonal carbapenems (ACR-GNR). This was a retrospective study over a 6-year period (2011-2016) evaluating cultures from any source from a mixed patient population of patients with malignancy, transplant patients, and those in the ICU.  The final analysis included 14292 GNR isolates, with 274 ER-GNR (majority Klebsiella species) and 618 ACR-GNR (mostly Pseudomonas species), and both groups of CRE were more common in respiratory cultures.

Multivariate analysis identified predictors of ER-GNR including renal disease, admission from another healthcare facility, mechanical ventilation prior to culture, receipt of any anti-MRSA agents within 30 days, and receipt of carbapenems within 30 days. Both test and validation models had a reliable c-statistic of 0.74 and 0.73 respectively. Predictors of ACR-GNR were similar. However, instead of renal disease, male sex was another predictor of ACR-GNR, and the test and validation models had reliable c-statistics of 0.76 and 0.77 respectively. They then assigned points to these models to predict likelihood of development of resistance.

Despite limitations including missing data, the authors suggest their risk scores may be more accurate at predicting carbapenem resistance than antibiograms since they are dynamic and can be automated. Carbapenem resistance was effectively ruled out (<5% likelihood) at scores of <6 in the ER-GNR model and <4 in the ACR-GNR model. This scoring system could be useful in guiding empiric antimicrobial therapy when patients present with sepsis, but may be less useful for locations where resistant GNRs are less prevalent.

Little is known about clinical outcomes in patients colonized with carbapenemase-producing carbapenem-resistant Enterobacteriaceae (CP-CRE) who develop CP-CRE of a different genotype. Chen et al. conducted a retrospective cohort study of patients colonized with CP-CRE who went on to develop clinical infection. Of the 73 CP-CRE carriers who went on to develop infection, 65 developed clinical infection with the same CP-CRE genotype with which they were colonized. Eight developed clinical infection with a different genotype. After adjusting for age, severe clinical presentation and clinical isolate genotype, the authors found that patients whose clinical CP-CRE isolate was different from that with which they were colonized, had significantly increased mortality at 14 days (aRR, 6.36; 95% CI, 1.75–23.06; P = .005) and 30 days (aRR, 3.29; 95% CI, 1.22–8.90; P = .019).

This is a very small study in an area where the authors state the general prevalence of CP-CRE carriage is low, and clinical infection with a different genotype of CP-CRE was not common. However, it generates questions about current isolation practices for patients with CRE. Geographically cohorting patients with CP-CRE may help to reduce transmission to uncolonized patients, but this study raises the questions as to whether this practice may have unintended consequences of transmission of different CP-CRE genotypes between colonized patients, leading to worse outcomes.

References:
Stefan E Richter, Loren Miller, Jack Needleman, Daniel Z Uslan, Douglas Bell, Karol Watson, Romney Humphries, James A McKinnell; Risk Factors for Development of Carbapenem Resistance Among Gram-Negative Rods, Open Forum Infectious Diseases, Volume 6, Issue 3, 1 March 2019, ofz027, https://doi.org/10.1093/ofid/ofz027

 

Wen Kai Chen, Yong Yang, Ban Hock Tan; Increased Mortality Among Carbapenemase-Producing Carbapenem-Resistant Enterobacteriaceae Carriers Who Developed Clinical Isolates of Another Genotype, Open Forum Infectious Diseases, Volume 6, Issue 2, 1 February 2019, ofz006, https://doi.org/10.1093/ofid/ofz006

Congratulations to UNMC ID Faculty designated as Top Teachers for 2018!

After every rotation, medical students and Internal Medicine Residents at UNMC submit evaluations on their faculty members. The Department of Internal Medicine pools all of the evaluation data and designates the faculty with the top 33% of evaluation scores as “Top Teachers”.  For the year 2018, three of our Infectious Disease faculty members who attend on the General ID Service and participate in Medical Student Education were awarded this honor.

Meet our Internal Medicine 2018 Top Teachers from UNMC ID!

Dr. Sara Bares 

Assistant Professor of Medicine; Associate Director of the Specialty Care Clinic; Director of the UNMC COM HIV Enhanced Medical Education Track; Co-Director of UNMC COM Defenses & Invaders Microbiology Course

Dr. Jasmine Marcelin

Assistant Professor of Medicine; Associate Medical Director, Nebraska Medicine Antimicrobial Stewardship Program; Associate Medical Director, Nebraska Medicine Infection Control & Epidemiology; Co-Director of the UNMC COM HIV Enhanced Medical Education Track; Co-Director of Digital Innovation & Social Media Strategy for Division of Infectious Diseases

Dr. Trevor Van Schooneveld

Associate Professor of Medicine; Medical Director, Nebraska Medicine Antimicrobial Stewardship Program; Program Director, UNMC Infectious Disease Fellowship; Associate Medical Director, Nebraska Medicine Infection Control & Epidemiology

The UNMC ID Division would like to congratulate Drs. Sara Bares, Jasmine Marcelin, and Trevor Van Schooneveld for being awarded Top Teachers in 2018.

This is the 4rd Top teacher award for Dr. Bares, and 9th for Dr. Van Schooneveld. Dr. Marcelin received the award for 2018 in her first year of eligibility since joining the UNMC ID faculty. 

This is yet another testament to our Division’s commitment to Medical Education and growing the next generation of Infectious Disease Doctors!


 

UNMC ID Ebola Expert Dr. Angela Hewlett shares the Nebraska Experience

Dr. Angela Hewlett presented ‘Clinical Management of Ebola: The Nebraska Experience’ at Grand Rounds at the University of Wisconsin on Friday April 19th 2019.  Dr. Hewlett was invited by Internal Medicine Chief Resident Dr. Samantha Murray-Bainer as part of the University of Wisconsin Dream Speaker series, where each Chief Resident is given the opportunity to select a Grand Rounds speaker that has been influential to them.

We are thrilled to celebrate this honor with Dr. Hewlett, a testament to her expertise, influence and contribution to the field of Infectious Diseases and Biopreparedness.

Here’s the link to Dr. Hewlett’s Grand Rounds presentation:

https://www.youtube.com/watch?v=5UuD5BJWyZY&list=PLdxJ3bo-hgxRcZ8JQAb8XATB4AElpqzXW&index=31

Photo: Dr. Samantha Murray-Bainer (Chief Resident), Dr. Angela Hewlett, and Dr. Elizabeth Trowbridge (Chair, Department of Internal Medicine), University of Wisconsin

Content courtesy: Dr. Hewlett

Does de-escalation of anti-MRSA therapy for culture-negative pneumonia affect patient outcomes?

Nosocomial pneumonia is a common hospital-acquired infection and has a high mortality rate in the critically ill.  Because drug-resistant bacteria like Pseudomonas aeruginosa and methicillin-resistant Staphylococcus aureus (MRSA) are commonly responsible for these infections, guidelines recommend broad-spectrum empirical therapy that includes anti-MRSA coverage.  Treatment is ideally de-escalated and refined based on culture results.  However, culture negative infections leave a conundrum for clinicians who want to protect their patients but also minimize morbidity and inappropriate antimicrobial use.

Cowley et al. recently published a retrospective study in Chest evaluating the safety of anti-MRSA de-escalation by measuring 28-day mortality, hospital mortality, intensive care unit (ICU) and hospital length of stay (LOS), incidence of treatment failure, and incidence of acute kidney injury (AKI) in patients who were de-escalated compared to those who were not after negative culture result.  De-escalation was defined as transition to a narrower spectrum antibiotic (without MRSA coverage) within 4 days of culture. Of the 279 patients identified with culture-negative nosocomial pneumonia, 79% received vancomycin for MRSA coverage and 92% had some pseudomonal coverage in their empiric treatment.  Ninety-two met the de-escalation criteria.

The de-escalation group had a significantly higher incidence of chronic kidney disease at baseline, but the groups were otherwise well matched. There was no significant difference in 28-day mortality or treatment failure between the groups.  The de-escalation group had a shorter time to transfer out of the ICU and discharge, and they also experienced less AKI.

As Dr. Cawcutt wrote in her review, “De-escalation in culture-negative pneumonia may result in lower AKI and ICU and hospital LOS. There is clear potential benefit for patients and overall health care systems in advocating for earlier de-escalation, regardless of whether or not nares swabs were completed.”

This post is based on Dr. Cawcutt’s review in IDSA Journal Club, available here.  You can read the original article here.


 

Inter-Professional Relationships in HIV Pre-exposure Prophylaxis

We’re excited to feature a recent publication borne from student-faculty collaboration that highlights the importance of interdisciplinary care!

Dr. Jordan Broekhuis, the lead author, is one of our former HIV Enhanced Medical Education Track (EMET) students who is now a surgery resident at Beth Israel Deaconess.  He completed his EMET work here at UNMC under the mentorship of Drs. Sara Bares and Susan Swindells.  Their paper, “Midwest pharmacists’ familiarity, experience, and willingness to provide pre-exposure prophylaxis (PrEP) for HIV,” was published in PLoS One in November.  We recently talked to the authors about their work.

Could you give us a short summary of your work and what motivated you to conduct this study?

Pharmacists in Nebraska and Iowa were asked to complete a survey to gauge their familiarity, experience and willingness to provide HIV pre-exposure prophylaxis (PrEP).  PrEP  is underutilized and pharmacists could potentially play a role in expanding access to PrEP providers, especially in states such as Nebraska and Iowa where regulations support the implementation of collaborative practice agreements which allow for the delegation of responsibilities from the collaborating prescriber to the pharmacist.

What were some of your key findings?

While respondents had limited familiarity and experience with PrEP, most indicated a willingness to provide PrEP if given the opportunity to do so via a collaborative practice agreement and after additional training. 

What do you see as future directions for this research and pharmacist education around the use of PrEP?

This survey laid the groundwork for implementation of a pharmacist-led PrEP (P-PrEP) initiative here in Omaha.  We shared preliminary results of our P-PrEP project at IDWeek 2018 and hope to disseminate the final results soon.

You can read their full article here.  Interested in learning more about UNMC’s EMET program?  See our features of current and former EMET students and read more about the program here.


 

EMET Student Profile – Harrison Greene

Meet Harrison Greene, a new M1 student in our HIV Enhanced Medical Education Track!

Tell us a little about yourself.

I grew up in Omaha, Nebraska and graduated from Creighton Prep High School. I completed my undergraduate education at the University of Kansas, with a degree in Human Biology. During my last year at KU, I decided that I wanted to take a leap and try pursuing a different passion following graduation. This led me back to Omaha, where I enrolled in the culinary arts program at Metropolitan Community College. While taking classes at Metro, I began working in kitchens and eventually earned a spot on the line at The Grey Plume. Working in the hot, fast-paced environment of a James Beard nominated kitchen was a dream come true, and an experience I’ll never forget. However, after four years in the kitchen, I was drawn back to the pursuit of medicine, left the kitchen, and obtained a Master’s Certificate in Biomedical Science from UNO. My untraditional path allowed me many great experiences, and I am thankful that it led me to UNMC.

Why did you decide to come to medical school at UNMC?

I decided to pursue my medical education at UNMC due to the excellence of the academic program, the renowned care provided at Nebraska Medicine, and my desire to live in Omaha during medical school. Furthermore, my father and grandfather are both graduates of UNMC, and having the opportunity to receive my education at the program that prepared them to be skilled care providers was significant to me.

Could you tell us more about HIV EMET program? What drew you to it?

The Comprehensive HIV Medicine EMET program is a four-year longitudinal experience that provides students the opportunity to advance their education in the care of patients living with HIV while also fostering relationships with faculty, residents, and other students throughout the program. This program is an invaluable asset to the student, as it allows extra-classroom learning experiences both in and outside of the clinical setting. Initially, I was interested in studying HIV because I was intrigued by the notion of it being a relatively new discovery in the history of medicine. As I learned more about HIV and those affected by it, through my classes and while shadowing at the UNMC HIV clinic, I became interested in the experience of the patients faced with the multifaceted nature of the disease. Care for patients infected with HIV requires a broad base of knowledge of immunology, care for opportunistic infections and other diseases, as well as an understanding of behavioral sciences and socioeconomic determinants of health. I am excited to be a part of the Comprehensive HIV Medicine EMET program, as it will help me to become a more well-rounded care provider and an activate participant in the fight against HIV.

What is something you enjoy outside of medicine?

Outside of school, I enjoy cooking, going to restaurant and bar pop-ups, seeing movies at Film Streams, and traveling. One of my favorite parts of traveling is experiencing the food scene in different cities.

We wish Harrison the best of luck over the next several years during his journey with us as part of the HIV EMET! More information about the EMET program can be found here.


 

MD/PhD brings clinical and basic science research together

Kelsey Yamada is an MD/PhD student in Dr. Tammy Kielian’s laboratory studying Staphylococcus aureus.  We enjoyed learning more about him and his work!

Tell us a little about yourself.

I am originally from Hawaii, but moved to Nebraska over a decade ago to attend Creighton University. After graduating with my B.S. Chemistry I moved to Bethesda, MD to work at the NIH. This gave me the opportunity to work along side of physician-scientists who were at the top of their fields, and ultimately helped me to decide on a career in translational medical research. My wife and I loved our time in Omaha, which led me back to Omaha and UNMCs M.D./Ph.D. program. While I am not sure what medical field I will ultimately choose, I am certain that I am interested in studying host-pathogen interactions during chronic disease. 

What are you studying for your thesis, and how do you think your work will inform your future practice of medicine?

My thesis research focused on trying to understand how orthopedic implant associated S. aureus biofilms modulates the metabolism of monocytes in order to promote the establishment and persistence of infection.  Though my current research is on a fairly specific ailment, it may not directly inform my clinical practice in the future (unless of course I go into orthopedics). However, I have had a lot of opportunities to work on both the clinical and basic science side of a clinical study on orthopedic implant infections. It has helped me to understand how important communication is when trying to develop and carry out a clinical study. In my future, it will be essential for me to bridge the gap between the clinical and research teams. 

Tell us something about yourself unrelated to medicine.

I’ve watched the office from episode 1, an embarrassing number of times. But I always skip over the episodes with Will Ferrell. My friends and I demolish trivia night, unless it has to do with Deangelo Vickers and his juggling. 

 

We’re always excited to learn about our students’ research that helps us understand problems we see all the time in clinic.  If you’re interested in learning more about Kelsey’s work, check out his publications below:

Yamada, K.J., Barker, T., Dyer, K.D., Rice, T.A., Percopo, C.M., Garcia-Crespo, K.E., Cho, S., Lee, J.J., Druey, K.M., Rosenberg, H.F. Eosinophil-associated Ribonuclease 11 is a Macrophage Chemoattractant. J. Biol. Chem., 290:8863-8875, 2015. PMID: 25713137

Yamada, K.J., Heim, C.E., Aldrich, A.L., Gries, C.M., Staudacher, A.G., Kielian, T. Arginase-1 Expression in Myeloid Cells Regulates Staphylococcus aureus Planktonic but Not Biofilm Infection. Infect Immun. 86:e206-218, 2018. PMID: 29661929

Yamada, K.J., Kielian, T. Biofilm-Leukocyte Cross-Talk: Impact on Immune Polarization and Immunometabolism. J. Innate Immun., 2018. PMID: 30347401

Zhou, C., Bhinderwala, F., Lehman, M.K., Thomas, V.C., Chaudhari, S.S., Yamada, K.J., Powers, R., Kielian, T., Fey, P.D. Urease is an essential component of the acid response network of Staphylococcus aureus and is required for a persistent murine kidney infection. PLoS Pathog., 2018. PMID: 30608981

Yamada, K.J., Xi, X., Attri, K.S., Zhang, W., Singh, P.K., Bronich, T.K., Kielian, T. Nanoparticle targeting of monocyte metabolism to treat Staphylococcus aureus prosthetic joint infection. (In revision at Journal of immunology).

Lehman, M.K., Nuxoll, A.S., Yamada, K.J., Kielian, T., Carson, S.D., Fey, P.D. Protease-mediated growth of Staphylococcus aureus on host proteins is opp3-dependent. (In submission to mBio).


 

MD/PhD Student on the Cutting Edge of HIV Research

Jonathan (Yoni) Herskovitz is an MD/PhD student working with Dr. Howard Gendelman studying therapies for HIV.  We were excited to talk to him about his work and his plans for the future!

Tell us a little about yourself and your career goals.

I am California native, and though pursuing a career as a physician-scientist occupies the majority of my time, I still enjoy astronomy and home renovating. After graduating with a BS from UCLA (Go Bruins!), I worked in research at a pharmaceutical company outside Los Angeles for two years. This fostered my love for translational research that I hope to integrate throughout my career. Since I still have my clinical rotations remaining, it’s hard to say what specific field of medicine appeals to me the most, but I am certainly considering fellowship in infectious disease.

Could you tell us a little about your thesis?

My research focuses on optimizing gene therapy for human immunodeficiency virus (HIV). An estimated 36.9 million individuals are infected with HIV worldwide, and unfortunately, require lifelong treatment with antiretroviral drugs. We are developing a targeted delivery scheme for CRISPR-Cas9 (pioneered by our collaborators), that could specifically excise viral DNA from human immune cells. Most importantly, this strategy bears the potential to free patients from chronic reliance on anti-HIV medications.

How do you think your current work will inform your practice of medicine in the future?

Laboratory research has instilled within me a number of disciplines that I hope to carry with me to clinical practice. I have learned how to formulate and test scientific hypotheses, just as I plan to create differential diagnoses and utilize labs to evaluate possible etiologies for illness. Although HIV infects individual cells, it has the potential to cause damage in almost every major organ system. This notion has taught me that it is important to remember that as clinicians, we treat people, not strictly diseases. Additionally, HIV impacts certain patient populations (e.g. communities in Africa, MSM, and IV drug users) with higher frequencies. It is therefore imperative to seek out opportunities to volunteer in at-risk and medically underserved areas so that I can best understand potential treatment complexities in my regular practice. Finally, my project has taught me to always think about how a particular product or finding can be improved upon. Frequently the answer to these questions requires help from others and it is this dynamic teamwork for the betterment of patients that excites me most about becoming a doctor.

Tell us something about yourself unrelated to medicine and your research.

I am an avid amateur stargazer / space enthusiast. Looking at our universe through my telescope and learning about various technologies to explore it inspires me too look past my immediate concerns towards something greater. Plus, my wife usually joins me for these astronomy outings, which is always a bonus.

 

We’re proud to have people like Yoni at UNMC who are furthering our understanding of complicated diseases and helping us provide the best care.  If you’re interested in learning more about his work, check out his publications below:

Kinderman F, Yerby B, Jawa V, Joubert MK, Joh NH, Malella J, Herskovitz J, Xie , Ferba J, McBride H. Impact of Precipitation of Antibody Therapeutics following Subcutaneous Injection on Pharmacokinetics and Immunogenicity. J Pharm Sci. doi: 10.1016/j.xphs.2019.01.015 (2019).

Herskovitz J, & Gendelman, HE. HIV and the macrophage: from cell reservoirs to drug delivery to viral eradication. J Neuroimmune Pharmacology. doi: 10.1007/s11481-018-9785-6 (2018).

Herskovitz J, Ryman J, Thway T, Lee S, Zhou L, Chirmule N, Meibohm B, & Jawa V. Immune Suppression During Preclinical Drug Development Mitigates Immunogenicity-Mediated Impact on Therapeutic Exposure. J AAPS 19, 447-455, doi:10.1208/s12248-016-0026-8 (2017).

Joubert MK, Deshpande M, Yang J, Reynolds H, Bryson C, Fogg M, Baker MP, Herskovitz J, Goletz TJ, Zhou L, Moxness M, Flynn GC, Narhi LO, & Jawa V. Use of In Vitro Assays to Assess Immunogenicity Risk of Antibody-Based Biotherapeutics. PLoS One 11, e0159328, doi:10.1371/journal.pone.0159328 (2016).

Pandey P, Sliker B, Peters HL, Tuli A, Herskovitz J, Smits K, Purohit A, Singh RK, Dong J, Batra SK, Coulter DW, & Solheim, J. C. Amyloid precursor protein and amyloid precursor-like protein 2 in cancer. Oncotarget 7, 19430-19444, doi:10.18632/oncotarget.7103 (2016).

Cunningham CR, Champhekar A, Tullius MV, Dillon BJ, Zhen A, de la Fuente JR, Herskovitz J, Elsaesser H, Snell LM, Wilson EB, de la Torre JC, Kitchen SG, Horwitz MA, Bensinger SJ, Smale ST, & Brooks DG. Type I and Type II Interferon Coordinately Regulate Suppressive Dendritic Cell Fate and Function during Viral Persistence. PLoS Pathog 12, e1005356, doi:10.1371/journal.ppat.1005356 (2016).

Wilson EB1, Yamada DH, Elsaesser H, Herskovitz J, Deng J, Cheng G, Aronow BJ, Karp CL, Brooks DG. Blockade of chronic type I interferon signaling to control persistent LCMV infection. Science. 340(6129):202-7. doi: 10.1126/science.1235208.


 

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