Immunization Status at the Time of Liver Transplant in Children and Adolescents | Gastrointestinal Surgery | JAMA | JAMA Network
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Table 1.  Percentage of Children and Adolescents Up to Date for Individual Vaccines at the Time of Liver Transplant Based on the Centers for Disease Control and Prevention Schedule
Percentage of Children and Adolescents Up to Date for Individual Vaccines at the Time of Liver Transplant Based on the Centers for Disease Control and Prevention Schedule
Table 2.  Characteristics of Patients Up to Date and Not Up to Date With Immunizations at the Time of Liver Transplant Based on the Centers for Disease Control and Prevention Schedule
Characteristics of Patients Up to Date and Not Up to Date With Immunizations at the Time of Liver Transplant Based on the Centers for Disease Control and Prevention Schedule
1.
Feldman  AG, Beaty  BL, Curtis  D, Juarez-Colunga  E, Kempe  A.  Incidence of hospitalization for vaccine-preventable infections in children following solid organ transplant and associated morbidity, mortality, and costs.  JAMA Pediatr. 2019;173(3):260-268. doi:10.1001/jamapediatrics.2018.4954PubMedGoogle ScholarCrossref
2.
National Immunization Surveys (NIS). About NIS. Centers for Disease Control and Prevention website. https://www.cdc.gov/vaccines/imz-managers/nis/about.html. Updated January 23, 2018. Accessed August 1, 2019.
3.
US Department of Health and Human Services. Recommended immunization schedule for children and adolescents aged 18 years or younger: United States, 2017. Centers for Disease Control and Prevention website. https://www.cdc.gov/vaccines/schedules/downloads/child/0-18yrs-child-combined-schedule.pdf. Published February 22, 2019. Accessed August 1, 2019.
4.
Rubin  LG, Levin  MJ, Ljungman  P,  et al; Infectious Diseases Society of America.  2013 IDSA clinical practice guideline for vaccination of the immunocompromised host.  Clin Infect Dis. 2014;58(3):e44-e100. doi:10.1093/cid/cit684PubMedGoogle ScholarCrossref
5.
Hill  HA, Elam-Evans  LD, Yankey  D, Singleton  JA, Kang  Y. Vaccination coverage among children aged 19-35 months—United States, 2016.  MMWR Morb Mortal Wkly Rep. 2017;2018(67):1123-1128. doi:10.15585/mmwr.mm6643a3PubMedGoogle Scholar
6.
Feldman  AG, Kempe  A, Beaty  BL, Sundaram  SS; Studies of Pediatric Liver Transplantation (SPLIT) Research Group.  Immunization practices among pediatric transplant hepatologists.  Pediatr Transplant. 2016;20(8):1038-1044. doi:10.1111/petr.12765PubMedGoogle ScholarCrossref
Research Letter
November 12, 2019

Immunization Status at the Time of Liver Transplant in Children and Adolescents

Author Affiliations
  • 1Section of Gastroenterology, Hepatology, and Nutrition, University of Colorado, Denver, Aurora
  • 2Adult and Child Consortium for Health Outcomes Research and Delivery Science (ACCORDS), University of Colorado, Denver, Aurora
  • 3Section of Pediatric Infectious Diseases, University of Colorado, Denver, Aurora
JAMA. 2019;322(18):1822-1824. doi:10.1001/jama.2019.14386

Vaccine-preventable infections are a serious complication following transplant. In a multicenter retrospective cohort study of 6980 pediatric solid organ transplant recipients between 2004 and 2011, 15.6% were hospitalized with a vaccine-preventable infection in the first 5 years after transplant at a rate of up to 87 times higher than in the general pediatric population.1 Immunizations are a minimally invasive, cost-effective way to reduce the incidence of these infections. We quantified the percentage of patients at Society of Pediatric Liver Transplantation centers who were up to date for their age on immunizations at the time of transplant and determined whether demographic and clinical factors were associated with immunization status at the time of transplant.

Methods

We collected clinical and demographic data on all patients younger than 18 years who underwent a liver transplant between August 2017 and August 2018 at 39 centers in the United States and Canada. Each center used state registries and electronic medical, primary care, and parental records to determine which vaccines had been given by the date of transplant. Patients who underwent transplant for acute liver failure were excluded. Up-to-date immunization status was determined using 3 vaccine schedules: (1) the 7-vaccine benchmark used by the National Immunization Survey (NIS)2; (2) the Centers for Disease Control and Prevention (CDC) immunization schedule for healthy children3; and (3) the 2013 Infectious Diseases Society of America (IDSA) Clinical Practice Guideline for Vaccination of the Immunocompromised Host,4 which includes recommendations to accelerate measles, mumps, and rubella (MMR); varicella; and human papillomavirus immunizations in transplant candidates (Supplement). Bivariable analysis was performed to explore factors associated with being up to date on immunizations (using CDC guidelines) at the time of transplant. Statistical significance was set at P < .05 by 2-sided tests. Data were analyzed using SAS version 9.4. Participation in the Society of Pediatric Liver Transplantation registry was approved by institutional review or research ethics boards; parents or legal guardians provided written informed consent and patient assent was obtained when appropriate.

Results

Immunization records were available for 281 (93%) of 301 eligible patients. Of these patients, 55% (95% CI, 49%-61%) were up to date on immunizations based on the NIS requirements, 29% (95% CI, 24%-35%) based on the CDC schedule, and 19% (95% CI, 14%-24%) based on the IDSA accelerated schedule. Based on the CDC schedule, the percentage of children up to date (for age) for individual vaccines ranged from 50% for Haemophilus influenzae type b to 94% for meningococcus (Table 1). Of the 199 children not up to date based on the CDC schedule, 51% (95% CI, 44%-58%) were missing at least 4 immunizations. Of the 52 patients aged 6 to 11 months at the time of transplant who were eligible using the IDSA guidelines for accelerated live vaccines, 13 (25%) received MMR vaccinations (95% CI, 14%-39%) and 8 (15%) received varicella vaccinations (95% CI, 7%-28%). There were no demographic or clinical factors significantly associated with underimmunization, including administration by primary care physicians vs other clinicians (Table 2). Only 13 patients (5%) were reported to have had delayed transplant listing to allow for immunization compliance.

Discussion

In this high-risk population of pediatric liver transplant recipients with a lifetime of anticipated exposure to immunosuppressive therapy, there were low rates of age-appropriate immunization at the time of transplant. Only 55% of transplant recipients were up to date on the least stringent NIS 7-vaccine series compared with 70% of US children aged 19 to 35 months.5 Transplant recipients had lower vaccine rates than the overall population of children aged 19 to 35 months for each of the 7 core vaccines.5 Particularly concerning was underutilization of live vaccines in young children, which are not routinely recommended after transplant.4,6

The study was limited by reliance on individual centers to collect immunization records using state registries and electronic medical, primary care, and parental records. Incomplete records could lead to a falsely increased underimmunization rate; however, included data were the only data available to transplant centers. Cloud-based digital immunization records or a national immunization registry might help overcome data barriers in the future.

Further research is needed to understand barriers to immunization in the pediatric transplant population. Novel tools that provide pretransplant vaccine education and enhance communication between primary care and subspecialty clinicians are needed to increase immunization rates in these high-risk children.

Section Editor: Jody W. Zylke, MD, Deputy Editor.
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Article Information

Accepted for Publication: August 15, 2019.

Corresponding Author: Amy G. Feldman, MD, MSCS, Section of Gastroenterology, Hepatology, and Nutrition, University of Colorado, Denver, 13123 E 16th Ave, B290, Aurora, CO 80045 (amy.feldman@childrenscolorado.org).

Author Contributions: Dr Feldman and Ms Beaty had full access to all of the data in the study and take responsibility for the integrity of the data and the accuracy of the data analysis.

Concept and design: Feldman, Sundaram, Kempe.

Acquisition, analysis, or interpretation of data: All authors.

Drafting of the manuscript: Feldman, Sundaram, Torres.

Critical revision of the manuscript for important intellectual content: Feldman, Sundaram, Beaty, Curtis, Kempe.

Statistical analysis: Feldman, Beaty, Torres.

Obtained funding: Feldman.

Administrative, technical, or material support: Curtis, Kempe.

Supervision: Sundaram, Curtis, Kempe.

Conflict of Interest Disclosures: Dr Curtis reported receiving funding from Sanofi-Pasteur for a separate high-dose influenza vaccine study. No other disclosures were reported.

Funding/Support: Dr Feldman’s time and research was funded by a Children’s Hospital Colorado Research Institute Research Scholar Award and grants from the National Institutes of Health/National Center for Advancing Translational Sciences (TR002534) and the Agency for Healthcare Research and Quality (HS026510-01A1).

Role of the Funder/Sponsor: The funders had no role in the design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Additional Contributions: We acknowledge the following centers, investigators, and coordinators who contributed data to this study: Alfred I. Dupont Hospital for Children, Wilmington (Stephen Dunn, MD; Dana Mannino, MSN); Ann and Robert H. Lurie Children’s Hospital of Chicago (Estella M. Alonso, MD; Mary Riordan, BA, CCRP); Boston Children’s Hospital (Scott Elisofon, MD); Children’s Healthcare of Atlanta (Nitika Gupta, MD; Hillary Espinoza, BS); Children’s Hospital Cincinnati (Alexander Miethke, MD; Amanda Schreibeis, CRC); Children’s Hospital Colorado, Aurora (Michelle Hite, CCRC); Children’s Hospital of Los Angeles (George Yanni, MD; Steven Grantham, CCRP); Children’s Hospital at Montefiore, Bronx (Nadia Ovchinsky, MD, MBA; Preeti Malik, MD, MPH); Children’s Hospital of Philadelphia (Elizabeth Rand, MD; Lucia Sanchez, BS); Children’s Hospital of Pittsburgh (George Mazariegos, MD; James E. Squires, MD, MS; Alexis Rzempoluch, MS); Children’s Hospital of Wisconsin, Wauwatosa (Grzegorz Telega, MD, MBA; Stacee Lerret, PhD, RN, CPNP); Children’s Medical Center of Dallas (Dev M. Desai, MD, PhD; Jatin Moghe, MBBS, MPH); Children’s Mercy Hospital, Kansas City (Walter S. Andrews, MD; Vicki Fioravanti, RN, CCTC, CCTN); Duke University School of Medicine, Durham (Debra Sudan, MD; Alisha Mavis, MD; Lynnette Moats, MSN, RN); Hospital for Sick Children Toronto (Vicky Lee Ng, MD, FRCPC; Blossom Dharmaraj, MEd); Georgetown University, Washington, DC (Nada Yazigi, MD; Andrea Hobby, BA); Indiana University Medical Center, Indianapolis (Girish Rao, MD; Benjamin Maccaby, BS, CCRP); Levine Children’s Hospital, Charlotte (Vani Gopalareddy, MD; Mary Alice Boulware, CPNP); Mayo Medical School, Rochester (Samar H. Ibrahim, MB, ChB; Katryn N. Furuya, MD, FRCPC); Monroe Carell Jr Children’s Hospital at Vanderbilt, Nashville (Sophoclis Alexopoulos, MD; Rachel Schillo, BSN, RN); Mount Sinai Medical Center, New York (Ronen Arnon, MD; Megan Czurda, MPH); Medical University of South Carolina, Charleston (Nagraj Kasi, MBBS; Mark Law); New York Presbyterian Hospital (Steven Lobritto, MD; Danilo Gamino, MD); Phoenix Children’s Hospital (Sylvie Lebel, MD; Katie Knafla, CCRP); Primary Children’s Medical Center, Salt Lake City (Linda Book, MD; Christa Jennings, MSN, PNP); Sainte-Justine Hospital, Montreal (Mona Beaunoyer, MD); Seattle Children’s Hospital (Simon Horslen, MB, ChB, FRCPCH; Kelly Wallace-Boughter, BA); St Louis Children’s Hospital (Ajay Jain, MD, DNB; Erin Foristal, RN, BSN, CCTC); Texas Children’s Hospital, Houston (Tamir Miloh, MD; Julie Economides, RN, BS); University of Alabama, Birmingham (Janaina Nogueira, MD; Robin Greer, MSN, CPNP-AC); University of Alberta, Edmonton (Susan M. Gilmour, MD, MSc, FRCPC; Cheri Robert, MSc); University of California Los Angeles Medical Center (Suzanne McDiarmid, MD; Susan Fiest, RN, BSN); University of California, San Francisco (Emily R. Perito, MD, MAS; Lisa Gallagher, PNP; Melissa Zerofsky, PhD); University of Chicago (J. Michael Millis, MD; Ruba Azzam, MD, MPH; Pamela Boone, RN); University of Florida, Gainesville (Jeffrey Fair, MD); University of Michigan, Ann Arbor (John Magee, MD; Jessica Hollenbeck, RN; Victoria Shieck, RN, CCTN); University of North Carolina, Chapel Hill (Steven Lichtman, MD; Nancy Garbarino, MS; Marc Lalonde, RN, BSN, CCTC); Washington University, St Louis (Yumirle P. Turmelle, MD, MSPH; Stacy Postma, BS); Yale New Haven Children’s Hospital (Udeme Ekong, MD, MPH; Ricarda Tomlin, BS, CCRP); and EMMES Corporation (Jeff Mitchell, BS).

References
1.
Feldman  AG, Beaty  BL, Curtis  D, Juarez-Colunga  E, Kempe  A.  Incidence of hospitalization for vaccine-preventable infections in children following solid organ transplant and associated morbidity, mortality, and costs.  JAMA Pediatr. 2019;173(3):260-268. doi:10.1001/jamapediatrics.2018.4954PubMedGoogle ScholarCrossref
2.
National Immunization Surveys (NIS). About NIS. Centers for Disease Control and Prevention website. https://www.cdc.gov/vaccines/imz-managers/nis/about.html. Updated January 23, 2018. Accessed August 1, 2019.
3.
US Department of Health and Human Services. Recommended immunization schedule for children and adolescents aged 18 years or younger: United States, 2017. Centers for Disease Control and Prevention website. https://www.cdc.gov/vaccines/schedules/downloads/child/0-18yrs-child-combined-schedule.pdf. Published February 22, 2019. Accessed August 1, 2019.
4.
Rubin  LG, Levin  MJ, Ljungman  P,  et al; Infectious Diseases Society of America.  2013 IDSA clinical practice guideline for vaccination of the immunocompromised host.  Clin Infect Dis. 2014;58(3):e44-e100. doi:10.1093/cid/cit684PubMedGoogle ScholarCrossref
5.
Hill  HA, Elam-Evans  LD, Yankey  D, Singleton  JA, Kang  Y. Vaccination coverage among children aged 19-35 months—United States, 2016.  MMWR Morb Mortal Wkly Rep. 2017;2018(67):1123-1128. doi:10.15585/mmwr.mm6643a3PubMedGoogle Scholar
6.
Feldman  AG, Kempe  A, Beaty  BL, Sundaram  SS; Studies of Pediatric Liver Transplantation (SPLIT) Research Group.  Immunization practices among pediatric transplant hepatologists.  Pediatr Transplant. 2016;20(8):1038-1044. doi:10.1111/petr.12765PubMedGoogle ScholarCrossref
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