Journal of Autoimmunity 80 (2017) 10e27

Contents lists available at ScienceDirect

Journal of Autoimmunity
journal homepage: www.elsevier.com/locate/jautimm

Vaccination recommendations for the adult immunosuppressed

patient: A systematic review and comprehensive field synopsis
Anthony Lopez a, Xavier Mariette b, Herve
Bachelez c, Alexandre Belot d,
Bernard Bonnotte e, Eric Hachulla f, Morad Lahfa g, Olivier Lortholary h, Pierre Loulergue i,

phane Paul j, Xavier Roblin k, Jean Sibilia l, Mariela Blum m, Silvio Danese n,
Ste
Stefanos Bonovas o, Laurent Peyrin-Biroulet a, *
a
Department of Gastroenterology and Hepatology and Inserm U954, Nancy University Hospital, Lorraine University, Vandoeuvre-l es-Nancy, France
b
Universit

e Paris Sud, INSERM, U1184, Center for Immunology of Viral Infections and Autoimmune Diseases, AP-HP, Ho ^pitaux Universitaires Paris-Sud, Le
Kremlin-Bic^ etre, Paris, France
c
Sorbonne Paris Cit
e Universit
e Paris Diderot, INSERM U1163, Institut Imagine, Service de Dermatologie, AP-HP Ho ^pital Saint-Louis, Paris, France
d
Pediatric Nephrology, Rheumatology, Dermatology Unit, Femme M ere Enfant Hospital, INSERM U1111, Hospices Civils de Lyon, Universit
e Lyon 1, France
e
Department of Internal Medicine and Clinical Immunology, Dijon University Hospital and INSERM U1098, University of Bourgogne-Franche Comt
e, Dijon,
France
f
Service de M
edecine Interne et Immunologie Clinique, Universit
e de Lille, Centre national de r

ef

erence Maladies syst

emiques et auto-immunes rares, Lille,
France
g
Dermatologist, 6, Rue du Helder, 64200, Biarritz, France
h
University Paris Descartes, Necker Pasteur Center for Infectious Diseases and Tropical Medicine, IHU Imagine, AP-HP, Paris, France
i
Cochin Teaching Hospital, AP-HP, 75014, Paris, France
j
Laboratory of Immunology and Immunomonitoring, CIC 1408 INSERM, GIMAP EA3064, University Hospital of Saint-Etienne, France
k
Service de Gastroent
erologie, CHU de Saint-Etienne, France
l
Department of Rheumatology, Reference Center for Rare Autoimmune Diseases, Division of Internal Medicine, Hautepierre Hospital, University Hospital of
Strasbourg, France
m
Department of Gastrointestinal Medical Oncology, The University of Texas MD Anderson Cancer Center, Houston, TX, USA
n
Department of Gastroenterology and Department of Biomedical Sciences, Humanitas Research Hospital, Rozzano, Milan, Italy
o
IBD Center, Department of Gastroenterology, Humanitas Clinical and Research Center, Milan, Italy

a r t i c l e i n f o a b s t r a c t

Article history:
Background: Immunosuppressed patients are at risk of severe viral infections-related complications.
Received 11 January 2017
National and international vaccination guidelines have been developed to decrease the mortality risk
Received in revised form
23 March 2017 associated with these infections. However, a summary of these guidelines and the value of immunisation
Accepted 27 March 2017 in this population is missing.
Available online 2 April 2017 Objectives: To summarize specific guidelines regarding vaccination in immunosuppressed patients.
Methods: We performed a literature search based on last update vaccine guidelines in immunosup-
Keywords: pressed adult patients published between 1/1/2005e1/31/2016 in English or French language using
Immunocompromised PubMed, Cochrane and Embase, as well as relevant medical society websites.
Vaccine Results: Of the 389 citations identified, 12 guidelines were selected Three additional guidelines were
Guideline selected by searching on the websites from medical societies of each specialty. 15 guidelines were
included, involving 19 medical societies issued from the US (n ¼ 6), international collaboration (n ¼ 3),
UK (n ¼ 2), Canada (n ¼ 1), Australia (n ¼ 1), France (n ¼ 1), and Germany (n ¼ 1). These guidelines
provide recommendations on vaccination in asplenic patients (n ¼ 5), cancer patients (n ¼ 4), HIV pa-
tients (n ¼ 5), hematopoietic stem cell recipients (n ¼ 4), inflammatory bowel diseases patients (n ¼ 5),
psoriasis patients (n ¼ 4), primary immunocompromised patients (n ¼ 3), inflammatory rheumatic
diseases patients (n ¼ 6), and solid organ transplant recipients (n ¼ 5). All guidelines recommended
pneumococcal and injectable influenza vaccines. Other inactivated vaccines were recommended only in

* Corresponding author. Department of Gastroenterology and Hepatology and

Inserm U954, Nancy University Hospital, Lorraine University, 54511, Vandoeuvre-
s-Nancy, France.
le
E-mail address: peyrinbiroulet@gmail.com (L. Peyrin-Biroulet).

http://dx.doi.org/10.1016/j.jaut.2017.03.011
0896-8411/© 2017 Elsevier Ltd. All rights reserved.

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 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27 11

high risk patients. Live vaccines were usually contraindicated in patients under immunosuppressive
therapy and/or in HIV patients with a CD4 count under 200/mm3.
Conclusion: Pneumococcal and injectable influenza are the two essential vaccines recommended in all
immunocompromised patients. Other inactivated vaccines are only indicated in high risk patients. Live
vaccines are usually contraindicated.
© 2017 Elsevier Ltd. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
2. Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
2.1. Data sources and searches . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 11
2.2. Study selection . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
2.3. Data extraction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
2.4. Data synthesis and analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
3. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
3.1. Literature search results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
3.2. Asplenic patients (Appendix Table 1) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
3.3. Patients with oncologic malignancies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 12
3.4. HIV patients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 13
3.5. Hematopoietic stem cell recipients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
3.6. Inflammatory bowel disease patients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
3.7. Primary immunocompromised patients (Appendix Table 3) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
3.8. Patients with psoriasis (Appendix Table 4) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
3.9. Inflammatory rheumatic disease patients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 15
3.10. Solid organ transplant recipients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 17
4. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 18
5. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Registration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Funding source . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Guarantor of the article . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Specific author contribution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Financial support . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Potential competing interests . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 19
Asplenic patients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
Primary immunocompromised patients . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
Patients with psoriasis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 26

1. Introduction efficacy [10]. Over the past decade, academic societies from
different specialties have developed their own guidelines con-
Immunosuppression related to disease process and/or immu- cerning vaccination modalities in clinical situations of immune
nosuppressive therapies is frequently encountered in patients with defects. Despite all these struggling guiding efforts, vaccination
asplenia, cancer, chronic inflammatory diseases, transplantation, coverage seems to remain low, being less than 20% in patients with
and human immunodeficiency virus (HIV) infection [1]. Various malignancies treated in referral centers [11]. Our aim is to review
mechanisms may be involved in a given patient, leading to quali- available recommendations regarding vaccination in the following
tative and/or quantitative immune deficiency [2]. In patients with immune deficient conditions: 1) asplenia, 2) cancer, 3) HIV, 4) he-
solid tumors receiving chemotherapy, the relative risk (RR) of matopoietic stem cell and solid organ transplantation, 5) inflam-
invasive pneumococcal infection is nearly multiplied by 23, and matory bowel diseases (IBD), 6) primary immune deficiency, 7)
even close to 50 in case of HIV infection [3], compared to general psoriasis and 8) inflammatory rheumatic diseases (IRD).
population. Among asplenic patients, consequences could be
deadly, due to increased risk of pneumococcal sepsis with a mor-
2. Materials and methods
tality rate up to 60% [4,5]. Patients with hematologic malignancies
and solid tumors are at increased risk of influenza-related com-
2.1. Data sources and searches
plications [6]. Hospitalization is required in 14e21% of cases, and
mortality rate ranges between 8 and 50%, higher in HIV patients
A literature search was conducted on PubMed, EMBASE,
compared to oncologic patients [7]. Vaccination against influenza is
Cochrane Library, and in main professional society websites
effective in immunocompromised patients, with a reduction of 85%
including the World Health Organization (WHO) and the National
of laboratory-confirmed infections compared to placebo [8]. How-
Institute for Health and Care Excellence (NICE), and websites from
ever, seroprotection appears significantly lower in immunocom-
each medical specialty such as oncology-hematology, gastroenter-
promised than in immunocompetent patients [9] raising the
ology, infectious diseases, dermatology and rheumatology issued
interest for alternative strategies aiming to improve vaccination
from any country worldwide. We used the following search terms:

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12 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27
((“Vaccination”[Mesh]) OR “Vaccines”[Mesh]) AND “Guideline”
[Publication Type]. The last research was conducted on January, the
31st of 2016.
2.2. Study selection
Only guidelines focusing on recommendations for vaccination
in adult patients (18 years) were selected. The search was
limited to English and French language documents published
between January 1, 2005 and January, the 31st of 2016. Only the
last update of guidelines was included in this article. We did not
include sub-national recommendations, such as American states'
guidelines.
2.3. Data extraction
Titles and abstracts identified by the literature searches were
screened by two independent reviewers (AL and LPB), who con-
ducted a full-text review to determine inclusion eligibility. All ci-
tations whose abstract or full text was not available were excluded.
Discrepancies regarding inclusion criteria were resolved through
consensus.
2.4. Data synthesis and analysis
The following information was extracted from each included
article: name of the learned society, country of origin, year of
publication, and recommendation for vaccination. We summarized
all vaccination recommendations listed by the type of immuno-
suppression: asplenia, cancer, HIV, hematopoietic stem cell trans-
plantation, IBD, primary immune deficiency, psoriasis, IRD, and
solid organ transplantation. In each immunocompromised group of
patients, vaccination recommendations were listed by type of
vaccine: live vaccines and inactivated vaccines. The current study
was performed in accordance with the Cochrane Handbook guid-
ance [12] and the PRISMA (Preferred Reporting Items for Systematic
reviews and Meta-Analyses) statement [13].
3. Results
3.1. Literature search results
During the last decade, 389 citations were identified on Med-
line, Embase and Cochrane, using the search keywords listed above
(Appendix Fig. 1). After reviewing the title and/or the abstract of the
389 citations that were identified using the predefined search
terms, a total of 12 guidelines were selected in this systematic re-
view. Reasons for exclusion were: irrelevant articles (n ¼ 149) (e.g.
management of infectious diseases, reports, safety studies, position
on only one vaccine …), guidelines in non-immunocompromised
patients (n ¼ 82), pediatric guidelines (n ¼ 61), non-English or
French language guidelines (n ¼ 42), animal recommendations
(n ¼ 20), duplicates (n ¼ 10), reviews (n ¼ 6), guidelines' evalua-
tions (n ¼ 5), sub-national recommendations (n ¼ 2). During search
from the professional societies websites of each specialty, 3 addi-
tional guidelines were selected, including the 2014 Canadian
Immunisation Guide, the 2015 Australian Immunisation Handbook
and the 2014 French recommendations for vaccination of immu-
nocompromised or asplenic patients. Thus, a total of 15 guidelines
were included in this systematic review: US (n ¼ 6) [14e19], UK
(n ¼ 2) [20,21], European (n ¼ 2) [22,23], Canadian (n ¼ 1) [24],
Australian (n ¼ 1) [25], French (n ¼ 1) [26], German-Austrian-Swiss
(n ¼ 1) [27] and German (n ¼ 1) [28] recommendations. Overall, 19
learned societies provided recommendations on vaccination in
different situations of immunosuppression: asplenia (n ¼ 5)
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[14,20,24e26], cancer (n ¼ 4) [14,24e26], HIV (n ¼ 5)
[14,21,24e26], hematopoietic stem cell transplantation (n ¼ 4)
[15,25e27], IBD (n ¼ 5) [16,22,24e26], psoriasis (n ¼ 4) [17,24e26],
primary immunosuppression (n ¼ 3) [14,24,26], IRD (n ¼ 6)
[14,19,23e26] and solid organ transplantation (n ¼ 5)
[14,18,24e26]. Six different specialties (infectious diseases, hema-
tology, gastroenterology, dermatology, rheumatology and epide-
miology) have developed guidelines on vaccination of
immunocompromised patients. For each specialty, we could iden-
tify the following learned societies:
- The IDSA (Infectious Diseases Society of America), the AMMI
(Association of Medical Microbiology and Infectious Diseases), the
BHIVA (British HIV Association), the ACIP (Advisory Committee on
Immunisation Practices), the ATAGI (Australian Technical Advisory
Group on Immunisation), the SIKO (Vaccination Committee for the
State of Saxony) and the STIKO (Standing Committee on Vacci-
nation of the Robert Koch Institute) for infectious diseases.
- The BCSH (British Committee for Standards in Haematology), the
CIBMTR (Center for International Blood and Marrow Transplant
Research), the NMDP (National Marrow Donor Program), the
EBMT (European Blood and Marrow Transplant), the ASBMT
(American Society for Blood and Marrow Transplant), the CBMTG
(Canadian Blood and Marrow Transplant Group), the DAGKBT
(German working group on bone marrow and blood stem cell
transplantation), the DGHO (German Society of Hematology and
Oncology), the ASHO (Austrian Society of Hematology and
Oncology), the SBST (Swiss Blood Stem Cell Transplantation
Group), the Pa €d-AG-KBT (GermaneAustrianeSwiss Pediatric
Working Group on bone marrow and blood stem cell trans-
plantation) for hematology.
- The ECCO (European Crohn's and Colitis Organization) for
gastroenterology.
- The NPF (National Psoriasis Foundation) for dermatology.
- The EULAR (European League Against Rheumatism) and the ACR
(American College of Rheumatology) for rheumatology.
- The SHEA (Society for Healthcare Epidemiology of America) for
epidemiology.
Additionally, three national agencies provided recommenda-
tions on vaccination for immunocompromised patients: the CDC
(Centers for Disease Control and Prevention), the PHAC (Public Health
Agency of Canada), and the HCSP (Haut Conseil de la Sant
e Publique
or Public Health Council).
3.2. Asplenic patients (Appendix Table 1)
See Appendix.
3.3. Patients with oncologic malignancies
Four guidelines are currently available in patients with
neoplasia treated with chemotherapy [14,24e26] (Table 1). All live
vaccines are not recommended during chemotherapy and after
cancer chemotherapy [14,24e26] but some of them are possible
respecting a delay after the end of chemotherapy. In US and French
guidelines, BCG (bacillus Calmette-Gue
rin) administration is not
recommended during or after chemotherapy [14,26], but possible
three months after treatment in Canadian and Australian guide-
lines [24,25]. This delay of three months after chemotherapy is also
the most recommended for the measles, mumps, and rubella
(MMR), the varicella, the rotavirus, the intranasal influenza and the
yellow fever vaccinations. However, in the French guidelines, a
waiting period of 12 months is encouraged for the varicella vacci-
nation. Also, a waiting period of 6 months is recommended for the
 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27 13

Table 1
Vaccination recommendations in cancer patients.

Professional society, country, year

IDSA, U.S.A., 2013 PHAC, Canada, 2014 ATAGI, Australia, 2015 HCSP, France, 2014

Vaccine
Live vaccines
BCG (Bacillus Calmette-
Gu

erin)
Measles, mumps, and rubella
Varicella
Rotavirus
Influenza (intranasal)
Yellow fever
Inactivated vaccines
Tetanus-diphteria-acellular
pertussis (Tdap)-polio
Haemophilus influenzae type b
Hepatitis B
Meningococcal vaccination
Pneumococcal vaccination
Human papillomavirus
Influenza (injectable)
Hepatitis A
Not recommended Not recommended during CT but possible 3 months Not recommended during or after CT
during or after CT after CT treatment treatment
treatment
Not recommended during CT but possible 3 months after CT treatment
Not recommended during CT but possible 3 months after CT treatment Not recommended during CT but
possible 12 months after CT treatment
Not recommended Not recommended during CT but possible 3 months Not recommended during or after CT
during or after CT after CT treatment treatment
treatment
Not recommended Not recommended during CT but possible 3 months Not recommended during CT but
during CT treatment after CT treatment possible 6 months after CT treatment
Not recommended during CT but possible 3 months after CT treatment Not recommended during CT but
possible 6 months after CT treatment
Not recommended during CT but possible 3 months Not recommended but Not recommended during CT but
after CT treatment possible during CT possible 3 months after CT treatment
treatment
Not recommended during CT but possible 3 months Not recommended but Not recommended during CT but
after CT treatment possible CT treatment possible 3 months after CT treatment
Not recommended during CT but possible 3 months Not recommended but Recommended during CT for at risk
after CT treatment possible during CT patients, with a supplementary
treatment injection 6 months CT treatment
Not recommended during CT but possible 3 months Not recommended but MenC: not recommended during CT, 3
after CT treatment possible during CT months after CT treatment, a single
treatment dose is recommended
MenACWY (2 doses with an interval of 8
weeks: not recommended except for
asplenic, immunocompromised,
international travelers)
Recommended 2 weeks before CT treatment, with Not recommended but Recommended 2 weeks before CT
PCV13 and PPSV23 8 weeks later possible during CT treatment, with PCV13 and PPSV23 8
treatment weeks later
Not recommended during CT but possible 3 months Not recommended but Not recommended during CT but
after CT treatment possible during CT possible 3 months after CT treatment
treatment
A single dose of influenza vaccination is recommended 2 doses at least 4 weeks Recommended during CT and during
annually apart are the 6 months after (a second dose is
recommended, and 1 possible at least 1 month after if
dose annually patients were vaccinated at the
thereafter beginning of the epidemic period)
Not recommended during CT but possible 3 months Not recommended but Not recommended during CT but
after CT treatment possible during CT possible 3 months after CT treatment
treatment for at risk patientsa

IDSA, Infectious Diseases Society of America; PHAC, Public Health Agency of Canada; ATAGI, Australian Technical Advisory Group on Immunisation; HCSP, Haut Conseil de la
Sante
Publique; CT, chemotherapy; MenC, meningococcal C vaccination; MenACWY, quadrivalent meningococcal vaccination; PCV13, 13-valent pneumococcal conjugate
vaccine; PPSV23, 23-valent pneumococcal polysaccharide vaccine.
a
Young handicapped people, cystic fibrosis, hepato-biliary diseases with a risk of cirrhosis, men who have sex with men, family of patients infected with hepatitis A, young
children and handicapped people workers, waste water workers.

intranasal influenza and the yellow fever vaccinations [26]. For
inactivated vaccines, Tdap-polio (tetanus, diphtheria, acellular
pertussis and polyomyelitis) and Hib (Haemophilus influenzae type
b) are not recommended but possible three months after the end of
chemotherapy [14,24,26], or even during chemotherapy (only for
the Australian guidelines) [25]. Hepatitis B vaccination is not rec-
ommended, except in French guidelines, for at risk patients, with a
supplementary injection six months after the end of chemotherapy
[26]. Meningococcal, hepatitis A and human papillomavirus (HPV)
vaccinations are not recommended during chemotherapy
[14,24e26]. For a majority of learned societies, pneumococcal
vaccination is recommended two weeks before chemotherapy with
PCV13, and PPSV23 eight weeks after, regardless patient's age
[14,24,26]. Finally, injectable influenza is unanimously recom-
mended annually, with different regimen depending on learned
societies [14,24e26].
3.4. HIV patients
Five guidelines provided guidelines for immunisation of HIV-
infected adults [14,21,24e26] (Table 2). Concerning live vaccines,
BCG is strictly contraindicated regardless of the CD4 level
[14,21,24e26]. Rotavirus vaccination is not recommended
[14,21,24e26]. Yellow fever vaccination is not recommended but
possible if CD4 200/mm3, especially in at risk patients [21,25,26].
All learned societies agree that varicella-zoster vaccine must be
considered if CD4 200/mm3, in particular in patients over 50 years
[25]. It is the same for the MMR vaccination [14,21,24e26]. For
inactivated vaccines, Tdap-polio, hepatitis B, pneumococcal and
injectable influenza vaccinations are universally recommended
[14,21,24e26]. Hib vaccination in HIV patients is only recom-
mended by the Public Health Agency of Canada [24]. Some learned
societies advised vaccinating against meningococcal infection with
MenC in patients under 25 years and with MenACWY in at risk

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14 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27

Table 2
Vaccination recommendations in HIV patients.

Professional society, country, year

IDSA, U.S.A., 2013 BHIVA, U.-K., 2008 PHAC, Canada, 2014 ATAGI, Australia, 2015 HCSP, France, 2014

Vaccine
Live vaccines
BCG (bacillus Calmette- Contraindicated
Gu

erin)
Measles, mumps, and Recommended if CD4 200/mm3a Recommended if CD4 Recommended if CD4 200/mm3a
rubella Contraindicated if CD4 <200/mm3 200/mm3 and 15% CD4a Contraindicated if CD4 <200/mm3
Contraindicated if CD4
<200/mm3
Varicella-zoster Recommended if CD4 Recommended if CD4 Recommended if CD4 Recommended if CD4 Recommended if CD4
200/mm3a 400/mm3 but also 200/mm3 and 15% CD4a 200/mm3a 200/mm3a
consider if  200/mm3a Contraindicated if CD4 Contraindicated if CD4 Contraindicated if CD4
Contraindicated if CD4 <200/mm3 <200/mm3 <200/mm3
<200/mm3 Zoster vaccine in patients
50 years
Rotavirus Not recommended
Yellow fever Not recommended but Consider if at true risk of Possible if CD4 200/mm3 Consider in at risk patients Recommended in patients
possible if CD4 200/ infection and if CD4 200/ Contraindicated if CD4 and if CD4 200/mm3 living in French Guiana
mm3 mm3 <200/mm3 Contraindicated if CD4 Contraindicated if CD4
Contraindicated if CD4 Contraindicated if <200/mm3 <200/mm3
<200/mm3 aged > 60 years or CD4
<200/mm3
Inactivated vaccines
Tetanus-diphteria- Recommended Recommended (3 doses at Recommended Recommended (with a
acellular pertussis (Tdap)- least 1 month apart, with a booster dose every 10
polio booster dose at 5 and 10 years)
years)
Haemophilus influenzae b Not recommended Recommended (1 dose) Not recommended
Hepatitis B Recommended (3 high Recommended (3 doses Recommended (3 high Recommended (4 double doses at 0, 1, 2 and 6 months)
doses of 40 mg; a second with Ig anti-HBs ± a booster doses of 40 mg; a second
scheme is dose and Ig anti-HBs in scheme is recommended if
recommended if anti- non-responders anti-HBs <10mUI/mL 1e2
HBs <10mUI/mL 1e2 months after)
months after)
Meningococcal Not recommended MenC is recommended Recommended Recommended (MenC and MenC is recommended
vaccination <25years or at risk patients (MenACWY) MenACWY) <25years
(one or 2 doses in asplenic MenACWY is
patients) recommended in
MenACWY in at risk complement deficit or
patients (one dose with a asplenic patients
booster dose 5 years after)
Pneumococcal vaccination Recommended (one Recommended if CD4 Recommended (one dose of PCV13, one dose of PPSV23 8 Recommended (one dose of
dose of PVC13, one dose 200/mm3 weeks later, with a booster dose 5 years after) PCV13, one dose of PPSV23
of PPSV23 8 weeks Consider if CD4 <200/mm3 8 weeks later)
later, with a booster (one dose of PPSV23, with a
dose 5 years after) booster dose every 5e10
years)
Human papillomavirus Recommended in Not recommended Recommended (HPV4 at 0, 2, and 6 months) Recommended in females
females and males and males (HPV4 at 0, 2,
(HPV4 at 0, 2, and 6 and 6 months)
months)
Influenza (injectable) Recommended (annual vaccine with the TIV) Recommended (annual Recommended (annual
vaccine with the TIV, with vaccine with the TIV)
initially 2 doses 4 weeks
apart if CD4 <200/mm3)
Hepatitis A Not recommended Recommended in at risk Recommended in at risk Recommended in at risk Recommended in at risk
patients (2 doses at 0 and 6 patientsb (2 doses at 0 and 6 patientsc (2 doses at 0 and 6 patientsd (2 doses at 0 and 6
e12 months if CD4 > 300/ e12months) e12months) e12months)
mm3, 3 doses over 6e12
3
months if CD < 300/mm ,
with a booster dose every 5
years. Consider Ig in very
high risk patients

IDSA, Infectious Diseases Society of America; BHIVA, British HIV Association; PHAC, Public Health Agency of Canada; ATAGI, Australian Technical Advisory Group on
Immunisation; HCSP, Haut Conseil de la Sante
Publique; MenC, meningococcal C vaccination; MenACWY, quadrivalent meningococcal vaccination; PCV13, 13-valent
pneumococcal conjugate vaccine; PPSV23, 23-valent pneumococcal polysaccharide vaccine; HPV4, quadrivalent HPV vaccine; TIV, trivalent inactivated vaccine.
a
In patients without protective antibodies.
b
Travellers to areas of high or intermediate endemicity those who were born in or lived for extensive periods in geographic areas that have a high to-intermediate
endemicity of HAV infection, patients living close to infected persons, men who have sex with men, IV drug users, hepatitis B or C, chronic liver disease, hemophilic, vets
and zoo workers, researchers on HAV.
c
Travellers to areas of high or intermediate endemicity those who were born in or lived for extensive periods in geographic areas that have a high to-intermediate
endemicity of HAV infection, men who have sex with men, injecting drug users and persons above the age of 50 years.
d
Hepatitis B or C, chronic liver disease, men who have sex with men, IV drug users.

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 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27
patients [21,26], whereas other guidelines recommended this
vaccination in all HIV patients, either with MenACWY [24] or with
MenC then MenACWY [25]. Quadrivalent HPV vaccine is almost
recommended in all guidelines, with a three injections scheme at
zero, two, and six months [14,24e26]. Most of learned societies
agree with a targeted vaccination against hepatitis A, in at risk
patients (e.g. travelers to areas of high or intermediate endemic,
those who were born in or lived for extensive periods in geographic
areas that have a high to-intermediate endemic risk of HAV infec-
tion, men who have sex with men, injecting drug users, and persons
above the age of 50 years) [21,24e26].
3.5. Hematopoietic stem cell recipients
Two international consensus [15,27] and two national agencies
websites [25,26] exposed their recommendations for vaccinating
hematopoietic stem cell recipients (Appendix Table 2). BCG is
universally contraindicated [15,25e27]. MMR vaccine was advised
in seronegative patients with one or two doses at least 24 months
after stem cell transplantation in three guidelines [15,25,26]
whereas it was not recommended but possible for the remaining
one [27]. Zoster vaccination was not recommended whereas vari-
cella vaccine was sometimes recommended in seronegative pa-
tients at least 24 months after transplantation [25,26]. Rotavirus
and yellow fever vaccinations were never advised but the latter
remains possible in patients residing in or traveling to endemic
areas respecting a period of 24 months after the stem cell trans-
plantation [15,26]. Tdap-polio, Hib, pneumococcal and influenza
vaccines are universally recognized as essential in case of stem cell
transplantation [15,25e27], with a minimum period of six months
after the treatment, even if some learned societies authorized a
period of three months for the pneumococcal vaccination [15,26].
Most of guidelines recommended the hepatitis B vaccination in
seronegative patients at least six months after the stem cell
transplantation [24,26,27], generally with a three doses scheme in
monthly intervals, with a booster dose 18 months after the trans-
plantation [26,27]. Meningococcal vaccination was recommended
in Australian and French guidelines, with two different protocols
[25,26]. HPV vaccine was recommended by the ATAGI in at risk
patients (likelihood of previous exposure to HPV, future risks of
HPV exposure, extent/duration of immunosuppression), at least 12
months after the transplantation with three doses at zero, two, and
six months [25]. French authorities recommended the same
scheme, at least 6 months after transplantation, and only in females
[26]. Finally, protection against the hepatitis A was not recom-
mended but possible 6e12 months after the stem cell trans-
plantation in patients living in or traveling to endemic areas or in
patients on risk due to occupational exposure starting [27]. Three
doses in monthly intervals are recommended, with a booster dose
18 months after the transplantation [27].
3.6. Inflammatory bowel disease patients
In these patients, six guidelines about vaccination are currently
available (Table 3) [16,22,24e26,28]. All live vaccines are contra-
indicated in case of immunosuppressive therapy [16,22,24e26].
Half of guidelines recommended MMR and varicella-zoster vacci-
nations before starting immunosuppressive therapy [16,22,28]. The
period between vaccination and the first administration of treat-
ment varied between two weeks in the German guidelines [28] to
one to three months in the U.S. guidelines [16]. Rotavirus and yel-
low fever vaccines were universally not recommended
[16,22,24e26,28]. Pneumococcal and influenza vaccinations were
the only two recommended in all guidelines [16,22,24e26,28]. For
pneumococcal infection prevention, the most advised scheme was
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15
one dose of PCV13 then one dose of PPSV23 eight weeks after, with
a booster dose of PPSV23 five years later [16,22,24e26]. Concerning
influenza, a single dose of the trivalent inactivated vaccine was
recommended every year [16,22,24e26,28]. The Tdap-polio vacci-
nation was recommended in three guidelines if it was not given
over the past ten years [16,26,28]. Only one professional society
agreed with a vaccination against Hib, in analogy to anti-
pneumococcal vaccine, with a single dose in patients under an
immunosuppressive therapy [28]. Meningococcal [28] and hepati-
tis A vaccines [16] were also poorly recommended. Both U.S. and
European guidelines advised the hepatitis B vaccination with a
three doses scheme [16,22]. Interestingly, if no response is observed
one month after finishing last dose, revaccinating with a double
dose scheme is recommended [16,22]. HPV vaccination with a three
doses regimen (0, two and six months) was recommended in three
guidelines [16,22,25].
3.7. Primary immunocompromised patients (Appendix Table 3)
See Appendix.
3.8. Patients with psoriasis (Appendix Table 4)
See Appendix.
3.9. Inflammatory rheumatic disease patients
Six guidelines are currently available about vaccination in IRD
patients (Appendix Table 5) [14,19,23e26]. As above, most of live
vaccines are not recommended and even contraindicated in case of
immunosuppressive therapy, but there were some exceptions. First,
varicella vaccine should be considered for patients without evi-
dence of varicella immunity at least four weeks prior to initiation of
immunosuppression [14], especially after 50 years [19]. Second,
zoster vaccination should be considered for patients beyond 60
years prior to initiation of treatment or being treated with low-dose
of immunosuppressive therapy, and those who aged 50e59 years
and varicella positive prior to initiation of treatment or being
treated with low-dose of immunosuppressive therapy 4 weeks
prior to initiation of treatment [14]. In European guidelines, zoster
vaccine may be considered in mildly immunocompromised pa-
tients (e.g. patients treated with short-term corticosteroid therapy
[<14 days], low to moderate doses of corticosteroids [<20 mg/day
of prednisone or equivalent], intra-articular, bursal or tendon cor-
ticosteroids injections, long-term alternate-day treatment with low
to moderate doses of short-acting systemic corticosteroids, therapy
with methotrexate [<0.4 mg/kg/week], azathioprine [<3.0 mg/kg/
day] or 6-mercaptopurine [<1.5 mg/kg/day]) who are seropositive
for varicella zoster antibodies [23]. Third, the MMR vaccine may be
considered in mildly immunosuppressed patients on a case-by-
case basis [23]. All guidelines added that live vaccines were con-
traindicated in highly immunocompromised patients, that is, pa-
tients treated with corticosteroids, TNFa blocking agents and non-
biological disease-modifying antirheumatic drugs, particularly
cyclophosphamide, azathioprine and leflunomide [14,23e26].
Pneumococcal and influenza vaccinations were universally rec-
ommended, with administration protocols described above
[14,23e26]. On the other hand, Hib and meningococcal vaccines
were not recommended [14,23e26]. Tdap-polio must be consid-
ered according to the French guidelines if it was not given over the
past ten years [26]. Moreover, in case of major and/or contaminated
wounds in patients who received rituximab within the last 24
weeks, tetanus immunoglobulin should be administered [23].
Several guidelines also underlined that response to certain killed
vaccines may be reduced after rituximab therapy [19,23]. European
 Table 3

16
Vaccination recommendations in inflammatory bowel disease patients.

Professional society, country, year

ACIP, U.S.A., 2010 ECCO, Europe, 2014 PHAC, Canada, 2014 ATAGI, Australia, 2015 HCSP, France, 2014 STIKO, Germany, 2010
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Vaccine
Live vaccines
BCG (Bacillus Calmette- Not recommended
Gu

erin) Contraindicated during IT
Measles, mumps, and Recommended at least 6 weeks Recommended at least 3 Not recommended Recommended at least 2
rubella before starting IT weeks before starting IT Contraindicated during IT weeks before starting IT
Contraindicated during IT Contraindicated during IT Contraindicated during IT
Varicella-zoster Recommended at least 1e3 months Recommended at least 3 Not recommended Recommended at least 2
For personal use only. No other uses without permission. Copyright ©2018. Elsevier Inc. All rights reserved.

Rotavirus
Yellow fever
Inactivated vaccines
Tetanus-diphteria-
before starting IT weeks before starting IT Contraindicated during IT weeks before starting IT
Contraindicated during IT Contraindicated during IT Contraindicated during IT
Not recommended
Contraindicated during IT
Not recommended
Contraindicated during IT
Administer vaccine if not given over Not recommended but possible during IT Administer vaccine if not given over the past 10 years, with

A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27

acellular pertussis (Tdap)- the past 10 years or give Tdap if a booster dose every 10 years
polio Td  2 years, with a booster dose Possible during IT
every 10 years
Haemophilus influenzae b Not recommended but possible during IT A single dose is
recommended in patients
with IT
Hepatitis B Recommended (3 doses at 1, 1e2 Recommended (double Not recommended but possible during IT
and 4e6 months; if no response 1 dose at 0,1 and 2 months; if
month after finishing last dose thenno response 1 month after
revaccinate with double dose) finishing last dose then
Possible during IT revaccinate with double
dose)
Possible during IT
Meningococcal Not recommended but possible during IT A single dose of Men ACWY
vaccination is recommended in patients
with IT
Pneumococcal vaccination Recommended (PCV13 and PPSV23 8 weeks later; re-vaccinate with a single dose of PPSV23 5 Recommended (PCV13 and Recommended (PCV13 and Recommended (a single
years after) PPSV23 8 weeks later; PPSV23 8 weeks later; re- dose of PPSV23, with a
Possible during IT second dose of PPSV23 5 vaccinate with a single dose second dose 5 years in case
e10 years after, third dose of PPSV23 5 years after) of IT)
at 65 years) Possible during IT Possible during IT
Possible during IT
Human papillomavirus Recommended through age 26 years (3 doses 0,2 and 6 months Not recommended but Recommended through age Not recommended but possible during IT
with HPV4) possible during IT 18 years in patients with IT
Possible during IT (3 doses 0,2 and 6 months
with HPV4)
Possible during IT
Influenza Recommended (annual vaccine with the TIV)
Possible during IT
Hepatitis A Recommended (2 doses at 0 and 6 Not recommended but possible during IT
e12 months or 0 and 12e18
months with a booster dose > 10
years)
Possible during IT

ACIP, Advisory Committee on Immunisation Practices; ECCO, European Crohn's and Colitis Organization; PHAC, Public Health Agency of Canada; ATAGI, Australian Technical Advisory Group on Immunisation; HCSP, Haut Conseil

Publique; STIKO, Vaccination Committee of the State of Saxony; IT, immunosuppressive therapy; MenACWY, quadrivalent meningococcal vaccination; PCV13, 13-valent pneumococcal conjugate vaccine; PPSV23, 23-
de la Sante
valent pneumococcal polysaccharide vaccine; HPV4, quadrivalent HPV vaccine; TIV, trivalent inactivated vaccine.
 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27 17

guidelines recommended the hepatitis A and B vaccines in at risk
patients when protective antibodies were absent [23], whereas
American guidelines only recommended the hepatitis B vaccination
if risk factors were present such as intravenous drug users, persons
with multiple sex partners in the previous 6 months, or health care
personnel [19]. Concerning HPV immunisation, it was recom-
mended in three guidelines [19,23,25].
3.10. Solid organ transplant recipients
In this situation, five guidelines are currently available (Table 4)
[14,18,24e26]. Varicella vaccine was universally recommended
before transplantation but not after [14,18,24e26]. Three learned
societies advised a zoster vaccination before transplantation,
especially in patients over 60 years [14,18,24]. The MMR vaccine

Table 4
Vaccination recommendations in solid organ transplant recipients.

Professional society, country, year

AST, U.S.A., 2009 IDSA, U.S.A., 2013 PHAC, Canada, 2014 ATAGI, Australia, 2015 HCSP, France, 2014

Vaccine
Live vaccines
BCG (Bacillus Recommended before Not recommended before Possible if indicated before transplantation Contraindicated before
Calmette-Gu
erin) transplantation transplantation Contraindicated after transplantation transplantation
Not recommended after Not recommended after Possible if indicated before transplantation Contraindicated after
transplantation transplantation Contraindicated after transplantation transplantation
Measles, mumps, and Recommended before Not recommended before Recommended before Recommended before transplantation
rubella transplantation transplantation transplantation Contraindicated after transplantation
Not recommended after Not recommended after Not recommended after
transplantation transplantation transplantation
Varicella-zoster Varicella: recommended before transplantation not Varicella: recommended Varicella: recommended before transplantation
recommended after transplantation before transplantation not contraindicated after transplantation
Zoster: recommended before transplantation in patients recommended after Zoster: not recommended before transplantation not
60 years not recommended after transplantation transplantation recommended after transplantation
Zoster: recommended
before transplantation not
recommended after
transplantation
Rotavirus Recommended before Not recommended before Recommended before Not recommended before transplantation
transplantation transplantation transplantation Not recommended after transplantation
Not recommended after Not recommended after Not recommended after
transplantation transplantation transplantation
Yellow fever Possible before Not recommended before Possible if indicated before Not recommended Possible before
transplantation in patients transplantation transplantation before transplantation transplantation in patients
traveling to endemic areas Not recommended after Contraindicated after Not recommended after native or traveling to
Not recommended after transplantation transplantation transplantation endemic areas
transplantation Contraindicated after
transplantation
Inactivated vaccines
Tetanus-diphteria- Recommended before Not recommended before Recommended before transplantation
acellular pertussis transplantation transplantation Recommended after transplantation
(Tdap)-polio Recommended after Not recommended after
transplantation transplantation
Haemophilus Not recommended before transplantation Recommended before Not recommended before transplantation
influenzae b Not recommended after transplantation transplantation Not recommended after transplantation
Recommended after
transplantation
Hepatitis B Recommended before transplantation
Recommended after transplantation
Meningococcal Recommended before or Not recommended before Recommended before or after transplantation in at risk patientsa
vaccination after transplantation in at transplantation
a
risk patients Not recommended after
transplantation
Pneumococcal Recommended before transplantation
vaccination Recommended after transplantation
Human Recommended before or Recommended before or Recommended before Recommended before Recommended before or
papillomavirus after transplantation in after transplantation in transplantation or after transplantation after transplantation in
females aged 9e26 years females aged 11e26 years Recommended after in females aged >9 females aged 9e19 years
transplantation years
Influenza (injectable) Recommended before transplantation
Recommended after transplantation
Hepatitis A Recommended before transplantation Recommended before or Recommended before Recommended before or
Recommended after transplantation after transplantation in or after transplantation after transplantation in
patients with chronic liver in patients with chronic patients with chronic liver
disease or traveling to liver disease, chronic B disease, chronic B or C
endemic areas (with or C hepatitis, liver hepatitis, drug users, men
immunoglobulins) recipients, transplant who have sex with men,
candidates traveling to endemic areas

AST, American Society of Transplantation; IDSA, Infectious Diseases Society of America; PHAC, Public Health Agency of Canada; ATAGI, Australian Technical Advisory Group on
Immunisation; HCSP, Haut Conseil de la Sante
Publique.
a
Members of the military, travelers to high risk areas, properdin deficient, terminal complement component deficient, those with functional or anatomic asplenia, and
college freshman living on campus.

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18 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27
was mostly recommended before transplantation [18,24e26].
Concerning BCG, recommendations were very heterogeneous,
some of them advised a pre-transplantation vaccination, but only
when exposure to tuberculosis is unavoidable and when measures
to prevent its spread have failed or are not possible [18]. Other
guidelines considered BCG as possible if indicated [24,25], other did
not recommended it [14] and other contraindicated it [26]. The
rotavirus vaccination was mostly not recommended before or after
transplantation [14,25,26], as the yellow fever vaccine, but the
latter was possible before transplantation in patients native or
traveling to endemic areas and without an immunosuppressive
therapy [18,24,26]. Before transplantation, pneumococcal, inject-
able influenza and HPV vaccines were universally recommended
[14,18,24e26]. An immunisation against the hepatitis A was
advised, especially in at risk patients (e.g. chronic liver disease,
patients traveling to endemic areas, drug users, men who have sex
with men, …) [14,18,24e26]. Four guidelines recommended a
meningococcal vaccination, especially in at risk patients (e.g.
members of the military, travelers to high risk areas, properdin
deficient, terminal complement component deficient, those with
functional or anatomic asplenia, and college freshman living on
campus, …) [18,24e26]. Tdap-polio vaccination was mostly rec-
ommended, before or after transplantation [18,24e26]. Finally, the
Hib vaccine was poorly recommended [24].
4. Discussion
Many of our patients have an immunosuppression state,
inherited [29] or due to several drugs prescribed for a malignancy
[30], a chronic inflammatory disease [31] or after transplantation
[32]. In these situations, there is a significant increase of life
threatening infections [5,7]. Vaccines can decrease the mortality
risk associated with infection-related complications, but vaccina-
tion coverage appears low in immunosuppressed patients. In some
countries, a sense of mistrust exists against vaccines. For example, a
potential increased risk of central nervous system demyelinating
diseases was pointed out with hepatitis B vaccine. However, a
systematic review published in 2013 including 12 studies, did not
find any association between the onset or relapse of these affec-
tions and hepatitis B vaccination [33]. Guidelines are a valuable tool
to help clinicians translate best research evidence into best prac-
tice, improving the quality of care and patient outcomes. We pre-
sented here a systematic review and a comprehensive field
synopsis of all guidelines published over the past decade about
vaccination in all types of immunocompromised patients. A field
synopsis must follow rigid methodology to make the literature
review complete, unbiased, objective, transparent, and repeatable.
Usually, it is too large and broad in scope, thus formal meta-analysis
(e.g. quantitative synthesis) cannot be used. To our knowledge, this
is the first systematic review addressing this issue.
In general, live vaccines are contraindicated in patients under
immunosuppressive therapy or in HIV patients with a CD4 count
under 200/mm3 [34]. This is also valid for non-HIV patients with
less than 200/mm3 CD4 due to an immunosuppressive therapy.
Serious adverse events are possible, especially with BCG and
disseminated infections in children with a severe combined im-
munodeficiency [35]. One fatal case was also reported in infants
born to mothers taking infliximab for Crohn's disease [36].
Although live vaccines are not recommended, there are few ex-
ceptions where they can be administered. The MMR and the vari-
cella vaccine are often recommended in seronegative patients
before transplantation or those with psoriasis and HIV. In a sys-
tematic review conducted in renal transplant recipients, overall
mortality rate was 30% in case of disseminated varicella zoster virus
infection [37]. This poor prognosis should prompt to better
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immunisation coverage for VZV. Interestingly, in a recent large
survey from Medicare of VZV vaccination in patients with auto-
immune diseases, more than 600 patients treated with anti-TNF
received it and achieved the same protection and the same safety
as the whole population without high immunosuppression [38].
Non-live peptidic vaccine for VZV could solve this issue [39]. In the
same way, HIV patients can develop severe forms of MMR infection,
but only half of them were vaccinated in an Austrian cohort of 713
patients [40]. In case of deep immunosuppression, as HIV or
transplant patients, the yellow fever vaccine can be considered, but
only if a true risk of infection exists (e.g. patients residing in or
traveling to endemic areas). Safety profile of yellow fever vaccine
seems acceptable in solid organ recipients [41]. The rotavirus
vaccination was never recommended, except in one guideline in
solid organ recipients [24].
Pneumococcal vaccination is universally recommended in all
immunocompromised patients. In a multicenter observational
prospective study including almost 800 cases of invasive pneu-
mococcal infection, mortality rate was 9% in the general popula-
tion compared to 24% in the immunosuppressed population [42].
Moreover, pneumococcal disease carries a high economic burden.
Direct healthcare costs were $3.5 billion in the USA in 2004 [43].
They will increase annually by $2.5 billion until 2040, essentially
due to the population ageing [44]. Despite these alarming data,
vaccine utilization appears dramatically low. For PCV13, it was
56.6% vs 64.5% in immunosuppressed and general population,
respectively (p ¼ 0.05) [42]. All guidelines recommended a
vaccination scheme with PCV13 then PPSV23 at least eight weeks
after the first dose, with booster doses of PPSV23 every five years.
This strategy improves efficacy of vaccination due to comple-
mentary mechanisms of action of these two vaccines. It should be
pointed out that in case of prescription of rituximab, first pneu-
mococcal vaccination must be made at least two to three weeks
before initiation of treatment otherwise the immune response
will be nil.
Influenza vaccination is recommended for immunocompro-
mised patients in all guidelines. In a population-based study con-
ducted in almost 14,000 influenza-like illness patients, influenza
virus was detected in 28% of cases [45]. As described above, inci-
dence of influenza in immunosuppressed patients is nearly twice
than the general population. Moreover, hospitalization and mor-
tality rates can be as high as 20% and 50%, respectively [7]. A recent
meta-analysis showed that efficacy and safety of the influenza
vaccine in immunocompromised patients were adequate [46]. In
our systematic review, some learned societies recommended a two
doses regimen separated by four weeks, especially in cancer pa-
tients or in hematopoietic stem cell recipients [25]. In a randomized
controlled-study conducted in 85 immunocompromised patients
(27 with leukemia, 17 with solid tumor, and 41 with HIV), two doses
of high-dose influenza vaccine were compared to a standard-dose
regimen [47]. Seroconversion and seroprotection were signifi-
cantly higher in the high-dose group in leukemia patients. In a
multicentric European study, only 35.6% of high-risk patients
received an influenza vaccination [48]. This is far away from the EU
Council's recommendations, which planned a vaccination coverage
rate of 75% in risk groups [49]. However, optimal vaccination
coverage could prevent each year at least 3.2 million cases of
influenza, 69,100 hospitalizations, 35,000 deaths, 678,500 physi-
cian visits and 883,800 lost days of work across Europe. Influenza-
related costs averted because of vaccination would increase by an
additional $204 to $243 million yearly, in vaccination target groups
[50]. Indeed, guidelines and there dissemination towards physi-
cians should be emphasized more, but should also be accompanied
with patients-centered strategies in order to deal with their beliefs,
and to overcome these hurdles.
 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27
Other inactivated vaccines are not universally recommended,
but only in high risk patients. They all can be administered safely in
immunocompromised patients, sometimes respecting a safety time
of three to six months in case of chemotherapy or transplantation.
Immunosuppressive therapy is not a contraindication to inacti-
vated vaccines. For example, Tdap-polio vaccination is recom-
mended in HIV patients and transplant recipients, Hib in case of
hematopoietic stem cell transplantation or asplenia, which is a rare
but possible complication of systemic lupus erythematosus [51]. In
the same way, meningococcal vaccine is recommended in case of
transplantation, asplenia, or in HIV patients, who had an 11-fold
increased risk of invasive meningococcal disease compared to
HIV-negative adults, with a mortality rate of 20% [52]. We can also
underline that HPV vaccination is part now of many guidelines, in
particular in patients with chronic inflammatory diseases or in case
of HIV infection. HPV prevalence is up to 90% in HIV patients, but
vaccination coverage against HPV appears very low in this popu-
lation, under 5%, whereas the seroconversion rate is >75% with the
quadrivalent HPV vaccine [53]. In case of immunosuppression,
immune response to vaccination can be decreased [54]. In HIV
patients, long-term immune response to hepatitis B virus vacci-
nation can be improved using a 4-injection intramuscular double-
dose regimen [55]. In this population, the key determinant of
antibody response seems to be the HIV replication status at
immunisation [56]. Effectiveness of any vaccine depends on degree
of immune suppression, which must be evaluated by prescribers,
especially in primary immunocompromised patients. For example,
in case of X-linked agammaglobulinemia or common variable im-
munodeficiency, efficacy of any vaccine dependent only on hu-
moral response is doubtful. Moreover, these patients often received
intravenous immunoglobulins, and the benefit of vaccination is not
demonstrated in this situation, particularly with measles and
varicella vaccines.
A potential limitation of our study is the exclusion of guide-
lines not in English or French. Moreover, we did not systemati-
cally appraise the guidelines for quality; however, this was not
within the scope of this systematic review. Most of the guide-
lines were made after a systematic review of the literature in
order to synthesize evidence for the benefits and harms of vac-
cinations in different subgroups of immunocompromised pa-
tients. However, some guidelines were also partially built on
existing recommendations. The consequence is that included
guidelines were not strictly independent. It could be a limitation
of this work.
5. Conclusions
In conclusion, this is the first systematic review and compre-
hensive field synopsis of all guidelines published over the past
decade on vaccination in all types of immunocompromised pa-
tients. Pneumococcal and injectable influenza are the only two
vaccines universally recommended in all cases of immunosup-
pression. Other inactivated vaccines are not universally recom-
mended, but only indicated in high risk patients. Live vaccines are
contraindicated in patients under immunosuppressive therapy or
in HIV patients with a CD4 count under 200/mm3. Consequences of
infectious diseases in immunocompromised patients can be serious
in terms of morbi-mortality. An international collaborative effort
should be made to increase awareness of available guidelines and
vaccination coverage in this population.
Registration
None.
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19
Funding source
None.
Guarantor of the article
Laurent Peyrin-Biroulet, M.D., Ph.D.
Specific author contribution
LPB designed research; AL and LPB conducted literature search;
AL and LPB analyzed data; AL and LPB wrote the paper; LPB had
primary responsibility for final content. All authors read and
approved the final manuscript.
Financial support
This research did not receive any specific grant from funding
agencies in the public, commercial, or not-for-profit sectors.
Potential competing interests
AL: board for Amgen, lecture fees from Vifor Pharma, research
grants from Roche; XM: consulting fees from BMS, GSK, LFB,
Medimmune, Novartis, Pfizer, Sanofi, UCB-Pharma; HB: consulting,
advisory board, speakers bureau or investigator for Abbvie, Amgen,
Baxalta, Boehringer-Ingelheim, Celgene, Eli-Lilly, Janssen, Leo
Pharma, MSD, Novartis, Pfizer, Sun Pharma and UCB Pharma; AB:
consulting, advisory board, speaker or investigator for Abbvie, GSK,
Novartis, Pfizer; BB: consulting fees from BMS, GSK, LFB, Novartis,
Pfizer, SOBI; EH: investigator for Roche, HGS, Astra-Zeneca, Merck
Serono, Neovacs, UCB, Pfizer, speaker for Roche, Astra Zeneca,
Novartis, Abbott, Roche, Pfizer, GSK, HGS, Actelion, Roche-Chugaï,
Wyeth, LFB, consulting fees from Roche, GSK, HGS,LFB, Astra-
Zeneca; ML: investigator, speaker and consultant for Pfizer,
Janssen-Cilag, Abbvie, Leo pharma, Astellas, Galderma, Lilly,
Novartis, MSD, Celgene; OL: consulting fees from Novartis, Pfizer,
UCB-Pharma, Gilead Sciences, Astellas, Merck; PL: board for Pfizer;
SP: consulting fees from Pfizer, MSD, Hospira, Theradiag; XR:
consulting fees from Abbvie, Janssen, MSD, Pfizer, Takeda; JS:
clinical trials: as main (head) clinical or laboratory investigator, or
study coordinator (Roche, BMS) and as co-investigator or study
contributor (BMS, Roche, Schering-Plough, UCB, Wyeth, Abbott,
Pfizer, Merck Serono, LFB, GSK, AMGEN); Occasional involvements:
expert reports (BMS, Roche, Schering-Plough, UCB, Wyeth, Abbott,
Pfizer, Merck Serono, LFB, GSK, AMGEN) and as advisory services
(BMS, Roche, Schering-Plough, UCB, Wyeth, Abbott, Pfizer, Merck
Serono, LFB, GSK, AMGEN); Conferences: attendance as contributor
(BMS, Roche, Schering-Plough, UCB, Wyeth, Abbott, Pfizer, Merck
Serono, LFB, GSK, AMGEN) and as audience member (BMS, Roche,
Schering-Plough, UCB, Wyeth, Abbott, Pfizer, Merck Serono, LFB,
GSK, AMGEN; SD: has served as a speaker, consultant, and advisory
board member for Schering-Plough, Abbott Laboratories, Merck,
UCB-pharma, Ferring, Cellerix, Millenium Takeda, Nycomed, Phar-
macosmos, Actelion, Danone, Alpha Wasserman, Genentech, Gru-
nenthal, Pfizer, Astra Zeneca, Novo Nordisk, Cosmo
Pharmaceuticals, Vifor, and Johnson & Johnson.; SB: none; LPB:
Consulting fees from Merck, Abbvie, Janssen, Genentech, Mitsu-
bishi, Ferring, Norgine, Tillots, Vifor, Therakos, Pharmacosmos,
ge, BMS, UCB-pharma, Hospira, Celltrion, Takeda, Biogaran,
Pile
Boerhinger-Ingelheim, Lilly, Pfizer, HAC-Pharma, Index Pharma-
ceuticals, Amgen, Sandoz, Forward Pharma GmbH, Celgene. Lecture
fees from Merck, Abbvie, Takeda, Janssen, Takeda, Ferring, Norgine,
Tillots, Vifor, Therakos, Mitsubishi, HAC-pharma.
20 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27

Appendix Fig. 1. Flow chart of the study selection process for the systematic review.

Appendix Table 1
Vaccination recommendations in asplenic patients.

Professional society, country, year

IDSA, U.S.A., 2013 BCSH, U.-K., 2011 PHAC, Canada, 2014 ATAGI, Australia, 2015 HCSP, France, 2014

Vaccine
Live vaccines
BCG (Bacillus Calmette- Not recommended but Not recommended but Not recommended but Not recommended but Not recommended but
Gu

erin) possible possible possible possible possible
Measles, mumps, and Not recommended but Not recommended but Not recommended but Not recommended but Not recommended but
rubella possible possible possible possible possible
Varicella-zoster Not recommended but Not recommended but Not recommended but Not recommended but Not recommended but
possible possible possible possible possible
Rotavirus Not recommended but Not recommended but Not recommended but Not recommended but Not recommended but
possible possible possible possible possible
Yellow fever Not recommended but Not recommended but Not recommended but Not recommended but Not recommended but
possible possible possible possible possible
Inactivated vaccines
Tetanus-diphteria- Not recommended but Not recommended but Not recommended but Not recommended but Not recommended but
acellular pertussis (Tdap)- possible possible possible possible possible
polio
Haemophilus influenzae b Before elective splenectomy A single dose of Hib A single dose of Hib A single dose of Hib A single dose of Hib
A single dose of Hib conjugate vaccine conjugate vaccine conjugate vaccine conjugate vaccine
conjugate vaccine
After splenectomy
Recommendations are
similar
Hepatitis B Not recommended but Not recommended but Not recommended but Not recommended but Not recommended but
possible possible possible possible possible
Meningococcal Before elective splenectomy MenC and MenACWY 1 MenC and MenACWY 1 A dose of MenACWY and a A dose of MenACWY
vaccination A single dose of MenACWY, month after month after and a second dose 6
second dose 8 weeks after,
with a months after(frequence
with a booster dose every 5
After splenectomy years of booster doses
2 doses of MenACWY with remains to be clarified)
an interval of 8e12 weeks A dose of MenB and a
Booster dose every 5 years second dose 1 month
in all cases after
Pneumococcal vaccination Before elective splenectomy PCV13 and PPSV23 8 weeks PCV13 and PPSV23 8 weeks PCV13 and PPSV23 8 weeks PCV13 and PPSV23 8
PCV13 and PPSV23 8 weeks after and at least weeks after and at least 2 weeks after and at least 2 weeks weeks after and at least
after and at least 2 weeks before or 2 weeks after before or 2 weeks after before or 1 week after 2 weeks before or 2
before splenectomy, with a splenectomy with a second splenectomy, with a second splenectomy ± a second weeks after
second dose of PPSV23 5 dose of PPSV23 5 years after dose of PPSV23 5 years after dose 5 years later splenectomy, with a
years after second dose of PPSV23
After splenectomy 5 years after
PCV13 and PPSV23 8 weeks

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 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27 21

Appendix Table 1 (continued )

Professional society, country, year

IDSA, U.S.A., 2013 BCSH, U.-K., 2011 PHAC, Canada, 2014 ATAGI, Australia, 2015 HCSP, France, 2014

after
PPSV23 at least 2 weeks
after splenectomy if patient
has previously received an
age-appropriate PCV13
regimen
A second dose of PPSV23 5
years after
Human papillomavirus Not recommended but Not recommended but Not recommended but Not recommended but Not recommended but
possible possible possible possible possible
Influenza (injectable) Before elective splenectomy A single dose of influenza A single dose of influenza A single dose of influenza A single dose of
A single dose of influenza vaccination annually vaccination annually vaccination annually influenza vaccination
vaccine annually annually
After splenectomy
Recommendations are
similar
Hepatitis A Not recommended but Not recommended but Not recommended but Not recommended but Not recommended but
possible possible possible possible possible

IDSA, Infectious Diseases Society of America; BCSH, British Committee for Standards in Haematology; PHAC, Public Health Agency of Canada; ATAGI, Australian Technical
Advisory Group on Immunisation; HCSP, Haut Conseil de la Sante
Publique; MenC, meningococcal C vaccination; MenACWY, quadrivalent meningococcal vaccination; MenB,
meningococcal B vaccination; PCV13, 13-valent pneumococcal conjugate vaccine; PPSV23, 23-valent pneumococcal polysaccharide vaccine.

Appendix Table 2
Vaccination recommendations in hematopoietic stem cell recipients.

Professional society, country, year

International consensus, U.S.A.- International consensus, ATAGI, Australia, 2015 HCSP, France, 2012
Europe-Canada, 2009 Germany-Austria-Swiss, 2011

Vaccine
Live vaccines
BCG (Bacillus Calmette- Contraindicated Contraindicated Contraindicated Contraindicated
Gu

erin)
Measles, mumps, and Indicated in seronegative Not recommended Possible 24 months after HSCT (1 Recommended 24 months after
rubella patients (1e2 doses 24 Possible 24 months after HSCT e2 doses separated by a minimum HSCT (1e2 doses separated by a
months after HSCT) (1e2 doses) interval of 4 weeks) minimum interval of 4 weeks)
Varicella-zoster Varicella vaccine is possible Not recommended Varicella vaccine is recommended Varicella vaccine is recommended
24 months after HSCT Possible 24 months after HSCT in seronegative patients 24 in seronegative patients 24
Zoster vaccine is months after HSCT (2 doses months after HSCT (2 doses
contraindicated separated by a minimum interval of separated by a minimum interval of
4 weeks) 8 weeks)
Zoster vaccine is not recommended Zoster vaccine is not recommended
Rotavirus Not recommended Not recommended Not recommended Not recommended
Yellow fever Not recommended Not recommended Not recommended Not recommended
Possible in patients residing in Possible in patients residing in or
or traveling to endemic areas traveling to endemic areas 24
24 months after HSCT months after HSCT
Inactivated vaccines
Tetanus-diphteria- Recommended 6e12 months Recommended 6 months after Recommended 6 months after HSCT Recommended 6e12 months after
acellular pertussis (Tdap)- after HSCT (3 doses) HSCT (3 doses in monthly (3 doses 6, 8, 12 months after HSCT) HSCT (3 doses in monthly intervals
polio intervals with a booster dose 18 with a booster dose 12 months after
months after HSCT, then every the first dose)
10 years)
Haemophilus influenzae b Recommended 6e12 months Recommended 6 months after Recommended 6 months after HSCT Recommended 6 months after HSCT
after HSCT (3 doses separated HSCT (3 doses in monthly (3 doses 6, 8, 12 months after HSCT) (3 doses in monthly intervals with a
by a minimum interval of 8 intervals with a booster dose 18 booster dose 18 months after HSCT)
weeks) months after HSCT)
Hepatitis B Follow country Recommended in seronegative Recommended 6 months after HSCT Recommended in seronegative at
recommendations for general patients 6 months after HSCT (3 (3 doses 6, 8, 12 months after HSCT) risk patients 6 months after HSCT (3
population doses in monthly intervals with doses in monthly intervals with a
Possible 6e12 months after a booster dose 18 months after booster dose 18 months after HSCT)
HSCT (3 doses) HSCT)
Meningococcal Follow country Not recommended Recommended 6 months after HSCT 2 doses of MenC vaccine 12e18
vaccination recommendations for general Possible 6e12 months after (2 doses 6 and 8 months after HSCT) months after HSCT in monthly
population HSCT (3 doses in monthly interval followed by 1 dose of
Possible 6e12 months after intervals) MenACWY 4 weeks after
HSCT (1 dose)
Pneumococcal vaccination Recommended 3e6 months Recommended 6 months after Recommended 6 months after HSCT Recommended 3 months after HSCT
after HSCT (3 doses of PCV13 HSCT (3 doses in monthly (3 doses PCV13 6, 8 and 12 months (3 doses of PCV13 in monthly
followed by one dose of intervals with a booster dose 18 after HSCT with a dose of PPSV23 24 intervals with a dose of PPSV23# 12
PPSV23) months after HSCT) months after HCST) months after HSCT)
(continued on next page)

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Appendix Table 2 (continued )

Professional society, country, year

International consensus, U.S.A.- International consensus, ATAGI, Australia, 2015 HCSP, France, 2012
Europe-Canada, 2009 Germany-Austria-Swiss, 2011

Human papillomavirus Follow country Not recommended Recommended in at risk patientsa Not recommended
recommendations for general Possible after HSCT >12 months after HSCT (3 doses at Possible 6 months after HSCT
population 0,2 and 6 months)
Possible after HSCT
Influenza Recommended 6 months after Recommended 6 months after Recommended 6 months after HSCT Recommended 6 months after HSCT
HSCT (1 annual dose of TIV) HSCT (1 annual dose of (2 doses of TIV with an interval of 4 (1 annual dose of TIV)
TIV) weeks then a single dose annually)
Hepatitis A Follow country Not recommended Not recommended Not recommended
recommendations for general Possible 6e12 months after Possible after HSCT Possible after HSCT
population HSCT (3 doses in monthly
Possible after HSCT intervals with a booster dose 18
months after HSCT)

Publique; HSCT, hematopoietic stemcell transplantation; MenC, meningococcal
ATAGI, Australian Technical Advisory Group on Immunisation; HCSP, Haut Conseil de la Sante
C vaccination; MenACWY, quadrivalent meningococcal vaccination; PCV13, 13-valent pneumococcal conjugate vaccine; PPSV23, 23-valent pneumococcal polysaccharide
vaccine; TIV, trivalent inactivated vaccine.
a
Previous exposure to HPV, future risks of HPV exposure, extent/duration of immunosuppression.

Appendix Table 3
Vaccination recommendations in primary immunocompromised patients.

Professional society, country, year

IDSA, U.S.A., 2013 PHAC, Canada, 2014 HCSP, France, 2014

Type of immune deficiency

Phagocytic deficit
Severe chronic neutropenia
Complement deficit
X-linked
agammaglobulinemia
Common variable
immunodeficiency
IgG subclass deficiencies
IgA subclass deficiencies
Complete T lymphocytes
defects (eg, severe combined
immunodeficiency, complete
DiGeorge syndrome)
Not recommended vaccines: BCG, Ty21a
Salmonella typhi vaccine
Recommended vaccines: all inactivated
vaccines are safe and probably
effective; live viral vaccines are
probably safe and effective
Not recommended vaccines: BCG, Ty21a
Salmonella typhi vaccine
Recommended vaccines: all inactivated
vaccines are safe and probably
effective; live viral vaccines are
probably safe and effective
Not recommended vaccines: none
Recommended vaccines: pneumococcal
and meningococcal vaccines
All routine vaccines are probably
effective
Not recommended vaccines: oral polio,
smallpox, influenza (nasal), yellow
fever, BCG, Ty21a Salmonella typhi
vaccine, consider measles vaccine; no
data for varicella or rotavirus vaccines
Effectiveness of any vaccine dependent
only on humoral response is doubtful;
intravenous immunoglobulins
interferes with measles and possibly
varicella immune response
Not recommended vaccines: oral polio
Other live vaccines seem to be safe but
caution is urged
All other vaccines are probably effective
but immune response may be
attenuated
Not recommended vaccines: oral polio
Other live vaccines seem to be safe but
caution is urged
All other vaccines are probably effective
but immune response may be
attenuated
Not recommended vaccines: all live
vaccines
All vaccines are ineffective
Not recommended vaccines: BCG,
Ty21a Salmonella typhi vaccine
Recommended vaccines: hepatitis B,
influenza (injectable),
pneumococcal vaccine,
Haemophilus influenzae b
Other vaccines can be administered
Not recommended vaccines: BCG,
Ty21a Salmonella typhi vaccine
Recommended vaccines: hepatitis B,
influenza (injectable),
pneumococcal vaccine,
Haemophilus influenzae b
Other vaccines can be administered
Not recommended vaccines: none
Recommended vaccines: hepatitis B,
influenza (injectable),
pneumococcal and meningococcal
vaccines, Haemophilus influenzae b
Other vaccines can be administered
Not recommended vaccines: BCG,
zona, influenza (nasal), rotavirus,
smallpox, Ty21a Salmonella typhi
vaccine, yellow fever
Recommended vaccines:
Haemophilus influenzae b, hepatitis
B, influenza (injectable),
meningococcal and pneumococcal
vaccines
Other vaccines can be administered
Not recommended vaccines: none
Recommended vaccines:
Haemophilus influenzae b, hepatitis
B, influenza (injectable),
meningococcal and pneumococcal
vaccines
Other vaccines can be administered
Not recommended vaccines: none
Recommended vaccines:
Haemophilus influenzae b, hepatitis
B, influenza (injectable),
meningococcal and pneumococcal
vaccines
Other vaccines can be administered
Not recommended vaccines: all live
vaccines
Recommended vaccines:
Haemophilus influenzae b, hepatitis
B, influenza (injectable),
Not recommended vaccines: BCG
Recommended vaccines: infuenza (injectable),
pneumococcal vaccine
Other vaccines can be administered
Not recommended vaccines: BCG
Recommended vaccines: infuenza (injectable),
pneumococcal vaccine, varicella
Other vaccines can be administered
Not recommended vaccines: none
Recommended vaccines: meningococcal (Men
ACWY and MenB) and pneumococcal vaccines,
influenza, Haemophilus influenzae b
Other vaccines can be administered
Not recommended vaccines: BCG, yellow fever,
influenza (nasal), rotavirus?
Recommended vaccines: influenza (injectable),
pneumococcal vaccine
Other vaccines can be administered but the
benefit of vaccination is not demonstrated in
patients treated with intravenous
immunoglobulins
Not recommended vaccines: BCG, yellow fever,
influenza (nasal)
Recommended vaccines: influenza (injectable),
pneumococcal vaccine
Other vaccines can be administered but the
benefit of vaccination is not demonstrated in
patients treated with intravenous
immunoglobulins
Not recommended vaccines: none
Recommended vaccines: influenza,
pneumococcal vaccine
Not recommended vaccines: all live vaccines
All vaccines seem to be ineffective

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Appendix Table 3 (continued )

Professional society, country, year

IDSA, U.S.A., 2013 PHAC, Canada, 2014 HCSP, France, 2014

meningococcal and pneumococcal

Partial T lymphocytes defects
(eg, Wiskott-Aldrich
syndrome, ataxia-
telangiectasia)
IDSA, Infectious Diseases Society of America; PHAC, Public Health Agency of Canada; HCSP, Haut Conseil de la Sante
Not recommended vaccines: all live
vaccines
Recommended vaccines: inactivated
vaccines
Effectiveness of any vaccine depends on
degree of immune suppression
vaccines
Other vaccines can be administered
Not recommended vaccines: all live Not recommended vaccines: all live vaccines
vaccines Recommended vaccines: influenza (injectable),
Recommended vaccines: pneumococcal vaccine
Haemophilus influenzae b, hepatitis Effectiveness of any vaccine depends on degree
B, influenza (injectable), of immune suppression
meningococcal and pneumococcal
vaccines
Other vaccines can be administered

Publique; BCG, bacillus Calmette-Gue

rin.

Appendix Table 4
Vaccination recommendations in psoriasis patients.

Professional society, country, year

National Psoriasis Foundation, PHAC, Canada, 2014 ATAGI, Australia, 2015 HCSP, France, 2014
U.S.A., 2013

Live vaccines
BCG (Bacillus Calmette-
Gu

erin)
Measles, mumps, and rubella
Varicella-zoster
Rotavirus
Yellow fever
Inactivated vaccines
Tetanus-diphteria-Acellular
pertussis (Tdap)-polio
Haemophilus influenzae b
Hepatitis B
Meningococcal vaccination
Pneumococcal vaccination
Human papillomavirus
Influenza
Hepatitis A
Not recommended
Contraindicated during IT
Recommended at least 6 weeks
before starting IT
Contraindicated during IT
Recommended in patients 50
years (one dose)
Contraindicated during IT
Not recommended
Contraindicated during IT
Not recommended
Contraindicated during IT
Administer vaccine
Give Tdap if Td  2 years, with a
booster dose every 10 yearsa
Possible during IT
Unvaccinated adults can be
vaccinated
Possible during IT
Patients without evidence of
disease or immunity and risk
factors should be offered
vaccination before IT
Possible during IT with high-dose
regimen
Vaccination only in high risk
patients (asplenia, complement
deficiency or group living situation)
Possible during IT
Recommended (PPSV23 before
initiation of IT or PCV13 and PPSV23
8 weeks after during IT)
Recommended through age 26
years (3 doses 0,2 and 6 months
with the quadrivalent vaccine)
Possible during IT
Recommended (annual vaccine
with the TIV)
Possible during IT
Vaccination only in high risk
patients (diabetes, liver diseases,
injecting drug users, men who have
sex with men, employees or
residents in institutional settings)
Possible during IT
Not recommended
Contraindicated during IT
Not recommended
Contraindicated during IT
Not recommended
Contraindicated during IT
Not recommended
Contraindicated during IT
Not recommended
Contraindicated during IT
Not recommended but possible
during IT
Not recommended but possible
during IT
Not recommended but possible
during IT
Not recommended but possible
during IT
Recommended (PCV13 and PPSV23
8 weeks after; re-vaccinate with a
single dose of PPSV23 5 years after)
Possible during IT
Not recommended but possible
during IT
Recommended (annual vaccine
with the TIV)
Possible during IT
Not recommended but possible
during IT
Not recommended Not recommended
Contraindicated during IT Contraindicated during IT
Not recommended Not recommended
Contraindicated during IT Contraindicated during IT
Not recommended Not recommended
Contraindicated during IT Contraindicated during IT
Not recommended Not recommended
Contraindicated during IT Contraindicated during IT
Not recommended Not recommended
Contraindicated during IT Contraindicated during IT
Not recommended but possible Administer vaccine if not given
during IT over the past 10 years, with a
booster dose every 10 years
Possible during IT
Not recommended but possible Not recommended but possible
during IT during IT
Not recommended but possible Not recommended but possible
during IT during IT
Not recommended but possible Not recommended but possible
during IT during IT
Recommended (PCV13 and Recommended (PCV13 and
PPSV23 8 weeks after; second PPSV23 8 weeks after; re-
dose of PPSV23 5e10 years vaccinate with a single dose of
after, third dose at 65 years) PPSV23 5 years after)
Possible during IT Possible during IT
Recommended through age 18 Not recommended but possible
years in patients with IT (3 during IT
doses 0,2 and 6 months with
the quadrivalent vaccine)
Recommended (annual vaccine Recommended (annual vaccine
with the TIV) with the TIV)
Possible during IT Possible during IT
Not recommended but possible Not recommended but possible
during IT during IT

PHAC, Public Health Agency of Canada; ATAGI, Australian Technical Advisory Group on Immunisation; HCSP, Haut Conseil de la Sante
Publique; IT, immunosuppressive
therapy; PCV13, 13-valent pneumococcal conjugate vaccine; PPSV23, 23-valent pneumococcal polysaccharide vaccine; TIV, trivalent inactivated vaccine.

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Appendix Table 5
Vaccination recommendations in inflammatory rheumatic disease patients.
Vaccine
Live vaccines
BCG (Bacillus Calmette-
For personal use only. No other uses without permission. Copyright ©2018. Elsevier Inc. All rights reserved.
Gu

erin)
Measles, mumps, and
rubella(MMR)
Varicella-zoster
Rotavirus
Yellow fever
Inactivated vaccines
Tetanus-diphteria-
acellular pertussis (Tdap)-
polio
Haemophilus influenzae b
Professional society, country, year
IDSA, U.S.A., 2013
Not recommended
Contraindicated during IT
Not recommended
Contraindicated during IT
Varicella vaccine should be
considered for patients without
evidence of varicella immunity
4 weeks prior to initiation of
IT (2 doses separated
by > 4weeks)
Zoster vaccine should be
considered for patients 60
years prior to initiation of IT or
being treated with low-dose of
IT and those who aged 50e59
years and varicella positive
prior to initiation of IT or being
treated with low-dose of IT 4
weeks prior to initiation of IT (2
doses separated by > 4 weeks)
Contraindicated in highly
immunocompromised
patientsb
Not recommended
Contraindicated during IT
Not recommended
Contraindicated during IT
Not recommended
Possible 2 weeks prior to IT
ACR, U.S.A., 2015
Not recommended
Contraindicated during IT
Not recommended
Contraindicated during IT
Patients 50 years should be
vaccinated at least 2 weeks
before receiving biologic or
tofacitinib therapy herpes-
zoster vaccination is not
recommended in patients
receiving biologics
Not recommended
Contraindicated during IT
Not recommended
Contraindicated during IT
Not recommended
Not recommended
24
EULAR, Europe, 2011 PHAC, Canada, 2014 ATAGI, Australia, 2015 HCSP, France, 2014
Not recommended Not recommended Not recommended Not recommended
Contraindicated during IT Contraindicated during IT Contraindicated during IT Contraindicated during IT
MMR vaccine should be Not recommended Not recommended Not recommended
avoided whenever possible Contraindicated during IT Contraindicated during IT Contraindicated during IT
but it may be considered in
mildlya immunosuppressed
patients on a case-by-case
basis (4 weeks prior to IT)
Contraindicated in highly
A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27
immunocompromised
patientsb
Varicella and zoster vaccine Not recommended Not recommended Not recommended
should be avoided Contraindicated during IT Contraindicated during IT Contraindicated during IT
whenever possible
Zoster vaccine may be
considered only in mildly
immunocompromised
patientsa who are
seropositive for varicella
zoster antibodies
Contraindicated in highly
immunocompromised
patientsb
Not recommended Not recommended Not recommended Not recommended
Contraindicated during IT Contraindicated during IT Contraindicated during IT Contraindicated during IT
Not recommended Not recommended Not recommended Not recommended
Contraindicated during IT Contraindicated during IT Contraindicated during IT Contraindicated during IT
Not recommended Not recommended Not recommended Administer vaccine if not
Possible during IT in case of Possible during IT Possible during IT given over the past 10
major and/or contaminated years, with a booster dose
wounds in patients who every 10 years
received rituximab within Possible during IT
the last 24 weeks, tetanus
immunoglobulin should be
administered
 Not recommended Not recommended Not recommended Not recommended Not recommended
Possible 2 weeks prior to IT Possible during IT Possible during IT Possible during IT Possible during IT
Hepatitis B Not recommended Only recommendedc if hepatitis Only recommended in Not recommended Not recommended Not recommended
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Possible 2 weeks prior to IT
Meningococcal Not recommended
vaccination Possible 2 weeks prior to IT
Pneumococcal vaccination Recommended (PCV13 and
PPSV23 8 weeks after; re-
vaccinate with a single dose of
PPSV23 5 years after)
Possible 2 weeks prior to IT
For personal use only. No other uses without permission. Copyright ©2018. Elsevier Inc. All rights reserved.
B risk factors are presentd
Not recommended
Recommendedc (PCV13 and
PPSV23 8 weeks after; re-
vaccinate with a single dose of
PPSV23 5 years after)
patients at riskd without
protective antibodies
Not recommended
Possible during IT
Recommended (PCV13 and
PPSV23 8 weeks after)
Possible during IT
Possible during IT
Not recommended
Possible during IT
Recommended (PCV13 and
PPSV23 8 weeks after; re-
vaccinate with a single dose
of PPSV23 5 years after)
Possible during IT
Possible during IT
Not recommended
Possible during IT
Recommended (PCV13 and
PPSV23 8 weeks after;
second dose of PPSV23 5
e10 years after, third dose
at 65 years)
Possible during IT
Not recommended
Possible during IT
Recommended (PCV13 and
PPSV23 8 weeks after; re-
vaccinate with a single dose
of PPSV23 5 years after)
Possible during IT

Possible during IT
Human papillomavirus Not recommended Recommended Human papillomavirus Not recommended Recommended <18 in case Not recommended
Possible 2 weeks prior to IT vaccine should be Possible during IT of IT (3 doses 0,2 and 6 Possible during IT
considered in women until months with HPV4)
the age of 25 years Possible during IT
Influenza Recommended (annual vaccine Recommendedc Recommended (annual Recommended (annual Recommended (annual Recommended (annual
with the TIV) vaccine with the TIV) vaccine with the TIV) vaccine with the TIV) vaccine with the TIV)
Possible during IT Possible during IT Possible during IT Possible during IT Possible during IT
Hepatitis A Not recommended Not recommended Only recommended in Not recommended Not recommended Not recommended

A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27

Possible 2 weeks prior to IT patients at risk (travel to or Possible during IT Possible during IT Possible during IT
residence in endemic
countries, medical
profession, infected family
member or contacts) when
protective antibodies are
absent

IDSA, Infectious Diseases Society of America; ACR, American College of Rheumatology; EULAR, European League Against Rheumatism; PHAC, Public Health Agency of Canada; ATAGI, Australian Technical Advisory Group on
Immunisation; HCSP, Haut Conseil de la Sante
Publique; IT, immunosuppressive therapy; PCV13, 13-valent pneumococcal conjugate vaccine; PPSV23, 23-valent pneumococcal polysaccharide vaccine; HPV4, quadrivalent HPV
vaccine; TIV, trivalent inactivated vaccine.
a
Patients treated with short-term corticosteroid therapy (<14 days), low to moderate doses of corticosteroids (<20 mg/day of prednisone or equivalent), intra-articular, bursal or tendon corticosteroids injections, long-term
alternate-day treatment with low to moderate doses of short-acting systemic corticosteroids, therapy with methotrexate (<0.4 mg/kg/week), azathioprine (<3.0 mg/kg/day) or 6-mercaptopurine (<1.5 mg/kg/day).
b
Patients treated with corticosteroids, TNFa blocking agents and non-biological disease-modifying antirheumatic drugs, particularly cyclophosphamide, azathioprine and leflunomide.
c
Strongly recommended in patients receiving biologics.
d
e.g. travel to or residence in endemic countries, health care personnel, infected family member or contacts, intravenous drug abuse, multiple sex partners in the previous 6 months.

25
26 A. Lopez et al. / Journal of Autoimmunity 80 (2017) 10e27
Appendix
Asplenic patients
Five guidelines about vaccination are available [14,20,24e26]
(Appendix Table 1). None of them recommends live vaccines
administration, as BCG (Bacillus Calmette-Gue
rin), MMR (measles,
mumps and rubella), varicella-zoster, rotavirus and yellow fever.
However, it is still possible to give these vaccines in case of asplenia
[14,20,24e26]. Concerning inactivated vaccines, Tdap (tetanus,
diphtheria, acellular pertussis) and polio vaccine are not recom-
mended but possible, as HPV (human papilloma virus), and hepatitis
A [14,20,24e26]. Four vaccinations are unanimously recommended
by all guidelines, with different administration procedures, for
prevention of Hib (Haemophilus influenza type b), meningococcal,
pneumococcal and influenza infections [14,20,24e26]. Thus, a
single dose of Hib conjugate vaccine is recommended before or
after elective splenectomy. The IDSA recommends a single dose of
MenACWY quadrivalent meningococcal conjugate vaccine before
surgery, with a booster dose every five years. If vaccination is made
after splenectomy, 2 doses of MenACWY are needed with an in-
terval of 8e12 weeks between doses, with a booster dose every five
years [14]. Protocol is similar for the Australian Technical Advisory
Group on Immunisation [25]. Both British and Canadian guidelines
recommend a single dose of MenC and a single dose of MenACWY
one month after, without precision on the time for administrating
them before or after surgery [20,24]. French authorities also
recommend two doses of MenACWY, adding that frequence of
booster doses remains to be clarified [26]. Moreover, two doses of
MenB with an interval of one month were recommended in the
French guidelines [26]. Two main vaccines are currently available
against S. pneumoniae (pneumococcus): the PCV13 (13-valent
pneumococcal conjugate vaccine) and the PPSV23 (23-valent
pneumococcal polysaccharide vaccine). Majority of learned soci-
eties recommend PCV13 and PPSV23 eight weeks, at least two
weeks before or two weeks after splenectomy, with a second dose
of PPSV23 five years after [20,24,26]. Australian guidelines are
almost similar, other than the fact that vaccination is authorized
only one week after surgery [25]. US guidelines are similar too, with
slight differences in case of vaccination after surgery. In this situ-
ation, the booster dose of PPSV23 must be administrated two years
after the first administration scheme if patient has previously
received an age-appropriate PCV13 regimen. In all cases, a second
dose of PPSV23 is recommended five years after [14]. All guidelines
proposed a single dose of influenza vaccination annually
[14,20,24e26].
Primary immunocompromised patients
Primary immunodeficiency encompasses several diseases,
affecting cellular or humoral immunity. Three guidelines exist
about vaccination in these patients (Appendix Table 3) [14,24,26].
In case of phagocytic deficit, BCG and Salmonella typhi vaccines
were not recommended in any guideline [14,24,26]. On the other
hand, influenza and pneumococcal vaccinations were advised in
the Canadian and the French guidelines [24,26]. Furthermore,
hepatitis B and Hib immunizations were recommended by the
Public Health Agency of Canada [24]. In severe chronic neutropenia
patients, BCG and Salmonella typhi vaccines were not recom-
mended [14,24,26]. Recommended vaccines were similar than the
previous case, in addition to varicella vaccination for one guideline
[26]. In case of complement deficit, all vaccines can be adminis-
trated. Meningococcal and pneumococcal vaccinations were uni-
versally recommended [14,24,26], with influenza and Hib for two
guidelines [24,26], even hepatitis B for one guideline [24]. In
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For personal use only. No other uses without permission. Copyright ©2018. Elsevier Inc. All rights reserved.
patients with X-linked agammaglobulinemia or common variable
immunodeficiency, many vaccines are not recommended: BCG,
influenza (nasal), yellow fever, Salmonella typhi, oral polio and
varicella [14,24,26]. Only Canadian guidelines recommended some
vaccines: Hib, injectable influenza, hepatitis B, meningococcal and
pneumococcal [24]. U.S. guidelines specified that effectiveness of
any vaccine dependent only on humoral response is doubtful [14].
Moreover, these patients are often treated with intravenous im-
munoglobulins, and the benefit of vaccination is not demonstrated
in this situation, especially with measles and varicella vaccines
[14,26]. In case of IgG subclass deficiencies, BCG, yellow fever, nasal
influenza and oral polio are not recommended [14,26]. Advised
vaccinations were very variable between the different learned so-
cieties. Only pneumococcal and influenza vaccines in the French
guidelines [26], in addition to Hib, hepatitis B and meningococcal
vaccines in the Canadian guidelines [24]. In case of IgA subclass
deficiencies, recommendations were similar [14,24,26]. In com-
plete T lymphocytes deficient patients (e.g. severe combined im-
munodeficiency, complete DiGeorge syndrome, …), all live vaccines
were universally not recommended [14,24,26]. Concerning inacti-
vated vaccines, two guidelines considered that they all seemed to
be ineffective [14,26], whereas one guideline advised Hib, hepatitis
B, injectable influenza, meningococcal and pneumococcal vacci-
nations [24]. Finally, in case of partial T lymphocytes deficiency (e.g.
Wiskott-Aldrich syndrome, ataxia-telangiectasia), all live vaccines
are not recommended [14,24,26]. Pneumococcal and influenza
vaccines were recommended in two guidelines [24,26], with Hib,
hepatitis B and meningococcal vaccines in addition in one of these
guideline [24]. However, effectiveness of any vaccine depends on
degree of immune suppression [14,26].
Patients with psoriasis
Four guidelines proposed recommendations for immunisation
in patients with psoriasis (Appendix Table 4) [17,24e26]. BCG,
rotavirus and yellow fever vaccines were universally not recom-
mended and contraindicated in case of immunosuppressive treat-
ment, whereas the U.S. National Psoriasis Foundation
recommended the MMR vaccination at least six weeks before
starting immunosuppression, and the varicella-zoster vaccination
in patients beyond 50 years (one dose) [17]. All inactivated vaccines
are authorized in patients with psoriasis, including those under an
immunosuppressive therapy [17,24e26]. Pneumococcal vaccina-
tion was part of all the guidelines, essentially with a two doses
regimen, PCV13 then PPSV23 eight weeks after [24e26]. An
annually influenza vaccination was also recommended [17,24e26].
Tdap-polio vaccine was recommended in two guidelines if it was
not given over the past ten years [17,26]. Vaccination against the
HPV was found in two guidelines, with a three doses scheme at 0,
two and six months [17,25]. The U.S. guidelines recommended
vaccinating patients with psoriasis against the hepatitis A, B and
the meningococcal infection only in high risk patients [17].
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