Advertisement

Yellow fever vaccination status and safety in hemodialysis patients

Open AccessPublished:May 18, 2016DOI:https://doi.org/10.1016/j.ijid.2016.05.017

      Highlights

      • Yellow fever vaccination was assessed in chronic dialysis patients.
      • Vaccination coverage was lower than desired for a transition area.
      • The vaccine was overall safe and well-tolerated.

      Summary

      Background

      The adverse effects of yellow fever (YF) vaccine in dialysis patients are not well known. There is concern about the risks and benefits of the vaccine in immunocompromised patients living in endemic areas, particularly given the risk of resurgence of urban YF with the spread of Aedes aegypti mosquitoes. The purpose of this study was to assess the coverage and safety of YF vaccine in chronic dialysis patients.

      Methods

      A cross-sectional study of 130 chronic dialysis patients was performed. Data were collected on clinical characteristics and YF vaccine status. Patients not vaccinated against YF or without a booster vaccination within the last 10 years were referred to receive the vaccine, and adverse effects were monitored.

      Results

      Previous vaccination was verified in 44 patients within the last 10 years and in 26 patients at more than 10 years ago, with no mention of adverse effects. Thirty-six patients had never been vaccinated and 24 had an unknown vaccination status. Of the total 86 patients referred for immunization, 45 actually received the YF vaccine, with 24.4% experiencing mild local adverse effects and 4.4% experiencing fever. No serious adverse effects attributable to YF vaccine were observed (anaphylaxis, neurological or viscerotropic disease).

      Conclusions

      YF vaccine coverage among hemodialysis patients is low, and the vaccine appeared to be safe in this population with a small sample size.

      Graphical abstract

      Keywords

      1. Introduction

      Despite the past elimination of yellow fever (YF), its re-emergence in the urban setting remains a threat in Brazil, since the urban mosquito vector Aedes aegypti is widespread and this sylvatic disease is expanding into the more densely populated areas.
      • Câmara F.P.
      • Gomes A.L.
      • Carvalho L.M.
      • Castello L.G.
      Dynamic behavior of sylvatic yellow fever in Brazil (1954-2008).
      • Costa Z.G.
      • Romano A.P.
      • Elkhoury A.N.
      • Flannery B.
      Historical development and evolution of epidemiological surveillance and control of yellow fever in Brazil.
      YF control could be achieved either through vaccination or vector control.
      • Câmara F.P.
      • Gomes A.L.
      • Carvalho L.M.
      • Castello L.G.
      Dynamic behavior of sylvatic yellow fever in Brazil (1954-2008).
      The YF vaccine currently used in Brazil is the Bio-Manguinhos 17DD viral attenuated vaccine produced at the Oswaldo Cruz Institute.
      • Martins R.M.
      • Maia M.L.
      • dos Santos E.M.
      • Cruz L.S.
      • dos Santos P.R.
      • Deotti Carvalho S.M.
      • et al.
      Yellow fever vaccine post-marketing surveillance in Brazil.
      YF vaccine-associated side effects and serious adverse events have been reported, including viscerotropic disease, neurological disease, and severe hypersensitivity reactions.
      • Martins R.M.
      • Maia M.L.
      • dos Santos E.M.
      • Cruz L.S.
      • dos Santos P.R.
      • Deotti Carvalho S.M.
      • et al.
      Yellow fever vaccine post-marketing surveillance in Brazil.
      The US Vaccine Adverse Event Reporting System (VAERS) observed a rate of 4.7 serious YF vaccine adverse events per 100 000 doses distributed.
      • Lindsey N.P.
      • Schroeder B.A.
      • Miller E.R.
      • Braun M.M.
      • Hinckley A.F.
      • Marano N.
      • et al.
      Adverse event reports following yellow fever vaccination.
      The reporting rate was highest among persons aged ≥60 years (8.3 per 100 000 doses). According to the Brazilian Ministry of Health database, 1994 vaccine adverse events were notified between the years 2000 and 2008, when 101 564 083 YF vaccine doses were administered. The Bio-Manguinhos 17DD vaccine serious adverse event rate was 0.9/100 000 doses for hypersensitivity reactions, 0.084/100 000 doses for neurological disease, and 0.026/100 000 doses for viscerotropic disease, with no evidence of an increased adverse event risk in older people.
      • Martins R.M.
      • Maia M.L.
      • dos Santos E.M.
      • Cruz L.S.
      • dos Santos P.R.
      • Deotti Carvalho S.M.
      • et al.
      Yellow fever vaccine post-marketing surveillance in Brazil.
      YF vaccine neurological and viscerotropic diseases do not seem to be associated with the presence of any immunodeficiency or organ failure. Apparently, certain specific immune disorders and genetic factors may predispose the individual to viscerotropic disease, such as systemic lupus erythematosus and thyroid diseases.
      • Martins R.M.
      • Maia M.L.
      • dos Santos E.M.
      • Cruz L.S.
      • dos Santos P.R.
      • Deotti Carvalho S.M.
      • et al.
      Yellow fever vaccine post-marketing surveillance in Brazil.
      • Biscayart C.
      • Carrega M.E.
      • Sagradini S.
      • Gentile A.
      • Stecher D.
      • Orduna T.
      • et al.
      Yellow fever vaccine-associated adverse events following extensive immunization in Argentina.
      In a recent study in Brazil using passive surveillance data, the age group 5–9 years was the most vulnerable to vaccine neurotropic disease.
      • Martins R.M.
      • Pavão A.L.
      • de Oliveira P.M.
      • dos Santos P.R.
      • Carvalho S.M.
      • Mohrdieck R.
      • et al.
      Adverse events following yellow fever immunization: report and analysis of 67 neurological cases in Brazil.
      Live attenuated vaccines are generally contraindicated in pregnant women, immunocompromised patients, and children under 6 months old.

      Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de Vigilância das Doenças Transmissíveis. Manual of rules and procedures for vaccination. Brasília: Ministério da Saúde; 2014, p. 176.

      The recommendation for YF vaccine in immunocompromised patients will depend on the degree of immunosuppression and the epidemiological risk of YF.
      • Staples J.E.
      • Gershman M.
      • Fischer M.
      Centers for Disease Control and Prevention. Yellow fever vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP).
      However, reports of inadvertent vaccination of immunosuppressed patients have not found significant adverse effects or viscerotropic disease.
      • Azevedo L.S.
      • Lasmar E.P.
      • Contieri F.L.
      • Boin I.
      • Percegona L.
      • Saber L.T.
      • et al.
      Yellow fever vaccination in organ transplanted patients: is it safe?. A multicenter study.
      • Mota L.M.
      Vaccination against yellow fever among patients on immunosuppressors with diagnoses of rheumatic diseases.
      The geographic expansion of YF, with a continuous increase in the area where vaccine is recommended in Brazil, justifies the need to study the potential adverse effects of vaccine in special populations vulnerable to YF disease and candidates for the vaccine.
      Chronic kidney disease is characterized by immune dysfunction and an increased risk of infection. Apparently the hypercytokinemia and the uremic milieu promote several immune disorders, including neutrophil, monocyte, and lymphocyte dysfunction, possibly predisposing the individual to YF vaccine adverse effects.
      • Engelich G.
      • Wright D.G.
      • Hartshorn K.L.
      Acquired disorders of phagocyte function complicating medical and surgical illnesses.
      • Kato S.
      • Chmielewski M.
      • Honda H.
      • Pecoits-Filho R.
      • Matsuo S.
      • Yuzawa Y.
      • et al.
      Aspects of immune dysfunction in end-stage renal disease.
      São Carlos is a Brazilian municipality located in the central region of the state of São Paulo where YF vaccination is recommended; this is considered a transition area for YF risk because of a recent period of virus circulation.
      • Câmara F.P.
      • Gomes A.L.
      • Carvalho L.M.
      • Castello L.G.
      Dynamic behavior of sylvatic yellow fever in Brazil (1954-2008).
      • Jentes E.S.
      • Poumerol G.
      • Gershman M.D.
      • Hill D.R.
      • Lemarchand J.
      • Lewis R.F.
      • et al.
      Informal WHO Working Group on Geographic Risk for Yellow Fever. The revised global yellow fever risk map and recommendations for vaccination, 2010: consensus of the Informal WHO Working Group on Geographic Risk for Yellow Fever.
      • Hill D.R.
      Mapping the risk of yellow fever infection.
      No specific recommendation for YF vaccine exists for renal dialysis patients and patients with chronic renal disease.

      Chi C, Patel P, Pilishvili T, Moore M, Murphy T, Strikas R. Guidelines for vaccinating dialysis patients and patients with chronic kidney disease. US Department of Health and Human Services, CDC, Advisory Committee on Immunization Practices (ACIP); 2012, p. 12.

      Ministério da Saúde/SVS/DVE. Manual dos centros de referência para imunobiológicos especiais. Brasilia: Ministério da Saúde; 2006.

      The aim of this study was to assess the YF vaccination status and vaccine safety in dialysis patients.

      2. Methods

      A cross-sectional study assessing the YF immunization of adult patients with chronic kidney disease on regular dialysis therapy at the São Carlos Dialysis Service (Serviço de Nefrologia de São Carlos), São Carlos, SP, Brazil, was performed from August 2012 to March 2014. The Investigational Review Board of the Universidade Federal de São Carlos approved this study (CAAE00631012.0.0000.5504). The São Carlos Dialysis Service is a hospital-based unit that has 29 dialysis stations, with two isolation stations for patients with hepatitis B and hepatitis C, respectively. All adult patients (over 18 years old) on regular dialysis who agreed to participate and provided informed consent were included in the study.
      Patients underwent a structured interview and a review of medical and immunization charts during dialysis sessions, using an Epi Info version 3.5.1 questionnaire. Data were collected on sex, age, provenance, comorbidities, alcohol intake, smoking, type of kidney disease,
      • Levey A.S.
      • de Jong P.E.
      • Coresh J.
      • El Nahas M.
      • Astor B.C.
      • Matsushita K.
      • et al.
      The definition, classification, and prognosis of chronic kidney disease: a KDIGO Controversies Conference report.
      • Levey A.S.
      • Eckardt K.U.
      • Tsukamoto Y.
      • Levin A.
      • Coresh J.
      • Rossert J.
      • et al.
      Definition and classification of chronic kidney disease: a position statement from Kidney Disease: Improving Global Outcomes (KDIGO).
      duration of renal dysfunction and time on dialysis, current dialysis method, previous kidney transplantation, nutritional status,
      • Coutinho W.
      Consenso Latino-Americano de obesidade.
      use of immunosuppressive therapy, and YF vaccine status. Only immunization charts that had been filled out with information on YF vaccine were considered. Verbal information not recorded on the vaccination chart was ignored.
      Patients not vaccinated against YF or without a booster vaccination within the last 10 years were referred to receive the vaccine at the nearest basic health unit. YF vaccine was considered contraindicated in those with a severe immunodeficiency, defined by the diagnosis of a severe primary or secondary immunodeficiency, or by the use of high-dose steroids (at least 20 mg per day of prednisone or equivalent doses of other steroids), cancer chemotherapy, or radiation therapy in the last 3 months.

      Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de Vigilância das Doenças Transmissíveis. Manual of rules and procedures for vaccination. Brasília: Ministério da Saúde; 2014, p. 176.

      The dialysis service operates three shifts per day, 6 days a week. The patients were interviewed by three researchers. For the initial evaluation, each researcher returned at least twice per shift to interview all of the patients. After referring the patients for vaccination, the researchers returned at least 10 times per shift during the study period to assess compliance with the immunization and any untoward medical occurrences within 30 days after vaccination. Each patient was followed for at least 2 months. In the case of difficulty in follow-up, patients were contacted by telephone. Any adverse events were evaluated, counted, and classified in terms of extension (local versus systemic) and nature (fever, hypersensitivity, neurological, or viscerotropic disease).
      Data were collected and analyzed using Epi Info version 3.5.1 software; a descriptive statistical analysis was performed. Demographic, clinical, and YF vaccination characteristics of chronic kidney disease patients on dialysis were described. Frequency distribution tables were used for categorical variables and dispersion measurements were used for quantitative variables. Subsequently, frequency and type of adverse events were described in YF vaccinated patients.

      3. Results

      From a total of 181 chronic kidney disease patients on regular dialysis treatment at the dialysis service, 130 were effectively included in this study (Figure 1). Among the 35 patients who did not sign the informed consent form, three were in a severe clinical condition that required hospitalization and the other 32 did not consent and refused to participate.
      Figure thumbnail gr1
      Figure 1Flow diagram of patients with chronic kidney disease on dialysis included in the study (YF, yellow fever; *referred for YF vaccination).
      Most patients were male (63.8%) and white (50.8%); their mean age was 53.9 years. Current smoking and alcohol intake were reported by 13.8% and 12.3% of the patients, respectively. The most common comorbidities were hypertension (83.8%) and diabetes mellitus (26.9%). Vascular disease was the leading cause of renal loss (41.5%), followed by diabetes mellitus (23.1%), tubulointerstitial disease (16.2%), and glomerular disease (12.3%). The median time on dialysis was 12 months (interquartile range 4–48 months). Thirteen patients had returned to dialysis after kidney graft failure, and one of them was on low-dose corticosteroid therapy. The majority of patients (70%) had a normal weight; six were in a state of emaciation (4.6%) and the remaining patients were overweight/obese to some degree (23.1%) (Table 1).
      Table 1Demographic, clinical, and pathological characteristics of 130 dialysis patients at the Serviço de Nefrologia de São Carlos—2013
      CharacteristicTotalYF vaccinated patients
      Patients who were referred and received YF vaccine during the study period.
      Sex, male, n (%)83 (63.8)32 (71.1)
      Age, years, mean ± SD53.9 ± 14.953.8 ± 15.2
      Color/ethnicity, n (%)
       White66 (50.8)26 (57.8)
       Brown44 (33.8)16 (35.6)
       Black18 (13.8)2 (4.4)
       Yellow1 (0.8)0 (0.0)
       Indigenous1 (0.8)1 (2.2)
      Smoking, n (%)18 (13.8)7 (15.6)
      Alcohol intake, n (%)16 (12.3)5 (11.1)
      Comorbidities, n (%)
       Systemic arterial hypertension109 (83.8)36 (80)
       Diabetes mellitus35 (26.9)14 (31.1)
       Cancer6 (4.6)1 (2.2)
        Skin2 (1.5)1 (2.2)
        Prostate2 (1.5)0 (0.0)
        Mouth and kidney1 (0.8)0 (0.0)
        Multiple myeloma1 (0.8)0 (0.0)
       Rheumatologic diseases2 (1.5)0 (0.0)
      Pathological type of kidney disease, n (%)
       Vascular disease54 (41.5)19 (42.2)
       Diabetes mellitus30 (23.1)11 (24.4)
       Tubulointerstitial disease21 (16.2)7 (15.6)
       Glomerular disease16 (12.3)3 (6.7)
       Polycystic kidney disease4 (3.1)2 (4.4)
       Unknown3 (2.3)2 (4.4)
       Graft loss2 (1.5)1 (2.2)
      Duration of renal failure, months, median (IQR)25 (8–84)36 (8–96)
      Time on dialysis, months, median (IQR)12 (4–48)24 (5–48)
      Kidney transplant, n (%)13 (10)5 (11.1)
      Use of immunosuppressive drugs1 (0.8)0 (0.0)
      YF, yellow fever; SD, standard deviation; IQR, interquartile range.
      a Patients who were referred and received YF vaccine during the study period.
      Previous YF vaccination within the last 10 years was observed in 44 patients (33.8%), and more than 10 years ago in 26 patients (20%), with no mention of adverse effects. Thirty-six patients had never been vaccinated (27.7%) and 24 patients had an unknown vaccination status (18.5%).
      Of the total 86 patients with an indication for YF revaccination, only 45 actually received the vaccine after referral. Patients were undergoing hemodialysis three times a week in sessions lasting 3–5 h each. Some of them had transport barriers, such as low income and limited mobility. Some patients complained that it was necessary to go to the basic health unit more than once to obtain the YF vaccine. At the end of the study, the remaining 41 unvaccinated patients were referred again to receive the YF vaccine.
      Among the 45 effectively vaccinated patients, 21 had never been vaccinated before, nine had an unknown vaccination status, and 15 had been vaccinated more than 10 years ago (Figure 1). Adverse events were reported by 12/45 vaccinated patients (26.7%); mild local adverse events occurred in 11/45 patients, with pain in all of them and edema in three patients. Six patients who complained of local pain and three patients who reported localized edema had received a pneumococcal vaccine on the same day. Two patients developed fever, which resolved less than 24 h later. No patient developed anaphylaxis, or viscerotropic or neurological disease (Table 2).
      Table 2Adverse effects of yellow fever vaccination in 45 dialysis patients at the Serviço de Nefrologia de São Carlos—2013
      PatientSexAge, yearsComorbidityKidney diseaseTransplantDuration of renal failure, monthsTime on dialysis, monthsYF vaccine adverse effects
      Local
      P, pain; E, edema; R, redness.
      Systemic
      1
      Concomitant pneumococcal vaccination.
      F64AHVDNo7212PNo
      2F55AH/DMDMNo4848PNo
      3
      Concomitant pneumococcal vaccination.
      M51NoneUNNo13260P/ENo
      4M46NoneUNNo74PFever
      5M60AH/DMDMNo86PNo
      6F31AHGLYes12296NoFever
      7M59AHPKDYes156156PNo
      8
      Concomitant pneumococcal vaccination.
      F32AH/DMDMNo121P/E/RNo
      9
      Concomitant pneumococcal vaccination.
      M42AHTDNo606PNo
      10
      Concomitant pneumococcal vaccination.
      F73AH/DMDMNo2424P/E/RNo
      11
      Concomitant pneumococcal vaccination.
      F52AH/DMDMNo4812P/RNo
      12F57AHVDNo96PNo
      F, female; M, male; AH, arterial hypertension; DM, diabetes mellitus; VD, vascular disease; UN, unknown; GL, graft loss; PKD, polycystic kidney disease; TD, tubulointerstitial disease.
      a P, pain; E, edema; R, redness.
      b Concomitant pneumococcal vaccination.

      4. Discussion

      The present study found a low YF vaccine coverage in dialysis patients, with an occasional occurrence of minor adverse reactions. São Carlos is considered a transitional area for the risk of YF transmission, and YF vaccination with a booster every 10 years is recommended in this area.

      Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de Vigilância das Doenças Transmissíveis. Manual of rules and procedures for vaccination. Brasília: Ministério da Saúde; 2014, p. 176.

      There is concern whether this recommendation has been sufficiently followed by the health care services.
      Despite the recommendation, the proportion of hemodialysis patients who had been vaccinated less than 10 years ago was low (33%). The patients who were up to date with the YF vaccine had been vaccinated during the 2008 immunization campaign, when cases of the disease occurred in the region .

      Ministério da Saúde/SVS. Emergências em Saúde Pública de Importância Nacional (ESPIN) de Febre Amarela Silvestre em São Paulo e no Rio Grande do Sul e a Situação Epidemiológica Atual no Brasil (2008/2009). Brasília: Ministério da Saúde; 2009, p. 10.

      More recently, the guidelines of the Brazilian national immunization policy have recommended a single booster dose at 10 years after the primary YF vaccination .

      Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de Vigilância das Doenças Transmissíveis. Nota informativa n.143/CGPNI/DEVIT/SVS/MS de 18 de dezembro de 2014. Recomendações da vacinação contra a febre amarela, após a declaração da Organização Mundial da Saúde. Brasília: Ministério da Saúde; 2014.

      However, even considering the new World Health Organization (WHO) recommendation of a single dose of YF vaccine to confer lifelong protection,
      World Health Organization
      Vaccines and vaccination against yellow fever: WHO Position Paper, June 2013—recommendations.
      there would be only 70 patients (53.8%) with adequate YF vaccination. The 26 patients vaccinated more than 10 years ago had received the YF vaccine in the year 1992. This was probably associated with the introduction of YF vaccine in the routine immunization services of permanently endemic areas in 1991.

      Fundação Nacional de Saúde. 100 anos de saúde pública: a visão da Funasa. Brasília: Fundação Nacional de Saúde; 2004.

      There was no report of adverse events in the 70 subjects who had previously been vaccinated, but the data may be underestimated.
      Of the 86 dialysis patients with chronic renal failure who were referred for vaccination against YF, only 45 actually received the vaccine. This was probably due to several factors, such as non-availability of the YF vaccine in dialysis centers and vaccine hesitance among patients and health care workers.
      • Stefanelli P.
      • Rezza G.
      Contrasting the anti-vaccine prejudice: a public health perspective. Commentary.

      Centers for Disease Control and Prevention. History of vaccine safety. Vaccine safety. Atlanta, GA: CDC; 2011.

      The irregularity in vaccine availability in basic health units certainly played an important role in reducing vaccine uptake.
      • Gouws E.
      • Bryce J.
      • Pariyo G.
      • Armstrong Schellenberg J.
      • Amaral J.
      • Habicht J.P.
      Measuring the quality of child health care at first-level facilities.
      YF vaccine is contraindicated for people with a severe immunodeficiency, malignant neoplasm, transplantation, or whose immunological response is affected by drugs or radiation, because they are presumably at increased risk of serious adverse events.
      World Health Organization
      Vaccines and vaccination against yellow fever: WHO Position Paper, June 2013—recommendations.
      Patients with thymus disorders, such as thymoma or myasthenia gravis, are demonstrably more vulnerable to YF vaccine-associated serious adverse events.
      • DeSilva M.
      • Sharma A.
      • Staples E.
      • Arndt B.
      • Shieh W.J.
      • Shames J.
      • Cieslak P.
      Centers for Disease Control and Prevention. Notes from the field: fatal yellow fever vaccine-associated viscerotropic disease—Oregon, September 2014.
      However, there is growing evidence that YF vaccine is relatively safe in mild or moderately immunocompromised patients, such as in asymptomatic HIV-infected patients,
      • Sidibe M.
      • Yactayo S.
      • Kalle A.
      • Sall A.A.
      • Sow S.
      • Ndoutabe M.
      • et al.
      Immunogenicity and safety of yellow fever vaccine among 115 HIV-infected patients after a preventive immunisation campaign in Mali.
      rheumatologic patients on immunosuppressants,
      • Mota L.M.
      Vaccination against yellow fever among patients on immunosuppressors with diagnoses of rheumatic diseases.
      and even in some organ transplanted patients.
      • Azevedo L.S.
      • Lasmar E.P.
      • Contieri F.L.
      • Boin I.
      • Percegona L.
      • Saber L.T.
      • et al.
      Yellow fever vaccination in organ transplanted patients: is it safe?. A multicenter study.
      In line with population-based studies and pharmacovigilance databases,
      • Thomas R.E.
      • Lorenzetti D.L.
      • Spragins W.
      • Jackson D.
      • Williamson T.
      Active and passive surveillance of yellow fever vaccine 17D or 17DD-associated serious adverse events: systematic review.
      and although chronic renal failure is associated with both cellular and humoral immune dysfunction, no serious YF vaccine adverse effects occurred during the follow-up of these patients (anaphylaxis, neurological or viscerotropic disease). The high frequency of mild local adverse effects was probably associated with the concomitant use of anti-pneumococcal vaccine.
      Despite YF vaccine appearing to be safe in patients with chronic renal dialysis, the data obtained in this study are not robust enough to strongly recommend YF vaccine for all dialysis patients. Further studies with aggregate data should be performed. Conclusions regarding the safety of YF vaccine in dialysis patients are limited by the small study population and by the fact that prior YF vaccination could have diminished the expected incidence of serious adverse effects, so far only reported in first-time vaccinees.

      Acknowledgements

      We are grateful for the interest and support of Dr Afonso Thadeu de Souza Pannacci and Dr Fabrizio Margarido Albertini from the Serviço de Nefrologia de São Carlos. We would like to thank Blaranis Helena Paulletto from Centro de Municipal de Especialidades de São Carlos for support in the implementation of the Ambulatório de Imunização em Populações Especiais (Immunization Outpatient Clinic for Special Populations). We would also like to acknowledge the help of Andréa Cruz Ferraz de Oliveira in the study design and collection of data. This work was supported in part by FAPESP (Fundação de Amparo à Pesquisa do Estado de São Paulo; grant 2013/16215-6 (TF) and grant 2013/16207-3 (MNCG)).
      Conflict of interest: The authors declare that there are no conflicts of interest.
      Author contributions: TF, MNCG, and SDSS conceived the study, participated in its design, performed the data collection and statistical analysis, and drafted the manuscript. All authors read and approved the final manuscript.

      References

        • Câmara F.P.
        • Gomes A.L.
        • Carvalho L.M.
        • Castello L.G.
        Dynamic behavior of sylvatic yellow fever in Brazil (1954-2008).
        Rev Soc Bras Med Trop. 2011; 44: 297-299
        • Costa Z.G.
        • Romano A.P.
        • Elkhoury A.N.
        • Flannery B.
        Historical development and evolution of epidemiological surveillance and control of yellow fever in Brazil.
        Rev Pan Am Saude. 2011; 2: 11-26
        • Martins R.M.
        • Maia M.L.
        • dos Santos E.M.
        • Cruz L.S.
        • dos Santos P.R.
        • Deotti Carvalho S.M.
        • et al.
        Yellow fever vaccine post-marketing surveillance in Brazil.
        Global Vaccine Research Forum. 2010; 2: 178-183
        • Lindsey N.P.
        • Schroeder B.A.
        • Miller E.R.
        • Braun M.M.
        • Hinckley A.F.
        • Marano N.
        • et al.
        Adverse event reports following yellow fever vaccination.
        Vaccine. 2008; 26: 6077-6082
        • Biscayart C.
        • Carrega M.E.
        • Sagradini S.
        • Gentile A.
        • Stecher D.
        • Orduna T.
        • et al.
        Yellow fever vaccine-associated adverse events following extensive immunization in Argentina.
        Vaccine. 2014; 32: 1266-1272
        • Martins R.M.
        • Pavão A.L.
        • de Oliveira P.M.
        • dos Santos P.R.
        • Carvalho S.M.
        • Mohrdieck R.
        • et al.
        Adverse events following yellow fever immunization: report and analysis of 67 neurological cases in Brazil.
        Vaccine. 2014; 32: 6676-6682
      1. Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de Vigilância das Doenças Transmissíveis. Manual of rules and procedures for vaccination. Brasília: Ministério da Saúde; 2014, p. 176.

        • Staples J.E.
        • Gershman M.
        • Fischer M.
        Centers for Disease Control and Prevention. Yellow fever vaccine: recommendations of the Advisory Committee on Immunization Practices (ACIP).
        MMWR Recomm Rep. 2010; 59: 1-27
        • Azevedo L.S.
        • Lasmar E.P.
        • Contieri F.L.
        • Boin I.
        • Percegona L.
        • Saber L.T.
        • et al.
        Yellow fever vaccination in organ transplanted patients: is it safe?. A multicenter study.
        Transpl Infect Dis. 2012; 14: 237-241
        • Mota L.M.
        Vaccination against yellow fever among patients on immunosuppressors with diagnoses of rheumatic diseases.
        Rev Soc Bras Med Trop. 2009; 42: 23-27
        • Engelich G.
        • Wright D.G.
        • Hartshorn K.L.
        Acquired disorders of phagocyte function complicating medical and surgical illnesses.
        Clin Infect Dis. 2001; 33: 2040-2048
        • Kato S.
        • Chmielewski M.
        • Honda H.
        • Pecoits-Filho R.
        • Matsuo S.
        • Yuzawa Y.
        • et al.
        Aspects of immune dysfunction in end-stage renal disease.
        Clin J Am Soc Nephrol. 2008; 3: 1526-1533
        • Jentes E.S.
        • Poumerol G.
        • Gershman M.D.
        • Hill D.R.
        • Lemarchand J.
        • Lewis R.F.
        • et al.
        Informal WHO Working Group on Geographic Risk for Yellow Fever. The revised global yellow fever risk map and recommendations for vaccination, 2010: consensus of the Informal WHO Working Group on Geographic Risk for Yellow Fever.
        Lancet Infect Dis. 2011; 11: 622-632
        • Hill D.R.
        Mapping the risk of yellow fever infection.
        Curr Infect Dis Rep. 2012; 14: 246-255
      2. Chi C, Patel P, Pilishvili T, Moore M, Murphy T, Strikas R. Guidelines for vaccinating dialysis patients and patients with chronic kidney disease. US Department of Health and Human Services, CDC, Advisory Committee on Immunization Practices (ACIP); 2012, p. 12.

      3. Ministério da Saúde/SVS/DVE. Manual dos centros de referência para imunobiológicos especiais. Brasilia: Ministério da Saúde; 2006.

        • Levey A.S.
        • de Jong P.E.
        • Coresh J.
        • El Nahas M.
        • Astor B.C.
        • Matsushita K.
        • et al.
        The definition, classification, and prognosis of chronic kidney disease: a KDIGO Controversies Conference report.
        Kidney Int. 2011; 80: 17-28
        • Levey A.S.
        • Eckardt K.U.
        • Tsukamoto Y.
        • Levin A.
        • Coresh J.
        • Rossert J.
        • et al.
        Definition and classification of chronic kidney disease: a position statement from Kidney Disease: Improving Global Outcomes (KDIGO).
        Kidney Int. 2005; 67: 2089-2100
        • Coutinho W.
        Consenso Latino-Americano de obesidade.
        Arq Bras Endocrinol Metabol. 1999; 43: 21-67
      4. Ministério da Saúde/SVS. Emergências em Saúde Pública de Importância Nacional (ESPIN) de Febre Amarela Silvestre em São Paulo e no Rio Grande do Sul e a Situação Epidemiológica Atual no Brasil (2008/2009). Brasília: Ministério da Saúde; 2009, p. 10.

      5. Ministério da Saúde, Secretaria de Vigilância em Saúde, Departamento de Vigilância das Doenças Transmissíveis. Nota informativa n.143/CGPNI/DEVIT/SVS/MS de 18 de dezembro de 2014. Recomendações da vacinação contra a febre amarela, após a declaração da Organização Mundial da Saúde. Brasília: Ministério da Saúde; 2014.

        • World Health Organization
        Vaccines and vaccination against yellow fever: WHO Position Paper, June 2013—recommendations.
        Vaccine. 2015; 33: 76-77
      6. Fundação Nacional de Saúde. 100 anos de saúde pública: a visão da Funasa. Brasília: Fundação Nacional de Saúde; 2004.

        • Stefanelli P.
        • Rezza G.
        Contrasting the anti-vaccine prejudice: a public health perspective. Commentary.
        Ann Ist Super Sanita. 2014; 50: 6-9
      7. Centers for Disease Control and Prevention. History of vaccine safety. Vaccine safety. Atlanta, GA: CDC; 2011.

        • Gouws E.
        • Bryce J.
        • Pariyo G.
        • Armstrong Schellenberg J.
        • Amaral J.
        • Habicht J.P.
        Measuring the quality of child health care at first-level facilities.
        Soc Sci Med. 2005; 61: 613-625
        • DeSilva M.
        • Sharma A.
        • Staples E.
        • Arndt B.
        • Shieh W.J.
        • Shames J.
        • Cieslak P.
        Centers for Disease Control and Prevention. Notes from the field: fatal yellow fever vaccine-associated viscerotropic disease—Oregon, September 2014.
        MMWR Morb Mortal Wkly Rep. 2015; 64: 279-281
        • Sidibe M.
        • Yactayo S.
        • Kalle A.
        • Sall A.A.
        • Sow S.
        • Ndoutabe M.
        • et al.
        Immunogenicity and safety of yellow fever vaccine among 115 HIV-infected patients after a preventive immunisation campaign in Mali.
        Trans R Soc Trop Med Hyg. 2012; 106: 437-444
        • Thomas R.E.
        • Lorenzetti D.L.
        • Spragins W.
        • Jackson D.
        • Williamson T.
        Active and passive surveillance of yellow fever vaccine 17D or 17DD-associated serious adverse events: systematic review.
        Vaccine. 2011; 29: 4544-4555