Skip to main content
Top
Published in: BMC Immunology 1/2019

Open Access 01-12-2019 | Primary Immunodeficiency | Research article

Pneumococcal vaccination responses in adults with subnormal IgG subclass concentrations

Authors: Antony R. Parker, Markus Skold, Stephen Harding, J. Clayborn Barton, Luigi F. Bertoli, James C. Barton

Published in: BMC Immunology | Issue 1/2019

Login to get access

Abstract

Background

We sought to compare Pneumovax®23 responses in adults with subnormal IgG subclass concentrations. We studied adults with normal total IgG, frequent/severe respiratory infection, and subnormal IgG1, IgG3, or IgG1 + IgG3 before and after Pneumovax®23. We defined response as serotype-specific IgG > 1.3 μg/mL and aggregate response as IgG > 1.3 μg/mL for ≥70% of all serotypes tested. We compared patients with and without serotype-specific responses and performed logistic regression on aggregate responses using: age; male sex; body mass index; autoimmune condition(s); atopy; other allergies; subnormal IgGSc immunophenotypes; IgA; and IgM.

Results

There were 59 patients (mean age 44 ± 13 (SD) years; 83.1% women). Median days between pre- and post-Pneumovax®23 testing was 33 (range 19–158). The median post-vaccination summated concentration of serotype-specific IgG was higher in patients with subnormal IgG1 than subnormal IgG3 (responders and non-responders). All subnormal IgG1 + IgG3 non-responders responded to serotypes 8, 9 and 26, unlike other non-responders. Subnormal IgG3 responders had lower responses to serotypes 1, 4, 12, 23, 26, and 51. Subnormal IgG3 non-responders had higher responses to serotypes 1, 3, 8, 9, 12, 14, 19, 51, and 56. Response rates decreased with increasing age. Aggregate responders were: subnormal IgG1, 54%; IgG3, 46%; and IgG1 + IgG3, 46%. Regression on aggregate response revealed lower response with male sex (odds ratio 0.09 [95% CI 0.01, 0.77]) and atopy (0.17 [0.03, 0.83]).

Conclusions

Serotype-specific IgG responses to Pneumovax®23 were greater in patients with subnormal IgG1 than subnormal IgG3. Male sex and atopy were associated with lower aggregate responses.
Literature
1.
go back to reference Bonilla FA, Bernstein IL, Khan DA, Ballas ZK, Chinen J, Frank MM, Kobrynski LJ, Levinson AI, Mazer B, Nelson RP Jr, et al. Practice parameter for the diagnosis and management of primary immunodeficiency. Ann Allergy Asthma Immunol. 2005;94(5 Suppl 1):S1–63.PubMedCrossRef Bonilla FA, Bernstein IL, Khan DA, Ballas ZK, Chinen J, Frank MM, Kobrynski LJ, Levinson AI, Mazer B, Nelson RP Jr, et al. Practice parameter for the diagnosis and management of primary immunodeficiency. Ann Allergy Asthma Immunol. 2005;94(5 Suppl 1):S1–63.PubMedCrossRef
2.
go back to reference Bonilla FA, Khan DA, Ballas ZK, Chinen J, Frank MM, Hsu JT, Keller M, Kobrynski LJ, Komarow HD, Mazer B, et al. Practice parameter for the diagnosis and management of primary immunodeficiency. J Allergy Clin Immunol. 2015;136(5):1186–205.PubMedCrossRef Bonilla FA, Khan DA, Ballas ZK, Chinen J, Frank MM, Hsu JT, Keller M, Kobrynski LJ, Komarow HD, Mazer B, et al. Practice parameter for the diagnosis and management of primary immunodeficiency. J Allergy Clin Immunol. 2015;136(5):1186–205.PubMedCrossRef
3.
go back to reference Picard C, Bobby Gaspar H, Al-Herz W, Bousfiha A, Casanova JL, Chatila T, Crow YJ, Cunningham-Rundles C, Etzioni A, Franco JL, et al. International Union of Immunological Societies: 2017 primary immunodeficiency diseases committee report on inborn errors of immunity. J Clin Immunol. 2018;38(1):96–128.PubMedCrossRef Picard C, Bobby Gaspar H, Al-Herz W, Bousfiha A, Casanova JL, Chatila T, Crow YJ, Cunningham-Rundles C, Etzioni A, Franco JL, et al. International Union of Immunological Societies: 2017 primary immunodeficiency diseases committee report on inborn errors of immunity. J Clin Immunol. 2018;38(1):96–128.PubMedCrossRef
4.
go back to reference Ferrante A, Beard LJ, Feldman RG. IgG subclass distribution of antibodies to bacterial and viral antigens. Pediatr Infect Dis J. 1990;9(8 Suppl):S16–24.PubMed Ferrante A, Beard LJ, Feldman RG. IgG subclass distribution of antibodies to bacterial and viral antigens. Pediatr Infect Dis J. 1990;9(8 Suppl):S16–24.PubMed
6.
go back to reference Parker A, Irure Ventura J, Sims D, Echeverria de Carlos A, Gomez de la Torre R, Tricas Aizpun L, et al. Measurement of the IgG2 response to pneumococcal capsular polysaccharides may identify an antibody deficiency in individuals referred for immunological investigation. J Immunoassay Immunochem. 2017;38:514–22.PubMedCrossRef Parker A, Irure Ventura J, Sims D, Echeverria de Carlos A, Gomez de la Torre R, Tricas Aizpun L, et al. Measurement of the IgG2 response to pneumococcal capsular polysaccharides may identify an antibody deficiency in individuals referred for immunological investigation. J Immunoassay Immunochem. 2017;38:514–22.PubMedCrossRef
7.
go back to reference Lacombe C, Aucouturier P, Preud'homme JL. Selective IgG1 deficiency. Clin Immunol Immunopathol. 1997;84(2):194–201.PubMedCrossRef Lacombe C, Aucouturier P, Preud'homme JL. Selective IgG1 deficiency. Clin Immunol Immunopathol. 1997;84(2):194–201.PubMedCrossRef
8.
go back to reference Barton JC, Bertoli LF, Barton JC, Acton RT. Selective subnormal IgG1 in 54 adult index patients with frequent or severe bacterial respiratory tract infections. J Immunol Res. 2016;2016:1405950.PubMedPubMedCentralCrossRef Barton JC, Bertoli LF, Barton JC, Acton RT. Selective subnormal IgG1 in 54 adult index patients with frequent or severe bacterial respiratory tract infections. J Immunol Res. 2016;2016:1405950.PubMedPubMedCentralCrossRef
9.
go back to reference Siber GR, Schur PH, Aisenberg AC, Weitzman SA, Schiffman G. Correlation between serum IgG-2 concentrations and the antibody response to bacterial polysaccharide antigens. N Engl J Med. 1980;303(4):178–82.PubMedCrossRef Siber GR, Schur PH, Aisenberg AC, Weitzman SA, Schiffman G. Correlation between serum IgG-2 concentrations and the antibody response to bacterial polysaccharide antigens. N Engl J Med. 1980;303(4):178–82.PubMedCrossRef
10.
go back to reference Barrett DJ, Ayoub EM. IgG2 subclass restriction of antibody to pneumococcal polysaccharides. Clin Exp Immunol. 1986;63(1):127–34.PubMedPubMedCentral Barrett DJ, Ayoub EM. IgG2 subclass restriction of antibody to pneumococcal polysaccharides. Clin Exp Immunol. 1986;63(1):127–34.PubMedPubMedCentral
11.
go back to reference Hammarström L, Smith CI. IgG2 deficiency in a healthy blood donor. Concomitant lack of IgG2, IgA and IgE immunoglobulins and specific anti-carbohydrate antibodies. Clin Exp Immunol. 1983;51(3):600–4.PubMedPubMedCentral Hammarström L, Smith CI. IgG2 deficiency in a healthy blood donor. Concomitant lack of IgG2, IgA and IgE immunoglobulins and specific anti-carbohydrate antibodies. Clin Exp Immunol. 1983;51(3):600–4.PubMedPubMedCentral
12.
go back to reference Kuijpers TW, Weening RS, Out TA. IgG subclass deficiencies and recurrent pyogenic infections, unresponsiveness against bacterial polysaccharide antigens. Allergol Immunopathol (Madr). 1992;20(1):28–34. Kuijpers TW, Weening RS, Out TA. IgG subclass deficiencies and recurrent pyogenic infections, unresponsiveness against bacterial polysaccharide antigens. Allergol Immunopathol (Madr). 1992;20(1):28–34.
13.
go back to reference Oxelius VA, Hanson LA, Björkander J, Hammarström L, Sjöholm A. IgG3 deficiency: common in obstructive lung disease. Hereditary in families with immunodeficiency and autoimmune disease. Monogr Allergy. 1986;20:106–15.PubMed Oxelius VA, Hanson LA, Björkander J, Hammarström L, Sjöholm A. IgG3 deficiency: common in obstructive lung disease. Hereditary in families with immunodeficiency and autoimmune disease. Monogr Allergy. 1986;20:106–15.PubMed
14.
go back to reference Barton JC, Bertoli LF, Acton RT. HLA-A and -B alleles and haplotypes in 240 index patients with common variable immunodeficiency and selective IgG subclass deficiency in Central Alabama. BMC Med Genet. 2003;4:3.PubMedPubMedCentralCrossRef Barton JC, Bertoli LF, Acton RT. HLA-A and -B alleles and haplotypes in 240 index patients with common variable immunodeficiency and selective IgG subclass deficiency in Central Alabama. BMC Med Genet. 2003;4:3.PubMedPubMedCentralCrossRef
15.
go back to reference Aalberse RC, Stapel SO, Schuurman J, Rispens T. Immunoglobulin G4: an odd antibody. Clin Exp Allergy. 2009;39(4):469–77.PubMedCrossRef Aalberse RC, Stapel SO, Schuurman J, Rispens T. Immunoglobulin G4: an odd antibody. Clin Exp Allergy. 2009;39(4):469–77.PubMedCrossRef
16.
go back to reference Adjobimey T, Hoerauf A. Induction of immunoglobulin G4 in human filariasis: an indicator of immunoregulation. Ann Trop Med Parasitol. 2010;104(6):455–64.PubMedPubMedCentralCrossRef Adjobimey T, Hoerauf A. Induction of immunoglobulin G4 in human filariasis: an indicator of immunoregulation. Ann Trop Med Parasitol. 2010;104(6):455–64.PubMedPubMedCentralCrossRef
17.
go back to reference Sorensen RU, Hidalgo H, Moore C, Leiva LE. Post-immunization pneumococcal antibody titers and IgG subclasses. Pediatr Pulmonol. 1996;22(3):167–73.PubMedCrossRef Sorensen RU, Hidalgo H, Moore C, Leiva LE. Post-immunization pneumococcal antibody titers and IgG subclasses. Pediatr Pulmonol. 1996;22(3):167–73.PubMedCrossRef
18.
go back to reference Abrahamian F, Agrawal S, Gupta S. Immunological and clinical profile of adult patients with selective immunoglobulin subclass deficiency: response to intravenous immunoglobulin therapy. Clin Exp Immunol. 2010;159(3):344–50.PubMedPubMedCentralCrossRef Abrahamian F, Agrawal S, Gupta S. Immunological and clinical profile of adult patients with selective immunoglobulin subclass deficiency: response to intravenous immunoglobulin therapy. Clin Exp Immunol. 2010;159(3):344–50.PubMedPubMedCentralCrossRef
19.
go back to reference Barton JC, Bertoli LF, Barton JC, Acton RT. Selective subnormal IgG3 in 121 adult index patients with frequent or severe bacterial respiratory tract infections. Cell Immunol. 2016;299:50–7.PubMedCrossRef Barton JC, Bertoli LF, Barton JC, Acton RT. Selective subnormal IgG3 in 121 adult index patients with frequent or severe bacterial respiratory tract infections. Cell Immunol. 2016;299:50–7.PubMedCrossRef
20.
go back to reference May A, Zielen S, von Ilberg C, Weber A. Immunoglobulin deficiency and determination of pneumococcal antibody titers in patients with therapy-refractory recurrent rhinosinusitis. Eur Arch Otorhinolaryngol. 1999;256(9):445–9.PubMedCrossRef May A, Zielen S, von Ilberg C, Weber A. Immunoglobulin deficiency and determination of pneumococcal antibody titers in patients with therapy-refractory recurrent rhinosinusitis. Eur Arch Otorhinolaryngol. 1999;256(9):445–9.PubMedCrossRef
21.
go back to reference Van Kessel DA, Hoffman TW, Van Velzen-Blad H, Zanen P, Rijkers GT, Grutters JC. Response to pneumococcal vaccination in mannose-binding lectin-deficient adults with recurrent respiratory tract infections. Clin Exp Immunol. 2014;177(1):272–9.PubMedPubMedCentralCrossRef Van Kessel DA, Hoffman TW, Van Velzen-Blad H, Zanen P, Rijkers GT, Grutters JC. Response to pneumococcal vaccination in mannose-binding lectin-deficient adults with recurrent respiratory tract infections. Clin Exp Immunol. 2014;177(1):272–9.PubMedPubMedCentralCrossRef
22.
go back to reference Bousfiha A, Jeddane L, Picard C, Ailal F, Bobby Gaspar H, Al-Herz W, Chatila T, Crow YJ, Cunningham-Rundles C, Etzioni A, et al. The 2017 IUIS phenotypic classification for primary Immunodeficiencies. J Clin Immunol. 2018;38(1):129–43.PubMedCrossRef Bousfiha A, Jeddane L, Picard C, Ailal F, Bobby Gaspar H, Al-Herz W, Chatila T, Crow YJ, Cunningham-Rundles C, Etzioni A, et al. The 2017 IUIS phenotypic classification for primary Immunodeficiencies. J Clin Immunol. 2018;38(1):129–43.PubMedCrossRef
23.
go back to reference Barton JC, Bertoli LF, Barton JC. Comparisons of CVID and IgGSD: referring physicians, autoimmune conditions, pneumovax reactivity, immunoglobulin levels, blood lymphocyte subsets, and HLA-A and -B typing in 432 adult index patients. J Immunol Res. 2014;2014:542706.PubMedPubMedCentralCrossRef Barton JC, Bertoli LF, Barton JC. Comparisons of CVID and IgGSD: referring physicians, autoimmune conditions, pneumovax reactivity, immunoglobulin levels, blood lymphocyte subsets, and HLA-A and -B typing in 432 adult index patients. J Immunol Res. 2014;2014:542706.PubMedPubMedCentralCrossRef
24.
go back to reference American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2013;36(Suppl 1):S67–74.CrossRef American Diabetes Association. Diagnosis and classification of diabetes mellitus. Diabetes Care. 2013;36(Suppl 1):S67–74.CrossRef
25.
go back to reference Tomczyk S, Bennett NM, Stoecker C, Gierke R, Moore MR, Whitney CG, Hadler S, Pilishvili T, Centers for Disease C, Prevention. Use of 13-valent pneumococcal conjugate vaccine and 23-valent pneumococcal polysaccharide vaccine among adults aged >/=65 years: recommendations of the advisory committee on immunization practices (ACIP). MMWR Morb Mortal Wkly Rep. 2014;63(37):822–5.PubMedPubMedCentral Tomczyk S, Bennett NM, Stoecker C, Gierke R, Moore MR, Whitney CG, Hadler S, Pilishvili T, Centers for Disease C, Prevention. Use of 13-valent pneumococcal conjugate vaccine and 23-valent pneumococcal polysaccharide vaccine among adults aged >/=65 years: recommendations of the advisory committee on immunization practices (ACIP). MMWR Morb Mortal Wkly Rep. 2014;63(37):822–5.PubMedPubMedCentral
27.
go back to reference Kim JH, Park HJ, Choi GS, Kim JE, Ye YM, Nahm DH, Park HS. Immunoglobulin G subclass deficiency is the major phenotype of primary immunodeficiency in a Korean adult cohort. J Korean Med Sci. 2010;25(6):824–8.PubMedPubMedCentralCrossRef Kim JH, Park HJ, Choi GS, Kim JE, Ye YM, Nahm DH, Park HS. Immunoglobulin G subclass deficiency is the major phenotype of primary immunodeficiency in a Korean adult cohort. J Korean Med Sci. 2010;25(6):824–8.PubMedPubMedCentralCrossRef
28.
go back to reference Weinberger DM, Harboe ZB, Sanders EA, Ndiritu M, Klugman KP, Ruckinger S, Dagan R, Adegbola R, Cutts F, Johnson HL, et al. Association of serotype with risk of death due to pneumococcal pneumonia: a meta-analysis. Clin Infect Dis. 2010;51(6):692–9.PubMedPubMedCentralCrossRef Weinberger DM, Harboe ZB, Sanders EA, Ndiritu M, Klugman KP, Ruckinger S, Dagan R, Adegbola R, Cutts F, Johnson HL, et al. Association of serotype with risk of death due to pneumococcal pneumonia: a meta-analysis. Clin Infect Dis. 2010;51(6):692–9.PubMedPubMedCentralCrossRef
29.
go back to reference Song JY, Nahm MH, Moseley MA. Clinical implications of pneumococcal serotypes: invasive disease potential, clinical presentations, and antibiotic resistance. J Korean Med Sci. 2013;28(1):4–15.PubMedPubMedCentralCrossRef Song JY, Nahm MH, Moseley MA. Clinical implications of pneumococcal serotypes: invasive disease potential, clinical presentations, and antibiotic resistance. J Korean Med Sci. 2013;28(1):4–15.PubMedPubMedCentralCrossRef
30.
go back to reference Grabenstein JD, Musey LK. Differences in serious clinical outcomes of infection caused by specific pneumococcal serotypes among adults. Vaccine. 2014;32(21):2399–405.PubMedCrossRef Grabenstein JD, Musey LK. Differences in serious clinical outcomes of infection caused by specific pneumococcal serotypes among adults. Vaccine. 2014;32(21):2399–405.PubMedCrossRef
31.
32.
go back to reference Kim DG, Kim C, Park S, Jung KS. Incidence of Immunoglobulin G Subclass deficiencies in patients with bronchiectasis and the clinical characteristics of patients with immunoglobulin G subclass deficiency and bronchiectasis; 2009.CrossRef Kim DG, Kim C, Park S, Jung KS. Incidence of Immunoglobulin G Subclass deficiencies in patients with bronchiectasis and the clinical characteristics of patients with immunoglobulin G subclass deficiency and bronchiectasis; 2009.CrossRef
33.
go back to reference Mikolajczyk MG, Concepcion NF, Wang T, Frazier D, Golding B, Frasch CE, Scott DE. Characterization of antibodies to capsular polysaccharide antigens of Haemophilus influenzae type b and Streptococcus pneumoniae in human immune globulin intravenous preparations. Clin Diagn Lab Immunol. 2004;11(6):1158–64.PubMedPubMedCentral Mikolajczyk MG, Concepcion NF, Wang T, Frazier D, Golding B, Frasch CE, Scott DE. Characterization of antibodies to capsular polysaccharide antigens of Haemophilus influenzae type b and Streptococcus pneumoniae in human immune globulin intravenous preparations. Clin Diagn Lab Immunol. 2004;11(6):1158–64.PubMedPubMedCentral
34.
35.
go back to reference Hammarström L, Carbonara AO, DeMarchi M, Lefranc G, Moller G, Smith CI, Zegers BJ. Subclass restriction pattern of antigen-specific antibodies in donors with defective expression of IgG or IgA subclass heavy chain constant region genes. Clin Immunol Immunopathol. 1987;45(3):461–70.PubMedCrossRef Hammarström L, Carbonara AO, DeMarchi M, Lefranc G, Moller G, Smith CI, Zegers BJ. Subclass restriction pattern of antigen-specific antibodies in donors with defective expression of IgG or IgA subclass heavy chain constant region genes. Clin Immunol Immunopathol. 1987;45(3):461–70.PubMedCrossRef
36.
go back to reference Roberton DM, Björkander J, Henrichsen J, Söderström T, Hanson LA. Enhanced IgG1 and IgG3 responses to pneumococcal polysaccharides in isolated IgA deficiency. Clin Exp Immunol. 1989;75(2):201–5.PubMedPubMedCentral Roberton DM, Björkander J, Henrichsen J, Söderström T, Hanson LA. Enhanced IgG1 and IgG3 responses to pneumococcal polysaccharides in isolated IgA deficiency. Clin Exp Immunol. 1989;75(2):201–5.PubMedPubMedCentral
37.
go back to reference Söderström T, Söderström R, Avanzini A, Brandtzaeg P, Karlsson G, Hanson LA. Immunoglobulin G subclass deficiencies. Int Arch Allergy Appl Immunol. 1987;82(3–4):476–80.PubMedCrossRef Söderström T, Söderström R, Avanzini A, Brandtzaeg P, Karlsson G, Hanson LA. Immunoglobulin G subclass deficiencies. Int Arch Allergy Appl Immunol. 1987;82(3–4):476–80.PubMedCrossRef
38.
go back to reference Sarmiento E, Mora R, Rodriguez-Mahou M, Rodriguez-Molina J, Fernandez-Cruz E, Carbone J. Autoimmune disease in primary antibody deficiencies. Allergol Immunopathol (Madr). 2005;33(2):69–73.CrossRef Sarmiento E, Mora R, Rodriguez-Mahou M, Rodriguez-Molina J, Fernandez-Cruz E, Carbone J. Autoimmune disease in primary antibody deficiencies. Allergol Immunopathol (Madr). 2005;33(2):69–73.CrossRef
39.
go back to reference Barlan IB, Geha RS, Schneider LC. Therapy for patients with recurrent infections and low serum IgG3 levels. J Allergy Clin Immunol. 1993;92(2):353–5.PubMedCrossRef Barlan IB, Geha RS, Schneider LC. Therapy for patients with recurrent infections and low serum IgG3 levels. J Allergy Clin Immunol. 1993;92(2):353–5.PubMedCrossRef
40.
go back to reference Falagas ME, Mourtzoukou EG, Vardakas KZ. Sex differences in the incidence and severity of respiratory tract infections. Respir Med. 2007;101(9):1845–63.PubMedCrossRef Falagas ME, Mourtzoukou EG, Vardakas KZ. Sex differences in the incidence and severity of respiratory tract infections. Respir Med. 2007;101(9):1845–63.PubMedCrossRef
41.
go back to reference Park S, Nahm MH. Older adults have a low capacity to opsonize pneumococci due to low IgM antibody response to pneumococcal vaccinations. Infect Immun. 2011;79:314–20.PubMedPubMedCentralCrossRef Park S, Nahm MH. Older adults have a low capacity to opsonize pneumococci due to low IgM antibody response to pneumococcal vaccinations. Infect Immun. 2011;79:314–20.PubMedPubMedCentralCrossRef
42.
go back to reference Parker AR, Park MA, Harding S, Abraham RS. The total IgM, IgA and IgG antibody responses to pneumococcal polysaccharide vaccination (Pneumovax®23) in a healthy adult population and patients diagnosed with primary immunodeficiencies. Vaccine. 2019;37(10):1350–5.PubMedCrossRef Parker AR, Park MA, Harding S, Abraham RS. The total IgM, IgA and IgG antibody responses to pneumococcal polysaccharide vaccination (Pneumovax®23) in a healthy adult population and patients diagnosed with primary immunodeficiencies. Vaccine. 2019;37(10):1350–5.PubMedCrossRef
43.
go back to reference Martin RJ, Kraft M, Chu HW, Berns EA, Cassell GH. A link between chronic asthma and chronic infection. J Allergy Clin Immunol. 2001;107(4):595–601.PubMedCrossRef Martin RJ, Kraft M, Chu HW, Berns EA, Cassell GH. A link between chronic asthma and chronic infection. J Allergy Clin Immunol. 2001;107(4):595–601.PubMedCrossRef
44.
go back to reference Mao W, Cui EH. Distribution of pathogens causing nosocomial infection in patients with bronchial asthma. Genet Mol Res. 2015;14(4):16146–50.PubMedCrossRef Mao W, Cui EH. Distribution of pathogens causing nosocomial infection in patients with bronchial asthma. Genet Mol Res. 2015;14(4):16146–50.PubMedCrossRef
45.
go back to reference Iikura M, Hojo M, Koketsu R, Watanabe S, Sato A, Chino H, Ro S, Masaki H, Hirashima J, Ishii S, et al. The importance of bacterial and viral infections associated with adult asthma exacerbations in clinical practice. PLoS One. 2015;10(4):e0123584.PubMedPubMedCentralCrossRef Iikura M, Hojo M, Koketsu R, Watanabe S, Sato A, Chino H, Ro S, Masaki H, Hirashima J, Ishii S, et al. The importance of bacterial and viral infections associated with adult asthma exacerbations in clinical practice. PLoS One. 2015;10(4):e0123584.PubMedPubMedCentralCrossRef
46.
go back to reference Alho OP, Karttunen R, Karttunen TJ. Nasal mucosa in natural colds: effects of allergic rhinitis and susceptibility to recurrent sinusitis. Clin Exp Immunol. 2004;137(2):366–72.PubMedPubMedCentralCrossRef Alho OP, Karttunen R, Karttunen TJ. Nasal mucosa in natural colds: effects of allergic rhinitis and susceptibility to recurrent sinusitis. Clin Exp Immunol. 2004;137(2):366–72.PubMedPubMedCentralCrossRef
47.
go back to reference Ruben FL, Uhrin M. Specific immunoglobulin-class antibody responses in the elderly before and after 14-valent pneumococcal vaccine. J Infect Dis. 1985;151(5):845–9.PubMedCrossRef Ruben FL, Uhrin M. Specific immunoglobulin-class antibody responses in the elderly before and after 14-valent pneumococcal vaccine. J Infect Dis. 1985;151(5):845–9.PubMedCrossRef
48.
go back to reference Roghmann KJ, Tabloski PA, Bentley DW, Schiffman G. Immune response of elderly adults to pneumococcus: variation by age, sex, and functional impairment. J Gerontol. 1987;42(3):265–70.PubMedCrossRef Roghmann KJ, Tabloski PA, Bentley DW, Schiffman G. Immune response of elderly adults to pneumococcus: variation by age, sex, and functional impairment. J Gerontol. 1987;42(3):265–70.PubMedCrossRef
49.
go back to reference Lottenbach KR, Mink CM, Barenkamp SJ, Anderson EL, Homan SM, Powers DC. Age-associated differences in immunoglobulin G1 (IgG1) and IgG2 subclass antibodies to pneumococcal polysaccharides following vaccination. Infect Immun. 1999;67(9):4935–8.PubMedPubMedCentral Lottenbach KR, Mink CM, Barenkamp SJ, Anderson EL, Homan SM, Powers DC. Age-associated differences in immunoglobulin G1 (IgG1) and IgG2 subclass antibodies to pneumococcal polysaccharides following vaccination. Infect Immun. 1999;67(9):4935–8.PubMedPubMedCentral
50.
go back to reference Romero-Steiner S, Musher DM, Cetron MS, Pais LB, Groover JE, Fiore AE, Plikaytis BD, Carlone GM. Reduction in functional antibody activity against Streptococcus pneumoniae in vaccinated elderly individuals highly correlates with decreased IgG antibody avidity. Clin Infect Dis. 1999;29(2):281–8.PubMedCrossRef Romero-Steiner S, Musher DM, Cetron MS, Pais LB, Groover JE, Fiore AE, Plikaytis BD, Carlone GM. Reduction in functional antibody activity against Streptococcus pneumoniae in vaccinated elderly individuals highly correlates with decreased IgG antibody avidity. Clin Infect Dis. 1999;29(2):281–8.PubMedCrossRef
51.
go back to reference Kolibab K, Smithson SL, Rabquer B, Khuder S, Westerink MA. Immune response to pneumococcal polysaccharides 4 and 14 in elderly and young adults: analysis of the variable heavy chain repertoire. Infect Immun. 2005;73(11):7465–76.PubMedPubMedCentralCrossRef Kolibab K, Smithson SL, Rabquer B, Khuder S, Westerink MA. Immune response to pneumococcal polysaccharides 4 and 14 in elderly and young adults: analysis of the variable heavy chain repertoire. Infect Immun. 2005;73(11):7465–76.PubMedPubMedCentralCrossRef
52.
go back to reference Kim HW, Lee S, Kim KH. Serotype 6B from a pneumococcal polysaccharide vaccine induces cross-functional antibody responses in adults to serotypes 6A, 6C, and 6D. Medicine (Baltimore). 2016;95(37):e4854.CrossRef Kim HW, Lee S, Kim KH. Serotype 6B from a pneumococcal polysaccharide vaccine induces cross-functional antibody responses in adults to serotypes 6A, 6C, and 6D. Medicine (Baltimore). 2016;95(37):e4854.CrossRef
53.
go back to reference Wang X, Stollar BD. Immunoglobulin VH gene expression in human aging. Clin Immunol. 1999;93(2):132–42.PubMedCrossRef Wang X, Stollar BD. Immunoglobulin VH gene expression in human aging. Clin Immunol. 1999;93(2):132–42.PubMedCrossRef
54.
go back to reference Butterworth M, McClellan B, Allansmith M. Influence of sex in immunoglobulin levels. Nature. 1967;214(5094):1224–5.PubMedCrossRef Butterworth M, McClellan B, Allansmith M. Influence of sex in immunoglobulin levels. Nature. 1967;214(5094):1224–5.PubMedCrossRef
55.
go back to reference Rhodes K, Scott A, Markham RL, Monk-Jones ME. Immunological sex differences. A study of patients with rheumatoid arthritis, their relatives, and controls. Ann Rheum Dis. 1969;28(2):104–20.PubMedPubMedCentralCrossRef Rhodes K, Scott A, Markham RL, Monk-Jones ME. Immunological sex differences. A study of patients with rheumatoid arthritis, their relatives, and controls. Ann Rheum Dis. 1969;28(2):104–20.PubMedPubMedCentralCrossRef
56.
go back to reference Kocar IH, Yesilova Z, Ozata M, Turan M, Sengul A, Ozdemir I. The effect of testosterone replacement treatment on immunological features of patients with Klinefelter's syndrome. Clin Exp Immunol. 2000;121(3):448–52.PubMedPubMedCentralCrossRef Kocar IH, Yesilova Z, Ozata M, Turan M, Sengul A, Ozdemir I. The effect of testosterone replacement treatment on immunological features of patients with Klinefelter's syndrome. Clin Exp Immunol. 2000;121(3):448–52.PubMedPubMedCentralCrossRef
57.
go back to reference Sankilampi U, Honkanen PO, Bloigu A, Herva E, Leinonen M. Antibody response to pneumococcal capsular polysaccharide vaccine in the elderly. J Infect Dis. 1996;173(2):387–93.PubMedCrossRef Sankilampi U, Honkanen PO, Bloigu A, Herva E, Leinonen M. Antibody response to pneumococcal capsular polysaccharide vaccine in the elderly. J Infect Dis. 1996;173(2):387–93.PubMedCrossRef
58.
go back to reference Brandao AP, de Oliveira TC, de Cunto Brandileone MC, Goncalves JE, Yara TI, Simonsen V. Persistence of antibody response to pneumococcal capsular polysaccharides in vaccinated long term-care residents in Brazil. Vaccine. 2004;23(6):762–8.PubMedCrossRef Brandao AP, de Oliveira TC, de Cunto Brandileone MC, Goncalves JE, Yara TI, Simonsen V. Persistence of antibody response to pneumococcal capsular polysaccharides in vaccinated long term-care residents in Brazil. Vaccine. 2004;23(6):762–8.PubMedCrossRef
59.
go back to reference Hare ND, Smith BJ, Ballas ZK. Antibody response to pneumococcal vaccination as a function of preimmunization titer. J Allergy Clin Immunol. 2009;123(1):195–200.PubMedCrossRef Hare ND, Smith BJ, Ballas ZK. Antibody response to pneumococcal vaccination as a function of preimmunization titer. J Allergy Clin Immunol. 2009;123(1):195–200.PubMedCrossRef
60.
go back to reference Giudicelli V, Chaume D, Lefranc MP. IMGT/GENE-DB: a comprehensive database for human and mouse immunoglobulin and T cell receptor genes. Nucleic Acids Res. 2005;33(Database issue):D256–61.PubMedCrossRef Giudicelli V, Chaume D, Lefranc MP. IMGT/GENE-DB: a comprehensive database for human and mouse immunoglobulin and T cell receptor genes. Nucleic Acids Res. 2005;33(Database issue):D256–61.PubMedCrossRef
62.
go back to reference Aaberge IS, Michaelsen TE, Heier HE. IgG subclass antibody responses to pneumococcal polysaccharide vaccine in splenectomized, otherwise normal, individuals. Scand J Immunol. 1990;31(6):711–6.PubMedCrossRef Aaberge IS, Michaelsen TE, Heier HE. IgG subclass antibody responses to pneumococcal polysaccharide vaccine in splenectomized, otherwise normal, individuals. Scand J Immunol. 1990;31(6):711–6.PubMedCrossRef
Metadata
Title
Pneumococcal vaccination responses in adults with subnormal IgG subclass concentrations
Authors
Antony R. Parker
Markus Skold
Stephen Harding
J. Clayborn Barton
Luigi F. Bertoli
James C. Barton
Publication date
01-12-2019
Publisher
BioMed Central
Published in
BMC Immunology / Issue 1/2019
Electronic ISSN: 1471-2172
DOI
https://doi.org/10.1186/s12865-019-0310-3

Other articles of this Issue 1/2019

BMC Immunology 1/2019 Go to the issue