Generally, if primary immunodeficiency (PID) is suspected, referral to appropriate specialist centres for further investigations and definitive treatment is necessary; protocols for the different forms of PID vary significantly.
Management of secondary hypogammaglobulinaemia typically involves treating the underlying cause, with specialist referral reserved for selected cases.[2]Otani IM, Lehman HK, Jongco AM, et al. Practical guidance for the diagnosis and management of secondary hypogammaglobulinemia: a Work Group report of the AAAAI Primary Immunodeficiency and Altered Immune Response Committees. J Allergy Clin Immunol. 2022 May;149(5):1525-60.
https://www.jacionline.org/article/S0091-6749(22)00152-X/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/35176351?tool=bestpractice.com
The aim of treatments implemented by specialist centres is to reduce the risk of hypogammaglobulinaemia complications. This typically involves replacement immunoglobulin therapy (intravenous and subcutaneous therapies are both effective and well tolerated) and antibiotics (promptly or as prophylaxis).[35]Gardulf A, Andersen V, Bjorkander J, et al. Subcutaneous immunoglobulin replacement in patients with primary antibody deficiencies: safety and costs. Lancet. 1995;345:365-369.
http://www.ncbi.nlm.nih.gov/pubmed/7845120?tool=bestpractice.com
[36]Chapel HM, Spickett GP, Ericson D, et al. The comparison of the efficacy and safety of intravenous versus subcutaneous immunoglobulin replacement therapy. J Clin Immunol. 2000 Mar;20(2):94-100.
http://www.ncbi.nlm.nih.gov/pubmed/10821460?tool=bestpractice.com
[37]Na IK, Buckland M, Agostini C, et al. Current clinical practice and challenges in the management of secondary immunodeficiency in hematological malignancies. Eur J Haematol. 2019 Jun;102(6):447-56.
https://onlinelibrary.wiley.com/doi/10.1111/ejh.13223
http://www.ncbi.nlm.nih.gov/pubmed/30801785?tool=bestpractice.com
[38]Shrestha P, Karmacharya P, Wang Z, et al. Impact of IVIG vs. SCIG on IgG trough level and infection incidence in primary immunodeficiency diseases: A systematic review and meta-analysis of clinical studies. World Allergy Organ J. 2019 Oct;12(10):100068.
https://www.doi.org/10.1016/j.waojou.2019.100068
http://www.ncbi.nlm.nih.gov/pubmed/31641401?tool=bestpractice.com
[39]Shabaninejad H, Asgharzadeh A, Rezaei N, et al. A comparative study of intravenous immunoglobulin and subcutaneous immunoglobulin in adult patients with primary immunodeficiency diseases: a systematic review and meta-analysis. Expert Rev Clin Immunol. 2016;12(5):595-602.
http://www.ncbi.nlm.nih.gov/pubmed/26902306?tool=bestpractice.com
There are several immunoglobulin products (all primarily containing IgG), with availability being country dependent. Products vary in IgA, stabiliser, and sugar contents, and in viral purification steps. Limited evidence suggests that patients with a complete absence of IgA and presence of anti-IgA antibodies (some combined variable immunodeficiency [CVID] patients) require products with low IgA content in order to reduce the chance of immunoglobulin-related adverse reaction.[40]Horn J, Thon V, Bartonkova D, et al. Anti-IgA antibodies in common variable immunodeficiency (CVID): diagnostic workup and therapeutic strategy. Clin Immunol. 2007 Feb;122(2):156-62.
http://www.ncbi.nlm.nih.gov/pubmed/17137841?tool=bestpractice.com
Lifelong replacement immunoglobulin (with acute antibiotic courses as necessary) is important for patients with PID. There is evidence that patients receiving subcutaneous immunoglobulin at home may have improved health-related quality of life compared with patients administered intravenous immunoglobulin replacement therapy in a hospital setting.[41]Abolhassani H, Sadaghiani MS, Aghamohammadi A, et al. Home-based subcutaneous immunoglobulin versus hospital-based intravenous immunoglobulin in treatment of primary antibody deficiencies: systematic review and meta analysis. J Clin Immunol. 2012 Dec;32(6):1180-92.
http://www.ncbi.nlm.nih.gov/pubmed/22730009?tool=bestpractice.com
[42]Lingman-Framme J, Fasth A. Subcutaneous immunoglobulin for primary and secondary immunodeficiencies: an evidence-based review. Drugs. 2013 Aug;73(12):1307-19.
http://www.ncbi.nlm.nih.gov/pubmed/23861187?tool=bestpractice.com
Patients with secondary hypogammaglobulinaemia might require such treatment only until underlying causes are resolved.
Specialist centre treatment may involve polyethylene glycol-modified adenosine deaminase (PEG-ADA) replacement, Pneumocystis pneumonia prophylaxis, and emerging therapies such as haematopoietic stem cell transplantation (HSCT) and gene therapy.
Significantly reduced total IgG
If primary antibody deficiency syndromes causing marked reduction (<2 standard deviations below the mean) in IgG levels are suspected, patients should be referred to specialist centres. Specialist centres treat these conditions (including CVID, X-linked agammaglobulinaemia, autosomal-recessive agammaglobulinaemias, and immunoglobulin class-switch recombination defects) with replacement immunoglobulin therapy.
Evidence suggests achieving IgG levels >500 mg/dL reduces infection frequency, and levels >800 to 900 mg/dL may further improve respiratory outcomes.[43]Quartier P, Debre M, De Blic J, et al. Early and prolonged intravenous immunoglobulin replacement therapy in childhood gammaglobulinemia: a retrospective survey of 31 patients. J Pediatr. 1999;134:589-596.
http://www.ncbi.nlm.nih.gov/pubmed/10228295?tool=bestpractice.com
[44]de Gracia J, Vendrell M, Alvarez A, et al. Immunoglobulin therapy to control lung damage in patients with common variable immunodeficiency. Int Immunopharmacol. 2004;4:745-753.
http://www.ncbi.nlm.nih.gov/pubmed/15135316?tool=bestpractice.com
[45]Orange JS. Impact of trough IgG on pneumonia incidence in primary immunodeficiency: a meta-analysis of clinical studies. Clin Immunol. 2010;137:21-30.
http://www.ncbi.nlm.nih.gov/pubmed/20675197?tool=bestpractice.com
In most cases of primary antibody deficiency, treatment with immunoglobulin replacement is lifelong.
Reduced IgA or IgG subclass, or impaired specific antibody production
PIDs with a normal total IgG, but reduction in specific components, are often less severe than those with a reduction in total IgG. For example, IgA or IgG subclass deficiency may not require any treatment. If symptomatic, they can usually be managed with antibiotics alone.
Immunoglobulin replacement may be considered in cases of impaired specific antibody production where there is severe disease or complications. However, initial management should be with prophylactic and/or therapeutic antibiotics alone. If immunoglobulin replacement is commenced, it is worth stopping (preferably in the spring in temperate countries) after a period of time to re-assess immunological status.
Suspected severe combined immunodeficiency (SCID)
SCID is a medical emergency, and patients should be referred to specialist centres for confirmed diagnosis and treatment as soon as it is suspected. It must be urgently excluded in patients with low absolute lymphocyte counts and low immunoglobulins.
Specialist treatment should be undertaken as quickly as possible; outcomes are better with earlier diagnosis and intervention.[46]Myers LA, Patel DD, Puck JM, et al. Hematopoietic stem cell transplantation for severe combined immunodeficiency in the neonatal period leads to superior thymic output and improved survival. Blood. 2002 Feb 1;99(3):872-8.
https://ashpublications.org/blood/article/99/3/872/53489/Hematopoietic-stem-cell-transplantation-for-severe
http://www.ncbi.nlm.nih.gov/pubmed/11806989?tool=bestpractice.com
Definitive treatment is HSCT. Gene therapy is an emerging technology that has also been used in X-linked SCID and SCID due to ADA deficiency. Supportive therapy, including immunoglobulin replacement, protection from exposure to infectious agents, and Pneumocystis pneumonia prophylaxis, is given while awaiting definitive treatment.
PEG-ADA replacement can also be considered in ADA-deficient SCID.[27]Kohn DB, Hershfield MS, Puck JM, et al. Consensus approach for the management of severe combined immune deficiency caused by adenosine deaminase deficiency. J Allergy Clin Immunol. 2019 Mar;143(3):852-63.
https://www.jacionline.org/article/S0091-6749(18)31268-5/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/30194989?tool=bestpractice.com
Non-SCID cellular and antibody deficiency
In other combined immunodeficiencies (with both cellular and antibody defects), referral to specialist centres is important for definitive investigation and management. Specific treatment protocols are customised for the various individual diseases. Specialist therapy in the form of HSCT or gene therapy may be required. In these cases, immunoglobulin replacement and antibiotics are used for supportive care while awaiting treatment and after transplantation while awaiting B-cell reconstitution.
Secondary hypogammaglobulinaemia
Treatment of secondary hypogammaglobulinaemia mainly involves treating the underlying cause or discontinuing medications that might result in hypogammaglobulinaemia.[2]Otani IM, Lehman HK, Jongco AM, et al. Practical guidance for the diagnosis and management of secondary hypogammaglobulinemia: a Work Group report of the AAAAI Primary Immunodeficiency and Altered Immune Response Committees. J Allergy Clin Immunol. 2022 May;149(5):1525-60.
https://www.jacionline.org/article/S0091-6749(22)00152-X/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/35176351?tool=bestpractice.com
Guidelines support the use of replacement immunoglobulin in patients with severe or recurrent infections, ineffective antimicrobial treatment, and either proven specific antibody failure or serum IgG level of <4 g/L (<400 mg/dL).[2]Otani IM, Lehman HK, Jongco AM, et al. Practical guidance for the diagnosis and management of secondary hypogammaglobulinemia: a Work Group report of the AAAAI Primary Immunodeficiency and Altered Immune Response Committees. J Allergy Clin Immunol. 2022 May;149(5):1525-60.
https://www.jacionline.org/article/S0091-6749(22)00152-X/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/35176351?tool=bestpractice.com
[47]European Medicines Agency. Guideline on core SmPC for human normal immunoglobulin for intravenous administration (IVIg). Jun 2018 [internet publication].
https://www.ema.europa.eu/en/documents/scientific-guideline/guideline-core-smpc-human-normal-immunoglobulin-intravenous-administration-ivig-rev-5_en.pdf
[48]European Medicines Agency. Clinical investigation of human normal immunoglobulin for intravenous administration (IVIg). Dec 2021 [internet publication].
https://www.ema.europa.eu/en/clinical-investigation-human-normal-immunoglobulin-intravenous-administration-ivig#current-effective-version-section
Supportive treatment in the form of replacement immunoglobulin and antibiotics may be considered for hypogammaglobulinaemia secondary to haematological malignancy (B-cell chronic lymphocytic leukaemia, non-Hodgkin's lymphoma, multiple myeloma, other B-cell tumours) and after HSCT.[49]National Blood Authority, Australia. Criteria for the clinical use of immunoglobulin in Australia: version 3. 2018 [internet publication].
https://www.criteria.blood.gov.au/SupportingInformation
[50]Department of Health (UK). Clinical guidelines for immunoglobulin use: second edition update. Aug 2011 [internet publication].
https://assets.publishing.service.gov.uk/government/uploads/system/uploads/attachment_data/file/216671/dh_131107.pdf
[51]Raanani P, Gafter-Gvili A, Paul M, et al. Immunoglobulin prophylaxis in chronic lymphocytic leukemia and multiple myeloma: systematic review and meta-analysis. Leuk Lymphoma. 2009 May;50(5):764-72.
http://www.ncbi.nlm.nih.gov/pubmed/19330654?tool=bestpractice.com
[52]Vacca A, Melaccio A, Sportelli A, et al. Subcutaneous immunoglobulins in patients with multiple myeloma and secondary hypogammaglobulinemia: a randomized trial. Clin Immunol. 2018 Jun;191:110-5.
http://www.ncbi.nlm.nih.gov/pubmed/29191714?tool=bestpractice.com
Evidence supporting the use of immunoglobulin replacement in other causes of secondary hypogammaglobulinaemia, including following solid organ transplantation, is limited.[2]Otani IM, Lehman HK, Jongco AM, et al. Practical guidance for the diagnosis and management of secondary hypogammaglobulinemia: a Work Group report of the AAAAI Primary Immunodeficiency and Altered Immune Response Committees. J Allergy Clin Immunol. 2022 May;149(5):1525-60.
https://www.jacionline.org/article/S0091-6749(22)00152-X/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/35176351?tool=bestpractice.com
[53]Bourassa-Blanchette S, Knoll GA, Hutton B, et al. Clinical outcomes of polyvalent immunoglobulin use in solid organ transplant recipients: a systematic review and meta-analysis. Clin Transplant. 2019 Jun;33(6):e13560.
http://www.ncbi.nlm.nih.gov/pubmed/30938866?tool=bestpractice.com
[54]Bourassa-Blanchette S, Patel V, Knoll GA, et al. Clinical outcomes of polyvalent immunoglobulin use in solid organ transplant recipients: a systematic review and meta-analysis - Part II: non-kidney transplant. Clin Transplant. 2019 Jul;33(7):e13625.
http://www.ncbi.nlm.nih.gov/pubmed/31162852?tool=bestpractice.com
[55]Perez EE, Orange JS, Bonilla F, et al. Update on the use of immunoglobulin in human disease: a review of evidence. J Allergy Clin Immunol. 2017 Mar;139(3s):S1-46.
https://www.jacionline.org/article/S0091-6749(16)31141-1/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/28041678?tool=bestpractice.com
There are increasing reports of prolonged and symptomatic hypogammaglobulinaemia following certain treatments, including biologicals such as rituximab and other B-cell targeted therapies.[22]Levy R, Mahévas M, Galicier L, et al. Profound symptomatic hypogammaglobulinemia: a rare late complication after rituximab treatment for immune thrombocytopenia. Report of 3 cases and systematic review of the literature. Autoimmun Rev. 2014 Oct;13(10):1055-63.
http://www.ncbi.nlm.nih.gov/pubmed/25183241?tool=bestpractice.com
[23]Christou EA, Giardino G, Worth A, et al. Risk factors predisposing to the development of hypogammaglobulinemia and infections post-rituximab. Int Rev Immunol. 2017 Nov 2;36(6):352-9.
http://www.ncbi.nlm.nih.gov/pubmed/28800262?tool=bestpractice.com
[24]Khan DA. Hypersensitivity and immunologic reactions to biologics: opportunities for the allergist. Ann Allergy Asthma Immunol. 2016 Aug;117(2):115-20.
https://www.annallergy.org/article/S1081-1206(16)30263-0/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/27499538?tool=bestpractice.com
[25]Ottaviano G, Marinoni M, Graziani S, et al. Rituximab unveils hypogammaglobulinemia and immunodeficiency in children with autoimmune cytopenia. J Allergy Clin Immunol Pract. 2020 Jan;8(1):273-82.
http://www.ncbi.nlm.nih.gov/pubmed/31377437?tool=bestpractice.com
[56]Wijetilleka S, Jayne DR, Mukhtyar C, et al. Recommendations for the management of secondary hypogammaglobulinaemia due to B cell targeted therapies in autoimmune rheumatic diseases. Rheumatology (Oxford). 2019 May 1;58(5):889-96.
https://academic.oup.com/rheumatology/article/58/5/889/5262287?login=false
http://www.ncbi.nlm.nih.gov/pubmed/30590695?tool=bestpractice.com
[57]Wijetilleka S, Mukhtyar C, Jayne D, et al. Immunoglobulin replacement for secondary immunodeficiency after B-cell targeted therapies in autoimmune rheumatic disease: systematic literature review. Autoimmun Rev. 2019 May;18(5):535-41.
http://www.ncbi.nlm.nih.gov/pubmed/30844552?tool=bestpractice.com
While infectious risks are likely multifactorial, there is increasing adoption of sub-specialty guidelines which recommend screening with IgG levels and flow cytometry prior to initiation of rituximab, with monitoring after therapy in cases of recurrent infections.[2]Otani IM, Lehman HK, Jongco AM, et al. Practical guidance for the diagnosis and management of secondary hypogammaglobulinemia: a Work Group report of the AAAAI Primary Immunodeficiency and Altered Immune Response Committees. J Allergy Clin Immunol. 2022 May;149(5):1525-60.
https://www.jacionline.org/article/S0091-6749(22)00152-X/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/35176351?tool=bestpractice.com
[58]Barmettler S, Ong MS, Farmer JR, et al. Association of immunoglobulin levels, infectious risk, and mortality with rituximab and hypogammaglobulinemia. JAMA Netw Open. 2018 Nov 2;1(7):e184169.
https://jamanetwork.com/journals/jamanetworkopen/fullarticle/2712179
http://www.ncbi.nlm.nih.gov/pubmed/30646343?tool=bestpractice.com
[59]Khojah AM, Miller ML, Klein-Gitelman MS, et al. Rituximab-associated hypogammaglobulinemia in pediatric patients with autoimmune diseases. Pediatr Rheumatol Online J. 2019 Aug 28;17(1):61.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6712749
http://www.ncbi.nlm.nih.gov/pubmed/31462263?tool=bestpractice.com
[60]O'Donohue JM, Enzmann DR. Mycotic aneurysm in angiitis associated with herpes zoster ophthalmicus. AJNR Am J Neuroradiol. 1987 Jul-Aug;8(4):615-9.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8333680
http://www.ncbi.nlm.nih.gov/pubmed/3113199?tool=bestpractice.com
Additionally, there is increasing data that paediatric patients treated with rituximab may be at higher risk for hypogammaglobulinaemia and immunoglobulin levels should be monitored.[25]Ottaviano G, Marinoni M, Graziani S, et al. Rituximab unveils hypogammaglobulinemia and immunodeficiency in children with autoimmune cytopenia. J Allergy Clin Immunol Pract. 2020 Jan;8(1):273-82.
http://www.ncbi.nlm.nih.gov/pubmed/31377437?tool=bestpractice.com
[59]Khojah AM, Miller ML, Klein-Gitelman MS, et al. Rituximab-associated hypogammaglobulinemia in pediatric patients with autoimmune diseases. Pediatr Rheumatol Online J. 2019 Aug 28;17(1):61.
https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6712749
http://www.ncbi.nlm.nih.gov/pubmed/31462263?tool=bestpractice.com
Supportive therapies
Acute/recurrent bacterial infection
If patients present with acute infection or with frequent recurrent infection, therapeutic/prophylactic antibiotics may be started.[9]Bonilla FA, Khan DA, Ballas ZK, et al. Practice parameter for the diagnosis and management of primary immunodeficiency. J Allergy Clin Immunol. 2015 Nov;136(5):1186-205;e1-78.
https://www.jacionline.org/article/S0091-6749%2815%2900883-0/fulltext
http://www.ncbi.nlm.nih.gov/pubmed/26371839?tool=bestpractice.com
Hypogammaglobulinaemia predisposes typically to encapsulated bacteria (e.g., Streptococcus pneumoniae, Haemophilus influenzae), but sputum can also be positive for non-encapsulated Haemophilus. Stool culture can be positive for Campylobacter or Giardia. Cryptosporidium may be detected in hyper-IgM syndrome.
Appropriate therapeutic antibiotics can be started promptly in patients with acute bacterial infection. These are ideally bactericidal rather than bacteriostatic. Most physicians advocate prolonged courses (at least 10-14 days), although evidence supporting this is limited. Single-agent prophylactic antibiotics (one antibiotic used continuously) or rotating prophylactic antibiotics (several different antibiotics changed at fixed intervals) can also be considered if infections are frequent despite immunoglobulin therapy. Prophylaxis is usually considered if there are >2 to 3 mild infections per year or at least one severe infection per year, but this has not been clearly defined.
It is widely accepted that antibiotic use for acute infection in hypogammaglobulinaemia is beneficial. Exact antibiotic regimens are developed based on local policy, individual microbiological susceptibility, and patient characteristics.
Established bronchiectasis