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Colombia Médica

On-line version ISSN 1657-9534

Colomb. Med. vol.53 no.2 Cali Jan./June 2022  Epub May 30, 2022 

Original article

Antibody deficiencies with normal IgG in adults with Non-cystic fibrosis bronchiectasis or recurrent pneumonia: Cross-sectional study

1 Universidad del Valle, Escuela de Ciencias Básicas, Departamento de Microbiología, Grupo de investigación VIREM, Cali, Colombia



Inborn errors of immunity, mainly Predominantly Antibody deficiencies with normal IgG levels are unrecognized in adults with lung diseases such as bronchiectasis or recurrent pneumonia.


To determine IgM, IgA, IgG2 subclass deficiencies, and Specific antibody deficiency (anti-pneumococcal polysaccharide antibodies) in adults with non-cystic fibrosis bronchiectasis or recurrent pneumonia.


Cross-sectional study. Consecutive patients with non-cystic fibrosis bronchiectasis or recurrent pneumonia were recruited in Cali, Colombia. IgG, IgA, IgM, and IgE, IgG2subclass and IgG anti-pneumococcal serum levels were measured.


Among the 110 participants enrolled, Antibody deficiencies with normal serum IgG levels were found in 11(10%) cases. IgA deficiency (3 cases), IgM deficiency (2 cases) and IgG2 deficiency (2 cases) were the most frequent primary immunodeficiencies. In addition, IgG2+IgA deficiency, Ataxia-telangiectasia, Hyper-IgE syndrome and Specific Antibody Deficiency(anti-polysaccharides) were found in one case each.


Predominantly antibody deficiencies with normal IgG levels are an important etiology of non-cystic fibrosis bronchiectasis and recurrent pneumonia in adults.

Keywords: Bronchiectasis; recurrent pneumonia; predominantly antibody deficiencies; igg2 subclass deficiency; specific antibody deficiency; anti-polysaccharides antibodies



Los Errores Innatos de la Inmunidad principalmente las Deficiencias Predominantemente de anticuerpos con niveles normales de IgG no se conocen en adultos con enfermedades pulmonares como las bronquiectasias o la neumonía recurrente.


Determinar las deficiencias de IgM, IgA y de subclase de IgG2 y la Deficiencia Específica de Anticuerpos (anticuerpos antineumocócicos de polisacáridos) en adultos con Bronquiectasias no Fibrosis Quística (BQnoFQ) o neumonía recurrente.


Estudio observacional prospectivo. Se reclutaron 110 pacientes consecutivos con BQnoFQ o neumonía recurrente en Cali, Colombia. Se midieron los niveles séricos de IgG, IgA, IgM e IgE, subclase IgG2 y anticuerpos anti-neumococo.


Se encontraron deficiencias de anticuerpos con niveles normales de IgG en el 10% de los sujetos; Cuatro casos con IgG2 baja, incluido 1 caso de deficiencia de IgG2 + IgA, 1 caso de ataxia-telangiectasia, 3 deficiencias de IgA (IgAD), 2 deficiencias selectiva de IgM (IgMD), 1 síndrome de Hiper-IgE (HIES-AR) y 1 deficiencia específica de anticuerpos. Ocho pacientes fueron diagnosticados con enfermedades relacionadas con la hipogammaglobulinemia IgG.


Las deficiencias predominantemente de anticuerpos con niveles normales de IgG son una etiología importante de BQnoFQ y neumonía recurrente en adultos. Los sujetos con bronquiectasias o neumonía recurrente requieren una evaluación exhaustiva de la respuesta inmune humoral y clínica.

Palabras clave: Bronchiectasis; recurrent pneumonia; predominantly antibody deficiencies; igg2 subclass deficiency; specific polysaccharide antibody deficiency


1) Why was this study conducted?
Predominantly Antibody Deficiencies are the most frequent primary immune deficiency disorders affecting adults. Antibody deficiencies with normal IgG levels had been related with recurrent pneumonia and bronchiectasis. The frequency of humoral deficiencies in adults have not been evaluated in Colombia.
2) What were the most relevant results of the study?
We find Antibody deficiencies with normal IgG levels in 10% of adult patients evaluated. Although unknown rates of pneumococcal vaccination, protective IgG anti-pneumococcal titles were find in most of the patients.
3) What do these results contribute?
Immunological evaluation, including IgG, IgA, IgM, IgE IgG subclasses and IgG anti-polysaccharides could contribute to improve diagnosis and treatment outcomes in adult patients with bronchiectasis or recurrent pneumonia.


Predominantly Antibody Deficiencies are the most frequent primary immune deficiency disorders affecting adults. Predominantly antibody deficiencies clinical presentation is variable, but most patients are susceptible to recurrent infections, autoimmunity, inflammation, allergy or malignancy 1. Although, predominantly antibody deficiencies can manifest at any age, its diagnosis requires a high index of suspicion, but in most cases, its diagnosis is delayed, contributing to the development of complications 2. Antibody Deficiencies spectrum ranges from severe forms such as agammaglobulinemia (X-linked and autosomal recessive) to less severe conditions such as Specific Antibody Deficiency or IgG subclass deficiencies 3,4. Although IgG subclass deficiency or Specific Antibody Deficiency is an important cause of pulmonary complications, its frequency in adults is unknown.

Antibody deficiencies with normal IgG levels are related to infectious and non-infectious complications and lung damage. IgG response against Streptococcus pneumoniae is crucial to control and prevent pneumococcal complications 5. Antibodies are essential for encapsulated microorganism infection control because capsules inhibit macrophages and polymorphonuclear cells phagocytosis 6. Poor antibody response against polysaccharide antigens or Specific Antibody Deficiency increases susceptibility to encapsulated pathogens 7. Normal adults vaccinated with pneumococcal polysaccharide (23 serotypes vaccine) exhibit protective antibody titers against at least 70% of serotypes 8. Streptococcus pneumoniae and Hemophilus influenza infections in subjects with humoral deficiencies are associated with a high risk of morbidity and mortality.

Bronchiectasis is defined as the abnormal and permanent dilatation of the bronchi. Our research is focused on non-cystic fibrosis bronchiectasis. The etiology of bronchiectasis includes respiratory infections sequela, anatomical abnormalities, alpha-1-antitrypsin deficiency, inflammatory diseases, primary ciliary dyskinesia, and primary immunodeficiencies 6. Delayed diagnosis and inadequate management of Predominantly antibody deficiencies patients lead to irreversible lung damage or even death from severe infections. Unfortunately, many patients with Predominantly antibody deficiencies develop bronchiectasis due to delayed diagnosis 9. Previous studies 5,8 have shown that a proportion of patients with bronchiectasis may have a variety of immunodeficiency disorders, mainly subclass deficiency and specific antibodies against polysaccharide antigens. Recurrent pneumonia has been defined as at least two episodes of pneumonia in one year or more than three pneumonia throughout life, with radiographic resolution between episodes 4. Large series reports greater than 50% of the subjects with recurrent pneumonia criteria have disseminated bronchiectasis 9,10. However, the actual frequency of Predominantly antibody deficiencies in subjects with recurrent pneumonia in adults is unknown.

Predominantly Antibody Deficiencies are a neglected reality in Colombia and their frequency is unknown 11. Immune characterization of adults with bronchiectasis or recurrent pneumonia will establish specific therapeutic strategies, improve quality of life, and decrease disease burden. This study aimed to determine the frequency of antibody deficiencies with normal IgG levels in adults with bronchiectasis or recurrent pneumonia.

Materiales and Methods

Study design and participants

This is a cross-sectional study. We enrolled consecutive patients with non-cystic fibrosis bronchiectasis or recurrent pneumonia who were referred by pulmonologists, internists, or allergists from different clinical centers to the Clinical Immunology Service at Universidad del Valle (Cali, Colombia) from January 2nd to December 31st, 2019 for study porpoise.

Participants fulfilling the inclusion criteria were enrolled. Briefly: aged ≥14 and <65 years with bronchiectasis on chest computed tomography (CT) and the clinical syndrome of bronchiectasis (cough, sputum production, or recurrent respiratory infections) or with recurrent pneumonia (at least two cases of pneumonia in 1 year or more than three cases of pneumonia throughout life, with radiographic resolution between episodes) and not the exclusion criteria as an inability to give informed consent, bronchiectasis due to cystic fibrosis, and traction bronchiectasis associated with interstitial lung disease or another respiratory disorder, acquired immune defects or secondary immunodeficiencies (chronic myeloid leukemia, multiple myeloma, Human Immunodeficiency Virus HIV infection, immunosuppression secondary to drugs). Inborn errors of immunity were defined according to European. Society of Immunodeficiency classification and diagnostic criteria 12. Patients older than 65 were excluded from the study because the high frequency of bronchiectasis in this population is related to senescence.

Immunoglobulin quantification (IgG, IgA, IgM and IgE serum levels)

Blood samples were taken to measure serum immunoglobulin levels (IgG, IgA, IgM, and IgE) using nephelometry (Abbott, ARCHITEC c Systems, Germany). Hypogammaglobulinemia (IgG) was defined as serum IgG levels <700 mg/dL (reference value 700-1,600 mg/dL), this relative “high” value pretends increase possible immunodeficiency cases. IgA levels <70 mg/dL (reference value 70-400 mg/dL) or IgM levels <40 mg/dL (reference value of 40-230 mg/dL) 13. Selective Immunoglobulin A (IgA) deficiency was defined as serum IgA levels <7 mg/dL in two separate samples 12. Immunoglobulin deficiency was defined according to literature 14.

IgG subclass quantification

IgG2 subclass concentration was determined using the enzyme-linked immunosorbent assay method using the commercial kit (Human IgG2 ELISA Invitrogen, THERMO FISHER, Catalog number: BMS2093 -96 tests) 15 in all subjects. IgG2 ELISA values lower than 175 mg/dL (ELISA) were confirmed using nephelometry (SIEMENS, BN II System, Germany). In addition, patients with low IgA were evaluated using nephelometry for IgG subclasses (IgG1, IgG2, IgG3, and IgG4).

IgG levels against Streptococcus pneumoniae (anti-pneumococcal antibodies 10 serotypes)

Thirty subjects with suspicious Specific Antibody Deficiency after Clinical Immunologist evaluation (v.g. pneumococcal invasive infection, unknown cause recurrent pneumonia) were evaluated using ELISA for IgG anti-pneumococcal antibodies 16 regardless of their immunization status (non-vaccination, polysaccharide or conjugated pneumococcal vaccines) using an ELISA validated for Colombia 17. Ten pneumococcal serotypes were selected, included in both conjugate and polysaccharide vaccines, serotypes were evaluated were: 1 (1), 3 (3), 4 (4), 5 (5), 14 (14), 23 (23F), 26 (6B), 51 (7F), 56 (18) and 68 (9V). Anti-pneumococcal IgG was considered positive with ≥1.3 µg/mL and protective when antibody titers were positive >70% of serotypes evaluated (7 out of 10) 8. Subjects with less than 70% of serotypes positive were vaccinated with polysaccharide vaccine (indicated by the primary healthcare provider).

Statistical analysis

The sociodemographic, clinical and paraclinical information of each case was extracted from the clinical records provided by each volunteer. Data analysis was performed with either SPSS version 25 and statistical packages in R version 3.5.2. Continuous and categorical variables were subjected to an exploratory analysis to determine central tendency, frequency, and variability measures. Due to the descriptive nature of this study, the presentation of the data is done in terms of frequencies. Pneumococcal antibodies were compared between vaccinated and unvaccinated and their statistical differences were evaluated with the Mann-Whitney U two-tailed test.


The study was approved by the Ethics Committee of Universidad del Valle (internal code 057-016 of May 2, 2019 in Cali, Colombia). Written informed consents or assents to participate were obtained from all participants and all participants consent to publish results


One hundred ten volunteers with non-cystic fibrosis bronchiectasis or Recurrent pneumonia or non-cystic fibrosis bronchiectasis + Recurrent Pneumonia were enrolled. As a result, 8 volunteers (7.3%) were diagnosed with IgG hypogammaglobulinemia: Common Variable Immunodeficiency (6 cases), IgG hypogammaglobulinemia and X-Linked Lymphoproliferative Disease (one case each). The remaining 102 patients were eligible for evaluation, looking for predominantly antibody deficiency with normal IgG (Figure 1).

Figure 1 Patients Flowchart. non-cystic fibrosis bronchiectasis, non-cystic fibrosis bronchiectasis; RP, Recurrent Pneumonia; CVID, Common Variable Immunodeficiency; XLP1, X-Linked Lymphoproliferative Disease 1; Igs, Immunoglobulins; IgG2ScD, IgG2 Subclass Deficiency; IgAD, Selective IgA deficiency; IgMD, Selective IgM deficiency; AT, Ataxia Telangiectasia; HIES-AR, Hyper IgE Syndrome Autosomal Recessive; SAD, Specific Antibody Deficiency. 

Demographic and clinical characteristics are shown in (Table 1). 102 patients, including 63 females and 39 males, median age of 48 years Interquartile Range (35 - 58), 64 cases (62.7%) were diagnosed with non-cystic fibrosis bronchiectasis, 23 (22.5%) cases with non-cystic fibrosis bronchiectasis plus recurrent pneumonia and 15 patients (14.7%) recurrent pneumonia. In addition, 60 cases (58.8%) had spirometry. Only 25 subjects (24.5%) have received pneumococcal vaccine over a lifetime.

Table 1 Sociodemographic characteristics of participants with non-cystic fibrosis bronchiectasis or recurrent pneumonia with normal IgG levels (N =102). 

Baseline Characteristics  
Age*, years 48 (36-58)
Sex, female n (%) 63 (61.7)
Non-cystic fibrosis bronchiectasis, n (%) 64 (62.7)
Recurrent pneumonia, n (%) 15 (14.7)
Non-cystic fibrosis bronchiectasis + recurrent pneumonia, n (%) 23 (22.5)
P. pneumonia Vaccinated, n (%) 25 (24.5)
Mestizo, n (%) 73 (71.5)
Afro Colombian, n (%) 24 (23.5)
Indigenous, n (%) 4 (3.9)
Others, n (%) 1 (0.9)
Elementary, n (%) 31 (30.3)
High school, n (%) 49 (48)
University, n (%) 14 (13.7)
None, n (%) 8 (7.8)
<18.5 17 (16.6)
≥18.5 85 (83.3)
Sputum isolation
P. aeruginosa 7 (6.8)
No P. aeruginosa 8 (7.8)
Negative 27 (26.4)
No data 60 (58.8)
Smoking status
Never 38 (37.2)
Former 21 (20.5)
Current 7 (6.8)
Biomass 36 (35.2)
Spirometry n (%) 60 (58.8)
Mild 45 (51.7)
Moderate 23 (26.4)
Severe 19 (21.8)

* Age is expressed in median (years) and the interquartile range. Definition abbreviations; BMI, Body Mass Index; BSI, Bronchiectasis Severity Index.

Antibody deficiencies with normal IgG levels cases are shown in (Table 2). Selective IgA deficiency (3 cases) was the most frequent antibody deficiency with normal IgG followed by IgM deficiency (2 cases). IgG2 deficiency (2 cases) and IgG2+IgA deficiency were detected using ELISA. All cases with IgG2 <175 mg/dL were confirmed by nephelometry. IgG2 levels measured by ELISA were highly concordant with nephelometry (Figure 2).

Table 2 Predominantly Antibody Deficiencies with normal IgG levels 

Patient Age (years) Gender IgG2 mg/dL ELISA IgG2 mg/dL (nephelometry) IgG mg/dL IgA mg/dL IgM mg/dL IgE UI/mL BQ Type of deficiency
BQ007 34 F 154 124 1,030 3 97 0 Yes IgAD with IgG2ScD
BQ013 14 F 171 164 2,547 1342 103 331 Yes IgG2ScD
BQ023 29 F 122 77 1,028 113 65 473 Yes IgG2ScD
BQ054 14 M 100 112 1,163 7 144 2 No AT
BQ021 63 F 1,232 440 1,519 3 82 45 Yes IgAD
BQ072 50 F 412 304 1,946 10 72 29 Yes IgAD
BQ087 48 M 350 323 1,394 3 60 0 No IgAD
BQ090 64 F 228 245 1,207 406 25 44 No IgMD
BQ107 64 F 243 316 1,022 407 26 448 Yes IgMD
BQ052 19 M 365 ND 2,626 102 34 2,001 Yes HIES-AR
BQ102 14 M 323 ND 1,398 211 179 45 No SAD

BQ: Bronchiectasis; IgG2ScD: IgG2 Subclass Deficiency; IgAD: Selective IgA deficiency; IgMD: Selective IgM deficiency; AT: Ataxia Telangiectasia; HIES-AR: Hyper IgE Syndrome Autosomal Recessive; SAD: Specific Antibody Deficiency; ND: No Data.

Figure 2 IgG2 levels ELISA vs Nephelometry. Correlation analysis r2 = 0.776. Non-parametric test, Kendall tau.  

Two participants (BQ054 and BQ102) had less than 70% of protective anti-pneumococcal antibodies (Table 1S ); both were vaccinated with pneumococcal polysaccharide vaccine without changes in IgG anti-pneumococcal titers (data not shown). BQ054 was finally diagnosed with ataxia-telangiectasia, and BQ102 fulfilled the criteria for Specific Antibody Deficiency 7.

Anti-pneumococcal antibodies according with vaccination status are shown in Figure 3. Interestingly only 3 serotypes exhibited statistically significant difference between vaccinated and unvaccinated subjects: serotypes 4 (p= 0.0282), serotype 7F (p= 0.0357) and serotype 18C (p= 0.0437), unfortunately time from vaccination was not possible to determine.

Figure 3 IgG anti-pneumococcal titles vaccinated vs unvaccinated.Box-and-whisker plot according to quartiles 25, 50 and 75, of the IgG2 levels against different pneumococcal serotypes discriminated according to the vaccinated status. Danish nomenclature is shown in parentheses. 


Predominantly antibody deficiencies are frequent in Colombian patients with non-cystic fibrosis bronchiectasis or recurrent pneumonia. We identified 19 cases (17.2%) of Inborn Errors of Immunity. IgG measurement alone was able to identify 8 cases highlighting the importance of serum absolute immunoglobulin evaluation. Our finding is consistent with previous reports of primary immunodeficiency frequency in this conditions (ranging from 2% to 17%) 18-20. In our study, Common Variable Immunodeficiency frequency is slightly higher than reported in other series with recurrent upper/lower respiratory infections 14,21. Therefore, IgG measurement should be mandatory in all patients with bronchiectasis as a frontline test, and it is a standard that has been previously suggested 22.

IgG subclass and complete immunoglobulin workup (IgG, IgA, IgM and IgE determination) are useful strategies to approach the etiology of bronchiectasis and recurrent pneumonia in adults. Serum IgA, IgM and IgE evaluation allow us to identify other Predominantly antibody deficiencies with normal IgG levels previously unrecognized in these patients. Measurement of IgG subclass is a strategy that has been implemented in the evaluation of patients with a history of chronic infections 23. IgG subclasses evaluation has been suggested as a second-line test in patients with recurrent infections 24 and first line in IgA deficiency cases 25. IgG2 subclass measurement by ELISA allowed the diagnosis of four IgG2 deficiencies, two of them with IgA deficiency one patient is currently receiving replacement therapy with human IgG and the other has ataxia-telangiectasia.

IgG2 quantification using ELISA is a useful approach in settings without nephelometry quantification availability. A good correlation of serum IgG2 levels was observed between ELISA and nephelometry, as had been reported previously by Adebajo et al. 26, and Aazami et al 27. ELISA technique is widely used, versatile and sensitive but requires longer processing time than nephelometry. Therefore, ELISA may be a valuable alternative to nephelometry (if this one is not available) to detect samples with low IgG2 levels. However, when it is possible and available, all IgG subclasses should be measured. We recommend carrying out immunoglobulin levels together with IgG subclasses as a first-line approach.

Adults exhibit high IgG anti-pneumococcal titles regardless of their immunization status. IgG antibodies against 10 Pneumococcal serotypes were evaluated regardless of their immunization status (vaccinated or unvaccinated). Interestingly all subjects evaluated (except two cases) exhibited positive and protective IgG anti-pneumococcal antibodies despite low vaccination rates, suggesting a high rate of pneumococcal infection during life. We found that 3 out of 10 serotypes evaluated: 4 (4), 51 (7F) and 56 (18C) presented significantly higher antibody titers in the vaccinated individuals with no statistical difference in the other serotypes evaluated. Our findings suggest high pneumococcal exposure that correlates with the most prevalent serotypes in Colombia 28. Therefore, improve the pneumococcal vaccination rate is mandatory for Colombian patients with bronchiectasis or recurrent pneumonia.

More studies require specific antibody deficiency frequency in adults, including specific IgG evaluation pre- and post-vaccination. However, our study is just an approach that shows a high frequency of positive antibody responses. To the best of our knowledge, this is the first systematic humoral response evaluation in a Colombian population with respiratory complications as bronchiectasis or recurrent pneumonia.


Our results show that Inborn immunity errors, especially predominantly antibody deficiencies with normal IgG serum levels as IgG2 deficiency, IgA deficiency, IgM deficiency or hyper IgE, should be considered an underlying cause of bronchiectasis and recurrent pneumonia in Colombian adults.


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Funding: This study was sponsored by Baxalta Colombia S.A.S., now part of the Takeda group of companies , as an Investigator Initiated Research (IIR-BXT-COL-001923/ IISR-2017-104214) and by la Universidad del Valle through an internal call to support Master's students in 2019 (SICOP: 1864).

Suplementary material

Table 1S Antibody titers against 10 pneumococcal serotypes (μg/mL) 

Participant code Type of vaccine Age 1(1) 3(3) 4(4) 5(5) 14(14) 23(23F) 26(6B) 51(7F) 56(18C) 68(9V)
BQ006 P23 34 23 33 15 26 15 23 21 17 53 17
BQ049 P13 15 22 4 5 9 9 2 4 13 7 3
BQ008 No 15 8 8 5 10 14 24 17 6 3 17
BQ009 P13 46 6 8 10 8 28 24 15 7 5 9
BQ021 No 63 10 7 5 8 18 17 11 5 3 4
BQ022 No 40 10 3 3 5 7 8 6 4 2 2
BQ023 No 29 12 3 2 4 6 6 4 2 0 2
BQ026 No 65 10 9 5 13 31 24 19 5 7 8
BQ027 No 51 8 8 6 8 21 22 16 5 3 4
BQ028 No 48 8 3 3 6 15 7 5 4 1 4
BQ031 No 37 8 9 11 14 35 28 19 10 6 8
BQ039 P23 48 8 9 14 26 37 24 19 13 18 17
BQ042 P23 37 13 5 12 26 37 15 21 22 6 15
BQ048 P23 37 15 7 6 17 35 24 9 13 16 6
BQ051 No 30 15 8 5 6 15 16 9 5 2 4
BQ054 P13 14 3 1 6 2 3 2 5 1 0 1
BQ057 P13 47 39 5 14 6 37 24 19 11 10 4
BQ064 No 58 18 8 10 7 34 23 8 7 8 4
BQ075 P13 56 13 4 9 5 27 24 19 9 13 5
BQ087 P13 48 5 2 2 3 4 5 3 2 0 2
BQ089 No 38 5 3 2 3 6 5 5 2 1 3
BQ090 No 64 11 3 5 4 9 8 16 3 3 4
BQ091 No 37 10 2 2 2 11 4 3 2 0 2
BQ093 No 50 3 4 3 6 12 24 14 4 6 4
BQ099 No 56 3 2 3 2 15 6 3 5 5 5
BQ100 No 39 2 3 2 6 10 7 6 4 3 4
BQ102 P13 14 0 1 1 2 3 2 2 1 0 1
BQ106 No 51 8 3 3 6 37 5 8 12 4 4
BQ107 P13 64 8 4 4 11 37 24 19 13 14 9
BQ115 No 31 3 4 3 7 15 14 8 4 4 4

Received: May 10, 2021; Revised: February 25, 2022; Accepted: May 05, 2022

Corresponding author: Andres F Zea-Vera.

Conflict of interest:

Los autores no presentan conflictos de intereses asociados con esta publicación y que no ha habido un apoyo financiero significativo para este trabajo que pueda haber influido en su resultado.

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