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. 2022 Jan 20;20(4):329–337. doi: 10.2450/2022.0197-21

ABO antibody titres: a multisite comparative study of equivalency and reproducibility for automated solid-phase and haemagglutination titration, and manual dilution with gel column agglutination technology

Dana Schneider 1, Mariangela Vicarioto 2, Serelina Coluzzi 3, Antonella Matteocci 4, Nicoletta Revelli 5, Barbara Foglieni 6, Patrizia Artusi 7, Donatella Londero 8, Anna Quaglietta 9, Giancarla Barrotta 10, Domenico Visceglie 11, Giuseppina Portararo 12, Jonella Gilsdorf 1,✉
PMCID: PMC9256507  PMID: 35175183

Abstract

Background

ABO antibody titres are important in many clinical decisions; however, much variability is observed in titre results. For reliable and reproducible titre results, automated ABO titration methods have been developed. In this 10-site study, we evaluated the equivalency of the automated ABO titration assays on the Galileo NEO, a fully automated blood bank analyzer (Immucor, Inc.) to manual titration with gel Column Agglutination Technology (CAT), as well as the reproducibility of both methods.

Materials and methods

Ten different locations participated in this study. The equivalency study included 70 random samples at each site. The reproducibility study tested the same blinded 30-sample panel at each study site. Anti-A and anti-B IgM and IgG antibody titres were tested with both the automated and manual methods; additionally, dithiothreitol (DTT) treatment was used to inactivate IgM antibodies in the manual CAT method.

Results

The equivalency between CAT manual method and Galileo NEO automated titres at each site ranged from 38 to 88%; equivalency for each isotype was 66.2% for IgM, 60.6% for IgG, and 88.5% for DTT-treated IgG. The reproducibility study evaluated the titre variation of each sample obtained from the 10 sites. The average titre ranges (in doubling dilutions) for the automated and manual methods, respectively, were 2.15±1.0 and 4.03±1.8 for IgM, and 1.53±0.7 and 4.10±1.9 for IgG; for the manual DTT-treated IgG, the average titre range was 3.45±1.8 doubling dilutions.

Discussion

The results demonstrated that the Galileo NEO automated and manual CAT ABO titres are not equivalent. However, the study also demonstrated that titre reproducibility is enhanced with the Galileo NEO automated ABO titration assays relative to the manual CAT ABO titration method. Therefore, to improve management of patients receiving care across multiple institutions, our study supports the use of automated ABO titration.

Keywords: ABO automated titrations, isotype (IgM, IgG), titre range, ABO antibody

INTRODUCTION

Titration is a semi-quantitative method to determine the strength of antibody reactivity in plasma or serum. ABO antibody titre influences a variety of clinical decisions and manufacturing procedures. ABO antibody titres are evaluated in ABO-incompatible transplantation of solid organs (e.g. kidney and heart)1,2, stem cells3, and bone marrow4. ABO antibody titres are also significant in the selection of ABO-mismatched transfusion of plasma5 and platelets6. Ensuring low ABO titres in intravenous immunoglobulin (IVIG) and low-titre group A plasma (LTGAP) products can help reduce the risk of haemolysis following therapy7,8.

Despite the importance of ABO antibody titres, much variability is observed in titre results9–15. Since poor reproducibility precludes the application of universal critical titre values, the management of patients who receive care at more than one institution is problematic; such patients’ varying titre results could mistakably qualify them for high-risk procedures12,16.

Variable measurements in ABO antibody titres have been attributed to the lack of a standard method of titration12,13,15. However, Bachegowda and colleagues found that uniform methods to harmonize titration techniques did not reduce inter-laboratory variability10. Titre variation is inherent in any method that requires manual testing and/or manual serial dilutions, in which the numerous pipetting steps are sources of error for even the most skilled and experienced technicians. While techniques such as parallel testing of historical samples aim to control variability, these workarounds waste materials and add even more time to an already laborious procedure.

Due to the limitations of standardizing manual ABO titres, automation of the titration procedure has been developed by multiple suppliers. Automated ABO titres have been evaluated in several studies9,13,17–20; however, most of these studies only assessed equivalency between automated and manual titre results. The literature lacked a study that evaluated the reproducibility of automated and manual ABO titration with large number of samples and at multiple different sites. Adkins and colleagues evaluated the reproducibility of automated ABO titration, but only IgM for ABO antibodies and for only a limited number of replicates (15 samples tested on three instruments and five samples tested at two sites)9. The authors concluded that the automated method was highly reproducible; however, since they did not perform the reproducibility study with their manual reference method (tube testing), the extent of improved reproducibility by automation was not determined.

In this study, we evaluated both equivalency and reproducibility of the suite of automated ABO titration assays on the Galileo NEO, a fully automated blood bank analyzer (Immucor, Norcross, GA, USA), to manual titration with gel Column Agglutination Technology (CAT). Ten sites participated in the study, which included an equivalency evaluation of approximately 70 random samples at each site, and a reproducibility evaluation with a panel of 30 samples tested at each site. Both IgM and IgG ABO titres were assessed. Additionally, dithiothreitol (DTT) treatment was performed for the manual CAT method to differentiate IgG antibodies by inactivating IgM antibodies21,22. DTT treatment has been found to reduce variation of antibody titre by CAT method titrations18. Because the Galileo NEO automated ABO titration assays for IgG employ the Immucor Capture-R® technology, which only detects IgG antibodies, DTT treatment was not required for the Galileo NEO automated method.

MATERIALS AND METHODS

Study design and sample population

This multisite study included 10 different locations in Italy (Online Supplementary Content, Table SI). The study was two-part, equivalency and reproducibility.

The equivalency study determined the similarity between automated titre results using the Galileo NEO ABO titration assays (Immucor) and manual titre results using samples that were serial diluted followed by gel Column Agglutination Technology (CAT) (Figure 1A). Each site chose approximately 70 random remnant de-identified samples that were collected for routine clinical care or analysis and that otherwise would have been discarded. Non-compliant blood samples for haemolysis or lipemia were not used in this study.

Figure 1.

Figure 1

Figure 1

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(A) Equivalency study diagram.

Each manual titre and corresponding automated titre were compared to determine equivalency. Equivalent titres were defined as results that had two or less doubling dilutions difference. (B) Reproducibility study diagram. Titres were compared across all sites to determine the titre range for each result. The titre range was calculated as the number of doubling dilutions between the highest and lowest titre results for each sample.

The reproducibility study compared the reproducibility of the automated Galileo NEO ABO titration assays and the manual CAT titration methods (Figure 1B). The same blinded 30-sample panel (10 Group O, 10 Group A, and 10 Group B) was provided to each study site.

No additional blood was collected from any patients or blood donors for performing this study. The samples were not individually identifiable; i.e., the identity of the subject was not known to and not able to be ascertained by any study personnel.

Testing

Anti-A and anti-B IgM and IgG antibodies were serially diluted using the Galileo NEO automated ABO titration assay and manual dilution followed by CAT titration methods. Because IgG antibody titres can be masked by IgM antibodies in the CAT method, IgG antibodies were differentiated from IgM by dithiothreitol (DTT) treatment to inactivate IgM antibodies21,22. Since the Galileo NEO automated ABO titration assays for IgG employ the Immucor Capture-R® technology, which only detects IgG antibodies, DTT treatment was not required for the automated method (Figure 2).

Figure 2.

Figure 2

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Testing method diagram

Reagents

The same brand (Immucor) of red cell reagents were used for both the automated and manual assays at all sites. The same brand (Sigma-Aldrich, St. Louis, MO, USA) and concentration (0.01M) of DTT was used at all sites. The same brand of gel cards (BioRad Laboratories, Hercules, CA, USA) was used for manual testing at all sites. The same brand of Capture-R® Select and Galileo plates were used for automated testing at all sites. Because the study spanned longer than the expiry ranges of reagents, multiple lots of reagents had to be used. However, the same lot of reagent was used for each sample’s manual and automated testing.

Automated ABO Titration on the Galileo NEO

Samples were tested on the Galileo NEO ABO titration assays according to the manufacturer’s instructions. Referencells® A1 and B are utilized by the assays to detect anti-A and anti-B antibodies, respectively; haemagglutination and Capture-R® Select technology are utilized to detect IgM and IgG antibodies, respectively. The suite of automated assays includes low range titration (0–128 doubling dilutions) for anti-A and anti-B IgM and IgG antibodies, and high range titration (32–2,048 doubling dilutions) only for IgG antibodies.

The Galileo NEO automated ABO titration assays were used to test Group A samples with anti-B IgM and IgG titration, Group B with anti-A IgM and IgG titration, and Group O with anti-A and anti-B IgM and IgG titration. The sample was first tested on the low range titration assays; if the IgG titre result was ≥128, the sample was then tested on the corresponding high range titration assay. Interpretation of the titre results were determined by the instrument according to the parameters set in the assay programming.

Manual ABO Titration by Dilution and CAT

An aliquot of each sample was treated with DTT to inactivate IgM antibodies and differentiate IgG antibodies. Both the native and DTT-treated samples were manually titrated in serial doubling dilutions according to a shared protocol. Individual dilutions were tested by CAT IgG gel cards for IgG, and NaCl cards for IgM; dilutions from DTT-treated aliquots were tested only with CAT IgG gel cards.

Group A and O samples were tested with B reference cells, and Group B and O with A reference cells to determine anti-B and anti-A titres, respectively. The manual titre was defined as the last weak (0.5+) positive reaction of the dilution series on either the NaCl or Anti-IgG card.

Data analysis

Equivalency study

The equivalency study included approximately 70 random samples at each of the 10 sites. Each manual titre and corresponding automated titre were compared to determine equivalency. For this study, equivalent titres were defined as results that had two or less doubling dilutions difference. The percent of equivalency was calculated for each isotype (IgM, IgG, and DTT-treated IgG) and for each individual study site. One-sided lower 95% confidence intervals were calculated using SAS JMP® software for Windows, (version 9.4, SAS Institute, Cary, NC, USA).

Reproducibility study

The reproducibility study included a 30-sample panel that was tested by each of the 10 sites. Titres were compared across all sites to determine the titre range for each result. The titre range was calculated as the number of doubling dilutions between the highest and lowest titre results for each sample. The average titre range, with standard deviation, was calculated for each isotype (IgM, IgG, and DTT-treated IgG). Additionally, the percent of equivalent results (i.e., a titre range of two or less doubling dilutions as defined in the equivalency study) across all 10 sites was calculated for each isotype.

RESULTS

Equivalency study

A total of 672 samples (197 Group O, 231 Group A, 244 Group B) generated 2,515 pairs of corresponding automated and manual titre results. The differences observed between the automated and manual titre result ranged from zero to 10 doubling dilutions (Table I).

Table I.

The number of samples with 0 to 10 doubling dilutions difference between the automated and manual titre results. A difference of 10 doubling dilutions was the highest observed in this study

Antibody Isotype Doubling dilutions difference between the automated and manual titre results % Equivalency (One-sided lower 95% confidence interval)
0 1 2 3 4 5 6 7 8 9 10
Equivalent results Inequivalent results
IgM 81 229 270 160 75 16 5 4 1 0 0 68.9% (66.2% CI)
IgG 105 225 201 150 70 48 27 3 3 3 2 63.4% (60.6% CI)
DTT-Treated IgG * 327 276 153 63 12 4 1 0 1 0 0 90.3% (88.5% CI)
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*

DTT-treated IgG manual CAT titre compared to untreated IgG automated Galileo NEO titre. DTT-treatment was used to inactivate IgM antibodies, which can mask IgG titres in the CAT method; DTT treatment was not required for the automated method because the Galileo NEO ABO titration assays for IgG employ the Immucor Capture-R® technology, which only detects IgG antibodies.

Pairwise comparisons were heat mapped to visualize the equivalency trend for each isotype: IgM, IgG, and DTT-Treated IgG (Figure 3). A trend of higher titre results for the manual method was observed for IgM and IgG. By contrast, DTT-treated IgG CAT manual titres, in which IgM had been inactivated, tended to be more similar to the Galileo NEO automated IgG titres.

Figure 3.

Figure 3

Figure 3

Figure 3

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Equivalency results: heat mapped counts of results for the pairwise comparisons of automated NEO titre and manual gel titre for (A) IgM, (B) IgG, and (C) DTT-treated IgG

The thick boarder box indicates results defined as concordant (≤2 doubling dilutions difference between the automated NEO titre and the manual gel titre).

The equivalency between CAT manual method and Galileo NEO automated titres for was 62.2% for IgM and 60.6% for IgG; DTT-treated manual IgG and automated IgG titres had the highest equivalency at 88.5% (Figure 4A). The lower equivalency between manual and automated IgM and IgG titres may also be a consequence of masking effects in the CAT method. By contrast, equivalency was higher between DTT-treated IgG CAT manual titres, in which IgM had been inactivated, and Galileo NEO automated IgG titres, in which Immucor’s Capture-R® technology is implemented to detect only IgG.

Figure 4.

Figure 4

Figure 4

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Equivalency results

(A) Percent of equivalent results for each isotype; LCI is the one-sided lower 95% confidence interval. (B) Percent of equivalent results for each study site. Note: DTT-treated IgG manual CAT titre compared to untreated IgG automated Galileo NEO titre. DTT-treatment was used to inactivate IgM antibodies, which can mask IgG titres in the CAT method; DTT treatment was not required for the automated method because the Galileo NEO ABO titration assays for IgG employ the Immucor Capture-R® technology, which only detects IgG antibodies.

The percent of equivalent results obtained by each site ranged from 38 to 88%, with only three of the ten sites obtaining ≥80% equivalent results (Figure 4B).

Reproducibility study

The 30-sample panel tested at each site included 10 Group O, 10 Group A, and 10 Group B samples. The titre range was calculated as the number of doubling dilutions between the highest and lowest titre results for each sample. The average titre range, with standard deviation, was calculated for each isotype (IgM, IgG, and DTT-treated IgG) (Figure 5A). The Galileo NEO automated titration assays were the most precise as indicated by a lower average titre range: 2.15±1.0 doubling dilutions range for IgM and 1.53±0.7 for IgG. The manual CAT methods were the least precise with 4.03±1.8 and 4.10±1.9 average titre ranges for IgM and IgG, respectively. DTT treatment did improve the reproducibility of the IgG manual CAT method to an average titre range of 3.45±1.8.

Figure 5.

Figure 5

Figure 5

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Reproducibility results

(A) Average range of titre results across sites. The titre range was calculated as the number of doubling dilutions between the highest and lowest titre results for each sample. (B) Percent equivalent results across all 10 sites (i.e., a titre range of two or less doubling dilutions as defined in the equivalency study).

The percent of equivalent results (i.e., a titre range of two or less doubling dilutions as defined in the equivalency study) was also calculated to assess reproducibility for each method (Figure 5B). The Galileo NEO automated titration assays demonstrated the highest percent of equivalent results: 73% and 90% for IgM and IgG, respectively. The percent of equivalent results for the manual CAT methods were significantly lower: 25% and 13% for IgM and IgG, respectively. The DTT treatment of the IgG manual CAT method did improve the percent of equivalent results to 25%, but was still significantly lower than the 90% equivalent results observed for the Galileo NEO automated IgG titration assays.

DISCUSSION

In this multi-site study, we evaluated equivalency of the automated ABO titration assays on the Galileo NEO, a fully automated blood bank analyzer (Immucor, Inc), to manual titration with gel Column Agglutination Technology (CAT), and we determined the reproducibility of both methods. Additionally, DTT treatment was performed for the manual CAT method to differentiate IgG antibodies by inactivating IgM antibodies21,22 and to reduce variation of antibody titre by CAT method titrations18.

Our study determined that, over multiple sites, Galileo NEO automated ABO titration results are inequivalent to manual ABO CAT titre results. Our results agree with other previous studies concluding that automated ABO titre results are inconsistent with manual ABO titre results13,19,20. However, other studies have found that automated and manual titration methods yielded similar results9,17,18. The differences in these conclusions can be attributed to the low number of sites in those previous studies, most of which only included one site. In contrast, since our study included 10 sites, we were able to capture the breadth of equivalency variation across multiple sites (Figure 4B). Although eight of the 10 sites obtained ≥70% equivalency between the CAT manual method and Galileo NEO automated titres, the percent of equivalent results obtained by each site ranged from 38 to 88% (Figure 4B). Thus, across all 10 sites, results between the CAT manual method and Galileo NEO automated titres were not similar: 68.9% and 63.4% equivalency for IgM and IgG, respectively (Table I and Figure 4A).

DTT treatment for the manual IgG CAT method did increase the equivalency to 90.3%, indicating IgM interference in the untreated IgG CAT titres. This is further supported by our observation that untreated IgG CAT titres trended higher than Galileo NEO automated IgG titres (Figure 3). Higher titre results in the IgG CAT manual method are likely due to masking effects21,22: IgM reactivity increasing the strength, and therefore titre, for the IgG CAT result. The observed higher titres for the IgM manual method suggests that pentameric IgM may trap IgG present by increasing reactivity in CAT result as well. By contrast, DTT-treated IgG CAT manual titres, in which IgM had been inactivated, tended to be more similar to the Galileo NEO automated IgG titres, in which Immucor’s Capture-R® technology is implemented to detect only IgG. Since manual titres are known to be highly variable between laboratories9–15, it should be expected that equivalency assessments involving manual titration methods would reach mixed conclusions. By the very nature of being a variable method, manual titres will be similar to automated titre in some cases, but dissimilar in other cases. Therefore, we endeavored to evaluate the reproducibility of both manual and automated ABO titration methods to determine which would be a better candidate to address the problem of inter-laboratory variation in titre results.

Our reproducibility study demonstrated that the Galileo NEO automated ABO titration assays provide more precise titre results across multiple sites than the manual CAT titration method (Figure 5A). DTT treatment did increase the reproducibility of the IgG manual CAT method; however, the variability was still greater than the Galileo NEO automated IgG titres. In addition, the IgG Galileo NEO automated ABO titres had a titre range of two or less doubling dilutions (i.e., were equivalent as defined in the equivalency study) across all 10 sites. By contrast, the IgG manual CAT ABO titres showed significantly lower equivalent ranges for both IgM and IgG Titres (Figure 5B). Again, DTT treatment did increase the reproducibility of the titre ranges of the IgG manual CAT method; however, the precision was still less than the Galileo NEO automated IgG titres.

Accurate measurement of IgG antibodies is important because IgG antibodies have been shown to be a crucial factor in graft outcome4,12,21. Because the CAT method will detect both IgM and IgG antibodies, DTT treatment is necessary to inactivate IgM antibodies and precisely measure IgG antibody titres4,12,21,23,24. In both our equivalency and reproducibility studies, we did find that DTT treatment increased equivalency and reproducibility of manual CAT IgG titre results. However, DTT treatment adds time and effort to the manual titration method, which is already a time-consuming and labor-intensive process. In contrast, the Galileo NEO automated IgG titration assays measure IgG antibodies without DTT treatment because they utilize the solid phase red cell adherence (SPRCA) Capture-R® technology to detect only IgG antibodies.

CONCLUSIONS

In summary, our ten-site study demonstrated that the Galileo NEO automated and manual CAT ABO titres are not equivalent; however, the study also reveals the enhanced reproducibility of the Galileo NEO automated ABO titration assays relative to the manual CAT ABO titration method. Therefore, to improve management of patients receiving care across multiple institutions, our study supports the use of automated ABO titration. Since the equivalency between the automated and manual titres can be low, laboratories will need to determine how their own specific manual titres for critical cutoff values correlate to automated titre values. As with previous transitions from manual to automated methods (e.g., type and screen), the automation of ABO titre results will require a transition phase as clinicians and laboratory personnel build confidence in the benefits of automated ABO titration, including more efficient use of time and resources, as well as superior reproducibility.

Supplementary Information

ACKNOWLEDGEMENTS

The Authors from the Italian institutions acknowledge their participation on behalf of the Italian Society of Transfusion Medicine and Immunohaematology (SIMTI). The Authors would like to recognize the site co-investigators for their contributions: Cinzia Vio, Isabella Santilio, Luca Pierelli, Laura Curci, Sara Frison, Giovanni Battista Ceccherelli, Paola Zaninotti, Liliana Carinci, Guglielmo Giuca, Giovanni Mazzeo, and Maria Burciu. Additionally, all Authors would like to thank Mariagrazia Amelia Sciarrotta and Federica Pirelli for their efforts to complete this study.

Footnotes

AUTHORSHIP CONTRIBUTIONS

The following Authors contributed to study design and execution, as well as discussion of the results and conclusions: MV, SC, AM, NR, BF, PA, DL, AQ, GB, DV, GP and JG. DS performed data analyses and was the primary creator of the text, tables, and figures.

DISCLOSURE OF CONFICTS OF INTEREST

Dana Schneider and Jonella Gilsdorf are employed by Immucor, Inc. The other Authors declare no conflicts of interest.

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Associated Data

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Supplementary Materials

BLT-20-329_Online_Supplementary_Content.pdf (381.9KB, pdf)

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