Transfusion and Apheresis Science xxx (xxxx) xxx

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Transfusion and Apheresis Science

journal homepage: www.elsevier.com/locate/transci

High titers of anti-A1 and anti-B antibodies among Peruvian group O

platelet donors
Gissel Aguilar a, Nathalie Ortiz b, Donna Gonzales b, Steev Loyola b, c, d, José A. Paredes a, e, *
a
Facultad de Medicina, Universidad Nacional Mayor de San Marcos, Lima, Peru
b
Facultad de Medicina, Universidad Peruana Cayetano Heredia, Lima, Peru
c
Doctorado en Medicina Tropical, Facultad de Medicina, Universidad de Cartagena, Cartagena de Indias, Colombia
d
Grupo de Investigación UNIMOL, Facultad de Medicina, Universidad de Cartagena, Cartagena de Indias, Colombia
e
Servicio de Hemoterapia y Banco de Sangre, Hospital Nacional Edgardo Rebagliati Martins, Lima, Peru

A R T I C L E I N F O A B S T R A C T

Keywords: Critical antibody titers have been described as factors associated with hemolysis in ABO plasma-incompatible
Blood banks platelet (PLT) transfusions. This study was carried out to describe the frequency of high-titers anti-A and
ABO blood-group system antiB IgM and IgG antibodies in group O apheresis platelet donors, and to explore differences according to the
Antibody titers
donor characteristics. A cross-sectional study was carried out at the Blood Bank of a National Hospital in Peru
Plateletpheresis
from January to March 2019. IgM and IgG antibodies against A1 and B antigens were quantified in 339 platelet
Platelet transfusion
Platelet donor donors using the direct hemagglutination technique and the solid-phase adherence technique, respectively. For
analysis purposes, two cut-off points; ≥128 and ≥64, were used to define a critical titer for IgM due to a lack of
consensus. An IgG titer of ≥256 was also defined as critical. Of the donors, 22.1 % had critical IgM titers when
the cut-off point was defined as ≥128. However, when the IgM cut-off was ≥64, the frequency of platelet donors
with critical titers increased to 54.0 %. The frequency of donors with critical IgG titers was 23.5 %. Higher IgG
titers were associated with female donors while higher IgM titers were negative associated with age. One in two
or three platelet donors, depending on the cutoff point used to define a critical IgM titer, had at least one critical
titer of anti-A or anti-B antibodies. Early identification of platelet donors with critical antibody titers could
prevent passive transfusion of ABO antibodies to non-isogroup recipients.

1. Introduction
Platelet transfusion plays a key role in the prevention, management
and treatment of bleeding events. The platelet is one of the most
requested blood components in health services such as hematology,
oncology and intensive care units, therefore, its supply must be constant
and adequate in blood banks. Patients with low platelet counts often
need more than one platelet transfusion simultaneously or during
therapy [1–3].
Platelets can be collected and isolated by different methodologies,
however, the apheresis procedure allows the isolation of a greater
number of platelets from a single healthy donor. From this reason,
apheresis is one of the most used procedures in blood banks [4]. Blood
group O platelet donors are often considered as universal donors, hence,
they represent the major source of platelet concentrates (PCs) obtained
by apheresis. Apheresis PCs commonly contained 2.0–4.0 × 1011
platelets, less residual red blood cell and leukocyte content and ABO
antibodies according to the donor’s blood type, all suspended in
approximately 250 mL plasma [1,5]. Plasma from group O donors
contains immunoglobulins M (IgM) and G (IgG) against type A and B
antigens. Titration of IgG and IgM anti-A and anti-B allows the detection
of platelet donors or PC with critical antibody levels.
Acute hemolytic transfusion reactions can occur by non-isogroup
transfusions associated with high titers of anti-A and anti-B antibodies
in the donor plasma [6,7]. The occurrence of acute hemolytic trans­
fusion reactions has been documented in cases receiving PC with anti-A
and antibody titers equal or higher than 64 [6,8–10]. Similarly, PC
transfusion collected from donors with high antibody titers has been
described as a factor associated to death in non-isogroup recipients [11,
12].
Efforts to mitigate ABO incompatibilities in platelet transfusions
have resulted in several initiatives, including antibody titration to

* Corresponding author at: Quiroga 227 Mirones Bajo, Lima, Peru.

E-mail address: jparedesa@unmsm.edu.pe (J.A. Paredes).

https://doi.org/10.1016/j.transci.2021.103341
Received 30 June 2021; Received in revised form 22 November 2021; Accepted 8 December 2021
Available online 10 December 2021
1473-0502/© 2021 Published by Elsevier Ltd.

Please cite this article as: Gissel Aguilar, Transfusion and Apheresis Science, https://doi.org/10.1016/j.transci.2021.103341
G. Aguilar et al. Transfusion and Apheresis Science xxx (xxxx) xxx

identify donors or PC with critical titers. The implementation of anti-A Titers were analyzed as the inverse of the dilution at which agglutination
and anti-B antibody titration methods in blood banks may favor the was detected.
reduction of hemolytic transfusion reactions in non-group O recipients At the time of the study, antibody titration was not part of the routine
since the results can be used to selectively decide for isogroup trans­ Blood Bank processes, therefore, all titrations were performed pro­
fusions [13–16]. spectively and using the plasma collected from donors.
In Peru, approximately 70.0 % of donations are collected from blood
group O donors [17], therefore, the characterization of their anti-A and 2.3. Analysis of data
anti-B antibody titers is relevant. The aim of this study was to describe
IgM and IgG titers against A1 and B antigens in platelet donors by The cut-off point used to define a critical titer in IgG assays was ≥
apheresis and to explore differences between the critical titers and the 256 [24]. Due to the absence of a standard cut-off point to define critical
donor characteristics. titers for IgM and the lack of a reference method to titer, the two cut-off
frequently described elsewhere were used in this study; ≥ 64 and ≥ 128
2. Material and methods [20,24–26]. The inclusion of both cut-offs for IgM allowed generating
estimates for a conservative (titer ≥128) and a less conservative scenario
2.1. Design and participants (titer ≥64). The global risk was assessed for both scenarios considering
both IgM and IgG titers against A1 and B antigens.
A cross-sectional study was conducted during January to March 2019 Age was post hoc categorized into four age groups. Differences for
at the Blood Bank of the Edgardo Rebagliati Martins National Hospital. critical titers according to sex and age were explored using the Fisher’s
This Peruvian health facility is located in Lima (12◦ 04′ 43′′ S exact test or Mann Whitney’s U. A p-value of p < 0.05 was considered as
77◦ 02′ 25′′ O), and has a high level of complexity due to their speciali­ significant, and 95.0 % confidence intervals (95 % CI) were estimated.
zation and disease management. During 2017 and 2018, the Blood Bank Data analysis was performed in Stata v15 (StataCorp. 2017. Stata Sta­
received approximately 45,000 blood donors and 4200 platelet donors tistical Software: Release 15. College Station, TX: StataCorp LLC.)
by apheresis on an annual basis. Of the platelet donors, approximately
2900 were blood group O donors. The sample size was estimated at 339 3. Results
considering a finite population, assuming 50.0 % of donors with at least
one critical antibody titer, a 95.0 % confidence level of and an error of A total of 339 group O donors were enrolled and analyzed in the
5.0 %. study. All of them were negative for serologic markers for transfusion
The acceptance of the applicant as a platelet donor by apheresis was transmitted infections and negative for irregular antibodies. One PC was
in charge of the Blood Bank and was based on guidelines proposed by the extracted from each donor, resulting in 339 PCs collected during the
Peruvian Program of Hemotherapy and Blood Bank [18,19]. Multipa­ study period. All PCs were transfused to group A, B or O recipients in
rous donors are routinely excluded from the apheresis platelet donation different proportions and at the request of their physician.
process by the Blood Bank, so they were not included in the study. The donor’s age ranged from 18 to 59 years, being mostly repre­
This study had ethical and administrative approval by the Uni­ sented by donors under 40 years of age, and by male (Table 1). The IgM
versidad Nacional Mayor de San Marcos (RD Nº 1820-D-FM-2017). Also, and IgG titers against A1 and B antigens were summarized in Fig. 1.
the project was approved by the Office of Training, Research and Regardless of the cut-off used to define critical IgM antibody titers, the
Teaching of the Hospital Edgardo Rebagliati Martins National (No. 968- proportion of donors with critical anti-A1 titers was higher than the
2018). All enrolled subjects informed consent their participation and proportion of donors with critical anti-B titers (Table 1). Similarly, a
study procedures. higher proportion of donors with critical titers for anti-A1 IgG antibody
was observed compared to donors with anti-B IgG antibody (Table 1).
2.2. Laboratory procedures
Table 1
Regularly, two blood samples with EDTA-K2 anticoagulant for he­ Apheresis platelet donors’ characteristics, titers and critical titers of antibodies
matological studies and other blood sample without anticoagulant for in platelet concentrates (n = 339).
testing infectious disease pathogens are drawn from each donor [18]. Characteristic % (n) 95 %CI
Hematological studies include a complete blood count, ABO and D blood
Sex
group determination, Rh and Kell phenotype characterization, and the
Male 84.7 (287) 80.4–88.1
detection of irregular anti-erythrocyte antibodies. Age (years)
The titration of anti-A1 and anti-B IgM and IgG antibodies was per­ Mean ± SD * 34.8 (118) 29.9 - 40.0
formed in the NEO Iris platform using plasma obtained from blood 18 – 29 34.8 (118) 29.9 - 40.0
samples collected with EDTA-K2. Specifically, anti-A1 and anti-B IgM 30 – 39 36.6 (124) 31.6 - 41.9
40 – 49 21.8 (74) 17.7 - 26.6
antibodies were detected and titered using the direct hemagglutination 50 – 59 6.8 (23) 4.5–10.0
method, and anti-A1 and anti-B IgG antibodies using the solid-phase IgM anti-A1
adherence method according to the manufacturer’s instructions [20, Med. (min. – max.)** 32 (4–1024)
21]. Both techniques were developed in 96-well plates and using High-titer β 37.5 (127) 32.4–42.7
High-titer ¥ 16.5 (56) 12.9–20.9
reference cells that express A1 and B antigens; Immucor Inc; 02345. A
IgM anti-B **
total of seven serial dilutions of 1: 2 were prepared for each sample using Med. (min. – max.)** 16 (4–256)
15 μL of plasma as the initial volume and isotonic saline solution as the High-titer β 16.5 (56) 12.9–20.9
diluent. To each dilution, 15 u L of A1 or B cells were added, followed by High-titer ¥ 5.6 (19) 3.6–8.6
incubation for 10 min at 25 ◦ C for IgM and at 37 ◦ C for IgG. Finally, IgG anti-A1 **
Med. (min. – max.)** 64 (4–2048)
plates used in the direct hemagglutination method were centrifuged at High risk α 15.9 (54) 12.4–20.2
250 g, 25 ◦ C during 60 s, and plates used in the solid-phase adherence IgG anti-B **
method were also centrifuged at 600 g, 37 ◦ C during 2 min. Importantly, Med. (min. – max.)** 64 (1–512)
despite the recommendation for using dithiothreitol (DTT) in the IgG High-titer α 7.7 (26) 5.2–11.0
titration [22,23], DTT was not used to inactivate IgM antibody in the Note: The cut-off used to define high-risk titer was ≥64β or ≥128¥ for IgM, and
solid-phase adherence method, as this method is prepared to detect IgG ≥256α for IgG. * Mean ± standard deviation, ** Median (minimum – maximum
only. Samples with titers equal to 128 were serially diluted to 1:4096. values).

2
G. Aguilar et al. Transfusion and Apheresis Science xxx (xxxx) xxx

4. Discussion

Group O apheresis platelet donors are considered universal donors,

Fig. 1. Antibody titers in group O platelet donors. IgM and IgG titers against
A1 and B antigens in platelet donors by apheresis are presented in panel A and
B, respectively.
Females, compared to males, had a significantly higher frequency of
critical IgG anti-A1 (p = 0.001) and anti-B (p = 0.009) titers (Tables 2
and 3). Regarding critical titers for anti-A1 and anti-B IgM, females
displayed a higher frequency of critical titers compared to males when
the cut-off was 64 (p = 0.002; Tables 2 and 3). Though, when the cut-off
was defined at 128, the frequency of critical titers for anti-A1 and anti-B
IgM was comparable among males and females (Tables 2 and 3).
Regardless of the cut-off used for IgM, the median age was lower in
donors with critical titers (Tables 2 and 3). Correspondingly, marginally
significant differences were observed when age was analyzed categori­
cally for IgM titers (Tables 2 and 3).
The overall risk assessment was performed considering two scenarios
since there is no consensus to define a critical IgM titer. In both scenarios
the cut-off point for defining a critical IgG titer was 256. In a conser­
vative scenario, considering a cut-off point for critical IgM titers of 128
(Scenario A, Table 4), 34.5 % (95 % CI: 29.6 %–39.8 %) of the donors
had at least one critical anti-A1/B antibody titer. Whereas, in a less
conservative scenario using a cut-off of 64 for IgM, the frequency of
donors with at least one risk title increased to 49.5 % (95 % CI: 44.5 %–
55.2 %) (Scenario B, Table 4).
therefore, their platelets are frequently transfused to non-isogroup blood
recipients [26,27]. Increased titers of anti-A or –B antibodies in
passively transfused PCs have been described as a factor associated with
hemolytic reactions and even death [6,28–30]. Findings suggest that,
depending on the cut-off used to define a critical IgM titer, one in two or
three group O platelet donors had at least a critical anti-A and anti-B IgM
or IgG antibody titers.
The association between intravascular hemolysis, mortality and high
IgM and IgG anti-A or -B titers has been described by multiple studies in
various countries [6,10,12,26]. It is important to highlight that an
increased titer is not necessarily associated to negative outcomes on the
recipient health, but it does represent an avoidable risk. In this study,
apheresis platelet donors had titers of up to 1024 for anti-A1 IgM, 256
for anti-B IgM, 2048 for anti-A1 IgG and 512 for anti-B IgG. A study
carried out in Greece with 70 group O platelet donors using the manual
gel method reported anti-A IgM antibody titers ranging from 2 to 1024,
titers ranging from 2 to 256 for anti-B IgM, and averages of 64 and 32 for
anti-A and anti-B IgM antibodies, respectively [28]. In India, Tendulkar
et al. using the microplate technique reported anti-A IgM titers ranging
from 4 to 1024, while for anti-B IgM titers were in the range of 4–2048
[26]. Overall, titers observed in this study were comparable with those
reported in other studies.
As described by Godoy et al., the probability of being a dangerous
universal donor in young people between 18 and 28 years of age is 3.05
times higher compared to donors over 50 years of age [24]. De Franca
et al. suggested that group O male donors older than 50 years of age
represent a less dangerous source for obtaining blood products
frequently used in non-isogroup transfusions [31]. Our findings are
consistent with those previously described, since the frequency of do­
nors with critical titers decreased as the age of the donor increased. On
the other hand, the high frequency of critical anti-A IgM or IgG titers
described here could be explained by the abundance of structures highly
similar to the A antigen present in nature, as well as the higher immu­
nogenicity of A antigen [32,33]. Similarly, increased anti-A has been
reported to be associated with mosquito bites, intestinal parasitic in­
fections or vaccination, and higher anti-A and anti-B IgG titers were
previously associated with pregnancy and vaccination [32–34]. How­
ever, this study did not evaluate potential factors that could explain the
high frequency of anti-A antibody in our donor population.
The implementation of ABO antibody titer techniques is promoted
with the aim of improving the transfusion safety of PC [12]. However,
the criteria used to identify dangerous “universal donors” are hetero­
geneous given the lack of consensus on the cut-off to define critical titers
[26,35,36]. A study conducted in Brazil that used the tube technique
suggested that donors with critical titers vary between 30.0 % and 80.0
% depending on the antibody analyzed and the cut-off chosen to define a
risky titer [24]. Another similar study in India showed that slightly more

Table 2
Donor characteristics and high-risk titers of IgM and IgG anti-A1 antibodies.
IgM titer ≥ 64 IgM titer ≥ 128 IgG titer ≥ 256
p-value p-value p-value
Yes (n = 127) No (n = 212) Yes (n = 56) No (n = 283) Yes (n = 54) No (n = 285)

Sex 0.002 0.102 0.001

Female 30 (57.7) 22 (42.3) 13 (25.0) 39 (75.0) 17 (32.7) 35 (67.3)
Male 97 (33.8) 190 (66.2) 43 (15.0) 244 (85.0) 37 (12.9) 250 (87.1)
Age (years)
Med. (min - max)* 33 (18–58) 35 (18–58) 0.043 31 (18–58) 35 (18–58) 0.025 35 (19–58) 34 (18–58) 0.521
18 - 29 51 (43.2) 67 (56.8) 0.090 23 (19.5) 95 (80.5) 0.166 19 (16.1) 99 (83.9) 0.930
30 - 39 49 (39.5) 75 (60.5) 24 (19.4) 100 (80.6) 18 (14.5) 106 (85.5)
40 - 49 19 (25.7) 55 (74.3) 7 (9.5) 67 (90.5) 13 (17.6) 61 (82.4)
50 - 59 8 (34.8) 15 (65.2) 2 (8.7) 21 (91.3) 4 (17.4) 19 (82.6)

Note: The information is presented in n (%), and the percentages were calculated in rows.
*
Median (minimum – maximum values).

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G. Aguilar et al. Transfusion and Apheresis Science xxx (xxxx) xxx

Table 3
Donor characteristics and high-risk titers of IgM and IgG anti-B antibodies.
IgM titer ≥ 64 IgM titer ≥ 128 IgG titer ≥ 256
p-value p-value p-value
Yes (n = 56) No (n = 283) Yes (n = 19) No (n = 320) Yes (n = 26) No (n = 313)

Sex 0.002 0.749 0.009

Female 17 (32.7) 35 (67.3) 2 (3.9) 50 (96.2) 9 (17.3) 43 (82.7)
Male 39 (13.6) 248 (86.4) 17 (5.9) 270 (94.1) 17 (5.9) 270 (94.1)
Age (years)
Med. (min - max)* 30 (18–58) 35 (18–58) 0.001 30 (18–58) 35 (18–58) 0.007 34 (20–58) 35 (18–58) 0.655
18 - 29 27 (22.9) 91 (77.1) 0.025 9 (7.63) 109 (92.4) 0.051 12 (10.2) 106 (89.8) 0.414
30 - 39 21 (16.9) 103 (83.1) 9 (7.3) 115 (92.7) 6 (4.8) 118 (95.2)
40 - 49 5 (6.8) 69 (93.2) 0 (0.0) 74 (100.0) 6 (8.1) 68 (91.9)
50 - 59 3 (13.0) 20 (87.0) 1 (4.4) 22 (95.6) 2 (8.7) 21 (91.3)

Note: The information is presented in n (%), and the percentages were calculated in rows.
*
Median (minimum – maximum values).

anti-A and anti-B antibodies titers described here were similar to those
Table 4
reported in previous studies that used the microplate technique, the
Overall risk assessment considering for critical anti-A1 and anti-B antibody
manual gel method, the tube technique, or the saline method [24,26,28,
titers.
37]. However, as previously described [39], critical titers reported here
% (n) 95 %CI not necessarily constitute a threat for the transfusion safety. On the other
Scenario A * hand, the titration was performed in primary samples from donors and
None 65.5 (222) 60.2–70.4 not in their collected PC, the no access to transfusion reaction events or
≥ One 34.5 (117) 29.6–39.8
medical records of PC recipients during the study period, and the failure
One 25.4 (86) 21.0–30.3
Two 7.4 (25) 5.0–10.7 to assess the stability of critical titers in PCs, does not allow to measure
Three 1.5 (5) 0.6− 3.5 the real risk translated to the PC receptor. Despite the various limita­
Four 0.2 (1) 0.0–2.1 tions, increased antibody titers in group O platelet donors could pose a
Scenario B ** potential threat for the transfusion safety.
None 50.2 (170) 44.8–55.5
≥ One 49.8 (169) 44.5–55.2
The implementation of policies related to the use of PCs containing
One 28.9 (98) 24.3–33.9 ABO incompatible plasma is frequent and suggested by various organi­
Two 15.0 (51) 11.6–19.3 zations, however, the use of manual or automated laboratory methods,
Three 5.0 (17) 3.1–7.9 such as antibody titration, is infrequent [3,12,16,18,40,41]. The
Four 0.9 (3) 0.3− 2.7
implementation of fully automated antibody titration procedures, like
Note: The cut-off for critical IgG titers was 256 in both scenarios, while the cut- the described in this study, could assist healthcare facilities in the proper
off for IgM was 128 for scenario A* and 64 for scenario B**. and reliable identification of dangerous platelet donors [35,42]. In
conclusion, through the antibody titration, we identified that one out of
than half of group O donors had anti- A and anti-B titers higher than 128 two or three apheresis platelet donors of blood group O had at least one
using the microplate technique [26]. In Thailand, by using the saline critical titer of anti-A or anti-B IgM or IgG antibodies. This finding
method, it was reported that approximately 80.0 % of group O donors highlights the importance of early identification of donors with critical
had anti-A and anti-B IgM titers higher than 64, and more than 90.0 % antibody titers in order to prevent passive transfusion of antibodies to
had anti-A and anti-B IgG titers greater than 64 [37]. In this study, by non-isogroup recipients.
using the direct hemagglutination and the solid-phase adherence
method, and depending on the cut-off used, we estimated that the fre­ Financial support
quency of donors with risky titers varied from approximately 30.0%–
50.0%. Despite numerous reports globally, local evidence of donors with The project was supported by Immucor Inc., sponsored by Diag­
risky titers remains scarce and poor characterized, therefore, we nóstico UAL SAC and awarded to GA.
consider that our findings could support data-driven policies that
improved the transfusion safety in highly complex Peruvian hospitals Author contributions
like the studied health facility.
This study has multiple limitations. The absence of technical dupli­ Gissel Aguilar: Conceptualization; Methodology; Data curation;
cates and the diagnostic accuracy of each technique used in this study Funding acquisition; Investigation; Project administration; Resources;
could reveal results that differ in one dilution, and therefore there could Writing - original draft. Nathalie Ortiz: Data curation; Investigation;
be misclassification. The comparison of our findings with those reported Writing - review & editing. Donna Gonzales: Data curation; Investi­
by others is limited because; i) the absence of a standard antibody gation; Writing - review & editing. Steev Loyola: Formal analysis;
titration technique allow the use of multiple techniques with different Methodology; Investigation; Software; Validation; Visualization;
diagnostic accuracy, ii) age, phenotype, red blood cell concentration and Writing - review & editing. José A. Paredes: Conceptualization; Meth­
the use of automated methods influence the results, and iii) in the odology; Investigation; Project administration; Supervision; Validation;
absence of consensus to define risky titers various scenarios are not Writing - review & editing.
frequently evaluated. Titers obtained by the microplate technique were
not assessed by other methods. However, it has been previously sug­ Data availability
gested that titers obtained by the microplate and tube technique are
highly correlated [26]. Otherwise, it is likely that studies in which The data that support the findings of this study are available from the
methods with better analytical sensitivity were used found higher fre­ corresponding author, upon reasonable request.
quency of donors with critical antibody titers [1], and interlaboratory
variability and the method of titration limit the generalizability of re­
sults described here [38]. Though, ranges or frequencies of critical

4
G. Aguilar et al.
Declaration of Competing Interest
The sponsor did not participate in the conception or design of the
study, data collection, analysis, interpretation, nor manuscript prepa­
ration or revision. GA collaborated to Diagnostico UAL SAC during the
execution of the study and results were partially used in her academic
thesis entitled “Titer of natural anti-A and anti-B antibodies in platelet
donors by apheresis, in a Social Security hospital in Lima”. The thesis
was presented to the Escuela Profesional de Tecnología Médica, Facul­
tad de Medicina, Universidad Nacional Mayor de San Marcos during
2019. NO, DG, SL and JP declare that they have no conflict of interest.
Acknowledgements
Authors are grateful to Lilian Castilho for her feedback and critical
opinion.
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