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Distribution of antenatal
alloimmunization in the southern
districts of West Bengal and its
significant associated factor
Website:
www.ajts.org Archana Naik, Prasun Bhattacharya, Palash Das1, Krishnendu Mukherjee,
DOI:
Partha Mukhopadhyay2
10.4103/ajts.AJTS_105_18

Abstract:
OBJECTIVES: Detection of maternal irregular antibodies against red blood cell antigen is vital in the
management of hemolytic disease of fetus and newborn. There are no uniform guidelines related to
antenatal antibody screening and identification in the developing Country like India. This study was
aimed to identify such alloimmunization and its associations.
MATERIALS AND METHODS: This prospective study was conducted on antenatal mothers at a
tertiary care center. The mothers having a history of anti‑D administration, blood transfusion, and
autoimmune disorders were excluded from the study. Initial indirect antiglobulin test (IAT) was
performed in all blood samples by conventional tube technique (CTT) to identify alloimmunization.
IAT‑positive samples were screened for irregular antibody by column agglutination technology (CAT).
Antibody screen‑positive samples were further analyzed in 11‑cell panel by CAT. Antibody strength
was measured by serial double dilution by CTT. The source of isoimmunization was identified by
extended Rh phenotype of women, husband, and newborn.
RESULTS: A total of 12 (2.3%) women out of 530 were positive for IAT and antibody screen.
Antibody could be identified in 11 women, of which anti‑D (5) was the most common, followed
by anti‑C + anti‑D (4), anti‑C + anti‑E (1), and anti‑C (1). All four cases of anti‑D + anti‑C were
distinguished from anti‑G by differential adsorption and elution. There was a significant association
with alloimmunization versus increased gravid status, antepartum hemorrhage, and past history of
Department of newborns with neonatal jaundice.
Immunohaematology
CONCLUSION: All pregnant women with history of antepartum haemorrhage, newborn with neonatal
and Blood Transfusion,
Kolkata Medical jundice should be screened for alloantibody for early detection and better management of HDFN.
College, 1Department of Keywords:
Community Medicine,
Alloimmunization, antibody screening, column agglutination technology, indirect antiglobulin test
College of Medicine and
Sagore Dutta Hospital,
2
Department of Obstetrics
and Gynaecology, Medical Introduction the need to detect and monitor maternal
College, Kolkata, West alloantibodies capable of causing HDFN is
Bengal, India

Address for
correspondence:
T here are more than 50 red blood cell (RBC)
alloantibodies causing hemolytic
disease of the fetus and newborn (HDFN).[1]
still a concern.[1]

After ABO, Rh is the most immunogenic

Dr. Prasun Bhattacharya, Although Rh immunoglobulin prophylaxis blood group system. It is the most complex
Department of of the 36 human blood group systems
Immunohaematology
has significantly reduced the incidence
and Blood Transfusion, of pregnancies complicated by anti‑D, for its polymorphism. It comprises 54
Kolkata Medical College, antigens numbered RH1–RH61, with
88 College Street, seven numbers obsolete.[2] Rh antigens are
Kolkata ‑ 700 073, This is an open access journal, and articles are
West Bengal, India. distributed under the terms of the Creative Commons
E‑mail: pbhattach@gmail. Attribution‑NonCommercial‑ShareAlike 4.0 License, which
com allows others to remix, tweak, and build upon the work How to cite this article: Naik A, Bhattacharya P, Das P,
non‑commercially, as long as appropriate credit is given and Mukherjee K, Mukhopadhyay P. Distribution of antenatal
Submitted: 01‑09‑2018 the new creations are licensed under the identical terms. alloimmunization in the southern districts of West Bengal
Revised: 12‑09‑2019
and its significant associated factor. Asian J Transfus Sci
Accepted: 06‑06‑2020
2020;14:119-25.
Published: 19-12-2020 Forreprintscontact:[email protected]

© 2020 Asian Journal of Transfusion Science | Published by Wolters Kluwer - Medknow 119
 Naik, et al.: Distribution of antenatal alloimmunization in the southern district of West Bengal

encoded by two homologous, closely linked genes on who had a past history of blood transfusion, and (c) any
the short arm of chromosome 1: RHD, producing the pregnant women with a positive history of autoimmune
D antigen, and RHCE, producing the C, c, E, and e or other immunological disorders were excluded from the
antithetical antigens.[2] study to rule out other causes of sensitization.[6,7]

Isoimmunization in pregnant women has been Medical and obstetrical history documentation
extensively studied in different area of world, with A medical and obstetrical history and follow‑up records
the frequency being found to range from 0.4% to 2.7% were reviewed after counseling the antenatal mother and
worldwide.[3] Most of the developed countries have her spouse as per the investigation pro forma. The family
guidelines for screening all pregnant women for irregular history of consanguinity (if any) was also documented.
erythrocyte antibodies. According to the guidelines of
the British Committee for Standards in Haematology, all Blood sample collection and blood grouping of
pregnant women should be ABO and D antigen typed antenatal women, spouse, and their new born
and screened for the presence of red cell antibodies early A volume of 3 ml ethyldiaminetetra acetic acid (EDTA)
in pregnancy and at 28th weeks of gestation.[4] However, and 3 ml clotted blood sample were collected from
no screening guidelines are followed in developing the antecubital vein of the antenatal women and their
countries such as India.[3] Further, there is scarcity spouse during their first visit under strict aseptic
of data on the prevalence of pregnancy‑induced condition. These EDTA and clotted samples were
isoimmunization in Eastern India. Detection of maternal centrifuged at 3000 rpm × 3 min; then, plasma and
irregular antibodies against RBC antigen is vital in the serum were separated, respectively.[8] The cells from
management of HDFN. All other antibodies other than EDTA sample was processed for forward ABO blood
ABO system detected against RBC antigen are considered
grouping and extended Rh typing by conventional tube
irregular or unexpected antibodies.[5]
technique (CTT).[8] Reverse blood group was done using
in‑house freshly prepared reagent pooled A, B, and O
Here, we assessed the overall spectrum and profile of
cells.[8] The blood samples of newborn were sent from
pregnancy‑induced isoimmunization in developing
the ward in EDTA vials for ABO, extended Rh, and Kell
country. It was aimed to increase the awareness related
phenotype for forward grouping and direct antiglobulin
to antenatal antibody screening and their regular
follow‑up. Identification of associated cofactors for test (DAT).[8] Serum from clotted sample was used
the development of alloantibody(s), viz., age, gravid for antibody screening and identification. DAT of the
status, gestational weeks, past history of neonatal antenatal mother was not performed.
hyperbilirubinemia, previous pregnancy loss, and
antepartum hemorrhage (APH), was also analyzed. Irregular antibody screening and identification
An initial antibody screening was done by indirect
antiglobulin test (IAT) using pooled reagent O cell
Materials and Methods
and mother’s serum from clotted sample by CTT
The prospective study was conducted in the Department using poly‑specific Coomb’s sera (Tulip Diagnostics
of Immunohematology and Blood Transfusion (IHBT) Pvt. Ltd). [8] Then, both IAT‑positive and ‑negative
in collaboration with Department of Obstetrics and sera were further used for the antibody screening and
Gynaecology (G&O) of a Government Medical College identification in column agglutination technology (CAT)
and Hospital, at Kolkata, for a period of 1½ years (from using commercially available three cells (R1R1, R2R2,
January 2015 to June 2016). The study population consisted and rr) and 11 cells, respectively (Dia Panel, Bio‑Rad,
of antenatal mothers, irrespective of their gestational Switzerland).[9,10] The strength of agglutination was
weeks who attended G&O outpatient department (OPD) graded (1+ to 4+) in CAT. A flowchart of the initial
and were referred to the Department of IHBT for ABO workup procedure is given in Figure 1.
and Rh blood group and antibody screening. There were
5625 antenatal mothers who attended the OPD and 1512 Measurement of antibody strength/titer in case of
deliveries conducted during the study period. A total single antibody
of 530 antenatal women were evaluated, and informed Antibody strength was determined by the titration
consent was taken before blood sampling. The study was method in CTT using corresponding antigen‑positive
approved by the Institutional Ethical Committee (IEC). cells in doubling dilution with normal saline.[11] Any
antibody(s) strength ≥16 was consider to be significant
Patient selection criteria for Rh antibody(s), and titer ≥8 was significant for
Antenatal women of both primigravida and multigravida Kell antibody(s).[11] After initial titration, the serum/
were randomly chosen. The antenatal mothers (a) who had plasma sample was aliquot and preserved in −40°C for
received anti‑D prophylaxis within the last 3 months, (b) comparison of titer during follow‑up.
120 Asian Journal of Transfusion Science - Volume 14, Issue 2, July-December 2020
 Naik, et al.: Distribution of antenatal alloimmunization in the southern district of West Bengal

3 ml EDTA and 3 ml Clotted Blood Sample of pregnant women

(3000 rpm × 3 min)

3 times saline washed cells

from EDTA sample Serum(Clotted)
Reverse grouping ( plasma, EDTA)

IAT with pooled O cell by CTT

Forward grouping
and
Extended Rh Phenotype

IAT Positive IAT Negative

Repeat 3-cell Screening Repeat IAT with 3 cells

*Ab Screening Positive *Ab Screening Negative

3 cell Positive 3 cell Negative

**F.P IAT Excluded *Ab identification by 11 cell panel ***F.N IAT Excluded

*Ab identification by 11 cell panel *Ab unidentified

*Ab strength by titration

*Ab strength by titration in CTT method in CTT method

*Ab-Antibody
**F.P-False positive
***F.N-False negative
Figure 1: The flowchart of initial workup of the study population

Analysis of the antibody specificity and strength multigravida (G2–G7). The age group of these women
in case of multiple antibodies was 18–40 years. The spouses of 343 antenatal women
In case of antenatal mothers who were having multiple were available for analysis of their ABO and Rh
antibodies, the individual antibody and their strength phenotype. The blood group and extended Rh phenotype
were determined using differential adsorption of only 27 newborns delivered by these mothers were
methods (i.e., corresponding single antigen‑positive available for analysis.
and other antigen‑negative in‑house freshly prepared
individual blood group O donor cells).[4,5,12] Of them, 496 (93.58%) women were Rh (D) positive
and 34 (6.42%) were Rh D negative. A total of 12 (2.3%)
Statistical analysis of data women were IAT positive with both pooled O cell and
Categorical variables are expressed as number of patients 3‑cell panel. Samples that were positive in CAT were
and percentage of patients and compared across the groups also positive in CTT. Results in both the techniques
using Pearson’s Chi‑square test for the independence of were same.
attributes. The Statistical Software SPSS Version 20 (IBM
Corp, Armonk, NY, USA) has been used for the analysis. Among these 343 couples with known blood
An alpha level of 5% has been taken, i.e., if any P < 0.05, it groups, 32 women had Rh incompatibility with their
has been considered statistically significant. spouses (32 couples had Rh (D)‑negative women having
Rh (D)‑positive spouses). In these 32 Rh D‑incompatible
Results couples, 10 (31.25%) women developed alloantibody,
whereas only 2 (0.64%) women were alloimmunized
Profile and distribution of study population among the rest 311 Rh‑compatible couples (P < 0.0001).
A total of 530 antenatal women were randomly selected In the other 187 couple, spouse’s blood group could not
and followed up during their antenatal period. Among be done. IAT positivity was observed in nine women out
them, 153 were primigravida and the rest 377 were of 377 multigravida and three out of 153 primigravida.
Asian Journal of Transfusion Science - Volume 14, Issue 2, July-December 2020 121
 Naik, et al.: Distribution of antenatal alloimmunization in the southern district of West Bengal

Frequency and distribution of alloantibodies The course of gestation was uneventful in the rest 4
(n = 12) women, who had antibody titre of below critical label. In
In these 12 alloimmunized women, five developed single eight antenatal mothers whose titer was above the critical
alloantibody against D antigen (41.7%) followed by level, four of them had an uncomplicated gestational
anti‑C (1 woman). In the rest six mothers who developed journey with delivery of healthy newborn. In the rest
multiple alloantibodies, anti‑D + anti‑C combination four women (whose antibody titer was ≥16), one of
was seen in 4 (33.3%) and the other combination them had a premature delivery at 30 weeks, one had a
was anti‑C + anti‑E, who was also an Rh‑negative severe hydrops at 28 weeks, and another two women
primigravida. Antibody could not be identified in one delivered at 36 weeks of gestation with severe jaundice
woman. requiring exchange transfusion. An overall poor outcome
of 50% (4/8) was seen in mothers having antibody titer
All of the anti‑D + anti‑C combination of alloantibodies well above 16.
was distinguished from anti‑G (D + C antibody) by
differential adsorption and elution method as anti‑G Factors associated with development of antenatal
has a specificity for both D and C antigens at the same alloimmunization
time. Figure 2 shows the distribution of the identified There was a significant increase in alloimmunization
alloantibodies. The profile and spectrum of alloantibodies (P < 0.001) in the third gravida (G3) onward [Table 3].
in these 12 antenatal women in their course of gestational
journey are summarized in Table 1. The critical titer In 521 antenatal women who were without any history of
of ≥16 in Rh antibody was observed in eight women, APH, among them, 10 (1.92%) were IAT positive. In the
and the titer ranges from 16 to 2048. rest nine women who had a history of APH, 2 (22.22%)
of them were IAT positive, which was statistically
Extended Rh profile of isoimmunized women significant (P < 0.001) [Table 4].
(n = 12), their spouses, and new born
Among 502 women who did not have a previous history
To identify the cause of alloimmunization other than
of newborn with neonatal jaundice, 8 (1.59%) had a
alloanti‑D, an extended Rh phenotype was performed
positive IAT. In the rest 28 women, there was a past
in the women, their spouses, and the implicated
history of neonatal jaundice, and out of them, 4 (14.29%)
newborns [Table 2]. The underlined italicized antigen(s) were positive on IAT (P < 0.001) [Table 5].
was inherited from the father to the newborn.
There is no significant correlation between
Strength of alloantibody versus its outcome alloimmunization and age, gestational week, and
during the course of gestation previous pregnancy loss.
In 12 alloimmunized women, eight were having
antibody above the critical titer (i.e., ≥16, ranged Discussion
from 16 to 2048) during their gestational period, seven
women were during the first trimester, and one woman We observed that all the 16 antibodies in 11 women
during the mid‑trimester reached critical label of titer were against the antigen of Rh system except one which
[Table 1]. could not be identified. In our study, the patients with
a history of blood transfusion, RhD immunoglobulin
Not identified,
prophylaxis, and autoimmune disease were excluded
8.3 Anti -C, 8.3 by the selection criteria. This was not followed in most
Anti -C+E, 8.3 of the previous studies.[13‑15] The antibody other than Rh
system was mostly developed due to previous blood
transfusion.[16] Our results showed almost a similar
rate of isoimmunization among Rh‑negative women
Anti -D+C, 33.3 in comparison to earlier studies ranging from 0.4% to
2.7% [Table 6].

The present study showed that anti‑D was the

most common single alloantibody (41.7%), and
Anti -D, 41.7
alloantibody against multiple red cell antigens
anti‑D + anti‑C was the most common (33.3%).
This result is similar to the study by Pahuja et al. [3]
Anti-C Anti-C+E Anti-D Anti-D+C Not identified
from Northern India. In all of these four women,
Figure 2: Distribution of alloantibody specificity in pregnant women anti‑D + anti‑C was distinguished from anti‑G. It is
122 Asian Journal of Transfusion Science - Volume 14, Issue 2, July-December 2020
 Naik, et al.: Distribution of antenatal alloimmunization in the southern district of West Bengal

Table 1: Profile and titer of maternal alloantibodies during their gestational course
Gravida and parity Antibody specificity Titer at 1st trimester Titer at 2nd trimester Titer at 3rd trimester Range of titer
G6P3+2 Anti‑D 16* 32* 32* 16‑32
G3P2+1 Anti‑D 64* 64* 128* 64‑128
Anti‑C 4 4 8 4‑8
G4P1+2 Anti‑D 512* 512* 2048* 512‑2048
Anti‑C 4 4 8 4‑8
G2P1+0 Anti‑D Negative 4 8 4‑8
G3P2+1 Anti‑D 16* 64* 512* 16‑512
G6P5+0 Anti‑D 16* 32* 256* 16‑256
G2P1+0 Anti‑D 8 16* 16* 8‑16
G2P1+0 Anti‑D 512* 512* 1024* 512‑1024
Anti‑C 64* 64* 128* 64‑128
G1P0+0 Not identified NA NA NA NA
G1P0+0 Anti‑C 1 1 1 1‑1
G1P0+0 Anti‑C 2 2 2 2‑2
Anti‑E 4 4 4 4
G4P1+2 Anti‑D 32* 64* 128* 2‑4
Anti‑C 2 2 4 32‑128
*Significant titer ≥16. NA=Not available

Table 2: An overall distribution of ABO extended Rh phenotype

Alloantibody Women blood group and Husbands’ blood group New borns’ blood group
specificity extended Rh phenotype and Rh phenotype and extended Rh phenotype
Anti‑D B, dccee B, DCcee B, DCcee
Anti‑D+C B, dccee O, DCCee B, DCcEe
Anti‑D+C B, dccee B, DCcee B, DCcee
Anti‑D O, dccee O, DCcee Not done
Anti‑D B, dccee B, DCCee Not done
Anti‑D A, dccee AB, DCcEe Not done
Anti‑D A, dccee A, DCCee A, DCcee
Anti‑D+C A, dccee A, DCCee O, DCcee
Anti‑C+E O, dccee O, DCCee O, DCcee
Anti‑D+C B, dccee B, DCCee B, DCcee
The underlined italic antigens were inherited from the father to new born

Table 3: Correlation between gravid status versus of the anti‑D + anti‑C had a titer of anti‑C above anti‑D.
alloimmunization This rules out the possibility of anti‑G.
Gravida IAT Total P Significance
Negative Positive In Rh‑negative women, nine out of 16 antibodies (56.25%)
G1 150 (98.04) 3 (1.96) 153 (100) <0.001 Significant were anti‑D (alone or in combination with C), six were
G2 200 (99.01) 2 (0.99) 202 (100) anti‑C (37.5%) (in combination with anti‑D or alone), and
G3 117 (97.5) 3 (2.5) 120 (100) one was anti‑E (6.25%) in combination with anti‑C [Figure 2].
G4 40 (95.24) 2 (4.76) 42 (100)
G5 8 (100) 0 (0) 8 (100) Antibodies other than anti‑D were inherited from the
G6 2 (50) 2 (50) 4 (100) spouse’s phenotype are shown in the Table 2. One women
G7 1 (100) 0 (0) 1 (100) who developed a combination of anti‑C + anti‑E was
Total 518 (97.74) 12 (2.26) 530 (100) found to be mismatch phenotype with her spouse for C,
IAT=Indirect antiglobulin test, IAT=Indirect antiglobulin test
but the development of anti‑E could not be explained. To
explain this phenomenon of the development of anti‑E,
important to distinguish anti‑G from anti‑D + anti‑C molecular genetic analysis could have been helpful. She
as women with anti‑G without anti‑D should be had a history of APH during the second trimester.
eligible for anti‑D immunoprophylaxis. [4]
We found a statistically significant correlation between
A proportion of antibodies with apparent anti‑D + anti‑C the development of antibody versus gravid status of
specificity but with disproportionately high anti‑C pregnant women, APH, and past history of neonatal
titers may be demonstrated by advanced serological jaundice. Similar results were shown by Pahuja et al.,[3]
technique, to be anti‑G.[4] However, in our cases, none Al‑Joudi et al., [22] and Sidhu et al., [23] which shows
Asian Journal of Transfusion Science - Volume 14, Issue 2, July-December 2020 123
 Naik, et al.: Distribution of antenatal alloimmunization in the southern district of West Bengal

Table 4: Correlation between bleeding pervagina and alloimmunization

History of IAT Total P Significance
bleeding PV Negative Positive
No 511 (98.08) 10 (1.92) 521 (100) <0.001 Significant
Yes 7 (77.78) 2 (22.22) 9 (100)
Total 518 (97.74) 12 (2.26) 530 (100)
PV=Pervagina, IAT=Indirect antiglobulin test

Table 5: Correlation between history of neonatal jaundice and alloimmunization

History of NNJ IAT Total P Significance
Negative Positive
No 494 (98.41) 8 (1.59) 502 (100) <0.001 Significant
Yes 24 (85.71) 4 (14.29) 28 (100)
Total 518 (97.74) 12 (2.26) 530 (100)
NNJ=Neonatal jaundice, IAT=Indirect antiglobulin test

Table 6: Prevalence of alloimmunization among pregnant women in different areas of the world
Authors of Year Total Number of Number of Overall Type of antibodies Special comments
study (place) number patients antibodies prevalence
of women with identified
screened antibodies
Pahuja et al.[3] 2008‑2009 3577 45 51 1.25% Rh D contributed to 78.4%
(Delhi, India) of all the antibodies formed
Koelewijn et al.[15] 2008 305,000 1002 1.232% of First‑trimester screening
(The Netherlands) all, 0.328% enables timely treatment
of non‑RHD of HDFN caused by
patients antibodies other than Anti‑D
Gottvall et al.[17] 2008 78,145 316 376 0.4% 0.16% symptomatic Anti‑D
(Sweden) 60%, Fya 10%, c 7%, K 4%
Al‑Ibrahim et al.[18] 2008 1195 42 1.92% 52.38% Rh group, 2.38%
(Saudi Arabia) Kell, 2.38% Kidd, 2.38%
Lewis, 2.38% Duffy, 4.76%
nonspecific, 33.33%
autoantibodies
Lee et al.[19] (China) 2003 28,303 213 230 0.79% Clinically significant 0.27%, Routine antenatal antibody
Anti‑ Mi 57.6%, Anti‑E screening for Chinese
19.7%, Anti‑S 10.6%, women may not be
Anti‑c 7.6% worthwhile
Chandrasekar 2001 34,913 186 85 Antibody other than
et al.[20] (Ireland) Anti‑D
Howard et al.[21] 1998 22,264 244 244 1% 100 anti‑D, 144 non‑Rh D
(Liverpool, UK)
Present study 2015‑2016 530 12 16 2.3% Rh D contributes to 56.25%
(West Bengal, India) of all antibodies formed

increase in alloimmunization with increasing gravida Halder, Dr. Debapriya Basu, Dr. Abhijit Mandal,
status. Dr. Rathindranath Biswas, Dr. Eeshita Samanta, and Dr.
Nowroz Afroza, for their support.
Conclusion
Financial support and sponsorship
Alloimmunization due to Rh system antigen was the Nil.
most common. Anti‑D immunoprophylaxis may prevent
alloanti‑D‑induced HDFN, but it is ineffective against other Conflicts of interest
antibodies of the polymorphic Rh system‑like C and E. There are no conflicts of interest.
Antibody screening should be incorporated in antenatal
checkup of all pregnant women with history of antepartum
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