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Red blood cell alloimmunization among rhesus D-negative patients in a teaching hospital in Northeastern Malaysia

1 Department of Haematology, School of Medical Sciences, Universiti Sains Malaysia Health Campus, Kubang Kerian, Kelantan, Malaysia
2 School of Dental Sciences, Universiti Sains Malaysia, 16150 Kubang Kerian, Kelantan, Malaysia

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Date of Submission07-Dec-2021
Date of Decision13-Jun-2022
Date of Acceptance31-Jul-2022
Date of Web Publication12-Dec-2022


BACKGROUND: Rhesus D (RhD) negative is considered a rare blood group in Asian country including Malaysia. Thus, the red blood cell (RBC) alloimmunization among RhD negative is considered significant because the blood's availability and rarity makes it more challenging to find compatible blood. The aims of the study are to determine the prevalence, specificities of alloantibodies, and associated factors of RBC alloimmunization among RhD-negative patients admitted to our center.
METHODS: This cross-sectional study involved 562 RhD-negative patients who were admitted to Hospital Universiti Sains Malaysia from January 2011 to December 2019. Demographic, clinical, and transfusion data were collected from patients' records and laboratory information system retrospectively. The blood samples were subjected to the standard immunohematological procedure for RBC antibody screening and identification using Diamed ID gel microtyping system. Pearson's Chi-square and Fisher's exact test were used for statistical analysis and P < 0.05 was considered statistically significant.
RESULTS: The mean age of patients was 41-year-old, with the majority being female (71.4%), Malay (87.5%), blood group O (40.2%), and rr phenotype (64.1%). The main reason for admission was pregnancy related (48.6%) and trauma (18.7%). The prevalence of RBC alloimmunization was 3.6% (n = 20). Most of the alloimmunized patients had a single alloantibody (n = 18) and belonged to Rh antibody (n = 16). The most common alloantibody specificity was anti-D (n = 14) followed by anti-Le (n = 4). The significant associated factors with RBC alloimmunization were the history of blood transfusion (P = 0.049) and Rh phenotype (P = 0.047).
CONCLUSION: The rate of RBC alloimmunization in RhD-negative patients was low. Nevertheless, it is still mandatory that there should be one standard universal protocol to identify RhD-negative patients and screening for antibody especially anti-D, which is clinically significant.

Keywords: Alloantibody, alloimmunization, immunoprophylaxis, rhesus D negative

How to cite this URL:
Shaari N, Hassan MN, Mohd Noor NH, Ramli M, Iberahim S, Zulkafli Z, Yusoff SM, Bahar R, Abdullah M, Ab Rahman WS. Red blood cell alloimmunization among rhesus D-negative patients in a teaching hospital in Northeastern Malaysia. Asian J Transfus Sci [Epub ahead of print] [cited 2023 Jan 28]. Available from:

   Introduction Top

The International Society of Blood Transfusion recognize 345 blood group antigens, most of which belong to 43 genetically discrete blood group systems.[1] These red blood cell (RBC) antigens have different prevalence in different populations and ethnic groups worldwide. The ABO and rhesus (Rh) blood groups are among the most important blood groups system. The presence of Rh system (D, C, E, e, and c) was recognized in 1939, and it was confirmed within a few years.[2] An individual will be considered rhesus D (RhD) positive if they possess D antigen on the RBC surface, while the absence of D antigen will be considered to be RhD negative. Rh system appears as the second most clinically important blood group system after ABO since the antibody is able to cause hemolytic disease of fetus and newborn (HDFN) and hemolytic transfusion reaction (HTR).[3] RhD negative is considered a rare blood group in Malaysia since the prevalence of RhD negative among the overall Malaysian population and blood donors is only 0.5% and 2.5%, respectively and this is much lower than in other countries.[4]

RhD incompatibility can give a significant problem either when the RhD-negative mother is pregnant with RhD-positive fetus or transfused with RhD-positive blood that causes HDFN or HTR, respectively.[3] Prior to anti-D prophylaxis, the perinatal mortality rate from HDFN was approximately 40%–50%. Immunoprophylaxis has drastically reduced the cases of RhD-induced HDFN, where the rate of HDFN after anti-D prophylaxis implemented was reported as low as 0.04% rate.[5] Malaysia has a standard practice in managing RhD-negative patients, including pregnant mothers, giving blood products or immunoprophylaxis during pregnancy and postnatal.[6]

Besides anti-D, RhD-negative patients are also potential to develop other Rh antibodies (anti-c, -C, -E, and-e) and antibodies to other RBC antigens, which have the potential to be clinically significant. These antibodies also can facilitate accelerated destruction of RBC carrying the corresponding antigen and causing HDFN and HTR. There is no previous study on the prevalence of RBC alloimmunization in Malaysia involving many RhD-negative patients. Two local studies were reported on RBC alloimmunization, but the number of RhD-negative patients involved was minimal. One local study involving pregnant women reported that three out of 20 RhD-negative pregnant women were alloimmunized.[7] Another study involving transfused patients reported that only one RhD-negative patient was alloimmunized.[8] Thus, the study aimed to determine the prevalence and associated factors of RBC alloimmunization among RhD-negative patients admitted to our center. We hope this study can give better understanding regarding the importance of the antibody screening in managing the RhD-negative patients related to blood transfusion therapy and pregnancy.

   Methods Top

This cross-sectional study was conducted at Hospital Universiti Sains Malaysia (USM), involving RhD-negative patients admitted from January 2011 to December 2019. The study was Approved by the Human Research Ethics Committee USM using Protocol Code USM/JEPem/19120947. A total of 562 RhD-negative patients were included in this study. Those patients who were <12 years old were excluded from this study. Patients sociodemographic (age, race, gender, and occupation), clinical data (the reason for admission, history of anti-D immunoglobulin prophylaxis), and laboratory data (ABO blood grouping, Rh phenotype, transfusion history, type of blood product transfused, antibody screening, identification, and antibody specificity) were included for analysis. The RBC alloantibody can be either clinically significant or insignificant. A clinically significant alloantibody is defined as an antibody that can cause shortened survival of RBCs, leading to HDFN or HTR.[9] Examples of alloantibodies classified under clinically significant are antibodies toward rhesus, Kidd, and Duffy antigen groups.

The blood samples were subjected to the standard immunohematological procedure for RBC antibody screening and identification using the Diamed ID gel microtyping system (BIO-RAD, ID-DiaCell I-II-III Asia, and ID-DiaPanel, Switzerland). Sample with positive antibody screening were proceeded with antibody identification using an eleven-cell panel and antibody titer. Antibody titration was determined by testing serial twofold dilutions of the patient's plasma with selected RBC that express the antigen corresponding to the antibody specificities, in a 2% to 5% saline suspension using conventional tube technique in which the results are expressed as the reciprocal of the highest serum dilution that shows macroscopic agglutination.[10] Meanwhile, the Rh (C, c, E, and e) and RBC phenotyping of corresponding antigens (Lea, Leb) to the identified alloantibody was performed using conventional tube technique by testing patient's RBC with selected monoclonal antisera (Diaclon, DiaMed, Switzerland) as per the manufacturer's instructions and using our standard operating procedures.[10]

In order to differentiate between immune anti-D from the passive immunization by anti-D immunoglobulin among those with anti-D specificity, immune anti-D was considered based on these criteria: (1) no history of recent anti-D prophylaxis given on this current sample; (2) anti-D titer >1:8 despite on recent anti-D prophylaxis;[10],[11] and (3) increasing anti-D titer after follow-up.[12] Anti-G was confirmed using double adsorption and elution technique by the tube technique as described by Yousuf et al.[13] Anti-G in patient's plasma is confirm when there is no reaction of postadsorbed plasma and postadsorbed eluate with all three tested cells (R2R2, rr', and rr) and a reaction of eluate from the rr'-adsorbed cell with the R2R2 and rr' cells.

The data were analyzed using Statistical Package for the Social Sciences (SPSS) Statistics (IBM Corp. Released 2013. IBM SPSS Statistics for Windows, Version 26.0. Armonk, NY, USA: IBM Corp.). Mean and standard deviations (SDs) were calculated for numerical statistical analysis, descriptive data expressed as a percentage for categorical data, while Pearson's Chi-square and Fisher's exact test were used for association in categorical data. The prevalence of RBC alloimmunization and their specificities were described using descriptive statistics.

   Results Top

A total of 562 RhD-negative patients were included in this study. The mean age of the patients was 41 (SD ± 16.7) years old, with the majority were between 21 and 40 years. Most of the patients were Malay (84.0%), admitted due to pregnancy-related (48.6%), having blood group O (40.2%), and predominantly were rr phenotype (64.1%). Most of them did not have any transfusion history (85.6%). For those with transfusion history, 30 out of 81 (37.0%) patients had a history of transfusions with RhD-positive blood products. The details of demographic and descriptive data are illustrated in [Table 1].
Table 1: Demographic data and descriptive analysis of rhesus D-negative patients (n=562)

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Prevalence and specificity of red blood cell alloantibody among rhesus D-negative patients

We found that 30.2% (170) were positive for antibody screening. Out of all positive antibody screening, only 20 patients were alloimmunized. Patients with positive antibody screening due to passive immunization by anti-D immunoglobulin (n = 150) were considered to be nonalloimmunized. Thus, the prevalence of RBC alloimmunization among RhD negative was 3.6% (20 out of 562 patients) [Table 2].
Table 2: Prevalence of red blood cell alloimmunization among rhesus D-negative patients (n=562)

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Most of the alloimmunized patients had single alloantibody detected (n = 20) and belonged to Rh antibody (n = 16), the clinically significant antibody. The most common alloantibody specificity was anti-D (n = 14) followed by anti-Le (n = 4), anti-C (n = 1) and anti-G (n = 1), as described in [Table 3]. The rate of presence of clinically significant antibodies among alloimmunized RhD patients was 80.0% (16 out 20 patients).
Table 3: Specificity of red blood cell alloantibody among alloimmunized rhesus D patients (n=20)

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The details of clinical data for 20 alloimmunized RhD-negative patients are summarized in [Table 4]. The majority of them were female (n = 17), had anti-D alloimmunization (n = 14), were admitted due to pregnancy-related (n = 14), and without having history of transfusion (n = 15). We observed that only patients with rr (n = 17) and r'r (n = 3) phenotypes were alloimmunized. Surprisingly, we observed that ten patients were alloimmunized with anti-D despite receiving anti-D immunoglobulin prophylaxis, either during pregnancy (n = 7) or after RhD-positive blood product transfusion (n = 3). Seven patients who had a transfusion history developed RBC alloantibody. Of these patients, four patients had a history of transfusion with RhD-positive blood products. We also observed that three female patients with anti-D alloimmunization had a very high anti-D titer; 1:1024, 1:512 and 1:256, respectively.
Table 4: Details on the clinical data of alloimmunized rhesus D-negative patients (n=20)

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Factors associated with red blood cell alloimmunization in rhesus D-negative patients

The factors associated with RBC alloimmunization among RhD-negative patients that had been analyzed in this study were age, gender, history of transfusion, ethnicity, reasons of admission, ABO blood group, Rh phenotype, and the number of transfusions. This study showed significant associations between transfusion history (P = 0.049) and Rh phenotype (P = 0.047) with RBC alloimmunization among RhD-negative patients. There was no significant association of RBC alloimmunization with the other selected factors [Table 5].
Table 5: Factors associated with red blood cell alloimmunization in rhesus D-negative patients (n=562)

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   Discussion Top

We found that most RhD-negative patients in our center were blood Group O with rr phenotype. This result was concordant with RhD-negative donors in the Malaysian population as well as in Southwest Nigeria and Southern Ethiopia.[4],[14],[15] However, the results differed in other countries, which showed the highest prevalence of blood group B in Pakistan and Northern India among the RhD-negative populations.[14],[15] Almost all countries showed rr the most phenotype of RhD-negative patients.[11],[14],[15],[16],[17],[18] This indicates that although there are differences of ABO distribution within different countries and ethnicities, the common Rh phenotype distribution among the RhD-negative population is almost similar.

This current study showed that the overall prevalence of RBC alloantibodies among RhD-negative patients was considered to be low (3.6%). This finding was lower than reported in the previous local study (15% from 20 RhD-negative pregnant women) and among Oman RhD-negative pregnant women (10%).[7],[19] This current study also showed a much lower prevalence compared to the study among pregnant women before anti-D immunoprophylaxis (18%).[5] However, this study showed a slightly higher prevalence than a study done among pregnant women in Southeast Michigan and Southwest Nigeria (1.1% and 0%, respectively).[20],[21] We found that the alloimmunization with clinically significant alloantibodies was even much lower (n = 16). The rate of clinically significant alloantibodies were almost the same in tertiary center Maryland, which was 3.3%.[22]

The prevalence of alloantibodies in this study was expected to be low in view of the widespread use of Rh immunoglobulin (RhIg) prophylaxis in the Malaysian population, which subsequently decreased anti-D alloimmunization. We observed that most patients developed single RBC alloantibody, and anti-D was the most frequently RBC alloantibody identified followed by anti-Le and other Rh antibodies. Surprisingly, the RBC alloantibodies' specificities were quite different from the previous studies. Among all blood recipients and pregnant women, they found the most common RBC antibody was anti-E followed by anti-D, anti-M and other Rh antibodies.[8],[20] We found that none of the patients in this recent study was alloimmunized by anti-E.

Although the prevalence of RBC alloimmunization among RhD-negative patients was low, the alloimmunization continued to occur despite using RhIg prophylaxis. We found that 11 RhD-negative women developed anti-D despite being given RhIg prophylaxis. The probably reasons are due to nonstrict compliance to guidelines in managing RhD-negative patients, an insufficient dose of RhIg prophylaxis given, and failure in early detection of RhD-negative patients, which led to no initial RhIg prophylaxis given as shown in one of our reported cases. Another reason for RBC alloimmunization was the lack of immune globulins to other RBC antigens which gave additional attributed factors of developing other RBC alloantibodies such as anti-C, anti-G and other clinical insignificant antibodies as shown in this study.[23]

Our reported case showed one case of a 35-year-old gravida 4 para 3 woman who was wrongly labeled as RhD positive on her previous pregnancies. Thus, antenatal and postnatal prophylaxis anti-D was not given during her last three pregnancies, which led to anti-D alloimmunization with a very high anti-D titer (1: >1024) in this current pregnancy. However, the causes of the failure to prevent anti-D alloimmunization in ten other RhD-negative female patients was due to the following reasons: failure to administer an adequate dosage of antenatal or postnatal RhIg prophylaxis, failure to recognize clinical events that placed the patient at risk for alloimmunization during the pregnancy and inability to administer RhIg appropriately in posttransfusion with RhD-positive blood product. In our local guideline, transfusion of un-cross-matched blood, which is safe O-packed red cell (RhD positive), is considered in emergency and life-threatening situations, for example if the patient is suffering from a massive hemorrhage. In such a condition, RhD-negative patients might receive RhD-positive blood before the blood group is revealed, as shown in one of our reported cases, a 32-year-old man who was admitted for trauma [Table 4]. Apart from this, RhD-negative patients who required platelet transfusion also had to receive RhD-positive platelet concentrate because of the unavailability of the RhD-negative products.[24]

The other three cases of anti-D alloimmunization were male patients, and no RhIg was given despite being transfused with RhD-positive platelet concentrate. This was because of a lack of awareness in using RhIg prophylaxis after RhD-positive platelet concentrate transfusion in RhD-negative patients. The guideline suggested to administer 50 g (250 iu) RhIg following every three adult doses of platelets (PLT).[24]

Other than anti-D, we found that two of RhD-negative pregnant women were alloimmunized with either anti-C or anti-G, which were also part of the Rh antibody. Anti-C and anti-G are less immunogenic than anti-D, but both can also cause HDFN.[25] As the D antigen are highly immunogenic, in order of decreasing immunogenicity D > c >E > C >e, it is explained that RhD-negative patients are less likely to be alloimmunized from other alloantibodies than anti-D.[2],[25] However, this study showed that patients could also be alloimmunized by clinically insignificant naturally occurring alloantibodies such as anti-Le. We did not determine the thermal amplitude of anti-Le to confirm the nature of their clinical significance. Anti-Le is considered clinically significant when they react at 37°C.

One RhD-negative woman did not develop anti-D despite receiving RhD-positive platelet, possibly due to this patient's nonresponder status, perhaps related to underlying malignancy. A “responder” is defined as any patient with at least one detectable clinically significant RBC alloantibody that could have been induced by transfusion or pregnancy. Meanwhile, a “nonresponder” is a patient with at least one RBC alloantibody screen completed 15 days or later after the recorded issue date of RBC transfusion.[26]

This study demonstrated a significant association between RBC alloimmunization in RhD-negative patients and blood transfusion. Blood transfusion was the most important and known independent risk factor for RBC alloimmunization. This result was similar to other studies that showed a significant association between RBC alloimmunization and history of transfusion.[7],[27] Koelewijn et al. reported that RBC transfusion was the most important and known independent risk factor for non-RhD alloimmunization in pregnancy, followed by parity, major surgery and hematological disease.[23]

This study also showed a significant association between RBC alloimmunization and Rh phenotype. We found that patients with rr phenotype significantly associated with RBC alloimmunization and probably the first to report this finding since we could not find any other studies that reported the association of Rh phenotype with the RBC alloimmunization from the extensive literature that we made. The other known possible risk factors that may contribute to RBC alloimmunization in patients with rr phenotype include patient's immune status (immune activation status, function of regulatory immune cell) and genetic factors (MHC/HLA type and polymorphism of immunoregulatory gene).[28] However, further study needs to be explored for to prove this association.

In this study, there was no significant association between RBC alloimmunization in RhD negative and the number of pack cell transfusions. This finding was consistent, as shown in the other previous studies.[29],[30] However, this was in contrast with the conclusions of the other prior studies done where they found a significant association between RBC alloimmunization and the number of RBC transfusions.[31],[32],[33]

There was no significant association between RBC alloimmunization in RhD-negative patients and gender, age, ethnicity, and ABO blood group. This finding was consistent with those reported by previous studies.[32],[33] Meanwhile, these were in contrast with an earlier study that found a significant association between RBC alloimmunization and those risk factors.[26]

Our study also demonstrated no significant association between RBC alloimmunization and RhD type of blood product transfused. Previous study mentioned that even small quantities of RBCs (0.5 or 0.1 mL) were sufficient to trigger antibody formation in most RhD-negative individuals.[34],[35] Contaminating RBCs in PLT concentrates may also induce an antibody response.[36] The probable reason is that most of patients in this study were given RhIg prophylaxis after being transfused with RhD-positive blood products.

This study has a few limitations. There is a possibility that we missed some other antibodies that had not been tested by our screening panel, which is Diamed-ID screening panel cells for antibody screening, leading to failure to detect other irregular RBC alloantibodies. The other significant limitation is that our study only involved a small number of alloimmunized patients due to limited number of cases available within the study period. Thus, the findings need to be inferred with cautious since it might not be representative to reference population.

   Conclusion Top

Although the prevalence of RBC alloantibodies in this study was low (3.6%), the importance of antibody screening in patients with RhD negative, especially pregnant women would still be beneficial. In addition, strict compliance with the guidelines in managing of RhD-negative patients is also crucial, including following standard protocol for RhIg prophylaxis (actual timing and adequate dosage) either in pregnancy-related conditions (risk of HDFN) or in post transfusion with RhD-positive blood products. The results obtained may serve as an established database of RhD-negative patient distribution in Kelantan.


This research was funded by the Ministry of Higher Education Malaysia for Fundamental Research Grant Scheme with Project code: (FRGS/1/2020/SKK06/USM/02/3) and Geran Penyelidikan Sarjana Perubatan with grant number: (1001/PPSP/807001). We also thanked Puan Salamah binti Ahmad Syukri and Puan Faizatul Syima binti Abdul Manaf for their important work regarding extracting data from the laboratory information system.

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

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Correspondence Address:
Mohd Nazri Hassan,
Department of Haematology, School of Medical Sciences, Universiti Sains Malaysia 16150 Kubang Kerian, Kelantan
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/ajts.ajts_177_21


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