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Prevalence of Unexpected Antibodies in Pregnant Korean Women and Neonatal Outcomes
국내 임산부의 비예기항체 빈도와 신생아의 예후 분석
Korean J Blood Transfus 2019;30:23−32
Published online April 30, 2019;
© 2019 The Korean Society of Blood Transfusion.

Eu Jeen Yang1, Kyung-Hwa Shin2, Duyeal Song3, Sun-Min Lee3, In-Suk Kim3, Hyung-Hoi Kim2, Hyun-Ji Lee3
양유진1, 신경화2, 송두열3, 이선민3, 김인숙3, 김형회2, 이현지3

1Department of Pediatrics, Pusan National University Yangsan Hospital, Yangsan, Korea,
2Yangsan, Department of Laboratory Medicine, Pusan National University Hospital, Yangsan, Korea,
3Pusan, Department of Laboratory Medicine and Biomedical Research Institute, Pusan National University Yangsan Hospital, Yangsan, Korea
1양산부산대학교병원 소아청소년과,
2부산대학교병원 진단검사의학과,
3양산부산대학교병원 진단검사의학과
Hyun-Ji Lee Department of Laboratory Medicine and Biomedical Research Institute, Pusan National University Yangsan Hospital, 20 Geumo-ro, Mulgeum-eup, Yangsan 50612, KoreaTel: 82-55-360-1875, Fax: 82-55-360-1880, E-mail:, ORCID:
Received October 22, 2018; Revised January 14, 2019; Accepted January 14, 2019.
This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License ( which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited.


In pregnant women, the frequency of irregular antibodies that cause hemolytic disease of the fetus and newborn (HDFN) vary between study populations. The clinical manifestations of HDFN differ according to the specificities and degree of irregular antibodies. This study examined the frequency and nature of maternal alloimmunization and neonatal outcomes.


Pregnant women, who underwent irregular antibody screening for prenatal testing at an obstetrics clinic in a single center, were enrolled. Those who screened positive for irregular antibodies were selected as the test group, and age- and obstetrics history-matched pregnant women were selected as the control group to evaluate the pregnancy outcomes according to irregular antibodies.


The prevalence of irregular antibodies was 2.78% (42/1,508). With the exception of an unidentified antibody, anti-D was the most frequently identified antibody, followed in order by anti-E and anti-Lea. The rate of fetal death was higher in the test group (6/37, 16.2%) than in the control group (1/37, 2.7%) (P=0.047). Eight pregnant women had anti-C or anti-D, one woman had a stillbirth, and four living neonates developed hyperbilirubinemia. Of six pregnant women with anti-E alone or with other alloantibodies, three experienced a spontaneous abortion or stillbirth. Among the six newborns with maternal anti-Lea and anti-Jka, four developed hyperbilirubinemia, but their mothers did not experience a spontaneous abortion or stillbirth.


The prevalence of unexpected antibodies among pregnant Korean women was 2.78%. A significant difference in neonatal outcomes was observed, including the death rate, prematurity, and hyperbilirubinemia, depending on the specificity of the unexpected antibody.

Keywords : Hemolytic disease of the fetus and newborn, Alloimmunization, Hyperbilirubinemia, Pregnancy

Maternal alloimmunization via transfusion, transplantation, or fetomaternal hemorrhage in a previous or current pregnancy is a cause of hemolytic disease of the fetus and newborn (HDFN) [1]. HDFN is a disease, in which maternal red blood cell (RBC) alloantibodies of the Immunoglobulin G (IgG) class are passed actively across the placenta and destroy fetal erythroid cells carrying the antigen involved [1]. The clinical spectrum of the disease varies and includes mild hemolytic anemia, hyperbilirubinemia, hepatomegaly, severe anemia with hydrops, and even death of the fetus, according to the number of RBC antibodies (one vs. multiple) [1-3]. The causative antibodies of severe HDFN, which presents as severe anemia, jaundice, or death in either the fetus or neonate, are anti-D, anti-c, anti-K, anti-C, and anti-E. Other causative antibodies, including those against Rh, Duffy, Kidd, and MNS blood group systems, lead predominantly to anemia or jaundice during the neonatal period [3]. Therefore, an awareness of the prevalence of maternal alloantibodies is important for managing the health of the fetus and neonate. The prevalence of alloantibodies varies in pregnant women, and the expression of RBC antigens differs among ethnicities [4-8]. The prevalence of alloantibodies in pregnant women in Korea was first reported almost 20 years ago [9]; however, there are no reports on the correlation between maternal alloimmunization of RBCs and the health of the fetus and newborn.

This study examined the prevalence and nature of maternal RBC alloimmunization and neonatal out-comes. The fetal and neonatal outcomes of pregnancies with and without RBC antibodies were com-pared. This study is expected to encourage the establishment of a protocol to evaluate unexpected antibodies during pregnancy.

Materials and Methods

1. Subjects

Pregnant women, who underwent unexpected antibody screening for prenatal testing at the obstetrics and gynecology clinic at Pusan National University Yangsan Hospital from June 2012 to June 2017, were enrolled. This study was approved by the Institutional Review Board of Pusan National University Yangsan Hospital (IRB no. 1708–010–058).

A test group and control group were established to analyze the outcomes of pregnant women with unexpected antibodies. Pregnant women with a positive result were selected as the test group. The control group consisted of age- and obstetric history- matched pregnant women with negative results. The control group were selected randomly among pregnant women who underwent antibody screening from June 2012 to June 2017.

The ABO/Rh (D) type, age, past history of blood transfusion or surgery, obstetric history, and results of unexpected antibody screening of the pregnant women, as well as the ABO/Rh (D) type, gestational age at birth, phototherapy history, bilirubin levels, antiglobulin test results, and mortality of the babies of these women were recorded. For pregnant women displaying alloantibodies initially in the present pregnancy at the authors’ center, a serologic phenotyping test was performed for Rhesus, Kidd, Duffy, and MNS blood group antigens.

ABO/Rh (D) typing and antibody screening were performed using the Ortho AutoVue Innova System (Ortho Clinical Diagnostics, Raritan, NJ, USA). For ABO/Rh (D) typing, 0.8% Affirmagen A1, B Grouping Red Blood Cells (Ortho Clinical Diagnostics), and ABO/Rh Reverse Cassettes (Ortho Clinical Diagnos-tics) were used. Surgiscreen Reagent sub code D (3%) (Ortho Clinical Diagnostics), which was manufactured as a three-cell panel, including Dia, and the Polyspecific Anti-Human Globulin Cassette (Ortho Clinical Diagnostics) were used for antibody scree-ning. The antibodies were identified using the ID DiaPanel, ID-DiaPanel P (Bio-Rad, Cressier, Morat, Switzerland), LISS/Coombs card (Bio-Rad Laborato-ries, Hercules, CA, USA), and NaCl/Enzyme card (Bio-Rad) incorporating the antiglobulin and enzyme methods. Unidentified antibodies were defined as antibodies other than those against the Rh, Kell, Duffy, Kidd, Lewis, P, MNS, Lutheran, and the Xg blood group systems that could be identified using the ID DiaPanel (Bio-Rad) with the LISS/Coombs card and the NaCl/Enzyme card.

Antibody identification was not performed routinely in cases of weakly reactive results or patients lost to follow-up.

2. Other laboratory tests

The direct antiglobulin test [10] was performed using the gel-based Diamed-ID system (Bio-Rad). The total and direct bilirubin levels were measured using the Roche 8000 series Cobas c702 System (Roche Diagnostics, Basel, Switzerland). The reference range of indirect bilirubin differed according to the age of the neonate: 1~3 mg/dL at birth became 5~6 mg/dL between days 2 and 4, and decreased between days 5 and 7 after birth [11].

3. Anti-D prophylaxis

In the authors’ hospital, Rh D-negative pregnant women were given anti-D prophylaxis at 28 weeks of pregnancy. When pregnant women experienced vaginal hemorrhage, the physician gave anti-D prophylaxis earlier than 28 weeks.

4. Obstetric follow-up

The guidelines from the Korean Society of Obste-trics and gynecology recommend unexpected antibody screening testing during the prenatal period, including the third trimester of pregnancy [12]. In cases of a positive antibody screening test, the antibody screening test was performed every 72 h if the patient received a blood transfusion. Middle cerebral arterial peak systolic velocity tests were performed on each infant. No participant in this study received an intrauterine transfusion.

5. Statistical analyses

Pearson’s chi-square tests were used to compare the categorical variables. A Mann-Whitney U test was used to compare the median (range) value of the continuous variables between the two groups. All statistical analyses were performed using SPSS 18.0 software (SPSS, Inc., Chicago, IL, USA), and P values<0.05 were considered significant.


Overall, 2,493 samples from 1,508 pregnant women were tested within the study period. The median age of the pregnant women was 33 years (range, 16~46). Of the total samples, 2.36% (59/2,493) showed positive results in the antibody-screening test. After excluding duplicate samples from the same patient, the prevalence of unexpected antibodies was 2.78% (42/1,508). After excluding five cases of passive immunization of anti-D, the actual prevalence of unexpected antibodies was 2.45% (37/1,508).

With the exception of unidentified cases or those not tested, anti-D was the antibody identified most frequently, followed in order by anti-E and anti-Lea (Table 1). Of all of the Rh D-negative pregnant women, five and four had anti-D because of prophylactic immunization and active immunization. The most common alloantibodies belonged to the Rh system (14/28, 50.0%).

Specificities of the red blood cell antibodies in the 37 pregnant women

Blood group systemN%
 Anti-E, c25.4
 Anti-C, e12.7
 Anti-E, Fyb12.7
 Anti-E, Dib12.7
 Not tested821.6

Thirty seven pregnant women with unexpected antibodies were assigned to the test group. None of the women in the test group had received a blood transfusion or surgery before the present pregnancy. Thirty-seven pregnant women without unexpected antibodies were enrolled in the control group. Table 2 lists the characteristics of the pregnant women and their neonate or fetus according to the presence of maternal unexpected antibodies. No significant differences in obstetric history (including gravida and para), age, and ABO/blood type were observed between the two groups. Only the survival rate of the current pregnancy was significantly different (P=0.047). Perinatal transfusion was more frequent in the test group (14 pregnant women) than in the control group (seven pregnant women), although the difference was not significant (P=0.071). All blood products were cross-matched by the Coombs phase and transfused into alloimmunized pregnant women. In the test group, 31 neonates were born alive (six neonates, preterm; 25 neonates, full-term) and six fetuses or newborns were aborted or died at birth. In the control group, 36 neonates were born alive (10 neonates, preterm; 26 neonates, full-term) and one died at birth. No neonates with enzymopathies, hemoglobinopathies, or other forms of liver injury or CMV infection were noted.

Characteristics of pregnant women and their neonate or fetus according to the presence of maternal unexpected antibody

Maternal unexpected antibodyP value

Positive (test group)Negative (control group)
Total number of pregnant women3737
 Age (median, range)34 (25~44)33 (25~43)0.307
 ABO blood group (N, %)0.985
  A/B/AB/O13 (35.1%)/9 (24.3%)/12 (32.4%)/9 (24.3%)/
4 (10.8%)/11 (29.7%)5 (13.5%)/11 (29.7%)
 Rh D blood group (N, %)0.056
  Positive/negative30 (81.1%)/7 (18.9%)36 (97.3%)/1 (2.7%)
 Packed RBC transfusion before current pregnancy (N, %)0.115
  Yes/no4 (10.8%)/33 (89.2%)0 (0.0%)/37 (100.0%)
Obstetric history
 Gravida (median, range)2 (1~5)2 (1~6)0.562
 Para (median, range)0 (0~2)0 (0~2)0.210
 Abortion (median, range)0 (0~3)0 (0~2)0.149
 Live (median, range)0 (0~2)0 (0~2)0.604
Antenatal transfusion history in pregnant women (yes/no)3 (8.1%)/34 (91.9%)0 (0.0%)/37 (100.0%)0.240
Total number of fetuses or neonates3737
 Outcome of fetuses or neonates at birth (live/death)31 (83.8%)/6 (16.2%)36 (97.3%)/1 (2.7%)0.047
Total number of live neonates at birth3136
 Preterm birth/full-term birth9 (29.0%)/22 (71.0%)10 (27.8%)/26 (72.2%)0.910
 Phototherapy (yes/no)12 (38.7%)/19 (61.3%)7 (19.4%)/29 (80.6%)0.081
Total number of neonates with phototherapy12 (38.7%)7 (19.4%)0.081
 Times of phototherapy (median, range)2 (1~7)1 (1~3)0.536
 Peak total bilirubin (median, range)8.31 (5.2~14.52)9.26 (7.24~12.66)0.463

Among the six pregnancies in the test group (anti-E [one case], anti-E and anti-c [one case], anti-E and anti-Fyb [one case], unidentified antibody [two cases], and not tested [one case]) that ended in an abortion or stillbirth, two mothers may have experienced an abortion or stillbirth due to systemic lupus erythematosus. The remaining four pregnant women had no specific diseases or no other presumed cause. In addition, six pregnant women in the test group whose baby was born preterm had anti-D (2 cases), anti-Lea (2 cases), and an unidentified anti-body (one case), and one case did not undergo testing.

Table 3 lists the characteristics of the neonates with the presence of maternal unexpected antibody. One case (case no 22) was presumed to be ABO incompatible between the mother and her neonate. In case number 14, HDFN was suspected, which was confirmed by an elution study on the neonatal RBCs. Among the eight pregnant women with anti-C or anti- D antibodies, four neonates developed hyperbiliru-binemia and received phototherapy. An anti-G test was not performed on anti-C- and anti-D-positive pregnant women. Among the five newborns with maternal anti-Lea, three developed hyperbilirubine-mia. The newborn with maternal anti-Jka developed hyperbilirubinemia and had the Jka antigen. Of the six pregnant women with anti-E alone or with other alloantibodies, the surviving three neonates did not develop hyperbilirubinemia.

Characteristics of the neonates with presence of maternal unexpected antibody

Case numberMotherNeonate

Antibody specificityABO blood typeGestational age at birthABO blood typeDATPhoto-therapyTotal bilirubin (mg/dL)Hemo-globin (g/dL)Age (days) at test
1Anti-DA (–)38+5 wksA (+)NegativeNo6.6816.32
2Anti-DAB (–)40+0 wksA (+)NANo5.5915.23
3Anti-DO (–)35+5 wksB (+)NAYesNA16.21
4Anti-DO (–)38+4 wksO (+)NegativeYes7.4317.14
5Anti-DA (–)28+1 wksO (+)NAYes7.416.16
6Anti-DA (–)38+6 wksA (+)NANoNANANA
7Anti-DA (–)37+5 wksO (+)NANoNANANA
8Anti-C & eA (+)36+0 wksA (+)NAYes7.0416.74
9Anti-EO (+)17+5 wks******
10Anti-EA (+)37+1 wksB (+)NANoNANANA
11Anti-E & cA (+)41+1 wksA (+)NANo2.8314.91
12Anti-E & cO (+)7+1 wks******
13Anti-E & FybB (+)37+5 wks******
14Anti-E & DibB (+)36+2 wksO (+)PositiveNo6.2715.715
15Anti-JkaA (+)38+1 wksAB (+)NAYes5.214.13
16Anti-LeaA (+)36+4 wksA (+)NAYesNANANA
17Anti-LeaO (+)37+4 wksB (+)NANo7.2116.58
18Anti-LeaAB (+)33+4 wksAB (+)NAYes8.9413.96
19Anti-LeaA (+)36+4 wksA (+)NAYesNANANA
20Anti-LeaA (+)37+4 wksO (+)NANo2.5217.81
21Anti-MO (+)37+3 wksO (+)NANoNANANA
22Unidentified Ab.O (+)37+0 wksA (+)NAYes7.3615.13
23Unidentified Ab.O (+)37+6 wksO (+)NANo8.716.43
24Unidentified Ab.A (+)34+0 wksB (+)NAYes14.5214.74
25Unidentified Ab.B (+)34+5 wksA (+)NAYesNANANA
26Unidentified Ab.B (+)37+1 wksA (+)NANo7.8813.316
27Unidentified Ab.B (+)7+6 wks******
28Unidentified Ab.AB (+)37+0 wksAB (+)NANoNANANA
29Unidentified Ab.AB (+)22+4 wks******
30Positive, NTA (+)38+1 wksA (+)NAYes8.5515.65
31Positive, NTB (+)35+0 wksB (+)NAYes10.9517.46
32Positive, NTB (+)38+3 wksO (+)NANoNANANA
33Positive, NTO (+)37+5 wksA (+)NANoNANANA
34Positive, NTO (+)37+3 wksB (+)NANoNANANA
35Positive, NTB (+)5+3 wks******
36Positive, NTB (+)38+0 wksA (+)NANoNANANA
37Positive, NTO (+)38+0 wksB (+)NANoNANANA

*The cases of abortion or intra-uterine fetal death.

Abbreviations: Ab., antibody; DAT, direct antiglobulin test; NT, not tested of identification; NA, no data available.


HDFN is a preventable cause of fetal morbidity and mortality. Moreover, complications during intrauterine transfusion, the treatment for HDFN, can lead to death [2]. Early detection of HDFN and monitoring of disease progression are necessary to prevent death of the fetus or neonate. An awareness of the prevalence of maternal alloantibodies is important for managing the health of the fetus and neonate. The frequency of alloimmunization in pregnant women ranges from 0.4% to 4.5% worldwide [4-8,13]. To the best of the authors’ knowledge, this is the first report on the prevalence of maternal alloimmunization and the outcomes of fetuses and newborns in Korea. In this study, 2.78% of pregnant women had unexpected antibodies, and the live birth rate of pregnant women with unexpected antibodies was lower than that of the pregnant women without unexpected antibodies. In addition, the prevalence of unexpected antibodies was higher than that of previous studies. This can be attributed to use of three cells for antibody screening and to the positive to weak positive results.

According to the previous studies on alloimmunized pregnant women, the most common clinically significant alloantibodies are those of the Rh system, the frequencies of which are 6.46~58.9% [1,4,7]. Anti-E and anti-C are common alloantibodies among pregnant women [5,13]. In Korea, the prevalence of unexpected antibodies in pregnant women is 1.91% with anti-Lewis and anti-D being the most common [9]. Lee et al. [14], reported that the most frequent types of Rh phenotype discrepancy between pregnant Korean women and their neonates are E and c. Therefore, anti-E and anti-c could cause severe HDFN in Korea. Moreover, previous studies reported that anti-E alone or in combination with anti-c might cause HDFN and fetal hydrops in Korea [14-16]. In this study, the most common antibodies belonged to the Rh system (anti-D and anti-E combined with anti-c) with the second most common antibodies being anti-Lewis, which is similar to previous studies.

Anti-D has the strongest immunological effect on HDFN. In D-immunized pregnant women, the risk of severe HDFN was approximately 40% [17]. The chance of HDFN increases when anti-D is combined with any other RBC antibody [13]. The hemolytic effects of the anti-c antibody are similar to those of anti-D and are associated with severe HDFN [18]. Anti c induced HDFN results in hydropic stillbirth or perinatal death, or requires treatment, such as intrauterine transfusion or neonatal exchange transfusion [19]. Fetuses and neonates can develop severe HDFN when maternal anti-E is combined with anti c or anti-c alone. HDFN caused by anti-E is usually mild and occurs in neonates [3,5]. A Swedish study reported that alloimmunization with anti-D, anti-E, anti-C, and anti-c was associated with an increased risk of preterm birth and stillbirth, and anti-Lea was associated with an increased risk of stillbirth [20]. One study on Rh alloimmunization in pregnant women with Rh alloimmunization revealed a significantly higher rate of perinatal mortality (25%), admission at the neonatal intensive care unit, and neonatal transfusion compared to all pregnant women [21]. In the present study, the preterm birth rate did not differ significantly between the test group with unexpected antibodies (19.3%) and the control group (27.7%). The authors’ hospital is a tertiary hospital that can provide intensive care for neonates or any pregnant woman at risk of preterm birth transferred to the hospital. Therefore, the number of preterm births is more than in other hospitals. In the present study, 50% of newborns with maternal anti-D or anti- C developed hyperbilirubinemia and one was a stillbirth. Among six pregnant women with anti-E alone or with other alloantibodies, three (50%) experienced a spontaneous abortion or stillbirth; the surviving neonates did not develop hyperbilirubinemia. Among the two pregnant women who had both anti- E and anti-c, a patient with G4P1A3L1 experienced a spontaneous abortion. Recurrent abortion might have been the result of anti-E with anti-c. Among six newborns with maternal anti-Lea and anti-Jka, four developed hyperbilirubinemia but their mothers had not experienced a spontaneous abortion or stillbirth. Serial screening of unexpected antibodies in pregnant women will be needed if the antibody of the Rh group is revealed as a cause of severe fetal loss.

In most infants, unconjugated hyperbilirubinemia reflects a normal transitional phenomenon and is called physiological jaundice. The bilirubin level of most patients who require phototherapy remains within the physiological range [10,22]. In the present study, however, hyperbilirubinemia occurred earlier in four patients and at higher levels than general physiological jaundice. In these four cases, the effects of maternal RBC alloimmunization might have been overlooked. The possibility of HDFN as a cause cannot be ruled out because the cause of hyperbilirubinemia was not evaluated. Although the bilirubin level was within the level of physiological jaundice, in the other neonates who received phototherapy, it is possible that the hyperbilirubinemia was caused by mild HDFN. For example, in case seven, the physician did not consider HDFN at all, but the laboratory physician requested the workup for HDFN and the baby was confirmed to have mild HDFN. If a prospective evaluation of neonatal hyperbilirubinemia is performed, the prevalence of HDFN would be determined.

One limitation of this study was the lack of a sufficient workup of neonates with hyperbilirubinemia, including a direct antiglobulin test during treatment in most patients. In addition, the red cell phenotype of the fathers and infants was not determined. Furthermore, the titers of alloantibodies that were isolated were not evaluated. In Korea, the tests for Rh typing and phenotyping for other major antigen systems were not performed routinely. Therefore, the actual prevalence of HDFN could not be determined. A prospective multicenter study with a complete examination of the mothers and neonates is needed.


In conclusion, the prevalence of unexpected antibodies among pregnant Korean women was 2.78%. The most common significant antibodies belonged to the Rh blood group, namely, anti-D, and anti-E combined with anti-c. The death rate of the fetuses was higher in pregnant women with unexpected antibodies than in those without. Significant differences in the neonatal outcomes, including the death rate, prematurity, and hyperbilirubinemia, were observed depending on the specificity of the unexpected anti-body. Pregnant women who have an unexpected antibody need to be monitored and the neonates of such women should be evaluated for HDFN.


배경:임산부에서 태아와 신생아 용혈성 질환(HDFN)을 일으킬 수 있는 비예기항제의 빈도 및 종류는 연구마다 결과의 차이를 보인다. 태아와 신생아 용혈성 질환의 임상 양상은 비예기항제의 특이성과 정도에 따라 다르다. 이에 저자들은 국내 임산부의 동종면역 발생 빈도와 임상상 및 그에 따른 신생아의 예후를 분석하였다.

방법:양산부산대학교병원 산부인과에서 산전 검사로 비예기항체 선별 검사를 시행한 임산부를 대상으로 하였다. 비예기항체 선별 검사 결과 양성을 보인 환자군과 연령과 산과력을 맞춘 비예기항체 선별 검사 결과 음성의 임산부로 이루어진 대조군 간의 비예기항체에 따른 임신 예후와 신생아의 예후를 조사하였다.

결과:비예기항체의 빈도는 2.78% (42/1,508)였다. 동정된 비예기항체 중 항-D가 가장 많이 동정되었고, 그 다음으로 항-E와 항-Lea 순이었다. 주산기 사망률은 대조군보다 환자군에서 높은 결과를 보였다. 항-C 또는 항-D를 보인 8명의 임산부에서 1명은 사산, 생존 분만 중 4명의 신생아는 고빌리루빈혈증을 보였다. 단일 항체 또는 다른 동종 항체와 동시 동정된 항-E를 보인 6명의 임산부 중 3명에서 자연 유산 또는 사산을 확인했다. 모성 항-Lea와 항-Jka를 보인 6명의 신생아 중 4명에서 고빌리루빈혈증을 확인하였으나, 각각의 산모는 자연 유산 또는 사산 경력은 없었다.

결론:국내 임산부의 비예기항체의 빈도는 2.78%였다. 비예기항체의 특이성에 따라 주산기 사망률, 조산율 및 신생아 고빌리루빈혈증과 같은 신생아의 예후에 유의한 차이를 보였다.

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