Abstract
Introduction
Preterm neonates are at high risk for complications, and inflammation has been implicated in many of these pathologies. ABO incongruency occurs when the maternal and neonatal blood types are different and may cause complications when the mother creates antibodies against neonatal blood type antigens. In this study, we investigated whether preterm neonates with type A or B blood born to mothers with type O blood (ABO incongruent) had higher rates of neonatal complications than neonates with type O blood born to mothers with type O blood (ABO congruent). We hypothesized that preterm neonates who were ABO incongruent would have a higher incidence of neonatal morbidity.
Methods
This was a population-based single-center retrospective cohort study of 371 preterm neonates whose mothers had O blood type, were born between 21 0/7 and 32 6/7 weeks gestation, and admitted to University of Iowa Health Care Neonatal Intensive Care Unit between January 2018 and December 2022. Neonates were grouped by ABO incongruent versus congruent as well as by gestational age (GA) (22–26 and 27–32 weeks GA). Demographics data were collected. Outcomes included bronchopulmonary dysplasia, pulmonary hypertension, patent ductus arteriosus (PDA), necrotizing enterocolitis (NEC), packed red blood cell transfusions, intraventricular hemorrhage (IVH), periventricular leukomalacia, and survival to discharge.
Results
ABO incongruent neonates between 27 and 32 weeks GA were more likely to have NEC and had a trend toward an increased incidence of early pulmonary hypertension. There were trends toward more heart dysfunction and severity of IVH in neonates between 22 and 26 weeks GA.
Conclusion
ABO incongruency is associated with neonatal complications in the preterm population. This study is underpowered to adequately evaluate all neonatal morbidities. More studies are required to evaluate the effects of ABO incongruency on neonatal outcomes, particularly on NEC and pulmonary hypertension.
Keywords: ABO blood group, ABO incongruency, Prematurity, Neonatal, Necrotizing enterocolitis
Introduction
Preterm neonates are at high risk for perinatal morbidities, often leading to poor long-term outcomes. There is an inverse relationship between perinatal morbidities and gestational age (GA), with lower GA neonates more affected [1]. However, maternal and pregnancy factors also play a major role in neonatal outcomes, so some infants born at later GAs may still experience disproportionately worse outcomes. Currently, there is limited understanding regarding how maternal and pregnancy-related risk factors cause perinatal complications, but many involve the immune system, which is dysregulated in the preterm neonate.
Perinatal neonatal inflammation has been implicated in numerous neonatal morbidities. In particular, perinatal inflammation caused by chorioamnionitis [2, 3], preeclampsia [4], and neonatal sepsis [5] have been associated with worse long-term outcomes, such as poor neurodevelopment and cardiovascular disease [6], and short-term outcomes such as bronchopulmonary dysplasia (BPD) [7], stroke [8], and necrotizing enterocolitis (NEC) [9].
Another source of perinatal inflammation is neonatal blood type, or more specifically, ABO blood groups. ABO blood groups are determined by the ABO gene, which encodes glycosyltransferases that modify specific complex carbohydrates on the surface of various cell types, including erythrocytes, platelets, leukocytes, and endothelium [10]. Patients are grouped into four categories determined by the presence or absence of A and B antigenic modifications – AB, A, B, or O, which is the absence of both. It has long been known that blood groups are important predictors of adult cardiovascular, endocrine, immunologic, neurologic, and oncologic health [10]. More recently, studies have examined their role in neonatal health and found associations with increased severity of NEC [11, 12], BPD, patent ductus arteriosus (PDA) [13], and infection [14].
ABO incongruency occurs when the maternal blood group is not the same as the fetal blood group. Specifically, a mother that lacks an A or B blood type antigen that is present in their neonate, such as the case of maternal O-type blood with fetal A or B-type blood, can result in maternal antibodies against A or B antigens crossing the placenta, causing alloimmune hemolytic disease of the newborn, which is characterized by hemolysis and systemic inflammation [15]. While some studies have examined neonatal outcomes in term neonates with maternal-fetal ABO incongruency [16–18] or hemolytic and jaundice parameters in preterm neonates [19], further characterization of premature neonates affected by ABO incongruency has not been done. Our objective was to determine the incidence and severity of common preterm morbidities in preterm neonates with ABO incongruency. We hypothesized that ABO incongruent neonates would have a higher rate of complications.
Methods
Subjects
This was a population-based single-center retrospective cohort study of preterm neonates whose mothers had O blood type, were born between 21 0/7 and 32 6/7 weeks gestation, and admitted to University of Iowa Health Care Neonatal Intensive Care Unit between January 2018 and December 2022. Excluded were neonates without patient or maternal ABO data available. This population was chosen due to higher incidence of serious perinatal morbidities, which are often mild or absent after 33 weeks gestation. This study was approved by the Institutional Review Board at the University of Iowa (IRB #201410743). Demographics data collected included GA, birth weight, sex, race, maternal parity, timing of rupture of membranes, clinical chorioamnionitis, antenatal steroid administration, mode of delivery, 5-min APGAR, maternal blood type, neonatal blood type, and positive or negative direct antiglobulin tests. Antenatal steroids were considered “full course” if two doses were given separated by 24 h.
Definitions of Outcomes Parameters
Outcomes included BPD grade, heart dysfunction, early pulmonary hypertension, late pulmonary hypertension, hemodynamically significant PDA (hsPDA), need for definitive therapy for PDA closure, number of packed red blood cell (pRBC) transfusions, NEC diagnosis, intraventricular hemorrhage (IVH) diagnosis, periventricular leukomalacia diagnosis (PVL), mortality prior to discharge, and congenital anomalies.
hsPDA was determined by targeted neonatal echocardiography (TnECHO) by neonatal hemodynamics specialists at the University of Iowa based on the Iowa PDA Score [20]. Heart dysfunction was also determined by TnECHO [21]. Early pulmonary hypertension was defined by TnECHO or as hypoxemic respiratory failure requiring nitric oxide prior to 14 days of life (DOL). Late pulmonary hypertension was determined by TnECHO demonstrating pulmonary hypertension at >28 DOL. BPD grades were defined per Jensen criteria based on respiratory support requirement at 36 weeks post-menstrual age [22]. All pRBC transfusions were between 10-15 mL/kg. IVH was diagnosed by head ultrasound and graded according to the Papile classification [23]. PVL was diagnosed by head ultrasound or brain MRI. Severe congenital anomalies were defined as those considered life-threatening within the first year of life.
Analysis
Descriptive statistics, including mean and standard deviation, were performed on all variables. For categorical variables, the Chi-square testing was performed to determine significance. For continuous variables, normality testing was performed using the Shapiro-Wilk test. Normally distributed data were analyzed by one-way ANOVA test. Non-normally distributed data were analyzed by the Kruskal-Wallis testing. Significance was defined as p < 0.05.
Results
Baseline Characteristics of Study Population
A total of 462 neonates qualified for the study, with 91 infants excluded due to incomplete ABO data and 2 infants excluded for severe congenital anomalies, leaving a population of 369 neonates. Of these, 95 neonates had type A, 31 had type B, and 243 had type O blood (Fig. 1). Given that all mothers within the study population had type O blood, no neonates in this study had type AB blood [24, 25]. There were no significant differences in demographics between groups. The majority of neonates received a full course of antenatal steroids, were born by cesarean section, and were white. Average 5 min APGAR score was 7 for all groups (Table 1).
Fig. 1.
Inclusion and exclusion of patients in study.
Table 1.
Demographics of patients based on neonatal blood type
| | A (n = 95) | B (n = 31) | O (n = 243) | p value |
|---|---|---|---|---|
| GA | 27.92±2.43 | 27.46±5.69 | 28.32±2.86 | 0.17 |
| Male sex | 50 (52.6) | 19 (61.3) | 127 (52.3) | 0.64 |
| Birth weight | 1,110±448 | 1,013±361 | 1,157±445 | 0.19 |
| Race | | | | 0.07 |
| American Indian | 0 (0) | 0 (0) | 2 (1) | |
| Asian | 0 (0) | 0 (0) | 2 (1) | |
| Black | 12 (13) | 12 (39) | 54 (22) | |
| Hispanic or Latin(x) | 5 (5) | 1 (3) | 16 (7) | |
| White | 75 (79) | 18 (58) | 152 (63) | |
| Other | 3 (3) | 0 (0) | 17 (7) | |
| Maternal parity | 2.3±1.5 | 2.4±1.6 | 2.1±1.3 | 0.50 |
| PPROM | 19 (20) | 6 (19.4) | 62 (25.5) | 0.48 |
| Chorioamnionitis | 7 (7.4) | 3 (9.7) | 24 (9.9) | 0.77 |
| Antenatal steroids | | | | 0.54 |
| No steroids | 7 (7) | 4 (13) | 28 (12) | |
| Partial course | 24 (25) | 4 (13) | 51 (21) | |
| Full course | 64 (67) | 22 (73) | 164 (67) | |
| Delivery mode | | | | 0.25 |
| Vaginal-unassisted | 18 (19) | 8 (26) | 73 (30) | |
| Vaginal-assisted | 1 (1) | 0 (0) | 2 (1) | |
| Cesarean section | 76 (80) | 23 (74) | 168 (69) | |
| 5-minute APGAR | 7±1 | 7±1 | 7±2 | 0.58 |
Blood Type Outcomes
Neonates with type A, B, and O blood born to mothers with type O blood had no differences in outcomes in this study population (Table 2). However, there were nonsignificant increases in heart dysfunction, early pulmonary hypertension, hsPDA, NEC, and IVH severity in infants with types A and B blood as compared to type O. Therefore, neonates with incongruent blood types to mother (types A and B) were grouped together and compared to neonates with congruent, O-type blood (Table 3). In these data, there were again nonsignificant increases in rates of heart dysfunction, early pulmonary hypertension, and IVH severity. There was no difference in survival to discharge.
Table 2.
Tissue-specific neonatal outcomes in neonates compared between neonate blood types
| | A (n = 95) | B (n = 31) | O (n = 243) | p value |
|---|---|---|---|---|
| BPD, n (%) | 58 (61.1) | 18 (58.1) | 140 (57.6) | 0.85 |
| BPD grade, n (%) | | | | 0.83 |
| 1 | 21 (35.6) | 5 (27.8) | 46 (32.9) | |
| 2 | 33 (55.9) | 13 (72.2) | 84 (60) | |
| 3 | 4 (6.9) | 0 (0) | 10 (7.1) | |
| Heart dysfunction, n (%) | 12 (12.6) | 7 (22.6) | 25 (10.3) | 0.13 |
| Early pulmonary hypertension (days 0–14), n (%) | 10 (10.5) | 5 (16.1) | 22 (9.1) | 0.46 |
| Late pulmonary hypertension (after day 28), n (%) | 7 (7.4) | 1 (3.2) | 17 (7) | 0.89 |
| hsPDA, n (%) | 37 (38.9) | 15 (48.4) | 84 (34.6) | 0.28 |
| Need for definitive therapy (Cath closure or surgical ligation) of PDA, n (%) | 13 (13.7) | 7 (22.6) | 27 (11.1) | 0.17 |
| pRBC transfusions | 1 [0, 4] | 3 [1, 6] | 1 [0, 5] | 0.09 |
| NEC, n (%) | 6 (6.3) | 2 (6.5) | 8 (3.3) | 0.31 |
| IVH, n (%) | 16 (16.8) | 4 (12.9) | 44 (18.1) | 0.82 |
| Most severe IVH grade, n (%) | | | | 0.19 |
| 1 | 4 (25) | 0 (0) | 13 (29.5) | |
| 2 | 3 (18.8) | 2 (50) | 18 (40.9) | |
| 3 | 2 (12.5) | 0 (0) | 6 (13.6) | |
| 4 | 7 (43.8) | 2 (50) | 7 (15.9) | |
| PVL, n (%) | 7 (7.4) | 1 (3.2) | 11 (4.5) | 0.56 |
| Survival to discharge, n (%) | 91 (95.8) | 29 (93.5) | 237 (97.5) | 0.26 |
Data presented as n (%) or mean ± SD. For pRBC transfusion, data presented as median (95% confidence interval).
Significant p < 0.05.
Table 3.
Tissue-specific neonatal morbidities in infants with maternal-neonatal incongruent ABO status (neonates with A or B blood types born to mothers with type O) as compared to neonates with maternal-neonatal congruent ABO status (infants with O blood type born to mothers with type O)
| | Incongruent (n = 126) | Congruent (n = 243) | p value |
|---|---|---|---|
| BPD, n (%) | 76 (60.3) | 140 (57.6) | 0.66 |
| BPD grade, n (%) | | | 0.92 |
| 1 | 26 (34.2) | 46 (32.9) | |
| 2 | 46 (60.5) | 84 (60) | |
| 3 | 4 (5.3) | 10 (7.1) | |
| Heart dysfunction, n (%) | 19 (15.1) | 25 (10.3) | 0.18 |
| Early pulmonary hypertension (days 0–14), n (%) | 15 (11.9) | 22 (9.1) | 0.46 |
| Late pulmonary hypertension (after day 28), n (%) | 8 (6.3) | 17 (7) | >0.99 |
| hsPDA, n (%) | 52 (41.3) | 84 (34.6) | 0.21 |
| Need for definitive therapy (Cath closure or surgical ligation) of PDA, n (%) | 20 (15.9) | 27 (11.1) | 0.19 |
| pRBC transfusions | 2 [0, 5] | 1 [0, 5] | 0.24 |
| NEC, n (%) | 8 (6.3) | 8 (3.3) | 0.18 |
| IVH, n (%) | 20 (15.9) | 44 (18.1) | 0.66 |
| Most severe IVH grade, n (%) | | | 0.12 |
| 1 | 4 (20) | 13 (29.5) | |
| 2 | 5 (25) | 18 (40.9) | |
| 3 | 2 (10) | 6 (13.6) | |
| 4 | 9 (45) | 7 (15.9) | |
| PVL, n (%) | 8 (6.3) | 11 (4.5) | 0.46 |
| Survival to discharge, n (%) | 120 (95.2) | 237 (97.5) | 0.35 |
Data presented as n (%).
For pRBC transfusion, data presented as median (95% confidence interval).
Significant p < 0.05.
Neonates <27 weeks GA are at significantly higher risk for adverse neonatal outcomes compared with older preterm infants. Therefore, neonates were next split into two groups based on GA (Table 4). These data demonstrated significant increases in incidence of NEC in 27–32 week GA neonates with incongruent blood types, as well as a nearly significant increase in early pulmonary hypertension. In the 22–26 week GA neonates, there was a nearly two-fold increase in heart dysfunction in neonates with incongruent blood types compared to congruent blood type, but this difference was not significant. Data were also divided by specific neonatal blood type with similar findings (online suppl. Table 1; for all online suppl. material, see https://doi.org/10.1159/000551548) and by single week of GA at birth (online suppl. Table 2).
Table 4.
Tissue-specific neonatal outcomes in infants with maternal-infant ABO incongruency compared to neonates with maternal-infant ABO congruency separated into two GA groups
| | 22–26 weeks’ GA | p value | 27–32 weeks’ GA | p value | ||
|---|---|---|---|---|---|---|
| incongruent (n = 46) | congruent (n = 83) | incongruent (n = 80) | congruent (n = 160) | |||
| BPD, n (%) | 40 (87) | 73 (88) | 0.87 | 36 (45) | 67 (41.9) | 0.64 |
| BPD grade, n (%) | | | 0.46 | | | 0.50 |
| 1 | 6 (15) | 14 (19.2) | | 20 (55.6) | 32 (47.8) | |
| 2 | 32 (80) | 51 (69.8) | | 14 (38.9) | 33 (49.3) | |
| 3 | 2 (5) | 8 (11) | | 2 (5.6) | 2 (3) | |
| Heart dysfunction, n (%) | 13 (28.3) | 13 (15.7) | 0.09 | 6 (7) | 12 (7.5) | >0.99 |
| Early pulmonary hypertension (days 0-14), n (%) | 5 (10.9) | 13 (15.7) | 0.45 | 10 (12.5) | 9 (5.6) | 0.06 |
| Late pulmonary hypertension (after day 28), n (%) | 7 (15.2) | 14 (16.9) | 0.81 | 1 (1.3) | 3 (1.9) | 0.72 |
| hsPDA, n (%) | 32 (69.6) | 57 (68.7) | 0.92 | 20 (25) | 27 (16.9) | 0.13 |
| Need for definitive therapy (Cath closure or surgical ligation) of PDA, n (%) | 15 (46.9) | 21 (36.8) | 0.35 | 5 (25) | 6 (22.2) | 0.82 |
| pRBC transfusions | 5 [3, 8] | 6 [3, 9] | 0.51 | 0 [0, 2] | 0 [0, 1] | 0.12 |
| NEC, n (%) | 3 (6.5) | 6 (7.2) | 0.88 | 5 (6.3) | 2 (1.3) | 0.04 |
| IVH, n (%) | 13 (28.3) | 21 (25.3) | 0.84 | 7 (8.8) | 23 (14.4) | 0.30 |
| Most severe IVH grade, n (%) | | | 0.23 | | | 0.82 |
| 1 | 1 (7.7) | 3 (14.3) | | 3 (42.9) | 10 (43.5) | |
| 2 | 4 (30.8) | 11 (52.4) | | 1 (14.3) | 7 (30.4) | |
| 3 | 1 (7.7) | 3 (14.3) | | 1 (14.3) | 3 (13) | |
| 4 | 7 (53.8) | 4 (19) | | 2 (28.6) | 3 (13) | |
| PVL, n (%) | 5 (10.9) | 4 (4.8) | 0.28 | 3 (3.8) | 7 (4.4) | >0.99 |
| Survival to discharge, n (%) | 42 (91.3) | 77 (92.8) | 0.77 | 78 (97.5) | 160 (100) | 0.11 |
Data presented as n (%).
For pRBC transfusion, data presented as median (95% confidence interval).
Significant p < 0.05.
Discussion
Here, we demonstrate that incongruency between maternal and neonatal ABO blood groups is a risk factor for perinatal complications, specifically NEC, among neonates born between 27 and 32 weeks gestation. Our findings provide additional evidence that neonatal blood type and ABO incongruency may serve as useful predictors for neonatal complications. With current predictive tools for neonatal disease having limited clinical utility, further studies are needed to increase their predictive value. Such investigations should include blood type and ABO incongruency as potentially important clinical risk factors. Improved understanding of risk factors such as ABO incongruency also leads to better knowledge of the pathogenesis of disease and thereby improved preventative strategies.
Our data are in line with recently published literature demonstrating the importance of blood type in adult and neonatal outcomes and may provide an explanation for certain complications. Specifically, AB blood type has been associated with NEC requiring surgical intervention [11] and mortality from NEC [12]. Given the presence of both A and B-modifications, it is also the most likely to have maternal-fetal incongruency, which may explain the higher risk for complications. Our study design was unable to assess neonates with type AB blood due to maternal type O blood being an inclusion criterion.
We do not fully understand the mechanisms by which ABO incongruency contributes to neonatal complications. We know that mothers with O blood type have baseline levels of anti-A and anti-B antibodies that are higher in ABO incongruent pregnancies [26]. IgG antibodies, including anti-A and anti-B IgG, cross the placenta and can cause significant hemolytic disease [15, 27]. In addition, given that A and B antigens are present on numerous cell types in multiple organ systems, other processes are likely to contribute to neonatal disease [10]. Postnatal administration of mother’s breast milk, which contains anti-A and anti-B antibodies [28], may also contribute to neonatal complications, especially NEC. Finally, there are also known differences in A and B antigenicity that may account for variability in presentation of ABO incongruency [27].
22–26 week GA neonates have unique challenges compared to our older premature population of 27–32 week neonates. Their skin, lungs, brain, and immune system are significantly more immature and dysregulated, posing a substantial challenge for clinical management. As demonstrated here, there is nearly double the rate of BPD as well as a higher incidence of all other measured outcomes. Due to their increased risk for neonatal morbidities, we expected that younger GA infants would have higher rates of complications associated with ABO incongruency. However, besides a robust trend towards more heart dysfunction, 22–26 week GA neonates had less morbidity associated with ABO incongruency compared to those born at 27–32 weeks GA.
There are several potential reasons for a discrepancy in ABO incongruency effects at differing GAs. First, 22–26 week GA neonates have other, more common causes of NEC and early pulmonary hypertension that may mask the effect of ABO incongruency. 27–32 week GA neonates, being generally healthier than younger GA neonates, may require more insults, like ABO incongruency, to cause clinical disease. In support of this hypothesis, ABO incongruent 27–32 week neonates have nearly identical NEC and early pulmonary hypertension rates as ABO congruent 22–26 week neonates. Other reasons for the larger effect of ABO incongruency at later gestations could be that fetal A and B antigens are more developed later in gestation, there is more exposure time to maternal antibodies, and that larger amounts of maternal IgG antibodies cross the placenta later in gestation. Therefore, 22–26 week GA neonates may not have sufficient maternal A or B antibodies to contribute to neonatal perinatal complications. A third possibility is that older infants often have more rapid advancement of feeds, which, if mother’s breast milk contains anti-A and/or anti-B antibodies, may be a contributor to pathologies such as NEC.
Our study is limited in that it is a single-center study at an institution with low rates of NEC and severe IVH. Due to low incidence and our small cohort size, we have limited power to distinguish between rates of these neonatal complications. Conversely, the presence of a robust program of specialized neonatologists performing TnECHOs makes our institution uniquely positioned to evaluate incidence of cardiovascular complications, represented here by heart dysfunction, pulmonary hypertension, and PDA significance. A second limitation is that our institution utilizes early hydrocortisone treatment in extremely low birth weight infants demonstrating symptoms of adrenal insufficiency. We do not know whether groups had similar rates of hydrocortisone or other steroid administration in the neonatal period, which may impact inflammation and/or our observed outcomes. In addition, maternal variables, though not different between groups, were not included in statistical analysis of neonatal outcomes. While a multivariate analysis may control for maternal and neonatal confounders, our sample size was too small to draw meaningful conclusions. Third, we were unable to assess these neonates using a direct antiglobulin test (DAT). The DAT detects antibodies bound to the surface of red blood cells and is a risk factor for hemolysis in cases of ABO incongruency. Only one infant in the cohort had a positive DAT during hospitalization, which prevented any meaningful comparison between groups. Finally, our definitions of pulmonary hypertension are arbitrarily defined to attempt to distinguish between differing etiologies. Late pulmonary hypertension, presumed secondary to chronic lung disease of prematurity, was defined as occurring after 28 DOL, while early pulmonary hypertension prior to 14 days is presumed more likely to be secondary to transitional physiology or acute inflammation. However, these differing etiologies of pulmonary hypertension cannot be perfectly distinguished. Indeed, they are often challenging to tease apart even in high-level settings with robust clinical resources.
In conclusion, we demonstrate that 27–32 week GA preterm neonates with type A or B blood born to O-type mothers are at higher risk for NEC, with trends towards higher incidence of other neonatal complications. Our study is limited by small cohort size and low incidence of common preterm infant morbidities. Therefore, larger studies are needed to determine the full effect of ABO incongruency on preterm infant complications. Potential mechanisms are unknown, but may be mediated by cross-placental or breast milk transfer of anti-A and/or anti-B antibodies. Providers should consider ABO incompatibility as a risk factor for neonatal complications of prematurity.
Statement of Ethics
This study protocol was reviewed and approved by the Institutional Review Board at the University of Iowa, Approval No. 201410743. Written consent was not obtained from the included human participants as an exemption was granted by the Institutional Review Board given that all data collected was retrospective.
Conflict of Interest Statement
The authors have no conflicts of interest to declare.
Funding Sources
This study was not supported by any sponsor or funder.
Author Contributions
J.A.S. interpreted the data, wrote the initial manuscript, and integrated revisions. N.A.A. collected data and assisted in manuscript revisions. J.B.J. helped generate the initial study concept and assisted in manuscript revisions. J.R.B. provided study feedback and assisted in manuscript revisions. T.J.B. generated initial study concept, collected data, and assisted in manuscript revisions.
Funding Statement
This study was not supported by any sponsor or funder.
Data Availability Statement
The data presented can be made available by written request to the corresponding author.
Supplementary Material.
Supplementary Material.
References
- 1. Manuck TA, Rice MM, Bailit JL, Grobman WA, Reddy UM, Wapner RJ, et al. Preterm neonatal morbidity and mortality by gestational age: a contemporary cohort. Am J Obstet Gynecol. 2016;215(1):103.e1–4. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 2. Wu YW, Colford JM Jr. Chorioamnionitis as a risk factor for cerebral palsy: a meta-analysis. Jama. 2000;284(11):1417–24. [DOI] [PubMed] [Google Scholar]
- 3. Soraisham AS, Trevenen C, Wood S, Singhal N, Sauve R. Histological chorioamnionitis and neurodevelopmental outcome in preterm infants. J Perinatol. 2013;33(1):70–5. [DOI] [PubMed] [Google Scholar]
- 4. Wu CS, Nohr EA, Bech BH, Vestergaard M, Catov JM, Olsen J. Health of children born to mothers who had preeclampsia: a population-based cohort study. Am J Obstet Gynecol. 2009;201(3):269.e1–0. [DOI] [PubMed] [Google Scholar]
- 5. Fleischmann C, Reichert F, Cassini A, Horner R, Harder T, Markwart R, et al. Global incidence and mortality of neonatal sepsis: a systematic review and meta-analysis. Arch Dis Child. 2021;106(8):745–52. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 6. Bavineni M, Wassenaar TM, Agnihotri K, Ussery DW, Lüscher TF, Mehta JL. Mechanisms linking preterm birth to onset of cardiovascular disease later in adulthood. Eur Heart J. 2019;40(14):1107–12. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7. Hagman C, Björklund LJ, Bjermer L, Hansen-Pupp I, Tufvesson E. Perinatal inflammation relates to early respiratory morbidity and lung function at 12 years of age in children born very preterm. Acta Paediatr. 2021;110(7):2084–92. [DOI] [PubMed] [Google Scholar]
- 8. Giraud A, Guiraut C, Chevin M, Chabrier S, Sébire G. Role of perinatal inflammation in neonatal arterial ischemic stroke. Front Neurol. 2017;8:612. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9. Lambert DK, Christensen RD, Henry E, Besner GE, Baer VL, Wiedmeier SE, et al. Necrotizing enterocolitis in term neonates: data from a multihospital health-care system. J Perinatol. 2007;27(7):437–43. [DOI] [PubMed] [Google Scholar]
- 10. Ewald DR, Sumner SC. Blood type biochemistry and human disease. Wiley Interdiscip Rev Syst Biol Med. 2016;8(6):517–35. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 11. Martynov I, Göpel W, Rausch TK, Härtel C, Franke A, Franz AR, et al. Blood group AB increases risk for surgical necrotizing enterocolitis and focal intestinal perforation in preterm infants with very low birth weight. Sci Rep. 2021;11(1):13777. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 12. Thomson T, Habeeb O, Dechristopher PJ, Glynn L, Yong S, Muraskas J. Decreased survival in necrotizing enterocolitis is significantly associated with neonatal and maternal blood group: the AB isoagglutinin hypothesis. J Perinatol. 2012;32(8):626–30. [DOI] [PubMed] [Google Scholar]
- 13. Cakir U, Tayman C, Buyuktiryaki M. Unknown aspects of the relationship between ABO blood group system and preterm morbidities. Arch Argent Pediatr. 2020;118(2):e135–42. [DOI] [PubMed] [Google Scholar]
- 14. McMahon KE, Habeeb O, Bautista GM, Levin S, DeChristopher PJ, Glynn LA, et al. The association between AB blood group and neonatal disease. J Neonatal Perinatal Med. 2019;12(1):81–6. [DOI] [PubMed] [Google Scholar]
- 15. Longacre M, Bendapudi PK. Fatal hemolytic disease of the newborn due to anti-B Isohemagglutinin: an unfamiliar presentation of a familiar disease. Transfusion. 2024;64(1):185–8. [DOI] [PubMed] [Google Scholar]
- 16. Butler EA, Grandi SM, Matai L, Wang X, Cohen E, Ray JG. Differences in maternal-newborn ABO blood groups and risk of serious infant infection. Qjm. 2024;117(7):512–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17. Lin H, Luo P, Liu C, Lin X, Que C, Zhong W. Risk of low levels of blood group antibodies mediating hemolysis in ABO-incompatible neonates with negative three hemolysis tests. Front Pediatr. 2024;12:1392308. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18. Butler EA, Ray JG, Cohen E. Maternal-Newborn ABO blood groups and risk of bacterial infection in newborns. JAMA Netw Open. 2024;7(10):e2442227. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 19. Yogev-Lifshitz M, Leibovitch L, Schushan-Eisen I, Taran C, Strauss T, Maayan-Metzger A. Indication of mild hemolytic reaction among preterm infants with ABO incompatibility. Pediatr Blood Cancer. 2016;63(6):1050–3. [DOI] [PubMed] [Google Scholar]
- 20. Rios DR, Martins FDF, El-Khuffash A, Weisz DE, Giesinger RE, McNamara PJ. Early role of the atrial-level communication in premature infants with patent ductus arteriosus. J Am Soc Echocardiogr. 2021;34(4):423–32.e1. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21. McNamara PJ, Jain A, El-Khuffash A, Giesinger R, Weisz D, Freud L, et al. Guidelines and recommendations for targeted neonatal echocardiography and cardiac point-of-care ultrasound in the neonatal intensive care unit: an update from the American Society of echocardiography. J Am Soc Echocardiogr. 2024;37(2):171–215. [DOI] [PubMed] [Google Scholar]
- 22. Jensen EA, Dysart K, Gantz MG, McDonald S, Bamat NA, Keszler M, et al. The diagnosis of bronchopulmonary dysplasia in very preterm infants. An evidence-based approach. Am J Respir Crit Care Med. 2019;200(6):751–9. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23. Papile LA, Burstein J, Burstein R, Koffler H. Incidence and evolution of subependymal and intraventricular hemorrhage: a study of infants with birth weights less than 1,500 gm. J Pediatr. 1978;92(4):529–34. [DOI] [PubMed] [Google Scholar]
- 24. Cho D, Kim SH, Jeon MJ, Choi KL, Kee SJ, Shin MG, et al. The serological and genetic basis of the cis-AB blood group in Korea. Vox Sang. 2004;87(1):41–3. [DOI] [PubMed] [Google Scholar]
- 25. Olsson ML, Irshaid NM, Hosseini-Maaf B, Hellberg A, Moulds MK, Sareneva H, et al. Genomic analysis of clinical samples with serologic ABO blood grouping discrepancies: identification of 15 novel A and B subgroup alleles. Blood. 2001;98(5):1585–93. [DOI] [PubMed] [Google Scholar]
- 26. Oseni BS, Akomolafe OF. The frequency of ABO blood group maternal-fetal incompatibility, maternal iso-agglutinins, and immune agglutinins quantitation in Osogbo, Osun State, South-West of Nigeria. Asian J Transfus Sci. 2011;5(1):46–8. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 27. Grundbacher FJ. The etiology of ABO hemolytic disease of the newborn. Transfusion. 1980;20(5):563–8. [DOI] [PubMed] [Google Scholar]
- 28. Kumar S, Rasalam JE, David VT, Yenuberi H, Amalraj P, Jeyaseelan L, et al. Breast milk contains red cell isohaemagglutinins: an observational study of 176 mothers. Vox Sang. 2022;117(6):847–52. [DOI] [PubMed] [Google Scholar]
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Data Availability Statement
The data presented can be made available by written request to the corresponding author.