Abstract
Background
In vitro fertilisation (IVF) offers a solution for infertility but poses increased obstetrical and perinatal risks, including higher rates of preterm birth, low birth weight and congenital anomalies. Particularly, IVF-related multiple pregnancies face significantly higher risks for preterm birth and prolonged hospital stays. This study compares neonatal outcomes between IVF and natural conception, as well as between singleton and IVF-related multiple pregnancies over the past decade.
Method
This retrospective study reviewed the medical records of babies born at Cipto Mangunkusumo Kencana Hospital from 2013 to 2023. Neonatal morbidities (hypothermia, hypoglycaemia, respiratory distress, circulation problems, sepsis, congenital anomalies, all stages of intraventricular haemorrhage and retinopathy of prematurity of all babies, neonatal intensive care unit (NICU) admission and length of stay) were dependent variables, with the mode of conception as the independent variable.
Result
Of 609 subjects, 169 were IVF conceptions and 435 natural conceptions. The IVF group had higher rates of prematurity (27.8% vs 10.8%, p<0.001), multiple conceptions (37.9% vs 7.4%, p<0.001) and older maternal age (35 vs 30 years, p<0.001). Prematurity in the IVF group had an increased rate of respiratory distress (18.9% vs 12.6%, p=0.05), higher NICU admission rates (13.6% vs 3.2%, p<0.001) and longer hospital stays.
Conclusion
IVF pregnancies had higher risks of prematurity and respiratory distress, necessitating personalised antenatal care and close monitoring to optimise neonatal outcomes.
Keywords: Neonatology
WHAT IS ALREADY KNOWN ON THIS TOPIC
In vitro fertilisation (IVF) is widely recognised for helping infertile couples, yet it is associated with increased risks of obstetrical and perinatal complications, including prematurity, low birth weight and other morbidities.
WHAT THIS STUDY ADDS
The study was conducted in Indonesia, a developing country where IVF practices are done; however, it is often less available due to limited resources. Furthermore, patients who underwent IVF in Indonesia do not always deliver their babies in the same facilities where they received their IVF programme, highlighting potential gaps in continuity of care.
HOW THIS STUDY MIGHT AFFECT RESEARCH, PRACTICE OR POLICY
This research could inform policy by advocating for increased awareness and the implementation of more rigorous prenatal care protocols in IVF pregnancies, with the aim of enhancing neonatal outcomes in developing countries.
Introduction
In vitro fertilisation (IVF) is a method that involves ovarian stimulation followed by oocyte retrieval, fertilisation and embryo culture in a controlled environmental condition before transferring to the uterus.1 IVF is an assisted reproductive technology (ART) that has been widely used and has become one of the promising solutions for infertile couples.
Most babies born through ART are healthy; however, this method is often associated with an increased risk of obstetrical and perinatal complications.2 Pregnancy achieved through the IVF method increases the risk by 1.2–2 times for preterm birth and low birth weight (LBW), 1.2 times for small for gestational age and 1.5 times for congenital anomalies.3 4 Additionally, it has been reported that the rate of preterm birth is higher in multiple pregnancies conceived through IVF. However, other studies have found no differences in neonatal outcomes between pregnancies achieved through IVF and natural conception.3 In this study, we focus on the short-term outcomes of preterm birth, but at our centre, we are currently conducting a long-term study (called the Cohort of Indonesian Preterm Infants for Long-term Outcomes study) that examines the long-term outcomes of premature infants.5
A study conducted by Li et al found that multiple pregnancies are 8.78 times more likely to experience moderate-to-late preterm birth and 7.58 times more likely to have extremely preterm births compared with singleton pregnancies in IVF pregnancies.6 In a retrospective cohort study conducted by Wang et al, it was reported that babies born from IVF pregnancies had longer hospital stays (4 days vs 3 days), were at greater risk of being admitted to the neonatal intensive care unit (NICU; 50% vs 28.5%) and required respiratory assistance (25.8% vs 11.7%) compared with babies born from natural conception.7 A study by Muharam et al compared the neonatal outcomes of fresh and frozen embryos in IVF pregnancies in Indonesia, but did not specifically address outcomes during the neonatal period or whether the patients required NICU care.8
Therefore, this study aims to observe the differences in neonatal outcomes between babies born from pregnancies using the IVF method (fresh or frozen embryos) and those born from natural conception over the past 10 years. Additionally, we also compare neonatal outcomes between singleton and multiple pregnancies conceived through IVF.
Methods
Patients and public involvement
No patients were directly involved in this study, as it was based on a retrospective analysis of medical records.
Study design and participants
This is a retrospective study observing differences in neonatal outcomes between babies born from IVF pregnancies and those born from natural conception. The research was conducted at Cipto Mangunkusumo Kencana Hospital, the private sector of Cipto Mangunkusumo National Hospital, by collecting data from the medical records of all babies born at this hospital between 2013 and 2023. Cipto Mangunkusumo Kencana Hospital serves as a dedicated healthcare provider for private sector patients, operating independently from the regular Cipto Mangunkusumo Hospital. As part of Cipto Mangunkusumo Hospital, which offers both private and public healthcare services, IVF treatments—associated with relatively high costs—are exclusively available in the private sector. Consequently, the birth rate of IVF babies at our hospital remains lower, while the public sector of Cipto Mangunkusumo Hospital recorded an average of 1760 births per year between 2013 and 2023. The inclusion criteria for this study were all babies born at Cipto Mangunkusumo Kencana Hospital from 2013 to 2023. The exclusion criteria for this study were incomplete medical record data.
Variables
Dependent variables in this study are morbidities (hypothermia, hypoglycaemia, respiratory distress, circulation problems, sepsis, congenital anomalies, all stages of intraventricular haemorrhage (IVH) and retinopathy of prematurity (ROP)) of all babies, NICU admission and length of stay. Independent variables are naturally conceived or conceived through IVF.
The operational definition follows our hospital’s standard operational procedure. Hypothermia is defined as a body temperature of less than 36.5°C. Hypoglycaemia is defined as a blood glucose level of less than 50 mg/dL. Respiratory distress is defined as a condition of tachypnoea, grunting, retractions and nasal flaring. Sepsis is defined by the presence of a positive culture from at least one sample site, accompanied by clinical symptoms.
Statistical analysis
Statistical analysis was done using IBM SPSS V.29.0 for Macintosh. Normally distributed data will be presented as mean, otherwise as median. The χ² and Fisher exact tests were employed to examine two categorical variables. A p value of ≤0.05 indicated statistical significance for the data.
Results
Study population
From 2013 to 2023, a total of 968 babies were born at Cipto Mangunkusumo Kencana Hospital; however, 364 subjects were excluded due to missing data in medical records. A total of 604 babies born in our hospital were included in this study, of which 169 were conceived through IVF, while the remaining 435 were naturally conceived. IVF transfer techniques were performed in two ways: fresh embryos (n=87) and frozen embryos (n=82) (refer to figure 1).
Figure 1. Subject recruitment process. IVF, in vitro fertilisation; NICU, neonatal intensive care unit.
Demographic data
The demographic data of 604 subjects are shown in table 1. The median gestational age is 37 weeks in the IVF group and 38 weeks in the non-IVF group. The median age of mothers during conception is 35 years in the IVF group and 30 years old in the naturally conceived group. The incidence of preterm birth in our subjects is higher in the IVF group compared with the non-IVF group. All babies conceived through IVF in our hospital were born through caesarean section (C-section).
Table 1. Baseline characteristics.
| Variables | IVF | Non-IVF | P value |
| (n=169) | (n=435) | ||
| Maternal characteristics | |||
| Age during conception, years* | 35 (22–44) | 30 (20–44) | <0.001 |
| Number of fetuses, n (%)† | |||
| Singleton | 105 (62.1) | 403 (92.6) | <0.001 |
| Multiple | 64 (37.9) | 32 (7.4) | |
| Mode of delivery, n (%)† | |||
| C-section | 169 (100) | 350 (80.6) | <0.001 |
| Vaginal delivery gestational age, n (%)† | 0 (0) | 85 (14.1) | |
| <37 weeks | 47 (27.8) | 47 (10.8) | <0.001 |
| ≥37 weeks | 122 (72.2) | 387 (89.2) | |
| Infant characteristics | |||
| Birth weight, g‡ | 2767.2±486.51 | 3031.7±474.51 | <0.001 |
| Sex, n (%)† | |||
| Male | 89 (52.7) | 221 (50.8) | 0.68 |
| Female | 80 (47.3) | 214 (49.2) | |
Data represented as median (minimum-–maximum). P- value derived by Wilcoxon- rank -sum test.
Data represented as frequency (proportion). P- values derived by Chi-squareχ² test.
Data represented as mean (standard deviationSD). P- values derived by independent t-test.
C-sectioncaesarean sectionIVFin vitro fertilisation
We acknowledge that baseline characteristics, such as maternal age, number of fetuses, mode of delivery, gestational age and birth weight may act as confounding factors, potentially influencing study outcomes. To address this, we conducted a multivariable regression analysis (refer to table 2), incorporating baseline characteristics with a p value<0.25 as covariates to adjust for their potential confounding effects. This approach enabled us to isolate the impact of the exposure variable (IVF or natural conception) on the outcomes while accounting for differences in these confounders. However, we were unable to calculate adjusted relative risks (RR) for certain morbidities, including hypoglycaemia, ROP and IVH, as there were no cases in one or both exposure groups. This limitation has been discussed in the study.
Table 2. Multivariate analysis of the relationship between morbidities and baseline characteristics after considering confounding factors.
| Variables | P value | Adjusted RR | 95% CI |
| Respiratory distress | 0.287 | 0.719 | 0.39 to 1.32 |
| Circulatory problems | 0.160 | 0.185 | 0.70 to 1.04 |
| Sepsis | 0.264 | 0.409 | 0.09 to 1.04 |
| Congenital disorders | 0.398 | 2.033 | 0.39 to 10.54 |
RRrelative risks
Univariate analysis of morbidities among IVF and non-IVF babies will be shown in table 3, and the comparison of outcomes between singleton and IVF-related multiple pregnancies is shown in table 4. NICU admission is higher in IVF babies (13.6%), with 17.1% for frozen embryos and 10.3% for fresh embryos, compared with 3.2% for non-IVF babies. Respiratory distress occurs more frequently in the IVF group compared with the non-IVF group (18.9% vs 12.6%; RR 1.62; 95% CI 1.01 to 2.60), and it is more common in IVF-related multiple pregnancies compared with singleton IVF conceptions (31.3% vs 11.4%, RR 0.28; 95% CI 0.13 to 0.63). These differences are statistically significant, with a p value<0.001. Additionally, the variability in the length of stay is wider for IVF babies compared with non-IVF babies (p<0.001).
Table 3. Morbidities between IVF and non-IVF babies.
| Variables | IVF(n=169) | Frozen embryo (n=82) | Fresh embryo (n=87) | Non-IVF(n=435) | P value 1 | P value 2 |
| Hypothermia, n (%)* | 0 (0) | 0 (0) | 0 (0) | 2 (0.5) | 1.00 | 0.52 |
| Hypoglycaemia, n (%)* | 27 (16) | 16 (19.5) | 11 (12.6) | 46 (10.6) | 0.07 | 0.07 |
| Birth weight class, n (%)* | ||||||
| SGA | 24 (14.2) | 6 (7.3) | 18 (20.7) | 63 (14.5) | 0.25 | 0.20 |
| AGA | 144 (85.2) | 76 (92.7) | 68 (78.2) | 359 (82.7) | ||
| LGA | 1 (0.6) | 0 (0) | 1 (1.1) | 12 (2.8) | ||
| 1 min Apgar, n (%)* | ||||||
| 0–3 | 0 (0) | 0 (0) | 0 (0) | 4 (0.9) | 0.45 | 0.51 |
| 4–6 | 6 (3.6) | 2 (2.4) | 4 (4.6) | 17 (3.9) | ||
| 7–10 | 163 (96.4) | 80 (97.6) | 83 (95.4) | 414 (95.2) | ||
| 5 min Apgar, n (%)* | ||||||
| 0–3 | 0 (0) | 0 (0) | 0 (0) | 0 (0) | 0.58 | 0.27 |
| 4–6 | 0 (0) | 0 (0) | 0 (0) | 4 (0.9) | ||
| 7–10 | 169 (100) | 82 (100) | 87 (100) | 431 (99.1) | ||
| Respiratory distress, n (%)* | 32 (18.9) | 15 (18.3) | 17 (19.5) | 55 (12.6) | 0.05 | 0.14 |
| Circulatory problems, n (%)* | 1 (0.6) | 0 (0) | 1 (1.1) | 5 (1.1) | 1.00 | 0.42 |
| Sepsis, n (%)* | 4 (2.4) | 2 (2.4) | 2 (2.3) | 5 (1.1) | 0.27 | 0.57 |
| IVH, n (%)* | 1 (0.6) | 1 (1.2) | 0 (0) | 0 (0) | 0.28 | 0.14 |
| ROP, n (%)* | 0 (0) | 0 (0) | 0 (0) | 0 (0) | N/A | N/A |
| Congenital disorders, n (%)* | 5 (3.0) | 2 (2.4) | 3 (3.4) | 4 (0.9) | 0.13 | 0.20 |
| Hearing problems, n (%)* | 3 (1.8) | 2 (2.4) | 1 (1.1) | 2 (0.5) | 0.14 | 0.27 |
| NICU admission, n (%)* | 23 (13.6) | 14 (17.1) | 9 (10.3) | 14 (3.2) | <0.001 | <0.001 |
| LOS, days† | 3 (1, 2–38) | 3 (2, 2–14) | 3 (1, 2–38) | 3 (2, 2–28) | <0.001 | <0.001 |
Notes: p-p value 1: significance between IVF and non-IVF group; p-p value 2: significance between frozen embryo, fresh embryo, and non-IVF group.
Data represented as frequency (proportion). P- values derived by Chi-squareχ² test.
Data represented as median (IQR, minimum-–maximum). P- value derived by Wilcoxon- rank -sum test.
AGA, appropriate for gestational age; IVFin vitro fertilisationIVH, intraventricular haemorrhage; LGA, large for gestational age; LOS, length of stay (days); N/A, not applicableNICUneonatal intensive care unitROP, retinopathy of prematurity; SGA, small for gestational age
Table 4. Morbidities between singleton and IVF-related multiple pregnancies.
| Variables | Singleton (n=105) | Multiple (n=64) | P value |
| Hypothermia, n (%)* | 0 (0) | 0 (0) | N/A |
| Hypoglycaemia, n (%)* | 14 (13.3) | 13 (20.3) | 0.23 |
| Birth weight class, n (%)* | |||
| SGA | 8 (7.6) | 16 (25.0) | 0.006 |
| AGA | 96 (91.4) | 48 (75.0) | |
| LGA | 1 (1.0) | 0 (0) | |
| 1 min Apgar, n (%)* | |||
| 0–3 | 0 (0) | 0 (0) | 0.21 |
| 4–6 | 2 (1.9) | 4 (6.3) | |
| 7–10 5 min Apgar, n (%)* | 103 (98.1) | 60 (93.8) | |
| 0–3 | 0 (0) | 0 (0) | N/A |
| 4–6 | 0 (0) | 0 (0) | |
| 7–10 | 105 (100) | 64 (100) | |
| Respiratory distress, n (%)* | 12 (11.4) | 20 (31.3) | <0.001 |
| Circulatory problems, n (%)* | 1 (1.0) | 0 (0) | 1.00 |
| Sepsis, n (%)* | 1 (1.0) | 3 (4.7) | 0.15 |
| IVH, n (%)* | 0 (0) | 1 (1.6) | 0.38 |
| ROP, n (%)* | 0 (0) | 0 (0) | N/A |
| Congenital disorders, n (%)* | 1 (1.0) | 4 (6.3) | 0.07 |
| Hearing problems, n (%)* | 1 (1.0) | 2 (3.1) | 0.56 |
| NICU admission, n (%)* | 11 (10.5) | 12 (18.8) | 0.13 |
| LOS, days† | 3 (1, 2–16) | 4 (2, 2–38) | <0.001 |
Data represented as frequency (proportion). P values derived by χ² test.
Data represented as median (IQR, minimum–maximum). P value derived by Wilcoxon rank-sum test.
AGAappropriate for gestational ageIVFin vitro fertilisationIVHintraventricular haemorrhageLGAlarge for gestational ageLOSlength of stay (days)N/Anot applicableNICUneonatal intensive care unitROPretinopathy of prematuritySGAsmall for gestational age
Discussion
In our study, preterm birth is significantly more frequent in the groups of babies conceived via IVF compared with those conceived naturally. This result aligns with previous studies suggesting that babies born through IVF are more susceptible to preterm birth.9 Additionally, multiple pregnancies are more common in the IVF group. Both factors contribute to LBW in the IVF group.
We observed that babies conceived through IVF were all born through C-sections in our hospital. In reality, IVF pregnancy is similar to natural pregnancy, hence the necessity for C-section results from the pregnancy complications requiring C-section, rather than being inherently linked to IVF itself.10 11 Often the reason for a C-section is based on the maternal or obstetricians’ decision. By having elective procedures, both doctors and mothers can have more control over the procedure.12 These factors may contribute to high rates of C-sections in IVF pregnancies, especially in private hospitals.
At our centre, preterm birth rates are quite high, especially among IVF babies, leading to increased respiratory distress and many NICU admissions. This indicates a strong correlation between prematurity and the risk of Respiratory Distress Syndrome(RDS), particularly in IVF infants who are at higher risk, especially in cases of multiple gestations. This study aligns with findings by Guo et al, showing that neonatal respiratory distress is more prevalent in the IVF group (16%) than in naturally conceived babies (4%), with a statistically significant difference (p<0.05).13 These findings support the hypothesis that IVF infants have a higher risk of neonatal respiratory issues, possibly due to factors such as lung maturation.14 15 Another factor may contribute, such as older maternal age in the IVF group (35 vs 30 years), which is often linked to higher pregnancy and birth complications.16 Consequently, these factors may result in respiratory distress and other morbidities in newborns, requiring intensive care in the NICU.17 18 These studies support our hypothesis that IVF infants face a greater risk of respiratory issues, possibly due to factors like lung maturation and maternal age.
This study has several limitations, including its retrospective design and single-institution setting, which may restrict the generalisability of the findings. Moreover, significant differences in baseline characteristics, such as the higher maternal age in the IVF group compared with the natural conception group, could act as confounding factors. Despite these limitations, this research opens opportunities for future multicentre prospective studies that could address these issues and provide more comprehensive insights.
Conclusion
This study highlights significant differences in neonatal outcomes between IVF-conceived and naturally conceived infants. The findings show that IVF infants, especially from multiple gestations, have a higher risk of prematurity and respiratory distress, leading to more frequent NICU admissions. Older maternal age and the higher prevalence of C-sections in IVF pregnancies may contribute to these outcomes. This study emphasises the need for personalised antenatal care and close monitoring of IVF pregnancies to mitigate potential neonatal risks.
Acknowledgements
The authors would like to thank the doctors, nurses and all team members at the Neonatal Unit of Cipto Mangunkusumo Kencana Hospital, Jakarta for their participation in this study.
Footnotes
Funding: The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.
Patient consent for publication: Not applicable.
Provenance and peer review: Not commissioned; externally peer reviewed.
Patient and public involvement: Patients and/or the public were not involved in the design, or conduct, or reporting, or dissemination plans of this research.
Ethics approval: The research team obtained ethical approval from the Faculty of Medicine Universitas Indonesia-Cipto Mangunkusumo Hospital Research Ethics Committee (KET-712/UN2.F1/ETIK/PPM.00.02/2023).
Data availability statement
Data are available upon reasonable request.
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