https://orcid.org/0000-0002-2062-0616
ABSTRACT
The waning of maternal antibodies may cause infants to lose protection against measles before receiving measles-containing vaccine (MCV). The aim of this study is to investigate the changing characteristics and influencing factors of measles antibodies in preterm infants (PT), and to provide scientific basis for optimizing MCV vaccination strategy of the target population. Blood samples were collected from PT and full-term infants (FT) at the chronological age (CA) of 3, 6, and 12 months. Measles antibodies were quantitatively detected by enzyme-linked immunosorbent assay. Demographic and vaccination information were both collected. Kruskal–Wallis rank sum test was used to compare the measles antibodies among different gestation age (GA) groups, and multiple linear regression was performed to identify the correlative factors for the antibodies. Measles antibodies of PT decreased significantly with age increasing before MCV vaccination. The positive rates of antibodies of PT were 10.80% and 3.30% at the age of 3 and 6 months, respectively (p < .001). At 12 months, the measles antibodies and seropositive rate in the infants who received MCV vaccination increased sharply (p < .001). Regression analyzes showed that the younger the GA or the older the age, the lower the antibodies at 3 months(p < .001，p = .018); while the lower measles antibody levels at 3 months and older age predicted the lower antibodies at 6 months(p < .001, p = .029). PT were susceptible to measles due to the low level of maternally derived antibodies before MCV vaccination. More efforts should be considered to protect the vulnerable population during their early postnatal life.
Introduction
Measles is a vaccine-preventable viral disease causing significant morbidity and mortality in children.Citation1 Safe and effective vaccines are available since 1960s, but measles is still an important cause of death among young children worldwide. The global incidence of measles decreased during 2000–2016, however, its spread has been steadily on the rise since 2016. A report released by World Health Organization (WHO) recorded that the number of measles cases worldwide increased to 869,770 in 2019, and the number of measles deaths climbed by nearly 50% in all WHO regions.Citation2 Progress in eliminating measles seems to be slowing down, especially since the outbreak of the pandemic of COVID-19.Citation3 Data published by WHO and United Nations International Children’s Emergency Fund (UNICEF) revealed that in 2022 more than 22 million infants missed the vaccination of measles-containing vaccine (MCV) through routine immunization services in their first year of life,Citation4 the highest number in the past 20 years. Following years of declines in MCV coverage, the estimated number of measles cases increased by 18% and deaths increased by 43% globally in 2022 compared with 2021.Citation5 The failure to vaccination can be the fundamental reason leading to immunity gaps in both younger and older age groups and created the conditions for a rise in disease outbreaks.
In China, there was an epidemic of measles from 2013 to 2015. Data from China Centers for Disease Control and Prevention (CDC) showed that one of the main targets for the measles resurgence was infants under 8-month-old, who were ineligible for the MCV.Citation6 Morbidity and mortality related to measles frequently occur in infants without vaccine protection.Citation7,Citation8 By June 2019, the infantile reported measles cases had decreased from 20,654 (48.7%) in 2015 to 639 (34.7%) but still accounted for 1/3 of the total measles cases.Citation9
Preterm infants (PT) are more susceptible to vaccine-preventable infectious diseases.Citation10,Citation11 Our prior premature cohort demonstrated that vaccination deferral was common in this patient population, the rate of MCV vaccination was only 36.06%, which indicated that most PT were not protected by MCV at the specified age of the vaccination.Citation12 Maternal antibody is thought to be an important guarantee for infants to resist measles infection before MCV vaccination, but some early multicenter studies on general population reported that a considerable part of infants had lost the protection from maternal antibodies before immunization.Citation13,Citation14 So far, we know very little about whether preterm birth leads to an earlier immune gap in the first few months of life. The research in this field is very necessary and of great importance for the prevention of measles infection in PT.
In order to fill in the gap, we conducted the present study to gain insight into the secular trends of maternal antibodies against measles among PT; to evaluate whether these vulnerable infants have sufficiently high maternal antibodies to protect them against measles during early postnatal life; and to identify the correlative factors affecting the infantile measles antibodies among them.
Materials and methods
Study design
This was a longitudinal follow-up study on the changes of measles antibodies of PT in the early postnatal life, combining a cross-sectional analysis of the data of full-term infants (FT). The study was conducted at Children’s Hospital Zhejiang University School of Medicine from Feb 2019 to July 2021. The data of PT were a subset of participants in a cohort of the brain and behavioral effects of early iron supplementation. And the Data of FT came from the results of physical examination of infants in Child HealthCare Department.
Participants
A total of 415 PT (gestational age (GA) of 27–36 weeks) and 219 FT (GA of 37–42 weeks) were enrolled. Based on the GA, PT were further divided into two subgroups: those with GA < 32 weeks were classified as early preterm group (EPT), and those with GA ≥ 32 weeks were classified as moderate-late preterm group (MLPT). Exclusion criteria were measles infection, congenital, or acquired immunodeficiency. Participants who received immunosuppressant drugs and those had symptoms of acute illness at the time of blood test were also excluded.
Data collection
Information regarding demographics, perinatal data, past medical history, as well as maternal history of measles infection and MCV vaccination were collected through one-on-one interviews with parents at the first medical visit. And measles immunization records were collected according to the records on children’s vaccination booklets on their one-year-old physical examination. The information in vaccination booklets is synchronized with the Zhejiang Provincial Immunization Information System.
Blood collection and measurement
Considering that time is an important factor affecting the waning of measles antibodies in infancy, we performed the blood testing according to the chronological age (CA) in both PT and FT groups. CA refers to the duration of time from birth, which is calculated from the date of birth.Citation15
Venous blood samples of PT were collected at the CA of 3, 6, and 12 months, and FTs were collected at the CA of 6 or 12 months as well. 2-ml venous blood samples were drawn in gel tube from the enrolled study participants. Samples were centrifuged and tested for serum levels of immunoglobulin G (IgG) antibodies against measles using Enzyme-linked immunosorbent assay (ELISA) (SERION ELISA classic measles IgG, Institute Virion/Serion GmbH, Wurzburg, Germany) in the laboratory of Zhejiang CDC.
According to the calibration curve generated from the standard serum, the optical density values were converted to the titer units (mIU/ml). Measles antibodies ≥ 200 mIU/ml were considered as “protective” or “seropositive,” whereas titers below 200 mIU/ml were reported as “unprotective” or “seronegative.”Citation16
Statistical analysis
Data analysis was conducted using Statistical Analysis System software version 9.2 (SAS Institute Inc, Cary, North Carolina). The distributions of demographic characteristics and the measles antibodies were described by frequency and percentage for the categorical variables, mean and standard deviation for the normal distribution variables, and median and interquartile range for the non-normal distribution variables.
Pearson’s χ2 test and one-way ANOVA were used to compare the background characteristics among different groups. Kruskal-Wallis rank sum test was used to identify differences in the measles antibodies. Multiple comparisons between groups were assessed by Wilcoxon rank sum test, and the p-value was adjusted by Bonferroni method. Friedman’s M test was performed to compare the changes of measles antibodies in the preterm subjects. A multiple linear regression model was used to analyze correlative factors for measles antibody levels during early postnatal life among PT. Statistical significance was defined as p < .05.
Ethics statement
The procedures and protocols of this study were reviewed and approved by the ethics committee of the Children’s Hospital Zhejiang University School of Medicine (2019-IRB-027). Written informed consent was signed by parents before all study-related tests being performed.
Result
Sample characteristics
In the present study, 415 PT, including 150 EPT and 265 MLPT, as well as 219 FT were enrolled. The number of infants followed in each period is shown in . In total, measles antibodies were assessed in 371, 303, and 213 PT at their 3, 6 and 12 months, respectively. The longitudinal data of measles antibodies in 158 PT at 3, 6 and 12 months were collected. Meanwhile, cross-sectional data of measles antibodies of 101 FT at 6 months and 118 FT at 12 months were obtained.
Figure 1. Flow chart of study participation.
shows the sample background characteristics. There were significant differences in GA and birth weight (BW) among the three groups. Compared with the other two groups, the GA and BW of EPT were younger and lighter, and the utilization rate of antibody-containing blood products was higher (all p < .001). Besides, the rate of MCV vaccination among PT was obviously lower than that of FT (p < .001). There was no difference in the remaining background characteristics among groups. By comparing the baseline characteristics of the infants who dropped out with those stayed in the study, no differences were found (data not shown).
Table 1. The baseline characteristics.
Comparison of measles antibodies and seropositive rate of PT with different GA
At 3 months, the general seropositive rate of measles antibodies in PT was 10.80% (40/371). As shown in , MLPT had significantly higher antibody levels than that of EPT (p < .001), but the seropositive rate was comparable between the two subgroups (7.09% vs. 12.70%, χ2 = 2.741, p = .114).
Figure 2. Comparison of measles antibodies between different GA groups EPT, early preterm infants; MLPT, moderate to late preterm infants; FT, full term infants.
At 6 months, 3.30% (10/303) of PT were antibody positive for measles. The level of measles antibodies and seropositivity between EPT and MLPT were similar (p = .133), but the data were significantly lower than those in FT of the same age (p < .001) ().
At 12 months, the measles antibody levels and the seropositive rate of measles in three groups all increased significantly, but there were still significant differences in measles antibodies among the groups. Compared with FT, EPT and MLPT had lower antibody levels (p < .001), while there was no difference between EPT and MLPT (p = .910) (). FT had the highest level of positive rate of measles antibodies (99.15%), followed by MLPT (95.38%) and EPT (91.57%). A pairwise comparison found that the rate of EPT was significantly lower than FT (p = .007), and no difference was found between the other two groups (all p > .05). We further conducted a stratified analysis among vaccinated and unvaccinated infants. At the age of 12 months, 93.90% (200/213) of PT and 98.31% (116/118) of FT had been vaccinated with MCV. It was found that the measles antibodies of the infants vaccinated with MCV were significantly higher than those without MCV vaccination in three different GA groups (all p < .05, ). Antibodies in FT were significantly higher than that in EPT and MLPT (all p < .001), but no differences were between the latter two groups (p = .762). The seropositive rate of vaccinated infants in all groups reached 100%.
Figure 3. Comparison of measles antibodies between 12-month-old infants with and without MCV vaccination.
Changing characteristic of measles antibodies in PT in infancy
shows the characteristics of changes in measles antibody levels in PT during the first year of life. From 3 to 6 months, measles antibodies decreased significantly as age increasing [37.32 (56.74) vs. 19.28 (21.35), p < .001]. At 12 months, the antibody levels increased sharply, which was significantly higher than the data at 3 and 6 months (p < .001). Besides, the differences in measles antibodies between 3 and 6 months, 3 and 12 months, as well as 6 and 12 months were significant (all p < .001).
Figure 4. Longitudinal changing characteristic of measles antibodies in 158 PT in infancy.
Factors associated with infantile measles antibodies
To identify factors associated with measles antibodies among PT, multivariable linear regression analysis was performed, with GA, BW, gender, CA, feeding pattern, history of application of antibody-containing blood products, maternal age, and history of MCV vaccination as independent variables.
Through analysis, it was found that GA and CA were the main factors affecting the level of measles antibodies at 3 months. The result showed that the younger the GA or the older the CA, the lower their measles antibody levels at 3 months (p < .001，p = .018) ().
Table 2. Factors relating to measles antibodies at 3 months.
The measles antibodies at the age of 6 months were closely related to the antibodies at 3 months and CA. The lower level of measles antibody at 3 months or the older age predicted the lower measles antibodies at 6 months (p < .001, p = .029) ().
Table 3. Factors relating to measles antibodies at 6 months.
Discussion
The purpose of the study was to detect specific antibodies against measles so as to evaluate the immune status of PT in the first year of life. We found that PT do not have adequate protection against measles infection before the first dose of MCV during early infancy. GA and CA were the critical factors affecting the measles antibodies at 3 months; and the measles antibodies at 6 months were mainly related to the measles antibodies at 3 months and CA, but not to GA.
Measles is a highly contagious infectious disease, with the basic reproduction number (R nought, R0) of 12–18.Citation17 Despite the existence of effective MCV, the goal of global eradication of measles has not yet been achieved.Citation18 Clinically, the timing of the vaccination of the first dose of MCV usually needs to balance the influence of several factors, including the passive transfer of maternal specific antibodies, development of infant immune system, and the prevalence of measles.Citation19,Citation20 If the first dose is administered too early, immune responses can be blunted due to maternal transferred antibodies and infants’ immature immune system. Thus, the first dose of MCV is scheduled at the age of 8 months in China, while in countries where measles has been eliminated, the first dose is usually recommended within the age of 12 and 15 months.Citation8–23
In the current study, we found that the average measles antibody levels of the target population was much lower than the protective level, especially for PT with younger GA. Only 10% PT was seropositive at 3 months. The measles antibodies in MLPT were higher than that in EPT, but the seropositive rate was similar between the two subgroups. A previous cross-sectional seroepidemiological study on the waning of maternal specific antibodies in the general population in the same area showed that the seropositive rates of 3-month-old infants in 2009 and 2013 were as high as 83.8% and 69.6%, respectively.Citation24 By 2018, another follow-up study in western China reported that only 20.4% infants were positive for measles antibodies at 3 months.Citation25 Combining the previous research results of the past 10 years with the findings of this study, we speculate that a considerable number of young infants were susceptible to measles in their early postnatal life, especially for PT.
It is well known that, the primary protection of infants against measles in early infancy before MCV vaccination is mainly provided by maternal antibodies.Citation26,Citation27 In order to identify the difference of measles antibodies between PT and FT, we compared the antibody levels between the two groups at the age of 6 and 12 months. It was found that at the age of 6 months, most of the infants in both PT and FT were seronegative, yet the positive rate and antibody levels of PT were lower than those of FT. Similar results have been found in studies in the Netherlands and Israel.Citation28,Citation29 There was evidence that the geometric mean titer of measles antibodies in PT was 1.7–2.5 times lower than that in FT, which indicated that the protective effect of maternal antibodies in PT was obviously weak before MCV vaccination.Citation2,Citation29 In addition, we found that most infants had been vaccinated with MCV at 12-month-old, and the antibody levels and seropositive rate of infants who received the MCV in both PT and FT groups were significantly increased. These results indicated that both PT and FT had good immune responses to the specific vaccine.
In order to understand the changing characteristics of measles antibodies in PT during infancy, we longitudinally compared their antibody levels at 3, 6, and 12 months. We found that maternal measles antibodies of PT decreased significantly with age increasing before receiving MCV. The proportion of seropositive dropped from 10.78% at 3 months to 3.30% at 6 months. Notably, there was a window between 3 and 6 months of age where infants had not yet received MCV, leaving 2–5 months interval where they were potentially vulnerable. The early attenuation of antibodies in PT can greatly increase the risk of measles infection. This assertion was also corroborated by Chong’s research that general population at the age of 4–8 months, who were not eligible for MCV, were at risk due to the low antibody levels.Citation24 Besides, in clinic practice, it is often assumed that high levels of maternal antibodies in early infancy can interfere with the efficacy of MCV vaccination. However, the findings of this study indicated that PT exhibited the relatively low maternal antibody levels in the postnatal period of 3 to 6 months suggesting minimal impact on the immunogenic effect of MCV.
In this study, we further investigated the factors affecting the waning of maternal antibodies in the enrolled subjects at 3 and 6 months. We found that GA and CA were the two critical factors influencing the measles antibodies of PT during their early postnatal life. PT born with younger GA had the lower level of measles antibodies at 3 months, which indicated that duration of gestation determines the placental transfer of antibodies to the neonates. Thus, PT with younger GA receive fewer antibodies from their mothers and not sufficient to have themselves immunized. Another possible reason why infants are not sufficient to immunize can be related to the characteristics of maternal history of measles infection and MCV vaccination. Some previous studies reported that immunized mothers had lower and less durable antibodies in their offspring compared to naturally infected mothers.Citation28,Citation30,Citation31 In China, the Immunization Program has been implemented since 1978. The mean age of mothers in our cohort was around 30. A survey on measles antibodies of permanent residents in Zhejiang Province in 2018 found that the seropositive rate of measles antibodies among residents aged 20–40 years was 91.68–92.75%, of which 44.62–51.60% were above 800IU/L. The measles antibodies of residents with measles history were higher than those with unknown history of measles infection, and the antibody level of residents with the history of MCV vaccination was higher than those with unknown immunization history.Citation32 Among the mothers interviewed in this study, half of them had been vaccinated against measles and only two were infected with measles. Therefore, sustained low level of measles endemic transmission and vaccine-derived antibodies probably lead to seronegative in PT at an early stage.Citation33
At the age of 6 months, GA was no longer a critical factor affecting the measles antibodies. Instead, antibody levels at 3 months, as well as CA became the main factors. Infants with higher measles antibody levels at 3 months maintained greater maternal antibodies at 6 months, although the antibody level of most infants had not yet reached the protective level around this time. The above results revealed that the maternal antibodies of PT decreased gradually over time and were almost depleted at 6 months
Therefore, the above analysis provides evidence that measles antibodies in PT have subsided before receiving the MCV vaccination under the EPI schedule in China. We have reasons to speculate that the low level of maternal antibodies in PT, coupled with the current control measures, may not be sufficient to eliminate measles in China. In order to narrow the immunization gap, it is essential to explore interventions, including revising and strengthening vaccination programs and promoting MCV doses for infants under 8 months of age with low maternal antibody levels.
Limitation
There are several limitations in this study. Firstly, the present study was conducted in a single pediatric hospital, using a convenience sample of PT for data analysis, which may not be representative of all the premature infants. Secondly, we were unable to obtain the data regarding on the measles antibody levels in cord blood, so we cannot understand the characteristics of measles antibodies in neonatal PT. Thirdly, the data of FT were cross-sectional and there was a lack of data on measles antibody levels at the age of 3 months, so the difference of the trend of declining measles antibodies between PT and FT cannot be longitudinally compared. Finally, the sampling period of our study covered the global epidemic period of COVID-19. However, we did not collect the epidemiological information on COVID-19 infection, so it was impossible to determine whether the research results were affected by the epidemic. Therefore, further well-designed longitudinal multicenter investigations are needed to determine if our results can be generalized.
Conclusion
In conclusion, our result revealed that PT were susceptible to measles due to the rapid waning of maternally derived antibodies in early infancy. Prior to MCV vaccination, the specific antibodies decreased with age increasing, positive rate of measles antibodies among PT was very low within the age of 6 months. GA and CA were two main factors affecting measles antibodies at an earlier age, while measles antibodies at 3 months and CA contribute to the measles antibodies in the later infancy. The lack of protection in the vulnerable population during early postnatal life reminds us to reconsider the strategies for MCV for the target population, especially in the event of an outbreak.
Author contributions
Chai Ji and Yan Feng: Conceptualized and designed the study, and responsible for the quality control of laboratory testing; Mingyan Li and Weiwei Zhang conducted the analysis, interpreted the data, drafted the initial manuscript, and revised the manuscript; Shuangshuang Zheng conducted the statistical analysis, Junxia Guo, Yongjun Ma and Yan Huang collected data and contributed to the laboratory testing; Hanqing He critically reviewed and revised to the revision of the manuscript. All authors: approved the final content of the manuscript and agree to be accountable for all aspects of the work.
Acknowledgments
We are grateful to the study families for their participation, the nurses and colleagues at the Children’s Hospital of Zhejiang University School of Medicine for their dedicated assistance.
Disclosure statement
No potential conflict of interest was reported by the author(s).
Additional information
Funding
References
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