Parasitic infections during pregnancy in Gabon affect glycosylation patterns of maternal and child antibodies

Bibliographic Details
Title:	Parasitic infections during pregnancy in Gabon affect glycosylation patterns of maternal and child antibodies
Authors:	Yabo J. Honkpehedji, Anna O. Kildemoes, Koen A. Stam, Dieu L. Nguyen, Tom Veldhuizen, Angela van Diepen, Meral Esen, Peter G. Kremsner, Manfred Wuhrer, Ayôla A. Adegnika, Cornelis H. Hokke, Maria Yazdanbakhsh
Source:	Scientific Reports, Vol 14, Iss 1, Pp 1-9 (2024)
Publisher Information:	Nature Portfolio, 2024.
Publication Year:	2024
Collection:	LCC:Medicine LCC:Science
Subject Terms:	Antibody, Glycosylation, Parasitic infections, Pregnancy, Child, Gabon, Medicine, Science
More Details:	Abstract Antibody glycosylation patterns can affect antibody functionality and thereby contribute to protection against invading pathogens. During pregnancy, maternal antibodies can be transferred through the placenta and contribute to modulating both the mother’s and her child’s immune responses. Although several studies of IgG glycosylation during pregnancy have been carried out, very few cohorts studied were from sub-Saharan Africa, where exposure to microorganisms and parasites is high. In Lambaréné, Gabon, 106 pregnant women in their third trimester were enrolled into this study. At enrolment, urine, stool, and blood samples were collected from the mothers to assess Schistosoma haematobium (S. haematobium), Plasmodium falciparum (P. falciparum) and other parasite infections. During delivery, cord blood samples were collected. The children were followed, and blood samples were collected at 9 and 12 months of age. IgG Fc glycosylation was measured by liquid chromatography-mass spectrometry, determining fucosylation, galactosylation, sialylation, bisection, and sialylation per galactose (SA/gal). Among the 106 pregnant women, 33 (31%) were infected by at least one parasite. The antibody glycosylation patterns in maternal and cord blood showed distinct profiles when compared to that of infants at 9 and 12 months. IgG galactosylation was higher in maternal/cord blood, while fucosylated IgG was higher in children up to 1 year of age. Maternal parasitic infection was associated with lower IgG2 and IgG3/IgG4 galactosylation in cord blood and lower IgG3/IgG4 galactosylation in children. When maternal IgG galactosylation and, consequently, cord blood were categorized as high, children at 9 and 12 months of age showed higher IgG galactosylation compared to children of mothers with low IgG galactosylation. As IgG Fc galactosylation can have functional consequences, it might provide valuable information for developing effective preventive and treatment strategies for vulnerable populations.
Document Type:	article
File Description:	electronic resource
Language:	English
ISSN:	2045-2322
Relation:	https://doaj.org/toc/2045-2322
DOI:	10.1038/s41598-024-83366-8
Access URL:	https://doaj.org/article/bf911dd01aad4962ad3bd80ab5c67c8c
Accession Number:	edsdoj.bf911dd01aad4962ad3bd80ab5c67c8c
Database:	Directory of Open Access Journals
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FullText	Links: – Type: pdflink Url: https://content.ebscohost.com/cds/retrieve?content=AQICAHjPtM4BHU3ZchRwgzYmadcigk49r9CVlbU7V5F6lgH7WwFnIfC9IxxhJ_7CW-kKURLJAAAA4jCB3wYJKoZIhvcNAQcGoIHRMIHOAgEAMIHIBgkqhkiG9w0BBwEwHgYJYIZIAWUDBAEuMBEEDGQMAryBvXw3jIanlgIBEICBmnhPMCyB9Ps54aCTr5UA9jsB_H9Zkbqn8KGT6ztNprkqShqUy6O8p_hXDqc44QR9u95ZFzf-nS7GE0Lhe3XMrvzBDhBeFf4ql9wQjd08tlvi4hEiRnuWmzcndmuRfq0Jb4iQ8sfs7QFl4xDjiQwGtsAO0KG3unAXOa3f66BKWJkv8UYEGgBfIlNWyzxO-wvZY7XPNYMdz6XAvBI= Text: Availability: 1 Value: <anid>AN0181944202;[fkqs]30dec.24;2025Mar11.13:04;v2.2.500</anid> <title id="AN0181944202-1">Parasitic infections during pregnancy in Gabon affect glycosylation patterns of maternal and child antibodies </title> <p>Antibody glycosylation patterns can affect antibody functionality and thereby contribute to protection against invading pathogens. During pregnancy, maternal antibodies can be transferred through the placenta and contribute to modulating both the mother's and her child's immune responses. Although several studies of IgG glycosylation during pregnancy have been carried out, very few cohorts studied were from sub-Saharan Africa, where exposure to microorganisms and parasites is high. In Lambaréné, Gabon, 106 pregnant women in their third trimester were enrolled into this study. At enrolment, urine, stool, and blood samples were collected from the mothers to assess Schistosoma haematobium (S. haematobium), Plasmodium falciparum (P. falciparum) and other parasite infections. During delivery, cord blood samples were collected. The children were followed, and blood samples were collected at 9 and 12 months of age. IgG Fc glycosylation was measured by liquid chromatography-mass spectrometry, determining fucosylation, galactosylation, sialylation, bisection, and sialylation per galactose (SA/gal). Among the 106 pregnant women, 33 (31%) were infected by at least one parasite. The antibody glycosylation patterns in maternal and cord blood showed distinct profiles when compared to that of infants at 9 and 12 months. IgG galactosylation was higher in maternal/cord blood, while fucosylated IgG was higher in children up to 1 year of age. Maternal parasitic infection was associated with lower IgG2 and IgG3/IgG4 galactosylation in cord blood and lower IgG3/IgG4 galactosylation in children. When maternal IgG galactosylation and, consequently, cord blood were categorized as high, children at 9 and 12 months of age showed higher IgG galactosylation compared to children of mothers with low IgG galactosylation. As IgG Fc galactosylation can have functional consequences, it might provide valuable information for developing effective preventive and treatment strategies for vulnerable populations.</p> <p>Keywords: Antibody; Glycosylation; Parasitic infections; Pregnancy; Child; Gabon</p> <hd id="AN0181944202-2">Introduction</hd> <p>Pregnancy brings significant changes to a woman's immune system. These changes are essential to protect both the mother and her unborn baby from infections[<reflink idref="bib1" id="ref1">1</reflink>],[<reflink idref="bib2" id="ref2">2</reflink>]. A crucial aspect of the immune system's adaptation involves antibodies, which are vital in defending against infections. In many areas of low-middle-income countries (LMIC) where parasitic infections are endemic, such as Gabon, pregnant women and children are more susceptible to the diseases caused by these infections[<reflink idref="bib3" id="ref3">3</reflink>],[<reflink idref="bib4" id="ref4">4</reflink>]. Indeed, studies showed that parasitic infections are a significant concern in these regions, particularly during pregnancy and childhood[<reflink idref="bib3" id="ref5">3</reflink>],[<reflink idref="bib5" id="ref6">5</reflink>],[<reflink idref="bib6" id="ref7">6</reflink>]. Antibodies, including IgG, are modified by the addition of glycans, a process that may alter the effectivity of antibody-dependent immune responses to infections[<reflink idref="bib4" id="ref8">4</reflink>],[<reflink idref="bib7" id="ref9">7</reflink>]. Antibody glycosylation is known to be influenced by factors like age, genetic background, pregnancy and the presence of chronic infections[<reflink idref="bib4" id="ref10">4</reflink>],[<reflink idref="bib8" id="ref11">8</reflink>], and alterations in IgG subclass (IgG1, IgG2, IgG3, and IgG4) distribution and glycosylation patterns have been implicated in immune responses against various pathogens and various diseases[<reflink idref="bib8" id="ref12">8</reflink>]. Moreover, the presence of maternal antibodies can impact the development of the infant's immune system[<reflink idref="bib4" id="ref13">4</reflink>],[<reflink idref="bib9" id="ref14">9</reflink>]. For example, changes in the levels of IgG subclasses during pregnancy can increase susceptibility to malaria[<reflink idref="bib10" id="ref15">10</reflink>]. However, antibody glycosylation during pregnancy and early childhood in areas endemic to parasitic infections has been understudied. To this end, we have analysed the glycosylation pattern of maternal and infant IgG as a function of maternal parasitic infection status during pregnancy.</p> <hd id="AN0181944202-3">Results</hd> <p></p> <hd id="AN0181944202-4">Characteristics of the study population</hd> <p>Pregnant women from Lambaréné and its surroundings were recruited in the Helmvac2 study. In short, a total of 323 pregnant women who were eligible according to the inclusion/exclusion criteria were enrolled[<reflink idref="bib11" id="ref16">11</reflink>], and were followed up until delivery. After birth, their children were followed up to 12 months of age. From this cohort, we included 106 mother and child pairs from which at least 3 blood samples were available (maternal, cord blood, child 9 months and/or child 12 months). Table 1 shows the age, haemoglobin, location, parity and breastfeeding during the first year of life. The infants started eating solid food around 4–6 months. In addition, infection with parasites status was assessed (<emph>P. falciparum, S. haematobium, Trichuris trichiura, Ascaris lumbricoides</emph>, hookworms, <emph>Loa loa</emph>). It showed that 31% (33/106) of the enrolled mothers were positive for either one of the parasitic infections. The prevalence of single infections among infected women was 22/33 (66.7%), while the rest had co-infections, as shown in Fig. 1.</p> <p>Table 1 Baseline characteristics of the 106 pregnant women included in the analysis.</p> <p> <ephtml> &lt;table frame="hsides" rules="groups"&gt;&lt;thead&gt;&lt;tr&gt;&lt;th align="left"&gt;&lt;p&gt;Characteristics&lt;/p&gt;&lt;/th&gt;&lt;th align="left"&gt;&lt;p&gt;n&lt;/p&gt;&lt;/th&gt;&lt;th align="left"&gt;&lt;p&gt;%&lt;/p&gt;&lt;/th&gt;&lt;th align="left"&gt;&lt;p&gt;Mean (SD)&lt;/p&gt;&lt;/th&gt;&lt;/tr&gt;&lt;/thead&gt;&lt;tbody&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt;Haemoglobin (g/dl)&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;-&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;-&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;8.9.2 (1.70)&lt;/p&gt;&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt;Age (years)&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;-&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;-&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;22.1 (6.80)&lt;/p&gt;&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt;Location&lt;/p&gt;&lt;/td&gt;&lt;td align="left" /&gt;&lt;td align="left" /&gt;&lt;td align="left" /&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt; Rural&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;18&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;17&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;-&lt;/p&gt;&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt; Semi-Urban&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;88&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;83&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;-&lt;/p&gt;&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt;Parity&lt;/p&gt;&lt;/td&gt;&lt;td align="left" /&gt;&lt;td align="left" /&gt;&lt;td align="left" /&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt; Nulliparous&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;19&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;18&lt;/p&gt;&lt;/td&gt;&lt;td align="left" /&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt; Primiparous&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;26&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;24.5&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;-&lt;/p&gt;&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt; Multiparous&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;61&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;57.5&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;-&lt;/p&gt;&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt;Infection status&lt;/p&gt;&lt;/td&gt;&lt;td align="left" /&gt;&lt;td align="left" /&gt;&lt;td align="left" /&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt; Positive&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;33&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;31&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;-&lt;/p&gt;&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt; Negative&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;73&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;69&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;-&lt;/p&gt;&lt;/td&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt;Breastfeeding&lt;/p&gt;&lt;/td&gt;&lt;td align="left" /&gt;&lt;td align="left" /&gt;&lt;td align="left" /&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt; No&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;14&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;13.2&lt;/p&gt;&lt;/td&gt;&lt;td align="left" /&gt;&lt;/tr&gt;&lt;tr&gt;&lt;td align="left"&gt;&lt;p&gt; Yes&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;92&lt;/p&gt;&lt;/td&gt;&lt;td align="left"&gt;&lt;p&gt;86.8&lt;/p&gt;&lt;/td&gt;&lt;td align="left" /&gt;&lt;/tr&gt;&lt;/tbody&gt;&lt;/table&gt; </ephtml> </p> <p>The table includes the demographic and clinical characteristics of the 106 pregnant women. It contains data on haemoglobin levels (mean and standard deviation), age (mean and standard deviation), the percentage of location (rural vs. semi-urban), parity (nulliparous, primiparous, multiparous), infection status, and breastfeeding status.</p> <p>Graph: Fig. 1 Characteristics of the maternal infection status. The parasite counts among mothers are shown in this figure. The bar graph on the left shows the total count of each parasite detected among mothers, including Strongyloides stercoralis (S. stercoralis), Ascaris lumbricoides (A. lumbricoides), Plasmodium falciparum (P. falciparum), Hookworm, Loa loa (L. loa), Schistosoma haematobium (S. haematobium), and Trichuris trichiura (T. trichiura). The intersection matrix on the right indicates the co-infection of different parasites in individual mothers, with bars representing the number of mothers infected with each (poly)parasite. Each dot in the matrix corresponds to the presence of a specific parasite in the intersection group.</p> <hd id="AN0181944202-5">The overall analysis of antibody glycosylation in the study cohort</hd> <p>IgG Fc glycosylation was analyzed by LC–MS, resulting in the quantification of 24, 14 and 11 glycopeptides for IgG1, IgG2 and IgG3/IgG4, respectively (Table S1). The study population's glycosylation (galactosylation, fucosylation, sialylation and bisection) data were included in a principal component analysis (PCA). As shown in Fig. 2A, the first two principal components, PC1 and PC2, account for 25.3% and 45% of the variation in the glycosylation data, respectively. As expected, the similarity of maternal and cord blood due to the transfer of IgG across the placenta was reflected in the clustering of maternal and cord blood together. The similarity in the glycosylation profiles was also seen for children at 9 and 12 months of age.</p> <p>Graph: Fig. 2 Principal Component Analysis of IgG antibody glycosylation in maternal, cord, and child at 9- and 12-months blood. Principal component analysis (PCA) of IgG antibody glycosylation patterns. (A) PCA plot showing the distribution of samples based on common glycan structures. Each point represents a single sample, colour-coded by population (mother, cord blood, child at 9 months, child at 12 months) and shaped by maternal infection status (negative or positive). (B) Variables PCA plot showing the contribution of different glycosylation features to the principal components. PC1 explains 45% of the variance, while PC2 explains 25.3%.</p> <p>However, the maternal and cord blood glycosylation profiles segregate from children at 9 and 12 months of age. There was no segregation according to the infection status of the mothers. Figure 2B indicates that IgG galactosylation is largely associated with maternal and cord blood profiles, while IgG1 and IgG2 fucosylation are associated with children. Antibody sialylation and bisection also show differential associations with mothers and children; however, as galactosylation and fucosylation are more prominent and have been studied extensively in terms of function, we will focus on these two traits in the following sections.</p> <hd id="AN0181944202-6">Specific changes in IgG galactosylation and fucosylation patterns between mother, cord and ch...</hd> <p>Although cord blood IgG glycosylation profiles, in general, mirror those of maternal ones, we did observe a significant increase in IgG galactosylation and a decrease in IgG fucosylation from maternal and cord blood to infant blood at 9 months of age (Fig. 3).</p> <p>Graph: Fig. 3 IgG galactosylation and IgG fucosylation in different samples: maternal, cord, and child 9 and 12 months blood. Violin plots show the glycosylation trait distribution in IgG subclasses among different populations (mother, cord blood, child at 9 and 12 months). Each plot represents the percentage of total glycan structures for a specific trait: (A) IgG1 galactosylation, (B) IgG1 fucosylation, (C) IgG2 galactosylation, (D) IgG2 fucosylation, (E) IgG3/IgG4 galactosylation. Asterisks indicate statistical significance between groups (ns: not significant, p &lt; 0.05, p &lt; 0.01, p &lt; 0.001, *p &lt; 0.0001).</p> <p>The levels of IgG1 and IgG2 galactosylation were significantly higher in maternal and cord blood compared to infants at 9 and 12 months of age (Fig. 3A, 3C), whereas the galactosylation pattern of IgG3/IgG4 (Fig. 3E) showed no clear difference between any of the groups. Altogether, it was noted that there was a higher degree of variation in the galactosylation of maternal and cord blood antibodies compared to those of children.</p> <p>In contrast to galactosylation, maternal and cord blood IgG1 fucosylation was significantly lower compared to children at 9 and 12 months of age (Fig. 3B). This pattern was not seen when analysing IgG2 (Fig. 3D).</p> <hd id="AN0181944202-7">Does maternal infection status affect the IgG glycosylation patterns?</hd> <p>To answer this question, maternal, cord blood, and infant (9 and 12 months) IgG glycosylation data were analyzed as a function of whether pregnant women were negative or positive for any parasitic infection. There was a borderline statistical difference between IgG1 galactosylation in maternal blood when comparing negative (uninfected 69%) with positive (infected 31%) individuals (P = 0.053). The same borderline statistical difference was found in cord blood (Fig. 4A). However, no differences in the IgG1 galactosylation were found between children of 9 or 12 months of age born to negative or positive mothers. Regarding IgG2 (Fig. 4B) and IgG3/IgG4 (Fig. 4C), there was a statistically significant difference between negative and positive mothers when considering their maternal or cord blood IgG2 galactosylation (P = 0.039 and P = 0.042, respectively) and IgG3/IgG4 galactosylation (P = 0.0053 for maternal; P = 0.001 for cord blood). No statistically significant differences were found between the IgG2 galactosylation of 9-month-old children born to negative versus positive mothers (P = 0.420) (Fig. 4B). However, IgG3/IgG4 galactosylation significantly differed between children at 9 months of age, with mothers either negative or positive for parasitic infections at birth (P = 0.030) (Fig. 4C). Maternal infection status did not affect the IgG fucosylation, as shown in supplemental Fig S1.</p> <p>Graph: Fig. 4 Comparison of the IgG galactosylation in different samples (maternal, cord, and child at 9 and 12 months blood) based on maternal infection status. Violin plots showing the percentage for each trait of total glycan structures in IgG subclasses between different populations based on maternal infection status (negative vs. positive). The plots are divided by sample type (mother, cord blood, child at 9 and 12 months): (A) IgG1 galactosylation, (B) IgG2 galactosylation, (C) IgG3/IgG4 galactosylation. Asterisks indicate statistical significance between groups (ns: not significant, p &lt; 0.05, p &lt; 0.01, p &lt; 0.001).</p> <hd id="AN0181944202-8">Is the high/low antibody galactosylation and fucosylation status of a mother reflected in the...</hd> <p>The longitudinal data depicted in Fig. 5 show the changes in IgG galactosylation patterns over time, focusing on different IgG subclasses (IgG1, IgG2, and IgG3/IgG4). The analysis covers multiple time points, tracking the progression of galactosylation from mother to child at 9 and 12 months of age. In panels A-C, the line plots represent the relative abundance of galactosylation for each subclass of IgG across three groups: high, medium, and low galactosylation levels, which remain consistent across time points. The line plots help to visualise how these patterns evolve in each group. The progression of IgG1 galactosylation levels following the changes from mother to cord blood and cord blood to the child at 9 and 12 months is visualized in the mosaic-like plots in Fig. 5D. In addition, Fig. S3 illustrates the longitudinal analysis of IgG2 (panel A) and IgG3/IgG4 (panel B) galactosylation patterns from mother to child. The bars in these figures are divided into three categories representing low, medium, and high galactosylation levels. The height of each bar represents the proportion of individuals within each category at the different stages of development (birth (cord blood), 9 months and 12 months). The figure demonstrates both the consistency and the changes in galactosylation categories as the child matures, thereby highlighting the longitudinal stability or shifts in glycosylation patterns from mother to child. upplementary Figs. S2 and S4 shows the fucosylation profiles of antibodies in cord blood and in children based on the categorization of maternal IgG fucosylation (into high, medium or low. Taken together, it is clear that cord blood and children at 12 months show high galactosylation of IgG1 (Figs. 5A and 5D) if they belong to mothers with high galactosylation levels (P &lt; 0.001). For IgG fucosylation, the maternal levels of high, medium and low were only reflected in cord blood but not in children at 9 and 12 months of age (Figs. S2, S4 and Table S2).</p> <p>Graph: Fig. 5 Comparison of sub-classes of IgG galactosylation levels in different samples (maternal, cord, child at 9 and 12 months blood). Longitudinal analysis of IgG galactosylation patterns across different time points and groups. (A: IgG1 galactosylation, B: IgG2 galactosylation and C: IgG3/IgG4 galactosylation). Line plots showing the percentage of total glycan structures for IgG1, IgG2, and IgG3/IgG4 galactosylation from mother to child (9 and 12 months), categorized into three steady groups: high, medium, and low. (D) Plots showing the progression of IgG1 galactosylation levels (low, medium, high) from mother to cord blood and from cord blood to child at 9 and 12 months. These plots illustrate the changes in galactosylation levels over time for each group. The steady groups help to visualize the stability or changes in glycosylation patterns across the different stages of development.</p> <hd id="AN0181944202-9">Discussion</hd> <p>Antibody glycosylation is known to influence antibody function. There are an increasing number of studies analyzing the IgG Fc glycosylation profiles in pregnant women and from cord blood to adulthood. Still, most studies have been conducted in high-income countries, and few have examined antibody glycosylation in low- and middle-income countries. Here, we measured the IgG Fc glycosylation in pregnant women, cord blood, and their child at 9 and 12 months of age. We observe that the maternal and cord blood samples cluster closely together in PCA, as expected from the fact that there is a transfer of IgG antibodies across the placenta, which is consistent with findings from prior research[<reflink idref="bib12" id="ref17">12</reflink>]. The transfer of IgG antibodies across the placenta is mediated through neonatal Fc receptors, but there is no consensus on whether there is a glycosylation bias in this process. Whereas our data shows that galactosylation of IgG is higher in cord compared to maternal blood, in line with some earlier studies[<reflink idref="bib13" id="ref18">13</reflink>],[<reflink idref="bib14" id="ref19">14</reflink>], some reports refute this[<reflink idref="bib15" id="ref20">15</reflink>]. The factors contributing to such discrepancies are not clear. The discrepancies observed in studies reporting higher or lower IgG galactosylation in cord blood versus maternal blood may be attributed to a combination of biological factors, technical aspects, and population characteristics. Biological factors include selective IgG transfer, maternal inflammation, and infections. Technical aspects are related to differences in glycosylation analysis methodology. Population characteristics include genetic background and geographic location.</p> <p>The IgG glycosylation profiles of children at 9 and 12 months of age exhibit a distinct divergence from those observed in maternal samples. There is lower galactosylation, but fucosylation of IgG in children compared to mothers was higher. These data are in agreement with findings reported in a European cohort[<reflink idref="bib16" id="ref21">16</reflink>]. These results may indicate that the antibody profile of infants becomes more independent from maternal influence towards the end of the first year of life. Indeed, the changes in IgG glycosylation profiles from birth (cord blood) to 9 and 12 months could be attributed to the reduced presence of maternal antibodies, the exposure to diverse environmental factors resulting in the development of a more diverse antibody repertoire, and the ongoing maturation of the infant's immune system. The environmental factors to consider include nutrition, lifestyle and exposure to microorganisms and parasites. For example, the importance of diet and microbiome diversity for IgG glycosylation has been highlighted by Kirmiz et al.[<reflink idref="bib17" id="ref22">17</reflink>]. Overall, the maternal infection status seems to have some influence on the IgG galactosylation profiles but to a varying degree depending on the IgG subclass. It appears that the strength of the influence that the mother's infection status has on their own IgG galactosylation also translates into an effect for her child at 9 months of age. Moreover, the data on the infection status of pregnant women shows that IgG2 and IgG3/IgG4 galactosylation is lower in maternal and cord blood in those positive for any parasitic infections, again indicating a change in antibody glycosylation due to environmental exposure. There was a slight but statistically significant difference in IgG3/IgG4 galactosylation at 9 months of age seen in children born to mothers infected with parasites. Some studies have reported that higher galactosylation of antibodies might have anti-inflammatory characteristics[<reflink idref="bib18" id="ref23">18</reflink>],[<reflink idref="bib19" id="ref24">19</reflink>], while others have shown that in non-pregnant states, low levels of galactosylation are associated with increased inflammation[<reflink idref="bib20" id="ref25">20</reflink>]. It was interesting to find that when maternal IgG galactosylation and fucosylation were high, the levels of IgG galactosylation and fucosylation were also high in cord blood, which would be expected, but not in child of 9 and 12 months of age. This would not support a dominant role of genetic factors in the observed glycosylation patterns. Regarding the limitations of our study, the relatively small sample size and lack of data on environmental factors other than parasitic infections, genetics, and breastfeeding might limit the full interpretation of our results.</p> <p>In summary, our study conducted in Gabon, where parasitic infections are highly prevalent, shows that glycosylation patterns of pregnant women are affected by infection status. However, this effect was diminished in their child, which shows that factors beyond maternal influence increasingly determine glycosylation patterns as infants age. Understanding the understudied interplay between maternal and child glycosylation patterns in LMIC is needed to better define antibody function in health and disease.</p> <hd id="AN0181944202-10">Methods</hd> <p></p> <hd id="AN0181944202-11">Study design, study population</hd> <p>Healthy pregnant women and their unborn child from Lambaréné and surroundings in Gabon who were in their third trimester, from their 28 week of Pregnancy (WP), during the antenatal care (ANC) visit, and willing to give birth in one of the two maternities based in Lambaréné city, including Albert Schweitzer Hospital and Georges Rawiri Hospital, were enrolled to the HelmVac2 (German Federal Ministry of Education and Research (BMBF) [01KA1307]) study, which was conducted between February 2014 and February 2017[<reflink idref="bib11" id="ref26">11</reflink>]. Written informed consent was obtained from all participating pregnant women for themselves and their unborn child before enrollment. Socio-demographics, clinical and obstetrical data from the pregnant women at enrollment, and anthropometrics data from their newborns at delivery were collected. Four visits time points were scheduled for all subjects. Visit (V) 1 took place at screening (mothers only), V2 at delivery (mothers and their newborns), V3 9 months after delivery (infants only) and V4 12 months after delivery (infants only). At V1, the mother's stool, urine, and blood samples were collected to assess <emph>P. falciparum spp</emph>, soil-transmitted helminth infections, and filariasis. At V2, blood samples of the mother and the newborn (cord blood) were collected to assess the antibody. At V3 and V4, 4 ml of venous blood of the infant was collected.</p> <hd id="AN0181944202-12">Assessment of parasite infection</hd> <p>The parasite infections were assessed. One stool sample was analyzed for the presence of soil-transmitted helminths using the Kato-Katz and coproculture methods[<reflink idref="bib21" id="ref27">21</reflink>],[<reflink idref="bib22" id="ref28">22</reflink>], and three consecutive urine samples were analyzed using the filtration method to detect the ova of <emph>S. haematobium</emph>[<reflink idref="bib23" id="ref29">23</reflink>]. The maternal blood samples were analyzed to detect the presence of <emph>P. falciparum</emph> by microscopic examination of a thick blood smear; the presence and density of the parasite were determined using the Lambaréné method as described elsewhere[<reflink idref="bib24" id="ref30">24</reflink>], and microfilariae of <emph>Loa. loa</emph> (<emph>L. loa</emph>) were assessed by microscopy using the saponin method[<reflink idref="bib25" id="ref31">25</reflink>]. More details of the process of data collection, sampling and parasite detection were described in the previous report[<reflink idref="bib11" id="ref32">11</reflink>].</p> <hd id="AN0181944202-13">Analysis of antibody glycosylation by mass spectrometry</hd> <p>IgG antibodies were affinity-purified from serum samples using Protein G Sepharose® beads, followed by trypsinization and analysis of the resulting glycopeptides by using liquid chromatography-mass spectrometry (LC–MS)[<reflink idref="bib26" id="ref33">26</reflink>]. Glycopeptides were quantified using Lacy Tools, and IgG subclass-specific Fc glycosylation profiles were determined. The peptide sequence of the IgG3 glycopeptide shows allotype variation in the amino acid at the position N-terminal of the Asn227, causing a mass that is identical to either the IgG2 peptide (EEQFNSTFR; predominant allotype in Caucasian populations) or the IgG4 sequence (EEQYNSTFR; predominant allotype in Asian and African populations). Because of this allotype variation, IgG3/IgG4 glycopeptides cannot be discriminated in the current study[<reflink idref="bib27" id="ref34">27</reflink>],[<reflink idref="bib28" id="ref35">28</reflink>]. Glycosylation traits such as fucosylation, galactosylation, bisection, sialylation, and the amount of sialic acid linked to a galactose residue (SA/gal) were calculated for the Fc glycosylation sites of each subclass. The level of IgG fucosylation was determined by dividing the sum of all fucosylated N-glycopeptide species (G0F, G1F, G2F, G1FN, G1FS, and G2FS) by the total of all glycan species. Galactosylation was calculated by using the formula (0.5 (G1F + G1FN + G1FS + G1) + G2F + G2FS + G2 + G2S / Σ (all glycan species)). Sialylation was determined as 0.5 *(G1FS + G2FS) + G2F1S2 / Σ (all glycan species). Bisection was calculated by dividing G1FN by the sum of all glycan species. G, F, N and S refer to specific glycan structures and modifications associated with N-glycopeptides of IgG antibodies. G (Galactose), F (Fucose), S (Sialic acid) and N (N-acetylglucosamine) followed by a number indicating how many galactose units are attached to the core of the glycan; G0: no galactose attached (agalactosylated), G1: one galactose residue attached (monogalactosylated). G2: two galactose residues attached (digalactosylated).</p> <hd id="AN0181944202-14">Acknowledgements</hd> <p>We thank all mothers and their families for participating in the study and the entire clinical and laboratory team involved (all field workers, lab technicians, nurses, and midwives) and Y.D. Mouwenda, E.M. Betouke-Ongwe for their advice. We are also grateful for the support of the CERMEL and PARA/LUMC staff.</p> <hd id="AN0181944202-15">Author contributions</hd> <p>Conceptualization: C.H.H., M.Y., M.E.; Data curation and formal analysis: Y.J.H., K.A.S.; Funding acquisition: M.E., A.A.A., P.G.K., M.Y.; Investigation: Y.J.H., D.L.N., T.V., A.O.K., A.vD.; Supervision: A.O.K., C.H.H., A.A.A., M.E., M.Y., M.W.; QC and Validation of Data: Y.J.H., A.vD, C.H.H., M.Y.; Writing – original draft: Y.J.H.; Writing – review &amp; editing: Y.J.H., M.Y., C.H.H., A.vD., D.L.N., K.A.S., M.W., A.A.A., P.G.K., M.E., A.O.K.; Statistics analysis: Y.J.H., K.A.S. All authors have read and approved the manuscript.</p> <hd id="AN0181944202-16">Funding</hd> <p>This research was funded by the German Federal Ministry of Education and Research (BMBF) [01KA1307]. Furthermore, we appreciate the support from the NWO Spinoza Prize (SPI.2021.004) awarded to MY. AAA is a member of the Central African Network for Tuberculosis, HIV/AIDS, and Malaria (CANTAM network) funded through EDCTP [EDCTP-RegNet 2015–1045]. The work was also supported by funding from the European Union [Project 101080784—WORMVACS2.0]. Views and opinions expressed are, however, those of the author(s) only and do not necessarily reflect those of the European Union or the European Health and Digital Executive Agency (HADEA). Neither the European Union nor the granting authority (HADEA) can be held responsible for them. The funders had no role in study design, data collection and analysis, the decision to publish, or the preparation of the manuscript.</p> <hd id="AN0181944202-17">Data availability</hd> <p>The datasets generated during and/or analyzed during the current study are available from the corresponding author upon reasonable request.</p> <hd id="AN0181944202-18">Declarations</hd> <p></p> <hd id="AN0181944202-19">Competing interests</hd> <p>The authors declare no competing interests.</p> <hd id="AN0181944202-20">Ethical consideration</hd> <p>All participants gave their written informed consent before their inclusion in the study. The study was conducted in accordance with the Declaration of Helsinki and was approved by the Institutional Ethical Committee of the CERMEL (CEI-CERMEL Nº13/2013).</p> <hd id="AN0181944202-21">Statistical consideration</hd> <p>The principal component analysis was performed on all available antibody glycosylation data measured in this study. As variables, we included the main derived traits on the different IgG isotypes, namely galactosylation, bisection, fucosylation and sialylation of IgG1, IgG2 and IgG3/IgG4. Lastly, these variables were scaled to unit variance. The percentage of glycan structures between samples was compared using an unmatched two-sample Wilcoxon test. The identified low/medium/high group of glycosylation for the different traits was based on splitting the values into three equal-sized quantiles for each sample type. To compare these quantiles over time, each sample origin (cord blood, child 9 months, child 12 months) was compared to the mother with Fischer's exact test for a 3 × 3 table. Using the 'stats' package, the statistical test was performed in R (4.3.1), and p-values &lt; 0.05 were considered statistically significant.</p> <hd id="AN0181944202-22">Supplementary Information</hd> <p>Graph: Supplementary Information.</p> <hd id="AN0181944202-23">Supplementary Information</hd> <p>The online version contains supplementary material available at https://doi.org/10.1038/s41598-024-83366-8.</p> <hd id="AN0181944202-24">Publisher's note</hd> <p>Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.</p> <ref id="AN0181944202-25"> <title> References </title> <blist> <bibl id="bib1" idref="ref1" type="bt">1</bibl> <bibtext> Abu-Raya B, Michalski C, Sadarangani M, Lavoie PM. Maternal immunological adaptation during normal pregnancy. Front. 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Hokke and Maria Yazdanbakhsh</p> <p>Reported by Author; Author; Author; Author; Author; Author; Author; Author; Author; Author; Author; Author</p> </aug> <nolink nlid="nl1" bibid="bib10" firstref="ref15"></nolink> <nolink nlid="nl2" bibid="bib11" firstref="ref16"></nolink> <nolink nlid="nl3" bibid="bib12" firstref="ref17"></nolink> <nolink nlid="nl4" bibid="bib13" firstref="ref18"></nolink> <nolink nlid="nl5" bibid="bib14" firstref="ref19"></nolink> <nolink nlid="nl6" bibid="bib15" firstref="ref20"></nolink> <nolink nlid="nl7" bibid="bib16" firstref="ref21"></nolink> <nolink nlid="nl8" bibid="bib17" firstref="ref22"></nolink> <nolink nlid="nl9" bibid="bib18" firstref="ref23"></nolink> <nolink nlid="nl10" bibid="bib19" firstref="ref24"></nolink> <nolink nlid="nl11" bibid="bib20" firstref="ref25"></nolink> <nolink nlid="nl12" bibid="bib21" firstref="ref27"></nolink> <nolink nlid="nl13" bibid="bib22" firstref="ref28"></nolink> <nolink nlid="nl14" bibid="bib23" firstref="ref29"></nolink> <nolink nlid="nl15" bibid="bib24" firstref="ref30"></nolink> <nolink nlid="nl16" bibid="bib25" firstref="ref31"></nolink> <nolink nlid="nl17" bibid="bib26" firstref="ref33"></nolink> <nolink nlid="nl18" bibid="bib27" firstref="ref34"></nolink> <nolink nlid="nl19" bibid="bib28" firstref="ref35"></nolink> CustomLinks: – Url: https://resolver.ebsco.com/c/xy5jbn/result?sid=EBSCO:edsdoj&genre=article&issn=20452322&ISBN=&volume=14&issue=1&date=20241201&spage=1&pages=1-9&title=Scientific Reports&atitle=Parasitic%20infections%20during%20pregnancy%20in%20Gabon%20affect%20glycosylation%20patterns%20of%20maternal%20and%20child%20antibodies&aulast=Yabo%20J.%20Honkpehedji&id=DOI:10.1038/s41598-024-83366-8 Name: Full Text Finder (for New FTF UI) (s8985755) Category: fullText Text: Find It @ SCU Libraries MouseOverText: Find It @ SCU Libraries – Url: https://doaj.org/article/bf911dd01aad4962ad3bd80ab5c67c8c Name: EDS - DOAJ (s8985755) Category: fullText Text: View record from DOAJ MouseOverText: View record from DOAJ
Header	DbId: edsdoj DbLabel: Directory of Open Access Journals An: edsdoj.bf911dd01aad4962ad3bd80ab5c67c8c RelevancyScore: 1063 AccessLevel: 3 PubType: Academic Journal PubTypeId: academicJournal PreciseRelevancyScore: 1063.04321289063
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Items	– Name: Title Label: Title Group: Ti Data: Parasitic infections during pregnancy in Gabon affect glycosylation patterns of maternal and child antibodies – Name: Author Label: Authors Group: Au Data: <searchLink fieldCode="AR" term="%22Yabo+J%2E+Honkpehedji%22">Yabo J. Honkpehedji</searchLink><br /><searchLink fieldCode="AR" term="%22Anna+O%2E+Kildemoes%22">Anna O. Kildemoes</searchLink><br /><searchLink fieldCode="AR" term="%22Koen+A%2E+Stam%22">Koen A. Stam</searchLink><br /><searchLink fieldCode="AR" term="%22Dieu+L%2E+Nguyen%22">Dieu L. Nguyen</searchLink><br /><searchLink fieldCode="AR" term="%22Tom+Veldhuizen%22">Tom Veldhuizen</searchLink><br /><searchLink fieldCode="AR" term="%22Angela+van+Diepen%22">Angela van Diepen</searchLink><br /><searchLink fieldCode="AR" term="%22Meral+Esen%22">Meral Esen</searchLink><br /><searchLink fieldCode="AR" term="%22Peter+G%2E+Kremsner%22">Peter G. Kremsner</searchLink><br /><searchLink fieldCode="AR" term="%22Manfred+Wuhrer%22">Manfred Wuhrer</searchLink><br /><searchLink fieldCode="AR" term="%22Ayôla+A%2E+Adegnika%22">Ayôla A. Adegnika</searchLink><br /><searchLink fieldCode="AR" term="%22Cornelis+H%2E+Hokke%22">Cornelis H. Hokke</searchLink><br /><searchLink fieldCode="AR" term="%22Maria+Yazdanbakhsh%22">Maria Yazdanbakhsh</searchLink> – Name: TitleSource Label: Source Group: Src Data: Scientific Reports, Vol 14, Iss 1, Pp 1-9 (2024) – Name: Publisher Label: Publisher Information Group: PubInfo Data: Nature Portfolio, 2024. – Name: DatePubCY Label: Publication Year Group: Date Data: 2024 – Name: Subset Label: Collection Group: HoldingsInfo Data: LCC:Medicine<br />LCC:Science – Name: Subject Label: Subject Terms Group: Su Data: <searchLink fieldCode="DE" term="%22Antibody%22">Antibody</searchLink><br /><searchLink fieldCode="DE" term="%22Glycosylation%22">Glycosylation</searchLink><br /><searchLink fieldCode="DE" term="%22Parasitic+infections%22">Parasitic infections</searchLink><br /><searchLink fieldCode="DE" term="%22Pregnancy%22">Pregnancy</searchLink><br /><searchLink fieldCode="DE" term="%22Child%22">Child</searchLink><br /><searchLink fieldCode="DE" term="%22Gabon%22">Gabon</searchLink><br /><searchLink fieldCode="DE" term="%22Medicine%22">Medicine</searchLink><br /><searchLink fieldCode="DE" term="%22Science%22">Science</searchLink> – Name: Abstract Label: Description Group: Ab Data: Abstract Antibody glycosylation patterns can affect antibody functionality and thereby contribute to protection against invading pathogens. During pregnancy, maternal antibodies can be transferred through the placenta and contribute to modulating both the mother’s and her child’s immune responses. Although several studies of IgG glycosylation during pregnancy have been carried out, very few cohorts studied were from sub-Saharan Africa, where exposure to microorganisms and parasites is high. In Lambaréné, Gabon, 106 pregnant women in their third trimester were enrolled into this study. At enrolment, urine, stool, and blood samples were collected from the mothers to assess Schistosoma haematobium (S. haematobium), Plasmodium falciparum (P. falciparum) and other parasite infections. During delivery, cord blood samples were collected. The children were followed, and blood samples were collected at 9 and 12 months of age. IgG Fc glycosylation was measured by liquid chromatography-mass spectrometry, determining fucosylation, galactosylation, sialylation, bisection, and sialylation per galactose (SA/gal). Among the 106 pregnant women, 33 (31%) were infected by at least one parasite. The antibody glycosylation patterns in maternal and cord blood showed distinct profiles when compared to that of infants at 9 and 12 months. IgG galactosylation was higher in maternal/cord blood, while fucosylated IgG was higher in children up to 1 year of age. Maternal parasitic infection was associated with lower IgG2 and IgG3/IgG4 galactosylation in cord blood and lower IgG3/IgG4 galactosylation in children. When maternal IgG galactosylation and, consequently, cord blood were categorized as high, children at 9 and 12 months of age showed higher IgG galactosylation compared to children of mothers with low IgG galactosylation. As IgG Fc galactosylation can have functional consequences, it might provide valuable information for developing effective preventive and treatment strategies for vulnerable populations. – Name: TypeDocument Label: Document Type Group: TypDoc Data: article – Name: Format Label: File Description Group: SrcInfo Data: electronic resource – Name: Language Label: Language Group: Lang Data: English – Name: ISSN Label: ISSN Group: ISSN Data: 2045-2322 – Name: NoteTitleSource Label: Relation Group: SrcInfo Data: https://doaj.org/toc/2045-2322 – Name: DOI Label: DOI Group: ID Data: 10.1038/s41598-024-83366-8 – Name: URL Label: Access URL Group: URL Data: <link linkTarget="URL" linkTerm="https://doaj.org/article/bf911dd01aad4962ad3bd80ab5c67c8c" linkWindow="_blank">https://doaj.org/article/bf911dd01aad4962ad3bd80ab5c67c8c</link> – Name: AN Label: Accession Number Group: ID Data: edsdoj.bf911dd01aad4962ad3bd80ab5c67c8c
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RecordInfo	BibRecord: BibEntity: Identifiers: – Type: doi Value: 10.1038/s41598-024-83366-8 Languages: – Text: English PhysicalDescription: Pagination: PageCount: 9 StartPage: 1 Subjects: – SubjectFull: Antibody Type: general – SubjectFull: Glycosylation Type: general – SubjectFull: Parasitic infections Type: general – SubjectFull: Pregnancy Type: general – SubjectFull: Child Type: general – SubjectFull: Gabon Type: general – SubjectFull: Medicine Type: general – SubjectFull: Science Type: general Titles: – TitleFull: Parasitic infections during pregnancy in Gabon affect glycosylation patterns of maternal and child antibodies Type: main BibRelationships: HasContributorRelationships: – PersonEntity: Name: NameFull: Yabo J. Honkpehedji – PersonEntity: Name: NameFull: Anna O. Kildemoes – PersonEntity: Name: NameFull: Koen A. Stam – PersonEntity: Name: NameFull: Dieu L. Nguyen – PersonEntity: Name: NameFull: Tom Veldhuizen – PersonEntity: Name: NameFull: Angela van Diepen – PersonEntity: Name: NameFull: Meral Esen – PersonEntity: Name: NameFull: Peter G. Kremsner – PersonEntity: Name: NameFull: Manfred Wuhrer – PersonEntity: Name: NameFull: Ayôla A. Adegnika – PersonEntity: Name: NameFull: Cornelis H. Hokke – PersonEntity: Name: NameFull: Maria Yazdanbakhsh IsPartOfRelationships: – BibEntity: Dates: – D: 01 M: 12 Type: published Y: 2024 Identifiers: – Type: issn-print Value: 20452322 Numbering: – Type: volume Value: 14 – Type: issue Value: 1 Titles: – TitleFull: Scientific Reports Type: main
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