Maternal Multiple Sclerosis and Health Outcomes Among the Children: A Systematic Review

Figures & data

Figure 1 Search strategy and flowchart of exclusion and inclusion of studies.

Table 1 Maternal Multiple Sclerosis and the Effect on Neonatal Outcomes

First Author, Country, Year	Study Design	Population	Maternal MS Exposure, n	Reference Group, n	Neonatal Outcomes	Adjusted For Confounders	Main Results	Overall Conclusion	NOS Score
Andersen, Denmark, 2021^Citation24	Cohort study	Population-based, including all births from 1997–2016 from Danish registries and databases	2930 (live and still births, 70% without DMT)	56,958 (live and still births, 5% random sample from general population)	Preterm birth, SGA, low Apgar, CAs, “signs of asphyxia”, stillbirth^a	Yes: Prior abortion, prior cesarean section, maternal age, year of birth, parity, educational level	Low Apgar OR 0.90 (95% CI 0.56–1.44), signs of asphyxia OR 0.87 (95% CI 0.78–0.97), stillbirth OR 1.17 (95% CI 0.68–2.00), CAs OR 1.02 (95% CI 0.87–1.19), SGA OR 1.29 (95% CI 1.04–1.60), preterm birth OR 1.12 (95% CI 0.95–1.33)	Higher prevalence of infants being SGA and lower prevalence of “signs indicating asphyxia” in the study cohort	Selection: **** Comparability: * Outcome: *** 8 points
Soler, Chile, 2021^Citation13	Cohort study	Questionnaire study with clinical data, pre-MS and post-MS patients, Programa de Esclerosis Multiple UC	76 (pregnancies post-MS diagnosis)	223 (pregnancies pre-MS diagnosis)	MCAs	No	MCAs (n=1 in post-MS, n=5 in pre-MS) OR 0.66 (95% CI 0.3–1.4)	No firm conclusions can be drawn	Selection: *** Comparability: Outcome: * 4 points
Mueller, USA (Washington), 2002^Citation36	Cohort study	ICD codes from 1987–1996 hospital data from Washington	198 (with/without DMT not described, they were older, more often married, with more education, more insurance)	1584 (randomly selected from the birth cohort in Washington, frequency-matched on year of delivery)	Birth weight, SGA, low Apgar, CAs, infant death, fetal distress, preterm birth, length of infant’s hospitalization	Yes: Maternal age	Birth weight <2500 g RR 0.9 (95% CI 0.5–1.7), preterm birth RR 0.9 (95% CI 0.5–1.5), low Apgar RR 0.8 (95% CI 0.2–2.5) hospital stay 4–6 days RR 1.5 (95% CI 0.9–2.3), CAs RR 0.6 (95% CI 0.1–2.3), infant death RR 1.1 (95% CI 0.3–5.1)	No firm conclusions can be drawn	Selection: *** Comparability: * Outcome: * 5 points
Goldacre, UK (Oxford), 2017^Citation32	Cohort study	Mother–child record linkage 1970–1989 on 850,000 people (part of the Oxford Record Linkage Study) – maternity dataset	181 (with/without DMT not described, MS mothers were in higher social class)	244,573 (without MS)	Birth weight, SGA, gestational age, Apgar 1 and 5 min, preterm birth, stillbirth	Yes: Maternal age, year of birth	Birth weight <2000 g, n=5, OR 2.7 (95% CI 1.1–6.6), SGA OR 1 (95% CI 0.6–1.8), preterm birth OR 0.9 (95% CI 0.4–2.1) Apgar 1/1–7 OR 1.9 (95% CI 0.9–3.7), no difference in 5 minutes Apgar, no stillbirths	Increased risk of low birth weight <2000 g (n=5)	Selection: **** Comparability: * Outcome: ** 7 points
Dahl, Norway, 2008^Citation25	Cohort study	Norwegian registries and databases, 1967–2002	308 (women with MS, no DMT or steroids)	1910 (women with pre-MS, prior to year of onset)	Preterm birth, SGA, low birth weight <2500 g, CAs, perinatal mortality	Yes: Maternal age and time period, when relevant adjusted for gestational week	Preterm birth OR 1.15 (95% CI 0.92–1.45), low birth weight <2500 g OR 1.13 (95% CI 0.86–1.47), SGA OR 1.20 (95% CI 0.99–1.45), no difference in perinatal mortality and CAs (results not available)	No firm conclusions can be drawn	Selection: **** Comparability: * Outcome: ** 7 points
Dahl, Norway, 2005^Citation11	Cohort study	Medical birth registry of Norway, 1967–2002 – with MS diagnosis noted	649 (including 45 women/59 births where MS diagnosis was not noted in a consecutive birth)	2,102,430 pregnancies from general population)	SGA, birth weight, preterm, CAs, perinatal mortality	Yes: Maternal age and time period	SGA OR 1.45 (95% CI 1.14–1.84). SGA in term births only OR 1.61 (95% CI 1.26–2.05), no difference in perinatal mortality and CAs (results not available)	Increased risk of SGA in MS group	Selection: *** Comparability: * Outcome: ** 6 points
Chen, Taiwan, 2009^Citation12	Cohort study	Birth certificate registry and Taiwan National Health Insurance research dataset, 2001–2003	174 (only MS, no other diseases, mostly without medical treatment)	1392 (age-matched from birth register, no diseases)	Low birth weight <2500 g, preterm birth, SGA	Yes: Sex of the child, parity, maternal age, highest maternal and paternal educational levels, parental age difference, mother’s marital status, family monthly income	Preterm birth OR 2.25 (95% CI 1.37–3.70), SGA OR 1.89 (95% CI 1.29–2.70)	Higher odds of preterm birth and SGA in MS cohort	Selection: *** Comparability: * Outcome: * 5 points
Weber-Schoendorfer, Germany, 2009^Citation37	Cohort study	TIS, Berlin, structured questionnaire survey, 1996–2007	64 (MS, no DMT, some had glucocorticoids for relapse)	1556 (no MS, exposed to other known non-teratogenic drugs)	Preterm birth, MCAs	Yes: Birth weights adjusted for maternal age, gestational age at delivery, smoking, sex of the newborn, exposure to glucocorticoids	Preterm birth OR 2.43 (95% CI 0.96–5.4), MCAs OR 3.34 (95% CI 0.62–11.55) – syndromes and elective terminations excluded, 3 cases of MCAs in study group	No firm conclusions can be drawn	Selection: *** Comparability: * Outcome: ** 6 points
Fong, USA, 2018^Citation38	Cohort study	Health discharge data from general hospital in California, 2001–2009, ICD-9 codes	1185 (MS, DMT not described, significantly higher rate of private insurance (77% vs 49%) and comorbidity in study group)	4,422,864 (without MS)	Preterm birth, fetal demise (not clearly defined)	Yes: Maternal age, ethnicity, insurance type, comorbidities	Preterm birth OR 1.2 (95% CI 0.9–1.5), fetal demise OR 1.6 (95% CI 0.9–3.1)	No firm conclusions can be drawn	Selection: *** Comparability: * Outcome: ** 6 points
MacDonald, USA, 2019^Citation14	Cohort study	THS claims and NIS data, commercially insured population, 2011–2015	NIS 2436 THS 1439 (MS, unknown medication status)	NIS 4,1184,380 (no MS), THS 1,101,165 (no MS)	Preterm birth, IUGR, stillbirth, MCAs	Yes: Maternal age, delivery region, year of delivery, insurance type	Preterm birth RR THS 1.19 (95% CI 1.04–1.35), RR NIS 1.30 (95% CI 1.16–1.44); IUGR RR THS 1.03 (95% CI 0.87–1.19), RR NIS 1.23 (95% CI 0.94–1.54); stillbirth RR THS 0.82 (95% CI 0.23–1.52), RR NIS 0.96 (95% CI 0.5–1.48); MCAs RR THS 0.85 (95% CI 0.59–1.12)	Women with MS have elevated RR of preterm delivery in both of the MS cohorts	Selection: *** Comparability: * Outcome: ** 6 points

Notes: 0–9 points. *= 1 point, **= 2 points, ***= 3 points, ****= 4 points. ^aBased on Apgar parameters and umbilical cord blood samples.

Abbreviations: NOS, Newcastle–Ottawa quality assessment Scale for cohort studies; DMT, disease-modifying treatment; SGA, small for gestational age; low Apgar, 5-minute Apgar score <7; CAs, congenital anomalies, MCAs, major congenital anomalies; MS, multiple sclerosis; TIS, Teratology Information Service; THS, Truven Health Market Scan database; NIS, Nationwide Inpatient Sample; IUGR, intrauterine growth retardation.

Table 2 Women with Multiple Sclerosis Treated with Disease-Modifying Treatment and the Effect on Neonatal Outcomes

First Author, Country, Year	Study Design	Population	Type of Medication	Maternal MS + DMT Exposure, n	Reference Group, n	Neonatal Outcomes	Adjusted for Confounders	Main Results (95% CI)	Overall Conclusion	NOS Score
Weber-Schoendorfer, Germany, 2009^Citation37	Cohort study	TIS, Berlin; structured questionnaire survey, controls without MS who have contacted TIS with question about medicine, 1996–2007	GA, IFNβ1a, IFNβ1b	GA=31 IFNβ1a=48 IFNβ1b=21, mostly exposed in 1st trimester	Ref 1: 64 (MS, no DMT), Ref 2: 1557 (non-MS)	CAs, preterm birth, stillbirth	Not in the outcome of interest	MS+GA vs non-MS: preterm birth OR 0.59 (95% CI 0.01–3.74), all CAs OR 1.28 (95% CI 0.14–5.3), MCAs OR 4.99 (95% CI 0.54–22.19)	No firm conclusions can be drawn	Selection: *** Comparability: * Outcome: ** 6 points
Amato, Italy, 2010^Citation30	Cohort study	Enrolled from 21 nationwide main MS clinics; questionnaire study, 2002–2008	IFNβ	75 (MS + IFNβ administered <4 weeks prior to conception)	287 (MS and previous >4 weeks discontinuation of IFNβ or never treated)	Preterm birth	Yes: Age, educational level, disease duration, EDSS, previous pregnancy and abortion, smoking, alcohol or substances, gestational age, CS, sex of the child	IFNβ exposure as a predictor of preterm birth, OR 2.11 (95% CI 1.18–3.78)	IFNβ exposure is significantly related to preterm birth	Selection: **** Comparability: ** Outcome: *** 9 points
Herbstritt, Germany, 2016^Citation28	Cohort study	German pregnancy MS registry; telephone interviews every 3 months or visit to the outpatient clinic in Bochum, 2008–2013	GA	151	95 “MS, not exposed to DMT in pregnancy”)	CAs, preterm birth, low birth weight	Yes: Age, disease duration. BMI, smoking, relapse, steroid use, gestational week	CAs OR 0.3 (95% CI 0.07–1.23), MCAs OR 0.2 (95% CI 0.04–1.01), preterm birth OR 0.54 (95% CI 0.23–1.29)	No firm conclusions can be drawn	Selection: *** Comparability: ** Outcome: * 6 points
Thiel, Germany, 2016^Citation29	Cohort study	German pregnancy MS registry; telephone interviews every 3 months or visit to the outpatient clinic in Bochum, 2008–2013	IFNβ	251	194 “MS, not exposed to DMT in pregnancy”	Mean birth weight and length, preterm birth, CAs	Yes: Age, BMI, smoking, steroid use, relapses, sex of the child	MCAs: OR 0.53 (95% CI 0.2–1.41), preterm birth OR 0.6 (95% CI 0.29–1.22), SGA OR 0.77 (95% CI 0.26–2.22)	No firm conclusions can be drawn	Selection: **** Comparability: ** Outcome: *** 9 points
Portaccio, Italy, 2018^Citation31	Cohort study	Neurological service of 19 hospitals, standardized information forms, 2009–2015 and 2002–2008	NZB, IFNβ	NZB exposed n= 69, IFN exposed n=88	341 (318 unexposed or exposed to DMT injectable therapy, 23 previously exposed to NZB)	CAs, preterm birth, birth weight and length	Yes: Maternal age, disease duration, educational level, previous pregnancies and abortions, smoking, alcohol or substance exposure, gestational age, sex of the child	Preterm birth OR 2.1 (95% CI 1.2–3.7) between IFNβ-exposed and reference group; ratios of CAs not reported due to low numbers	Higher risk of preterm birth in IFNβ-exposed group	Selection: **** Comparability: ** Outcome: *** 9 points
MacDonald, USA, 2019^Citation14	Cohort study	THS, claims; commercially insured population, 2011–2015	GA, IFNβ, NZBDF, FLM	Overall women with MS and DMT n=574, GA n=225, IFNβ n=118, NZB n=39, DF n=19, FLM n=18	1075 (women with MS, no DMT)	Preterm birth, IUGR, CAs	Yes: Age, delivery region, year of delivery, pre-pregnancy relapses	Overall DMT exposure: preterm birth RR 1.22 (95% CI 0.9–1.64), IUGR RR 0.93 (95% CI 0.62–1.38), MCAs RR 1.49 (95% CI 0.7–3.0)	No firm conclusions can be drawn	Selection: **** Comparability: * Outcome: ** 7 points
Korjagina, Finland, 2021^Citation27	Cohort study	Finnish and Swedish registries and databases, 2005–2014 and 1996–2014	IFNβ	718 (MS + only IFNβ), stratified for duration of treatment before pregnancy: <2 years, 3–5 years, >5 years	1397 (MS and no DMT)	“Serious adverse pregnancy outcomes”, MCAs^a	Yes: Performed if the prevalence results indicated modified effect of IFNβ in specific strata	“Serious adverse pregnancy outcomes”, treated >5 years OR 1.68 (95% CI 0.63–4.48), MCAs, treated >5 years OR 1.93 (95% CI 0.66–5.66)	No firm conclusions can be drawn	Selection: **** Comparability: ** Outcome: *** 9 points
Andersen, Denmark, 2022^Citation39	Cohort study	Danish registries and databases, 2013–2018	TFL	28	364 (matched from background population)	Low Apgar, preterm birth, SGA, CAs	Yes: Prior abortion, prior CS, parity, education	“Any adverse outcome” OR 1.03 (95% CI 0.5–2.13)^b	No firm conclusions can be drawn	Selection: **** Comparability: * Outcome: *** 8 points
Andersen, Denmark, 2023^Citation18	Cohort study	Danish registries and databases, 1997–2018	GA IFNβ NZB DF	1009	1073 (women with MS, no DMT)	Preterm birth, SGA, low Apgar, CAs, stillbirth, any adverse event	Yes: Prior abortion, maternal age, education, prior CS, calendar year of birth	Any adverse event 1.05 (95% CI 0.84–1.30), preterm birth OR 1.1 (95% CI 0.72-1.72), SGA OR 1.32 (95% CI 0.75-2.33), APGAR <7 n/a, CAs OR 1.59 (95% CI 0.88-2.86)	No firm conclusions can be drawn	Selection: **** Comparability: * Outcome: *** 8 points

Notes: 0–9 points. *= 1 point, **= 2 points, ***= 3 points, ****= 4 points. ^a”Serious adverse pregnancy outcomes” include elective terminations of pregnancy due to fetal anomaly, live births with MCAs and stillbirths, ^b”Any adverse outcome” includes low Apgar score, preterm birth, small for gestational age, congenital anomalies and stillbirth.

Abbreviations: NOS, Newcastle-Ottawa quality assessment Scale for cohort studies; TIS, Teratology Information Service; MS, multiple sclerosis; GA, glatiramer acetate; IFNβ_1a, interferon-beta 1a; IFNβ_1b, interferon-beta 1b; DMT, disease-modifying treatment; CAs, congenital anomalies, MCAs, major congenital anomalies; EDSS, Expanded Disability Status Scale; CS, cesarean section; NZB, natalizumab; DF, dimethyl fumarate; FLM, fingolimod; IUGR, intrauterine growth restriction; TFL, teriflunomide.

Table 3 In Utero Exposure to Maternal Multiple Sclerosis Health Outcomes During Childhood and Adolescence (1 Month to 18 Years)

First Author, Country, Year	Study Design	Population	Maternal MS Exposure, n	Reference Group, n	Outcome, n	Adjusted for Confounders	Main Results	Overall Conclusion	NOS Score
Andersen, Denmark, 2018^Citation40	Cohort study	Danish registries and databases, 1996–2002; proxies/data from questionnaires filled out by parents and teacher, when children aged 11 years	N=40 for total difficulties (subgroup 1), n=17 for mental disorders (subgroup 2)	16,829 (subgroup 1), 42,016 (subgroup 2)	Any psychiatric diagnoses (subgroup 1), total difficulties (subgroup 2)	Yes: Sex of the child, social status of the mother	Subanalysis 1: total difficulties OR 0.91 (95% CI 0.41–1.98); subanalysis 2: any psychiatric disorder OR 0.63 (95% CI 0.21–1.72)	No firm conclusions can be drawn	Selection: *** Comparability: * Outcome: ** 6 points
Strom, Norway, 2021^Citation26	Cohort study	Norwegian registries and databases 1990–2012, children who survived to 2 years of age; information on maternal MS from the birth registry and CP diagnoses among children were obtained from the insurance scheme and the patient registry	n=1100 (children exposed to maternal MS)	1,360,149 (background population)	Cerebral palsy	Yes: Year of birth, maternal disease status in the birth registry, maternal age, education and single motherhood	Cerebral palsy RR 1.8 (95% CI 0.8–4.4)	No firm conclusions can be drawn	Selection: *** Comparability: * Outcome: *** 7 points
Razaz, Canada, 2016^Citation33	Cohort study	Canadian registries and databases, British Columbia, 1994–2006	543 (50% of children exposed during pregnancy)	2211 (matched reference group)	EDI measurements	Yes: Parental mental comorbidity, parental physical comorbidity, the duration of parental MS, parental disability level	Vulnerability on one or more domains of the EDI OR 0.75 (95% CI 0.60–0.95)	Lower risk of vulnerability among children of women with MS	Selection: **** Comparability: * Outcome: *** 8 points
Razaz, Canada, 2016^Citation34	Cohort study	Canadian registries and databases, British Columbia, 1985 −2011	727 (not all of these children were exposed during pregnancy)	2916 (matched reference group)	Mood or anxiety disorders in children^a	Yes: Socio-economic status, parental mental morbidity, parental physical morbidity, parental sex	HR 1.7 (95% CI 1.1–2.4), adjusted HR 1.4 (95% CI 0.9–2.1)	Children of mothers with MS had higher rates of mood or anxiety disorders; adjustment for mental health morbidity in mothers diminished the association	Selection: **** Comparability: * Outcome: *** 8 points

Notes: 0–9 points. *= 1 point, **= 2 points, ***= 3 points, ****= 4 points. Childhood development measured via teacher reports every 1–3 years from 5 years of age. 104 binary and three-category items designed to tap five core areas of early childhood development. ^aRanged from poor adjustment reactions and anxiety state to phobic disorders, obsessive–compulsive disorders, affective psychoses and neurotic depression.

Abbreviations: NOS, Newcastle–Ottawa quality assessment Scale for cohort studies; MS, multiple sclerosis; EDI, Early Development Instrument.

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