Original Article

Prevention of the First Occurrence of Neural-Tube Defects by Periconceptional Vitamin Supplementation

Andrew E. Czeizel, M.D., D.Sc., and István Dudás, M.D.

N Engl J Med 1992; 327:1832-1835December 24, 1992

Abstract

Abstract

Background.

The risk of recurrent neural-tube defects is decreased in women who take folic acid or multivitamins containing folic acid during the periconceptional period. The extent to which such supplementation can reduce the first occurrence of defects is not known.

Full Text of Background....

Methods.

We conducted a randomized, controlled trial of periconceptional multivitamin supplementation to test the efficacy of this treatment in reducing the incidence of a first occurrence of neural-tube defects. Women planning a pregnancy (in most cases their first) were randomly assigned to receive a single tablet of a vitamin supplement (containing 12 vitamins, including 0.8 mg of folic acid; 4 minerals; and 3 trace elements) or a trace-element supplement (containing copper, manganese, zinc, and a very low dose of vitamin C) daily for at least one month before conception and until the date of the second missed menstrual period or later.

Full Text of Methods....

Results.

Pregnancy was confirmed in 4753 women. The outcome of the pregnancy (whether the fetus or infant had a neural-tube defect or congenital malformation) was known in 2104 women who received the vitamin supplement and in 2052 who received the trace-element supplement. Congenital malformations were significantly more prevalent in the group receiving the trace-element supplement than in the vitamin-supplement group (22.9 per 1000 vs. 13.3 per 1000, P = 0.02). There were six cases of neural-tube defects in the group receiving the trace-element supplement, as compared with none in the vitamin-supplement group (P = 0.029). The prevalence of cleft lip with or without cleft palate was not reduced by periconceptional vitamin supplementation.

Full Text of Results....

Conclusions.

Periconceptional vitamin use decreases the incidence of a first occurrence of neural-tube defects. (N Engl J Med 1992;327:1832–5.)

Full Text of Conclusions....

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Media in This Article

Table 1Pregnancies in the Study Groups, According to Course of Supplementation.

Table 2Demographic Characteristics and Outcomes of Pregnancy in the Study Groups.

Article Activity

711 articles have cited this article

Article

THERE is considerable evidence that the periconceptional administration of multivitamin supplements1 , 2 or a folic acid supplement alone3 4 5 prevents recurrent neural-tube defects. However, about 95 percent of the women who deliver infants with neural-tube defects have not previously delivered infants with these defects. Several observational studies have indicated the efficacy of such supplementation in the prevention of neural-tube defects,6 7 8 9 although one study reported no effect.10 We undertook this trial to determine whether periconceptional vitamin supplementation can reduce the incidence of a first occurrence of neural-tube defects.

Methods

Subjects

Women planning a pregnancy who satisfied the following criteria were eligible for participation in the Hungarian Family Planning Program trial begun in 1984: they did not have delayed conception or infertility, they were not currently pregnant, and their participation was voluntary. During the first four years of the trial there were two other criteria: an age of less than 35 years folder women were referred to the genetic-counseling clinic) and no previous wanted pregnancy (induced abortion was not a reason for exclusion).

Study Design

The study design11 involved three steps performed or supervised by qualified nurses: a checkup of reproductive health; a three-month preparation for conception, including vitamin or trace-element supplementation and contraception; and protection of very early pregnancy with immediate prenatal care. At the first visit, the criteria for eligibility were reviewed, and eligible women were informed about the purpose of the trial, including supplement use, and were asked whether they agreed to random assignment to receive either supplement. The women were then asked to give written informed consent and to stop taking any other vitamins.

The women entering the study were randomly assigned to receive a vitamin supplement (Elevit Pronatal, Hoffmann—LaRoche) or trace-element supplement as a single tablet each day for at least one month before the planned conception. The women were asked to note that they had taken the tablet each day on a form used to record their basal body temperature, and to leave unused tablets in the box. The vitamin supplement contained 6000 IU of vitamin A until the end of 1989 and 4000 IU thereafter, 1.6 mg of vitamin B₁, 1.8 mg of vitamin B₂, 19 mg of nicotinamide, 2.6 mg of vitamin B₆, 4 μg of vitamin B₁₂, 100 mg of vitamin C, 500 IU of vitamin D, 15 mg of vitamin E, 10 mg of calcium pantothenate, 0.2 mg of biotin, 0.8 mg of folic acid, 125 mg of calcium, 125 mg of phosphorus, 100 mg of magnesium, 60 mg of iron, 1 mg of copper, 1 mg of manganese, and 7.5 mg of zinc. The trace-element supplement contained 1 mg of copper, 1 mg of manganese, 7.5 mg of zinc, and 7.5 mg of vitamin C.

At the second visit, three months later, the women were supplied with tablets for the next three months, advised to attempt to achieve conception within this period, and asked to return immediately after the first missed menstrual period. The purpose of the third visit was to confirm pregnancy with a sensitive serum pregnancy test if the woman had missed a menstrual period. Pregnancy was also confirmed by ultrasonography within two weeks after a positive serum pregnancy test. Tablets were supplied until the third month of gestation. If a woman had not conceived within this three-month period, she was given an additional three-month supply of supplement.

All deliveries and terminations of pregnancy took place in obstetrical inpatient clinics. All the informative pregnancies (those involving fetuses with prenatally diagnosed conditions that were aborted in the second trimester, stillborn fetuses, and liveborn infants) of the women were evaluated with particular attention to the appropriate diagnosis or description of congenital malformations. The women completed summaries of the outcome of their pregnancies, including the date of delivery; sex, weight, and gestational age; and the presence or absence of congenital defects. The results were reviewed and confirmed by their physicians, who sent the summaries to the study staff.

Evaluation

Compliance in taking the study supplements was verified by questioning, by checking the records of basal body temperature, and by counting unused tablets when the boxes were returned. Information regarding possible side effects was also obtained at the second and later visits.

Women who received a full course of a supplement were defined as those who took the supplement for 28 days before conception and at least until the date of the second missed menstrual period. Women who did not take the supplement on any one day during this time were also classified as having received a full course. Women who received a partial course of a supplement were defined as those who failed for more than one day to take the supplement during the periconceptional period (in general, these women failed to take the supplement for only a few days). Women who conceived before or during the first month of administration were considered not to have received a supplement.

Considerable effort was made to ensure that information about outcome was obtained for all the women with confirmed pregnancies. If a completed summary was not received within one month after the expected date of delivery, a letter was mailed to the woman asking her to send the completed summary or a hospital-discharge summary. If there was no response, one of the study staff members visited the woman at home. If the woman could not be contacted in this way, she was considered to have dropped out of the study. In cases of terminated pregnancy, stillbirth, and neonatal death, we reviewed the hospital records and autopsy reports. Finally, the data concerning congenital malformations were evaluated by an independent data-monitoring group every six months. According to the definitions established by this group, neural-tube defects included anencephaly, iniencephaly, encephalocele, spina bifida cystica, and their combinations and secondary consequences (e.g., hydrocephalus or clubfoot). Spinal dysraphism was excluded because of the difficulties of diagnosis in the perinatal period, as was spina bifida occulta. Patients with genetically determined syndromes, including those involving neural-tube defects (e.g., Meckel's syndrome or Patau's syndrome) were excluded.

After receiving a report of a neural-tube defect, we obtained as much clinical and pathological information as possible, including any ultrasound films and a detailed physician's description (e.g., an autopsy report, a written report from the examining physician, or a discharge summary). Cases involving obvious or suspected neural-tube defects were reviewed by a group of external experts.

The randomization code was broken twice. At the end of 1989 there was an official request to assess the possible teratogenic effect of vitamin A, which was a component of the vitamin supplement. No teratogenic effect was found.12 The second occasion was at the end of 1991, after the completion of the study.

We assessed cases with single and multiple congenital malformations separately13 in our statistical analysis, using two-tailed chi-square and Fisher's exact tests.

Results

Of 7540 women who entered the study, pregnancy was confirmed in 4753 (Table 1Table 1Pregnancies in the Study Groups, According to Course of Supplementation.). The outcome of pregnancy could not be determined in 49 women because of untraceable addresses or because they had moved abroad. Thus, the outcome of pregnancy was evaluated in 99.0 percent of the women who became pregnant.

In our final analysis, we evaluated all the results in the women in both study groups. The outcomes of all the pregnancies are shown in Table 2Table 2Demographic Characteristics and Outcomes of Pregnancy in the Study Groups.. Pregnancy was terminated during the first trimester in eight women. The reasons were family problems in six (mainly divorce) and medical problems in two (acute infectious disease in one and unipolar depression with lithium treatment in the other).

We defined informative pregnancies as those in which it was known whether the fetus or infant had a neural-tube defect or other congenital malformation (minor anomalies were excluded). The prevalence of cases with a congenital malformation was significantly higher in the group receiving the trace-element supplement (22.9 per 1000) than in the vitamin-supplement group (13.3 per 1000, P = 0.02). Demographic factors were similar in the two groups (Table 2).

The distribution of cases with congenital malformations (as defined by the International Classification of Diseases, 9th Revision) is shown in Table 3Table 3Congenital Malformations, According to Study Group.. There were no neural-tube defects among the 2104 informative pregnancies in the vitamin-supplement group, as compared with six cases of neural-tube defects among the 2052 pregnancies in the group receiving the trace-element supplement. Among these six cases there were four anencephalic fetuses, two with lumbal or thoracal rachischisis, whose condition was diagnosed prenatally, one fetus with spina bifida cystica with hydrocephalus and rib defects, and one fetus with lumbosacral spina bifida. (The cases of spina bifida were not identified by maternal alpha-fetoprotein screening and ultrasonography.) Of the six mothers, one was considered not to have received the trace elements, two to have received a partial course, and three to have received a full course. The expected number of cases of neural-tube defects was 5.7, based on previous records in Hungary.14 The difference in the incidence of neural-tube defects in the two study groups was significant (P = 0.029 by Fisher's exact test). None of the mothers whose fetuses or infants had neural-tube defects had taken valproic acid or other known teratogens, nor did they have a family history of neural-tube defects.

In the category of multiple congenital malformations (i.e., two or more defects in a single fetus or infant),13 two fetuses were suspected of having a neural-tube defect as one of the malformations. A macerated female stillborn fetus with bilateral cleft lip, cleft palate, spina bifida occulta, talipes equinovarus, and a weight of 1200 g at the 36th week of gestation was delivered by a woman in the vitamin-supplement group. Another fetus with a prenatal diagnosis of ureteral obstruction, hydronephrosis, Type IV multicystic kidneys, and exencephalic or microcephalic-like cranium was delivered by a woman in the group receiving the trace-element supplement. The various malformations in these fetuses were not considered to be manifestations of a neural-tube defect.

Discussion

The results of this trial indicate that periconceptional vitamin supplementation reduced the incidence of a first occurrence of neural-tube defects. The nutritional status of the women was good; their daily energy intake was estimated to be 2665 to 3040 kcal, and their intake of folic acid about 180 μg. We have previously found this form of periconceptional vitamin supplementation to be safe.15

Is it possible that the efficacy of this intervention differs in the prevention of first and recurrent neural-tube defects? In Hungary, the overall prevalence of isolated neural-tube defects is 2.8 per 1000 births14; the risks of recurrence after one, two, and three affected infants are 3 percent, 12 percent, and 25 percent, respectively.16 The vitamin supplement we used contained 0.8 mg of folic acid, whereas the supplements used in other studies, all of which were designed to prevent recurrences, were 4.0 mg and 0.36 mg.1 , 2 , 5 A lower dose may have some advantages (e.g., a high dose of folic acid may mask the hematologic effects of vitamin B₁₂ deficiency while its neurologic manifestations progress). A high dose of folic acid alone reduced the recurrence of neural-tube defects in the Medical Research Council Vitamin Study,5 and a combination of folic acid and other vitamins had no extra protective effect. We and others used a lower dose of folic acid in addition to other vitamins, so we cannot exclude the possibility of a synergistic effect.

The rate of cleft lip with or without cleft palate in the vitamin-supplement group (1.9 per 1000 births) was nearly twice the rate in the Hungarian population (1.0 per 1000).16 This finding is not in agreement with a previous report of a protective effect of vitamin supplementation,17 but the dose of folic acid used in that report was 10 mg per day.

Given the results of this study, we think that all women planning pregnancy should receive a vitamin supplement containing folic acid.

We are indebted to the members of the Scientific Advisory Committee: Dr. T.C. Chalmers (Boston), Dr. J.D. Erickson (Atlanta), Dr. F.C. Fraser (Montreal), Dr. L.B. Holmes (Boston), and Dr. R.W. Smithells (Leeds, U.K.); to the members of the External Experts Group: Dr. S. Gardó, Dr. L. Kovács, and Dr. K. Méhes; to Dr. A. Bendich (Nutley, N.J.) and Dr. N. Wald (London) for their continuous help; to Dr. A. Hanck, Dr. G. Kunovits, and Mr. J. Grueter of Hoffmann—LaRoche for supplying the supplements; and to Dr. Márta Dobó, Ms. Márta Eröss, Dr. Gabriella Fritz, Ms. Csilla Lehoczky, Ms. Zsuzsa Póti, Dr. Adél Técsoi, Ms. Eva Tökés, Ms. Csilla Vértesi, and Ms. Márta Zalatnay for their assistance.

Source Information

From the Department of Human Genetics and Teratology, National Institute of Hygiene, a World Health Organization Collaborating Center for the Community Control of Hereditary Diseases, Budapest, Hungary. Address reprint requests to Dr. Czeizel at H-1966 Budapest, OKI, Gyáli út 2–6, Hungary.

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