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Introduction
Central nervous system (CNS) anomalies appear to be the most common systemic congenital anomalies, with an incidence of about 1%1-3. In low-income countries, 17-70% of neonatal deaths resulting from birth defects are attributed to neural tube defects (NTDs)4. Unfortunately, the information available on birth defects in Latin America is scarce and fragmented, indicating inadequate epidemiological surveillance. This information is a vital element for the proper monitoring and evaluation of the impact of prevention and intervention programs. Hence, the ability to adequately assess efforts aimed at reducing the incidence of NTDs in the total births per year (∼11 million) is hindered5.
Moreover, the etiology and mechanisms of fetal CNS abnormalities are still poorly understood. One report has estimated that ∼40% of pathogenic factors may be genetic and environmental6. As an example of the environmental factor, human exposure to pesticides takes place by direct contact with sprayed crops, through consumption of residues in food and water, and during or after indoor/outdoor application7. Various studies have found an association between exposure to organophosphates during fetal development and early childhood and adverse neurodevelopmental effects8-10.
Regarding the preventative strategies to diminish CNS anomalies, various clinical trials have evidenced the importance of periconceptional folic acid intake to reduce the occurrence of NTDs in newborns11. According to long-term surveillance of NTDs in countries that have successfully implemented fortification (e.g., the United States, Canada, Costa Rica, South Africa, and Chile) and data from a supplementation program in China, folic acid intervention strategies can apparently decrease the incidence rate of NTDs to as low as 5-6 cases per 10,000 pregnancies12-14. However, epidemiological surveillance of NTDs and other birth defects is still limited worldwide15. The objective of the current contribution was to evaluate the annual incidence (2014) of congenital abnormalities of the CNS in newborns treated at a regional second-level public hospital in Tuxtla Gutiérrez, Chiapas, Mexico, and explore some factors that may be associated with this serious problem.
Materials and methods
During 2014, a descriptive study of a population of 113 newborns was carried out in a second-level hospital, the Regional Public Hospital “Dr. Rafael Pascacio Gamboa”, in the City of Tuxtla Gutiérrez, the State of Chiapas, Mexico. The diagnosis of each case with a congenital abnormality of the CNS was made by a certified neurosurgeon (the main author of the current report). A questionnaire was developed to explore diverse factors possibly associated with the incidence of NTDs. The sociodemographic factors included the age and education of the parents as well as the type of maternal prenatal control. An evaluation was also made of the maternal intake of folic acid (the dose and whether it began in the periconceptional stage or the first or second trimester of pregnancy) and maternal exposure to distinct types of pesticides (insecticides, herbicides, and fungicides). The questionnaire, expressly elaborated for this investigation, consisted of concrete, closed-ended, and categorical questions accompanied by mutually exclusive response options. Before its application to study participants, a pilot study was conducted with a sample of 25 mothers to test the validity and reliability of the different sections of questions (data not shown). Hence, the final version of the instrument was understandable and coherent.
This research was authorized by the Institutional Research Committee and also by its Bioethics Committee. Care was taken to maintain the anonymity of the participants.
Once the information was collected, a database was created in the statistical program Epi Info version 3.4.3. For each type of variable, a univariate descriptive analysis was carried out to calculate the average and the corresponding percentage. With such information, the general characteristics of the sample could be identified relative to each variable. Subsequently, a bivariate analysis was conducted to reveal the extent of the correlation between the sociodemographic and independent variables, using Pearson’s Chi-square statistic and considering significance at p < 0.05.
Results
The results included in the present study were 113 newborns with a diagnosis of congenital malformations of the CNS, of which 55 were boys (48.6%) and 58 girls (51.4%). The diagnosis with the greatest incidence was hydrocephalus, with 51 cases (45.1%), followed by Arnold-Chiari malformation and encephalocele with 37 and 9 patients (32.7% and 8.0%), respectively (Table 1).
Table 1 Distribution of the type of congenital defect of the CNS in the newborns under study
| Diagnosis | n (%) |
|---|---|
| Hydrocephalus | 51 (45.1) |
| Arnold Chiari malformation | 37 (32.7) |
| Encephalocele | 9 (8.0) |
| Anencephaly | 4 (3.5) |
| Lipomeningocele | 4 (3.5) |
| Hydroanencephaly | 2 (1.8) |
| Meningocele | 2 (1.8) |
| Total | 113 (100.0) |
n: the number of each malformation found.
The number and percentage of congenital malformations of the CNS in the newborns under study were analyzed in relation to each of the sociodemographic variables of the fathers and mothers (Table 2). A significant association was found between most of the sociodemographic variables of the parents of the newborns (age of each parent during the pregnancy, educational level of the father, and the type of prenatal care) and the existence of a congenital malformation of the CNS. The exception was the lack of relation with the educational level of the mother.
Table 2 Analysis of the sociodemographic variables of the fathers and mothers of newborns with congenital abnormalities of the central nervous system
| Variable | Number (%) | χ2; p |
|---|---|---|
| Age of the mother (years) | ||
| 12-19 | 32 (28.3) | 20.2;0.0003 |
| ≥20 | 81 (71.7) | |
| Age of the father (years) | ||
| 12-19 | 9 (8.0) | 35.2;0.0001 |
| ≥ 20 | 104 (92.0) | |
| Age of the mother (years) during her first pregnancy | ||
| 12-19 | 89 (78.8) | 21.2; 0.0001 |
| ≥ 20 | 24 (21.2) | |
| Years of schooling: Father | ||
| ≤ 5 years | 49 (43.4) | 3.98; 0.04598 |
| ≥ 6 years | 64 (56.6) | |
| Years of schooling: Mother | ||
| ≤ 5 years | 62 (54.9) | 2.14; 0.14335 |
| ≥ 6 years | 51 (45.1) | |
| Type of prenatal control | ||
| Doctor | 48 (71.7) | 55.84; 0.0000 |
| Mixed | 12 (17.9) | |
| Midwife | 7 (10.4) |
A significant association (Chi-squared test (χ2 ); p < 0.05) between congenital defects and the sociodemographic variables is indicated in bold type.
Although the majority of both parents was over 19 years old, the mothers 12-19 years of age during the first trimester of pregnancy corresponded to 78.8% of the newborns with congenital malformations of the CNS. Likewise, the majority of parents had over 6 years of schooling and prenatal control attended by a doctor, but the ones without these characteristics presented the highest percentage (71.7%) of newborns with congenital malformations of the CNS (Table 2).
The number and percentage of mothers of newborns with a congenital abnormality of the CNS were classified with respect to the time at which folic acid intake began (Table 3). Folic acid supplements were consumed by 77 of the 113 mothers interviewed (68.1%). However, 41 of these mothers (36.2%) started taking this treatment during the second trimester of pregnancy, while 17 (15.4%) did so during the first trimester. Only six of the mothers (5%) took folic acid supplements during the 3 months before pregnancy (Table 3).
Table 3 Distribution of mothers according to intake of folic acid supplements
| Time at which folic acid intake began | n (%) |
|---|---|
| Over 3 months before pregnancy | 6 (5.0) |
| 0-3 months before pregnancy | 8 (7.0) |
| During the 3rd trimester | 17 (15.4) |
| During the 1st trimester | 41 (36.2) |
| During the 2nd trimester | 5 (4.4) |
| Total | 77 (68%) |
n: the number of cases.
Positive substance dependence (alcoholism and/or smoking) was manifested in 99 fathers (87.6%) and 21 mothers (18.6%). On the other hand, 34 mothers (30.4%) were exposed to insecticides before pregnancy and 46 (40.2%) during pregnancy. Likewise, 45 mothers had contact with herbicides and one with fungicides (a total of 39.8%) (data not shown).
Discussion
The high number (113 cases) of congenital malformations of the CNS detected in the present study is alarming. The current data contrast sharply with that found in the report of the epidemiological surveillance system of neural tube and craniofacial defects (SVEDTN/DCF) for 2020 in relation to the State of Chiapas, which identified only 45 cases, corresponding to an incidence of 33.3 cases per 100,000 newborns16. This could be due to certain failures in the compilation of information by the national health system.
One of the strengths of the present study was the timely diagnosis of the 113 newborns encountered in daily medical practice in a second-level hospital, which demonstrates the feasibility of planning and executing observational research in similar clinical scenarios to provide key insights that can improve healthcare.
The most frequent diagnoses, in descending order, were hydrocephalus, Arnold-Chiari malformation, and encephalocele. According to the SVEDTN/DCF, hydrocephalus was one of the most frequent malformations in 2020 at the national level as well, followed by microcephaly and ODD17. Similar findings have been described in other Latin American countries, especially in Colombia, where hydrocephalus was one of the most frequent congenital anomalies18-21.
Another similarity with national reports became apparent when analyzing the proportion of congenital abnormalities in regard to the gender of the children. In the present study, congenital malformations of the CNS were disproportionately concentrated among female versus male newborns (58% vs. 42%, respectively)22. Likewise, the SVEDTN/DCF figures indicate that abnormalities at the national level were greater in female than male newborns in 2012 (51% vs. 46%, respectively)22, a trend also observed in 202016.
On the other hand, the proportion of cases was higher in children when the first pregnancy of their mother had taken place from 12 to 19 versus over 19 years of age (78.8% vs. 21.2%, respectively). In contrast, the greatest percentage of congenital abnormalities at the national level was in newborns from mothers from 20 to 24 year old, followed by those between 15 and 19 years of age16. This difference is probably associated with the high incidence of teenage pregnancies registered in the State of Chiapas23.
Concerning the capacity of folic acid intake to reduce NTDs, the timing of folic acid consumption is critical, being most effective when it begins during the periconceptional period (as of at least 1 month before pregnancy) and continuing to the end of the first trimester24-26. Unfortunately, the practice of most mothers in the current sample was not consistent with the aforementioned indications. Only 7.8% of the mothers started taking folic acid supplements 3 months before pregnancy, while 15.4% and 36.2% did so during the first and second trimester of pregnancy, respectively. Hence, the majority of mothers who gave birth to a child with a CNS abnormality had an inadequate consumption of this food supplement, which is probably related, at least in part, to deficiencies in the application of existing prenatal care programs of the Secretary of Health in Mexico. Consequently, it is essential to strengthen the application of these programs and at the same time promote health literacy.
Moreover, the considerable percentage of mothers presently evaluated who were exposed to pesticides (40.2%), herbicides, and fungicides (39.8%) during pregnancy points to toxicity as a possible cause of congenital malformations of the CNS. A study carried out in Paraguay found the following factors to be associated with this type of malformation: Living next to fumigated fields (OR = 2.5; p = 0.02) or < 1 km away from these (OR = 2.7; p = 0.008), the storage of pesticides at home (OR = 15.4; p = 0.003), and direct or accidental contact with pesticides (OR = 3.2, CI = 95%; p = 0.04)27.
The main weakness of the current contribution is the lack of information about the specific pesticide to which the mothers were exposed and the degree of exposure or the quantity of the toxic substance in the blood of the mother or the newborn. However, this weakness creates an opportunity for the future research in rural and urban areas, with the aim of gaining further insights into the hypotheses herein posed.
CNS malformations are a complex group of disorders that are being increasingly studied and diagnosed. Unfortunately, developing countries like Mexico face a complex reality for early diagnosis and follow-up of such malformations. The limited implementation of health programs due to the lack of government funding likely constitutes a key element involved in the slow progress of prevention28, early diagnosis, and health education. Several articles have emphasized the importance of prenatal care for the application of new strategies (e.g., fetal ultrasonography, fetal magnetic resonance imaging, and amniocentesis with advanced genetic techniques) to achieve an early diagnosis of these abnormalities29.
In conclusion, the alarmingly high number of congenital malformations of the CNS presently found in newborns in Chiapas could be associated with exposure to pesticides and/or a deficient folic acid intake. It is necessary to strengthen prenatal care and health literacy programs to contribute to the reduction of such disorders.
