by Dr. Yousra Benmakhlouf, PhD; Dr. Achraf Laghmich, PhD*; Kaoutar Ben Makhlouf, PhD*; Prof. Amina Barakat, PhD; Prof. Naima Ghailani Nourouti, PhD; and Prof. Mohcine Bennani Mechita, PhD

All authors are with Intelligent Automation and BioMed Genomics Laboratory, Faculty of Sciences and Techniques of Tangier, Abdelmalek Essaadi University in Tangier, Morocco.

*Drs. A. Laghmich and K. Ben Makhlouf contributed equally to this article.

Funding: No funding was provided for this article.

Disclosures: The authors have no conflicts of interest relevant to the content of this article.

Innov Clin Neurosci. 2024;21(10–12):9–14.

Abstract

Objective: Arab populations have a long tradition of consanguinity. In Morocco, consanguineous marriages are culturally favored. In this study, we assessed the effect of consanguinity on the occurrence of intellectual disability (ID) and investigated its association to education level and professional status in a series of Moroccan families.

Design: In total, 186 patients with ID were included in this study. Data were processed and analyzed with the IBM SPSS.

Results: The rate of consanguinity among the parents of children with ID was 34.95 percent. Marriages between first cousins accounted for 24.19 percent of consanguineous unions (FI=0.02). In the general population (n=300), 27.3 percent of marriages were consanguineous, with 22.66 percent being marriages between first cousins. Marriage between first cousins was the most common type of consanguineous marriage. The illiteracy rate was greater among women, compared to men (56.9% vs. 37.87%). The majority of mothers (81.11%) were housewives. A predominance of low professional status was observed among the men (62.22% of population, 22.7%). There was a high correlation between consanguinity and ID. The association between education level, professional status, and consanguinity rate in ID was not statistically significant (p>0.05).

Conclusion: The consanguinity rate in Moroccan families remains important. More strategies and efforts must be taken and reinforced for a better understanding and awareness of consanguinity risks to significantly reduce this practice. 

Keywords: Consanguinity, intellectual disability

Consanguineous marriage is defined as a union between two individuals who are related as second cousins or closer, with the inbreeding coefficient (F) equal to or higher than 0.0156.¹ It has been reported that about 20 percent of the global population resides in communities with a preference for consanguineous marriages.² They are traditionally respected in most communities of North Africa, the Middle East, and West Asia, where intrafamilial unions collectively account for 20 to 50 percent of all marriages.² The frequency of consanguineous unions depends on the size of the population, its degree of isolation, and the existence of socioeconomic and cultural practices that promote or avoid a certain type of union.^3–5 The union between first cousins is the most common form of family endogamy.⁶

The Moroccan population favors this type of union for several socioeconomic and cultural reasons. High levels of consanguinity (29%) have been reported.⁷ Frequencies vary from region to region depending on geographic, socioeconomic, and cultural characteristics.^4,7,8 Consanguinity generally coincides with the geographic distribution of recessive genetic diseases, as it increases the likelihood of homozygosis and, consequently, the incidence of these pathologies in the population,^9,10 the incidence of homozygosity, blindness, genetic disorders such as encephalopathy, and certain hematological conditions.¹¹  To our knowledge, few studies on the link between consanguinity and genetic diseases in Morocco are available.⁷ Our study aimed to determine the rate of consanguinity in intellectual disability (ID), its coefficient (F), its geographic distribution and the relationship between consanguinity, education level, and professional status and ID in the studied region.

Methods

The present study was conducted in three ID centers in the Fez region and comprised of 186 families with one or more individuals with mild ID aged between 2 and 36 years recruited during October 2014 and July 2019. All the participants in the studied region were of at least three ancestral generations. The Wechsler Intelligence Scale for Children (WISC) and Wechsler Adult Intelligence Scale (WAIS) were used to determine the intelligence quotient (IQ) of the studied children and their parents. Tutors of the participants or center directors, in the case of orphan subjects, provided informed, written consent. The study was approved by the University Hospital Ethics Committee of the Faculty of Medicine and Pharmacy, Fez, Morocco.

A questionnaire was established to assess individual participant characteristics, including nationality, sex, age, religion, dialect, place of birth, clinical symptoms, degree of consanguinity, education level, and professional status of parents.

The unions studied were classified according to their consanguinity coefficient (F), which is the probability that two equivalent genes are identical by descent.¹² Five categories of unions were present in our series: first cousin, double first cousin, second cousin, double second cousin, and nonconsanguineous (Figure 1). Consanguinity in the general population (absence of ID) was also studied for further statistical analysis. We randomly interviewed parents of 300 children using the same questionnaire. The mean coefficient of consanguinity (F) was calculated for the two populations using the equation below: 

 

where p equals the number of generations connecting the father of an individual to the common ancestor and m equals the number of generations connecting the mother of an individual to the common ancestor.

The dependence between consanguinity and ID was investigated using the Chi-squared test and odds ratio (OR), and the association between education level, professional status, and consanguinity were investigated using p-value. Data were analyzed using IBMSPSS software V. 24 statistical software. A p-value less than 0.05 was considered statistically significant.

The statistical significance of the bivariate relationship was tested by a Chi-squared test, as the variables considered in this study were all categorical variables. To identify the adjusted significant predictors of consanguinity, attitude toward consanguinity, and awareness of congenital effects of consanguinity, a multivariate logistic regression model was fitted considering these variables as dichotomous dependent variables and selected socioeconomic, demographic, and behavioral factors as explanatory variables. The category of an explanatory variable with theoretically low risk of having an outcome is considered as a reference category. ORs, associated 95-percent confidence intervals (CIs), and corresponding p-values were used for interpreting the results. By definition, the OR of the reference category is 1.00. An OR greater than 1.00 for a category of the predictor variable indicates a higher likelihood of an outcome in that category as compared to that of the reference category.

Results

Patient characteristics. Our series included 186 patients with ID from three different ID centers in the Fez region; 125 (67.62%) were male and 61 (32.8%) were female. In total, 34.95 percent of patients with ID were offspring of consanguineous marriages. All patients primarily spoke Arabic and were Muslim.

Our results showed a difference in the rates of consanguinity between ID patients and the general population (34.95% vs. 27.3%; p<0.05). Marriages between first cousins were the most prominent in our ID series (24.19%), followed by marriages between second cousins (6.98%). The prevalence of other consanguineous marriages was low (Table 1). Our data revealed that ID was associated with consanguinity (p<0.05), which was confirmed by the OR of 7.13.

Education level and consanguinity. Sociocultural and environmental characteristics can impact marital behavior and its components. Our results showed that the illiteracy rate was higher among women, compared to men. More than half (56.9%) of women and 37.87 percent of men were illiterate and had never attended school during their childhood. Among consanguineous spouses, 23.56 percent of women and 16.57 percent of men were illiterate, 4.02 percent of women and 6.51 percent of men went to primary school, 2.29 percent of women and 6.51 percent of men went to secondary school, 1.72 percent of women and 2.37 percent of men went to high school, and 2.29 percent of women and 2.96 percent of men went to a university (Table 2). Male individuals tended to have a higher education level compared to female individuals.

The results of the logistic regression analysis of the effect of the education level in consanguineous marriage in Fez revealed that illiterate women had an OR of 2.17 (95% CI: 0.586–8.068), and illiterate men had an OR of 4.35 (95% CI: 1.338–14.180). The association between education level and inbreeding rate was not statistically significant (p>0.05)
(Table 2).

Professional status and consanguinity. Analysis of our data revealed that almost half of parents are unemployed (43.88%) and this is more emphasized in women. In female individuals, 81.11 percent declared to be housewives, 31.11 percent of whom were in consanguineous unions. Only 6.67 percent of husbands were unemployed, 2.22 percent of whom were in consanguineous marriages. The majority (51.76%) of consanguineous parents were of low professional status (skilled and unskilled workers). The association of professional status and consanguinity rate in ID was not statistically significant (p>0.05) (Table 3).

Discussion

Consanguineous marriages vary with geography, religion, and caste.^13,14 ID represents an important public health issue worldwide. It affects 1 to 3 percent of the world population.^13,14 Currently, therapeutic and preventative resources for ID are limited.

ID is underdiagnosed in the Moroccan population due to the lack and high cost of diagnosis. It is confused with other neurodegenerative diseases or neurological disorders. No study on the impact of consanguinity on ID has been reported to date. Our work is the first to determine the rate of consanguinity in patients with ID in Morocco. This rate has been evaluated at 34.95 percent (F=0.02). It was significantly higher than the consanguinity rate in the general population, evaluated at 27.3 percent (F=0.016) (Table 1). This suggests the association between ID and consanguinity in the studied region.

Consanguinity was reported to be a crucial factor in the occurrence of genetic diseases in previous studies.^15–17 Moreover, several neurological disorders were associated with consanguineous marriages, such as epilepsy, cerebral palsy, disorders of the brain, and psychotic disorders.¹¹ Other studies have shown that consanguinity can affect life expectancy, IQ (IQ can be 10–16 points lower in children born to related parents), and social behavior development capacities.¹⁸ The risk of having an IQ below 70 was found to be greater in consanguineous marriages. Overall, 6.2 percent of children from consanguineous marriage (first cousin) had a reduced IQ.¹⁹

In the general population, consanguinity was evaluated at 27.3 percent. In Morocco, this practice is related to economic, sociocultural, and demographic factors that explain the high frequency (19.81–28%).²⁰ This rate is comparable to the frequencies reported in North Africa, but significantly lower than some Arab countries of the Gulf region, such as Saudi Arabia and Kuwait, where first cousin marriages reach 25 to 30 percent of all marriages and represent a favorable alliance system, referring to the creation or reinforcement of social bonds and/or the consolidation of family wealth, power, or social status through marriage.^21,22 

In total, 34.95 percent of patients with ID this study were born from consanguineous families (F1=0.02). This rate remains comparable to that reported in Indian patients with ID (30%)²² and less than that reported in Tunisian patients with ID (52.4%).²³ This difference could be explained by the different sociocultural, economic, and demographic factors of these countries.^15,24 The consanguinity in the studied families without ID was different from those with ID (F=0.01).

Our results showed that the rate of illiteracy was higher among women, compared to men (56.9% vs. 37.87%). Men tended to have a higher level of education, compared to women. This might be explained by cultural choices. This aligns with the results of the general census of 2014 in Morocco,²⁵ which revealed that girls have lower school enrollment rates than boys in both urban and rural areas. In 2014, 8.5 percent of the population reached a higher education level, (10.6% in men and 6.6% in women), while 44 percent of the population had never attended a school or was illiterate (57.9% for women and 28.2% for men). The disparity of education between men and women in Moroccan society could be explained by the beliefs that women have a specific mission: procreation and household chores. Early marriage can deprive the girls of continuing their studies, especially in families who admit that marriage is more important than schooling.²⁶ In rural areas, young girls are responsible for difficult tasks throughout the day, and thus they have no time to devote to their schooling. Generally, the dropout rate in elementary school is high (2.5% for girls vs. 1.5% for boys).²⁵ The results of the logistic regression analysis of the effect of the education level of spouses as a determinant of consanguineous marriage in the region of Fez (Table 2) revealed that illiterate women were 2.17 times more likely to have a consanguineous marriage than women with a high level of education (OR: 2.17; 95% CI: 0.586–8.068). Illiterate men were 4.35 times more likely to have a consanguineous marriage than men with high education (OR: 4.35; 95% CI: 1.338–14.180). The association between education level and consanguinity was not statistically significant (p>0.05). Our results were similar to those described in previous studies in Morocco and other countries.^26–29 In contrast, other studies confirmed that women’s education was related to consanguineous marriage.^22,30

Most of the men in this study (62.22%) had a low professional status. The majority of women were housewives and not engaged in any paid activity, 31.11 percent of whom were in consanguineous marriages. The association between professional status and consanguinity rate in ID was not statistically significant (p>0.05). Our results showed a remarkable imbalance in the distribution of professions between wives and husbands in our population. The women’s participation in labor remains lower than that of men in the whole country.³⁰ The rate of active working women in Morocco did not exceed 22.3 percent in 2012,³⁰ which was lower than that reported in developed countries. These results support those reported by Abbad et al,³¹  who found a large difference between the distribution of occupations between women and men in the general Moroccan population; almost all (98.6%) of the women were housewives, while the men had different jobs (30.70% were farmers and 31.50% had intermediate professions).

According to published data,³² it seems that professional status might influence the rate of consanguineous marriage, since unfavorable socioeconomic conditions increase the chance of being in consanguineous unions. Thus, the rural environment favors this traditional practice, especially among individuals who have a low level of education and economy³³ or wealthy families to preserve their family heritage.³⁴

Our data revealed that consanguinity increased in the general population (27.3%) compared to a previous study that indicated a decrease in consanguinity in the Moroccan population.³⁵ Other studies have shown an increase in consanguinity among couples, from 22.55 percent to 29.67 percent in the general population of Tangier-Tetouan region.^36,37 This extension of endogamy in Morocco is representative of other Arab countries.^30,38 Participant families perceived the advantage of this type of union in promoting stability and maintaining family properties. Despite factors such as the increase in women’s education and the decline in fertility, which has led to a reduced number of cousins, the rate of consanguineous marriages has not substantially decreased in some Arab countries (e.g., Jordan, Lebanon, Bahrain, and Palestine).³⁹

Our data showed that consanguineous marriages between first cousins were the most frequent in the ID and general populations, at 24.19 and 22.66 percent, respectively. Our results were comparable to those concluded in Jordan and Qatar, in which the rate of marriage between first cousins was 20 to 30 percent in Jordan^40–42 and 34.8 percent in Qatar.⁴⁰ Typically, in consanguineous unions, there is a preference for first cousin unions, followed by other types of first cousins.⁴⁰ The same preference was observed in North Africa,^43,44 Turkey,⁴⁵ Iran,⁴⁶ Pakistan,⁴⁴ and India.⁴⁷

Traditionally, consanguineous marriage is based on sociocultural determinants related to religion and socioeconomic factors and is still arranged by the parents.⁴⁸ It is believed to ensure the emotional and material security of the spouses, the stability of marriage, the acceptance of the partner in their family, the strengthening of interfamily bonds, the release of parents from their child’s burden, cohesion, and collective solidarity.^33,49

An association between consanguinity and ID in the studied population was highlighted (p<0.05). This type of union might increase the occurrence of ID, other mental disorders, and genetic diseases through homozygosity.⁵⁰ Previous studies confirmed this result, showing that parental consanguinity was a major factor in the development of recessive disorders in children, potentially increasing the rate of congenital malformations by 2 to 2.5 percent.^40,51 Our study made it possible to enrich the literature on the contribution of consanguinity being a risk factor in ID and to estimate the rate of its prevalence at the level of the population studied. The negative consequences of consanguineous marriage on the occurrence of ID in Morocco should be highlighted.

To combat the burden of consanguineous marriages, a multifaceted approach is necessary, as these unions are deeply ingrained in the communities in which they have been practiced. A strategic plan should be established to avoid the increase in the rate of ID related to inbreeding. Such a plan should include:

• Awareness and education: Awareness campaigns must be launched on the risks associated with inbreeding, using local media, social networks, and community events. In addition, educational programs must integrate courses on genetic risks due to consanguinity. The workshops must be organized for young people and adults.
• Strengthening the healthcare system: Training healthcare professionals (doctors, nurses, genetic counselors) on aspects of inbreeding and its health implications is recommended. Genetic counseling centers should be established in cities and rural areas. These centers should provide consultations, genetic testing, and personalized counseling.
• Integration of genetic counseling services: Premarital genetic counseling should be implemented, particularly in communities where consanguinity is common. Counseling services should be accessible and affordable. Continuing education sessions should be provided for couples considering marriage or childbearing, with a focus on the risks of inbreeding and the options available to minimize these risks.
• Policy and regulation: Collaboration with authorities should be undertaken to establish policies that support the prevention of consanguineous marriages, such as legislative recommendations for premarital genetic counseling and prohibition of consanguineous marriages. Regulations to prohibit consanguineous marriages should be considered in cases where genetic testing shows a high risk of severe IDs.
• Early identification and monitoring: Prenatal screening programs for genetic disorders should be accessible to all pregnant women. Systems to identify intellectual and developmental disorders in children early, with access to necessary care and interventions, should also be available.
• Collaboration and partnerships: Collaboration with local organizations, nongovernmental organizations (NGOs), and community groups could help support and promote inbreeding prevention initiatives and encourage research into the impacts of and effective strategies to reduce inbreeding.
• Health infrastructure: Health infrastructure should be improved to support new genetic counseling services and screening programs, ensuring that resources are available in rural and urban areas. Community advisors and local healthcare workers should be trained so that they can play an active role in awareness and prevention at the regional level.

Limitations. Our study has some limitations, including that this pathology is underdiagnosed in the Moroccan population due to the deficiency and the high cost of diagnosis. The availability of genetic counseling is still relatively limited. Including patientsa from only one region might have affected the consanguinity rate, because it can vary widely across different regions of Morocco. Several challenges exist to studying ID and consanguinity in Morocco as a consequence of sociocultural limitations and awareness of genetic counseling. 

Conclusion

There was a significant correlation between consanguineous marriage and ID. To our knowledge, no prior studies have been conducted about the negative consequences of consanguineous marriage on the onset of ID in Morocco. Our study was the first to determine the rate of consanguinity in patients with ID in Morocco, with a predominance of marriages between first cousins. The rate of illiteracy was increased among women due to many sociodemographic determinants. The association between education level and professional status and consanguinity was not statistically significant. Interdisciplinary collaboration between geneticists, sociologists, and healthcare providers is crucial to better understand the relationship between consanguinity and ID and develop effective interventions. Our study enriched the literature on consanguinity and ID.

Acknowledgement

The authors would also like to thank patients with ID and their families and would like to acknowledge Association of Espace Femme Marocaine, Attawassol Center for the mentally retarded, Entraide Nationale, Mafatih Arrahma, Prince Moulay Abdellah Foundation in Fez, for their collaboration and help to facilitate the recruitment of the patients.

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