Malnutrition is a pathological condition resulting from the deficiency or excess of one or more essential nutrients. This condition manifests clinically or is detectable by biochemical, anthropometric or physiological analyses [1] . Malnutrition can have irreversible effects on the growth, development and well-being of children. Stunting during the first 1000 days of life is associated with poorer educational outcomes, not only because malnutrition impairs brain development but also because malnourished children are more likely to fall ill and miss school [2] . WHO estimates that more than 3.5 billion people are infected with one or more species of digestive parasitic infections and 216 million (196 - 263 million) cases of malaria in 2016 [2] . Malaria and intestinal parasitic infections are the major causes of malnutrition in Chad and Africa [3] .

Plasmodium falciparum is the most prevalent malaria parasite in Africa. According to the latest World Health Organization report in 2020; the number of malaria cases worldwide was estimated at 241 million and the number of deaths at 627,000 of which 95% occurred in Africa. Children under five years of age were the most vulnerable group, with 80% of all deaths [4] [5] .

Anemia is a major public health problem and has been a concern of the World Health Organization (WHO) since 1949. It affects a significant proportion of the population at different ages. Approximately 35% of the world’s population suffers from anemia. It is significantly more common in developing countries, where approximately 47% of the affected population is affected, while in developed countries, the prevalence is around 10% [6] . The regions with the highest prevalence of anemia are South Asia and Africa [7] . The estimated prevalence rate for all groups, except adult males, reaches more than 40% in both regions [8] .

In Chad, the prevalence of malaria is 40.9% in the population and 40.9% in children aged 6 to 59 months. The prevalence of anemia is 49.9% in children and 17% in pregnant women aged 15 to 49 years [9] [10] .

The objective of this study was to evaluate the correlation between malaria, digestive parasitosis and anemia in order to better manage malnourished children in the province of N’Djamena in Chad.

During the 10 months of study, 325 children with severe acute malnutrition were sampled for malaria and intestinal parasitosis. All severely malnourished patients have infections, often multiple. The study area is endemic to malaria with a long transmission period because the child is more exposed than adults. Out of 17 national surveys conducted in sub-Saharan Africa between 2014 and 2016, the proportion of feverish children who had a blood sample taken from the finger or heel (suggesting that a malaria screening test had been carried out) was higher (34% - 59%). Screening of suspected malaria cases has increased in the public sector since 2010 in most WHO regions. The most pronounced increase in prevalence is observed in sub-Saharan African regions according to WHO with screening rates increasing from 36% in 2010 to 87% in 2016. The study area is endemic to malaria with a long transmission period, because the child is more exposed than adults. The prevalence of malaria infection is 74.6%, which is higher than that of WHO. Of 17 national surveys conducted in sub-Saharan Africa between 2014 and 2016, the proportion of feverish children who had a blood sample taken from the finger or heel (suggesting that a malaria test had been performed) was higher (34% - 59%). Screening of suspected malaria cases has increased in the public sector since 2010 in most WHO regions. The most pronounced increase in prevalence is observed in sub-Saharan African regions according to WHO with a screening rate increased from 36% in 2010 to 87% in 2016 [11] .

Speaking of malaria, the prevalence obtained in this study was 68.5%. This prevalence was higher than those obtained by: WHO, (2017), Doutoum et al. [12] in the city of Abéché in Chad in 2019 and Diarra [13] in the locality of Douguia in 2017 which were 36.57% and 26.5% respectively. In 2019, Niaré et al., in Mali had obtained a prevalence of 22.09% [14] , and Ademowo in Nigeria had obtained in 2014, 46.7% [15] . This high prevalence reported in this study could be explained by the significant vulnerability of malnourished children to this parasitosis and also by the endemic nature of Plasmodium falciparum malaria in Chad. Malnourished children aged 2 to 3 years were more parasitized, followed by those aged 1 to 2 years. This could be explained by the fact that during this age group, the child could stay awake at night, play for hours, and be a victim of mosquito bites. Moreover, it is during this age group that the child acquires his immunity, which would result in fevers and repeated malarial manifestations. In this study, the prevalence of intestinal parasitosis was 17.6%. This prevalence is lower than that of Bessimbaye et al. who found a prevalence of 50% in the children category during a study conducted in two provinces in southern Chad [16] . It is also lower than those of Hamit et al. in 2020 and Bechir et al. in 2012 who reported 64.5% and 60% respectively [17] [18] . The gap between the prevalence of this study and that of the other authors cited could be explained by the effectiveness of the management of malnourished children, which is based on a protocol including systematic treatments (antibiotics, antifungals, antiparasitic and nutritional treatment).

Regarding co-infection, the study had obtained a rate of 14% of malaria and intestinal parasitoses linked to malnutrition. This result is lower than that of Ademowo et al. in 2014 in Nigeria who found 18% of helminthic and plasmodial co-infestation but similar to that of Eyong et al. in Cameroon in 2021 [19] who found a prevalence of co-infection of 14.5% in the category of children under 5 years old and Njunda et al. in 2015 in Cameroon who found 11.9% [20] . Gbenoudon Satoguina et al., in 2016 in Togo found 15.32% of Plasmodium falciparum and nematode co-infection [21] . These studies differ in terms of the inclusion criterion and sample size. This coexistence of Plasmodium falciparum and intestinal parasites may be due to the frequent presence of larval breeding sites (ensuring the development of malaria vectors) and unfavorable hygiene conditions (ensuring the transmission of intestinal parasites) in the same study site [22] .

In terms of gender distribution, there is no significant difference. In both girls and boys, the frequency of malaria was 25% compared to the total population (68.5% malaria and 45.4% co-infection). This result provided us with a chi-square of 0.0135, which was below the critical threshold (3.811) at the margin of error of 5%. This allowed us to affirm that the occurrence of malaria in a malnourished child is not linked to gender.

Regarding the age group, the prevalence of plasmodial carriage reveals that there is a high positivity in the group children whose age varies from 2 to 3 years are more parasitized, followed by those whose age varies from 1 to 2 years. This could be explained by the fact that during this age group the child could stay awake at night have fun for hours and be a victim of mosquito bites. Moreover, it is during this age group that the child acquires his immunity, which would result in fevers and repeated malarial manifestations. Coulibaly in 2017 in Bamako [23] obtained a high prevalence in the age group of 0 to 12 months followed by the age group of 13 to 24 months with prevalence’s of 41.5% and 32.5% respectively. The result provided us with a chi-square of 5.018, which was lower than the critical value at the margin of error of 5%, and allowed us to affirm that the occurrence of malaria in malnourished children is not linked to age. We can explain these predominant rates in the age groups of 14 to 25 months and 2 to 13 months by the major population size of these two age groups within the total population. This large number would be linked to the increased vulnerability of children to malnutrition between the ages of 0 and 25 months, the age which corresponds to the period of strong growth of the child with higher food needs [24] .

The prevalence of intestinal parasitosis according to gender is remarkable in girls with 28.4% (47% for malaria-intestinal parasitosis co-infection) and 31.2% for boys. This result provided us with a chi-square of 1.833 which was lower than the critical threshold (3.811) at the margin of error of 5%. This allowed us to affirm that the occurrence of intestinal parasitosis in a malnourished child is not linked to gender. This result corroborates that of Kapiteni et al. who reported in 2019 in the Democratic Republic of Congo (DRC) that there is no statistically significant difference between the sex of children and the age group in the development of digestive parasitosis [25] .

Compared to the total population, the high positivity of intestinal parasitosis is 34% in the age group of 12 to 23 months followed by 31.5% in the age group of 24 to 35 months. Kapiteni et al. in 2019 in the Democratic Republic of Congo had found 28.6% in the age group of 18 to 29 months [25] , Enoka et al. in 2022 in Cameroon who had found a frequency of 52.33% and 76.12% in children whose age varies from 3 to 4 years and 4 to 5 years respectively [26] . The differences between the frequencies obtained in this study and in those of Kapiteni et al. and Enoka et al. could be explained by the fact that the frequency in this study is determined in relation to all malnourished children, it was in relation to infested children in the cases of the authors cited. However, they all reported that the occurrence of intestinal parasitosis is not related to age [26] .

According to the parasites identified, protozoa were the most common in this study. Entamoeba histolytica predominated at 46%, followed by Giardia intestinalis at 27.1%. This observation is consistent with those made by other authors including Camara et al. in 2019 in Bamako [27] who obtained 73.1% for Entamoeba histolytica and 15.18% for Giardia intestinalis.

Lango-yaya et al. reported that in 2021, the Central African Republic had a predominance of 30.37% for Entamoeba histolytica [28] . The specific prevalence of parasites varies depending on the study and the region. The high frequency of protozoa compared to helminths is favored by poor personnel and food hygiene, to which are added climatic conditions conducive to the development of these parasites. These species are transmitted in cystic forms through poorly washed raw foods (fruits, vegetables, salads) and drinking water most often drawn from sources polluted by human excreta. There were no systematic tests for pinworms.

The parasitic association is present in both sexes, with approximately equal proportions, 55.2% for males and 47% for females.

According to the origin: we divided the children into two groups: 176 (64.5%) of the children lived in the urban area of N’Djamena against 97 (35%) from rural areas (p = 0.001: there is a significant difference in favor of patients from the urban area). This can be explained by the wide availability of Therapeutic Nutritional Unit (UNT) in rural areas, which means that children are only transferred in case of complications.

In total, 51.33% of mothers with no education had malnourished, anemic children infected with malaria and 42.10% co-infected with malaria-intestinal parasitosis in this study ( Table 4 ). This result is lower than that of Yandaï et al. in 2016 in Chad who had obtained 71.13% of uneducated mothers [29] . This schooling rate is close to those of Tandina et al. in 2016 in Mali [30] . Malaria with 19.33% and intestinal parasitosis with 2% for the uneducated, and 27% and 2.67% for those who have completed primary education. A prevalence of 9.33% and 3.33% were found to be positive for malaria and intestinal parasitosis. The analysis we make is that parents have better monitoring of hygiene measures favorable to the reduction of parasite carriage of their child; thus illiteracy would not be a hindrance to general knowledge of fecal peril.

Anemia in association with malaria and intestinal parasitosis is common with high prevalence in malnourished children aged 0 to 5 years. The parasitic association is more widespread among subjects from peripheral districts than in the city center districts of N’Djamena. Malnourished children whose age vary from 23 to 35 months and from 11 to 22 months were the most parasitized. Entamoeba histolytica (intestinal parasite) and Plasmodium falciparum (hemoparasite) were the most predominant parasites. It is therefore imperative to continue investigations in all provinces of Chad to identify the different factors that contribute to the onset or worsening of anemia and to know how to better combat them in the future.

This work was the subject of a state doctoral thesis defense in pharmacy and was supported by the parents of the applicant.