A Listeria monocytogenes clone in human breast milk associated with severe acute malnutrition in West Africa : a multicentric case-controlled study

2021

Article référencé dans le Web of Science WOS:000670882400002

Sarr M., Tidjani Alou Maryam, Delerce J., Khelaifia S., Diagne N., Diallo A., Bassene H., Brechard L., Bossi V., Mbaye B., Lagier J. C., Levasseur A., Sokhna Cheikh, Million M., Raoult D.

PLoS Neglected Tropical Diseases, 2021, 15 (6), e0009555 [15 p.] ISSN 1935-2735

Author summary Severe acute malnutrition is a global public health issue which greatly impacts childhood mortality rates. Although still not fully understood, the multi-factorial pathology of severe acute malnutrition has been associated, among other factors, with sub-optimal feeding practices (including dysfunctional breastfeeding) and an altered gut microbiota. The serendipitous detection of Listeria monocytogenes in the breast milk of Malian women has raised the possibility of its involvement in the pathogenesis of severe acute malnutrition. To investigate this possibility, the presence of L. monocytogenes was assessed in a cohort of lactating Senegalese women, both mothers of healthy children as well as those of severely malnourished children using culture-dependent and independent methods. Our study confirms the previously unsuspected presence of L. monocytogenes in the breast milk of Senegalese women, which is increased in the milk of mothers of severely malnourished children. Moreover, breast milk samples from the mothers of healthy children more frequently induced a potent inhibition of L. monocytogenes than those from the mothers of severely malnourished children. An inhibition was also achieved using potential probiotics, Lactobacillus and Streptococcus species, isolated from breast milk. Our study reveals the previously unsuspected carriage of L. monocytogenes in the breast milk of West African women, which is associated with severe acute malnutrition. The inhibitory effect of human selected lactic acid bacterial species against L. monocytogenes might provide new therapeutic and inexpensive options to prevent and treat this neglected public health issue. Background Severe acute malnutrition (SAM) is a major public health problem affecting children under the age of five in many low- and middle-income countries, and its resolution would contribute towards achieving the several sustainable development goals. The etiology of SAM is pluri-factorial, including delayed maturation of the gut microbiota, suboptimal feeding practices and dysfunctional breastfeeding. The recent serendipitous detection of Listeria monocytogenes in the breast milk of Malian women, in contrast to French women, suggests a possible association with SAM. Methodology/ Principal findings To investigate the possible association of L. monocytogenes carriage in breast milk and SAM, a case-control study was performed in Senegal, with subjects recruited from two areas. Using 16S amplicon sequencing, a culture independent method, 100% (152/152) of the mothers were positive for L. monocytogenes in their breast milk while qPCR analysis gave lower recovery rates. Interestingly, after enrichment in Fraser broth and seeding on PALCALM agar, all 10 isolated strains were isolated from the milk of 10 mothers who had SAM children which also had a significantly increased relative abundance of L. monocytogenes (0.34 (SD 0.35) vs 0.05 (SD 0.07) in controls, p<0.0001). The high genomic similarity between these strains and Malian breast milk strains from a previous study supports the hypothesis of endemic clone carriage in West Africa. Moreover, the in vitro growth inhibition of L. monocytogenes using breast milk samples was obtained from only 50% of the milk of mothers who had SAM children, in contrast to control samples which systematically inhibited the growth of L. monocytogenes with a higher inhibition diameter (15.7 mm (SD 2.3) in controls versus 3.5 mm (SD 4.6) in SAM, p = 0.0001). Lactobacillus and Streptococcus isolated from the breast milk of controls inhibit L. monocytogenes in a species-dependent manner. Conclusions/Significance Our study reveals a previously unsuspected carriage of L. monocytogenes in the breast milk of West African women, which is associated with SAM. The inhibitory effect of human selected lactic acid bacterial species against L. monocytogenes might provide new therapeutic and inexpensive options to prevent and treat this neglected public health issue.

Santé : généralités [050] ; Nutrition, alimentation [054] ; Biotechnologies [084]

SENEGAL

Fonds IRD [F B010082288]

fdi:010082288