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Multicenter Study
. 2021 Jun 29;15(6):e0009555.
doi: 10.1371/journal.pntd.0009555. eCollection 2021 Jun.

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

Marièma Sarr  1   2   3 , Maryam Tidjani Alou  1   2 , Jeremy Delerce  1   2 , Saber Khelaifia  1   2 , Nafissatou Diagne  3   4 , Aldiouma Diallo  3   4 , Hubert Bassene  3   4 , Ludivine Bréchard  1   2 , Vincent Bossi  1   2 , Babacar Mbaye  1   2 , Jean-Christophe Lagier  1   2 , Anthony Levasseur  1   2 , Cheikh Sokhna  3   4 , Matthieu Million  1   2 , Didier Raoult  1   2
Affiliations
Multicenter Study

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

Marièma Sarr et al. PLoS Negl Trop Dis. .

Abstract

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.

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Conflict of interest statement

I have read the journal’s policy and the authors of this manuscript have the following competing interests: SK, J-CL, and DR are coinventors of a patent for the preservation of bacteria (1H53 316 CAS 25). DR and SK are cofounder of Culture Top.

Figures

Fig 1
Fig 1
Selection of the study population with (a) case selection based on exclusion criteria including lack of ethical approval, WHO anthropometric and clinical criteria and weaning (b) control selection based on exclusion criteria including lack of ethical approval, weaning and symptoms.
Fig 2
Fig 2. Endemic clonal circulation of L. monocytogenes in West Africa.
(a) Genomic similarity estimated using Orthologous Average Nucleotide Identity Tool (OAT) software. (b) Pangenome carried out using the ROARY software.
Fig 3
Fig 3. Detection of Listeria monocytogenes according to nutritional status.
(a) Spike graph representing the relative abundance estimated according to the 16S amplicon sequencing. Samples that are culture positive are coloured yellow. (b) Comparison of the absolute concentration of L. monocytogenes assessed using qPCR between mothers of malnourished children (SAM) and those of healthy children (CTL).
Fig 4
Fig 4
Antimicrobial activity of (a) breastmilk samples, ***: p < .0005, two-sided Mann-Whitney test, and (b) selected species isolated from breast milk samples against L. monocytogenes (strain CSUR Q0781 isolated in the present study from the breast milk of a mother with a severely malnourished child). n = 3 experiments, mean and standard deviation are reported. No anti-L. monocytogenes activity was found for the strains of Bifidobacterium longum, Bifidobacterium breve, Lactobacillus brevis, Lactobacillus delbrueckii, Lactobacillus gasseri, Lactobacillus gastricus or Lactococcus lactis isolated and tested in the present study.
Fig 5
Fig 5. Comparison of the breast milk bacterial diversity assessed through 16S amplicon sequencing between the mothers of healthy children and those of severely malnourished children.
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This study has received financial support from the French government through the "Agence Nationale pour la Recherche (ANR)" including the "Programme d'Investissement d'Avenir" under the reference Méditerranée Infection 10-IAHU-03. The funders had no role in study design, data collection and analysis, decision to publish or preparation of the manuscript.