Infection with Trichuris trichiura alters the gut microbial composition of mothers and children on Pemba Island, Tanzania

Soil-borne helminth infections (HST) are among the most common and widespread infections, with more than 1.5 billion people currently estimated to be infected with helminths globally, and more than a quarter of the world’s population is expected to be at risk of infection.

The four main groups of nematodes responsible for STH infections in humans include the giant roundworm (Ascaris lumbricoides), whipworm (Trichuris trichiura), filiform worm (Strongyloides stercoralis) and hookworms (Ancylostoma duodenale and Necator americanus).

Life cycle of Trichuris trichiura inside and outside the human body. Source: CDC, public domain – https://www.cdc.gov/dpdx/trichuriasis/index.html

These parasites nematodes enter the host by ingestion of soil contaminated with embryonated eggs. In the case of Trichuris trich Will, once the eggs hatch, the juvenile worms develop and mature, then migrate to the host’s cecum, where they enter the intestinal lining to feed on the host’s blood and tissue. In doing so, the penetrating worms destroy parts of the intestinal epithelium and disrupt normal intestinal homeostasis.

Chronic STH infections can lead to anemia, abdominal pain, diarrhea and malnutrition induced by blood loss disability-corrected life years (DALY) around the world.

Infection with HRTs, such as Trichuris trichiura, and the resulting disruption of the intestinal epithelium has been reported to interfere with the host’s intestinal microbial community (microbiome) and increase the abundance of potentially pathogenic intestinal bacteria.

Disruption of a healthy gut microbiome via HST infection opens up an interesting line of research, as the human gut microbial community has been shown to play a critical role in nutrient uptake and metabolism modulation. . It also facilitates the development of the immune system and is strongly involved in maintaining the health of the host.

The study of the interactions between helminths and the human gut microbiota could, therefore, lead to the development of alternative treatments for STH infection, to a better understanding of the pathology of the infection, and perhaps even to provide new treatments for autoimmune and chronic inflammatory diseases.

Hong-liang Chen and his colleagues decided to investigate this interaction and characterize the differences in intestinal bacterial communities between helminth-infected and uninfected individuals.

Their investigation
Researchers recruited 32 mother-child pairs from Pemba Island, off the coast of Tanzania, and monitored differences in the gut microbiota of uninfected and Trichuris trichiura– infected mothers and children.

Initially, fecal samples were taken from each participant and examined for the presence of T. trichiura. Parasitological diagnosis established that seventeen samples (11 mothers and 6 children) were positive for T. trichiura infection.

Then, to assess the differences in the composition of gut microbes between T. trichiura participants infected and uninfected with helminths, DNA from all participants’ feces was extracted. From this extracted DNA, the 16S ribosomal RNA (a genetic marker useful for bacterial identification) was amplified and sequenced as a means of identifying the presence of intestinal bacterial species from each participant. The abundances of bacteria identified between mothers and infants infected and uninfected with helminths were then analyzed at the phylum and gender levels.

Microbiological differences between T. trichiura– infected and uninfected participants
The researchers found that there were significant differences between the overall gut microbial community in mothers and children infected with helminths, compared to those who were not infected, showing that T. trichiura infection is associated with changes in the composition of the gut microbiome. Interestingly, infection with T. trichiura in fact appears to increase gut microbial biodiversity in mothers and children.

For example, Succinivibrio (phylum Proteobacteria) was a genus of anaerobic bacteria that showed less abundance in mothers and children infected with helminths, Ruminococcaceae family (phylum Firmicutes) showed greater abundance.

Infected helminths demonstrate an increase in gut microbial diversity in mothers (a) and children (b), achieved using three different measures; OTUs observed, Shannon index and Faith’s phylogenetic diversity index (from left to right). MN = uninfected dams, MP = dams infected with helminths. CN = uninfected children, CP = children infected with helminths.

Source: Chen et al., Parasites & Vectors 2021. CC BY 4.0.

T. trichiura the infection affects the intestinal bacterial communities of mothers and children differently
The team also demonstrated similarities and differences in the microbial composition of the gut between mothers and children infected with helminths. For example, the mutualistic bacteria of Akkermansia and Lactobacillus genera were more enriched in mothers infected with helminths than in uninfected mothers. However, the abundance of these normal gut bacteria was significantly reduced in children infected with helminths compared to uninfected children. The microbiota of children infected with helminths has also seen an increase in the abundance of opportunistic bacteria Enteroccocus.

Genre Campylobacter, known to contain several pathogenic bacteria, also showed different trends between mothers and children infected with helminths (increase in mothers compared to children).

Clear differences in the gut microbial community can be observed between uninfected and helminth-infected mothers (a) and children (b). Others represent all genera with relative abundance <0.5%.

Source: Chen et al., Parasites & Vectors, 2021.

Implications of an altered gut microbial community on the host
Despite participants infected with helminths showing increased biodiversity of gut microbes, abundances of useful and beneficial bacteria were lower in individuals infected with helminths, while opportunistic and possibly pathogenic bacteria showed much abundance. higher (dysbiosis).

The lower amount of Succinivibrio detected in children infected with helminths, for example, it has been proposed to disrupt the normal digestion of carbohydrates, since these bacteria are involved in the degradation of starch and hemicellulose. The significantly lower abundance of Lactobacillus in children infected with helminths is also of interest because Lactobacillus is a beneficial bacteria which aids the digestion process, protects against pathogenic bacteria and promotes / modulates normal immunological responses to infection.

Likewise, the decrease in the abundance of Akkermansia spp. in children infected with helminths compared to uninfected children is of particular concern, as these genera of bacteria are beneficial and protect the intestine through the conversion of mucins to short-chain fatty acids (SCFAs), which are believed to mediate anti-inflammatory effects in the intestine. In addition, other SCFA-producing gut bacteria, such as Blautia (in children infected with helminths) and Prevotella 2 (in mothers infected with helminths) exhibited lower abundance, possibly inflicting a double blow on anti-inflammatory protection induced by SCFAs, a process especially necessary during infection with intestinal wall helminths such as T. trichiura.

Finally, the significantly higher abundance of Campylobacter in mothers infected with helminths is particularly alarming, as an increasing number of Campylobacter spp. found in humans be resistant to a range of antibiotics, and as such, a global campylobacteriosis surveillance network has been proposed.

Possible advances in therapies and control measures
The knowledge gained on the effects of helminth colonization on the human gut microbiome, as well as on the possible roles and contributions of an important gut bacteria on the human host have led to a better understanding of helminth-microbiota interactions, and could support the development of new transmission interruption measures and strategies to control Trichuris trichiura, and potentially other STHs, in the future.

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