Abstract

Infection with parasitic helminths has been reported to improve insulin sensitivity and glucose homeostasis, lowering the risk for type 2 diabetes. However, little is known about its impact on whole-body lipid homeostasis, especially in obese individuals. For this purpose, a cross-sectional study was carried out in lean and overweight/obese adults residing in the Lambaréné region of Gabon, an area endemic for Schistosoma haematobium. Helminth infection status, peripheral blood immune cell counts, and serum metabolic and lipid/lipoprotein levels were analyzed. We found that urine S. haematobium egg-positive individuals exhibited lower serum total cholesterol (TC; 4.42 vs 4.01 mmol/L, adjusted mean difference [95%CI] -0.30 [-0.68,-0.06]; P = 0.109), high-density lipoprotein (HDL)-C (1.44 vs 1.12 mmol/L, -0.24 [-0.43,-0.06]; P = 0.009) and triglyceride (TG; 0.93 vs 0.72 mmol/L, -0.20 [-0.39,-0.03]; P = 0.022) levels than egg-negative individuals. However, when stratified according to body mass index, these effects were only observed in overweight/obese infected individuals. Similarly, significant negative correlations between the intensity of infection, assessed by serum circulating anodic antigen (CAA) concentrations, and TC (r = -0.555; P<0.001), HDL-C (r = -0.327; P = 0.068), LDL-C (r = -0.396; P = 0.025) and TG (r = -0.381; P = 0.032) levels were found in overweight/obese individuals but not in lean subjects. Quantitative lipidomic analysis showed that circulating levels of some lipid species associated with cholesterol-rich lipoprotein particles were also significantly reduced in overweight/obese infected individuals in an intensity-dependent manner. In conclusion, we reported that infection with S. haematobium is associated with improved lipid profile in overweight/obese individuals, a feature that might contribute reducing the risk of cardiometabolic diseases in such population.

Highlights

  • About one quarter of Earth inhabitants are infected with parasitic helminths and most of them are living in Africa [1]

  • Infection with parasitic helminths has been reported to be beneficial for metabolic homeostasis by improving insulin sensitivity and lowering the risk for developing type 2 diabetes

  • In the framework of a cross-sectional study conducted in an endemic rural area, we have investigated the impact of infection with Schistosoma hematobium on serum lipid homeostasis in adult individuals with a broad range of body weight

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Summary

Introduction

About one quarter of Earth inhabitants are infected with parasitic helminths and most of them are living in Africa [1]. Schistosomiasis affects 200 to 300 million people worldwide [1], especially in the poorest regions of the low and middle income countries (LMIC), and remains a major public health problem in these endemic areas [3, 4], where it co-exists with other health condition, including non-communicable diseases (NCDs). NCDs such as obesity, metabolic syndrome and type 2 diabetes (T2D) are increasing in industrialized countries and in developing countries that experienced rapid ruralurban transition, notably in Africa [5,6,7]. Obesity is often associated with chronic low-grade inflammation, called meta-inflammation, which contributes to peripheral and systemic insulin resistance, alterations of glucose and lipid metabolism, and leads to the development of T2D and related cardiovascular diseases [8]. Meta-inflammation mostly results from alterations in the composition and/or activation state of a variety of innate and adaptive immune cells in metabolic organs, notably in adipose tissue and the liver, creating a pro-inflammatory environment that contribute to tissue-specific insulin resistance and whole-body metabolic dysfunctions [9]

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