Got worms? Perinatal exposure to helminths prevents persistent immune sensitization and cognitive dysfunction induced by early-life infection

Williamson, Lillie D.; McKenney, Erin A.; Holzknecht, Zoie E.; Belliveau, Christine; Rawls, John F.; Poulton, Susan; Parker, William; Bilbo, Staci D.

doi:10.1016/j.bbi.2015.07.006

Cited by 71 publications

(63 citation statements)

References 75 publications

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“…In rats that were not infected by tapeworms, bacterial infection early in life hypersensitized the immune cells in the brain and led to cognitive dysfunctions (i.e. reduced memory, Williamson et al, 2016). This study highlights that when hosts are infected with helminths during early stages of life, the infection can tune host immune responses and have lifelong implications for host behaviour.…”

Section: Lessons For Behavioural Ecologymentioning

confidence: 89%

“…The degree of inflammatory response is linked to pace-of-life characteristics at both the species and individual level (Sears, Rohr, Allen, & Martin, 2011), and behavioural traits associated with pace-of-life characteristics include dispersal, activity levels, sociability, exploratory behaviour, boldness, aggressiveness and parental care (R eale et al, 2010). Other behaviours that change following immune system activation, and thus may be important for evolved dependence studies, include activity, depression-like behaviour, memory and feeding behaviour (McCusker & Kelley, 2013;Williamson et al, 2016). For example, a recent study found that adult rats, Rattus norvegicus, whose mothers were infected by tapeworms, Hymenolepis diminuta, and who were themselves infected by tapeworms and Escherichia coli as pups performed better in a memory task than uninfected rats following an immune system challenge (Williamson et al, 2016).…”

Section: Lessons For Behavioural Ecologymentioning

confidence: 98%

“…Other behaviours that change following immune system activation, and thus may be important for evolved dependence studies, include activity, depression-like behaviour, memory and feeding behaviour (McCusker & Kelley, 2013;Williamson et al, 2016). For example, a recent study found that adult rats, Rattus norvegicus, whose mothers were infected by tapeworms, Hymenolepis diminuta, and who were themselves infected by tapeworms and Escherichia coli as pups performed better in a memory task than uninfected rats following an immune system challenge (Williamson et al, 2016). In rats that were not infected by tapeworms, bacterial infection early in life hypersensitized the immune cells in the brain and led to cognitive dysfunctions (i.e.…”

Section: Lessons For Behavioural Ecologymentioning

confidence: 99%

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Better with your parasites? Lessons for behavioural ecology from evolved dependence and conditionally helpful parasites

Weinersmith

Earley

2016

Animal Behaviour

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Interest in how parasites shape host behaviour has increased dramatically in recent years. The main focus of behavioural ecologists has been on the negative effects of parasites on host behaviour. However, there are instances in which infected hosts express more adaptive behavioural phenotypes and have higher fitness relative to uninfected hosts, suggesting that it is sometimes beneficial to be parasitized. For example, hosts can exhibit evolved dependence, wherein the host coevolves with and comes to depend on parasites for the expression of adaptive host behaviours. Additionally, 'conditionally helpful parasites' modify the host phenotype in ways that benefit the host under particular conditions. These scenarios have been explored in the context of bacterial or fungal symbionts, but have been relatively unstudied with regard to metazoan parasites (e.g. trematodes, acanthocephalans, nematodes and cestodes). We explore how these scenarios apply to hosts infected by metazoan parasites, and consider implications for research in behavioural ecology. We examine conditions under which infection should result in more adaptive host behavioural phenotypes, and the implications for host fitness and evolution. We then discuss the implications of conditionally helpful parasites and parasites for which hosts have evolved dependence for laboratory studies of host behaviour and for conservation and reintroduction programmes.

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Section: Lessons For Behavioural Ecologymentioning

confidence: 89%

Section: Lessons For Behavioural Ecologymentioning

confidence: 98%

Section: Lessons For Behavioural Ecologymentioning

confidence: 99%

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Better with your parasites? Lessons for behavioural ecology from evolved dependence and conditionally helpful parasites

Weinersmith

Earley

2016

Animal Behaviour

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“…Mechanistic studies have revealed that T cells trafficking to the brain (primarily the meningeal space) can produce IL-4 that stimulates astrocytes to produce growth factors including BDNF, while also leading to the skewing of meningeal macrophages from a proinflammatory M1 phenotype to an anti-inflammatory, neuroprotective M2 phenotype (Derecki et al, 2010). Interestingly in this regard, the offspring of rats that were administered helminths during pregnancy, which stimulates a potent IL-4 response, were found to exhibited markedly attenuated CNS inflammatory responses to bacterial infection (Williamson et al, 2015). Taken together, these data indicate that T cells not only play a fundamental role in neuronal integrity especially as it relates to the processes of learning and memory, but also can support resilience in the context of stress-induced behavioral Cytokines, synaptic plasticity, and the response to antidepressants.…”

Section: Immunological Mechanismsmentioning

confidence: 96%

Therapeutic Implications of Brain–Immune Interactions: Treatment in Translation

Miller

Haroon

Felger

2016

Neuropsychopharmacol

118

124

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A wealth of data has been amassed that details a complex, yet accessible, series of pathways by which the immune system, notably inflammation, can influence the brain and behavior. These data have opened the window to a diverse array of novel targets whose potential efficacy is tied to specific neurotransmitters and neurocircuits as well as specific behaviors. What is clear is that the impact of inflammation on the brain cuts across psychiatric disorders and engages dopaminergic and glutamatergic pathways that regulate motivation and motor activity as well as the sensitivity to threat. Given the ability to identify patient populations with increased inflammation, the precision of interventions can be further tuned, in conjunction with the ability to establish target engagement in the brain through the use of multiple neuroimaging strategies. After a brief overview of the mechanisms by which inflammation affects the brain and behavior, this review examines the extant literature on the efficacy of anti-inflammatory treatments, while forging guidelines for future intelligent clinical trial design. An examination of the most promising therapeutic strategies is also provided, along with some of the most exciting clinical trials that are currently being planned or underway.

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“…Strong support for the potential of helminth therapy to treat a wide range of immune-related conditions has subsequently been gleaned from biological and immunological considerations (Rook, 2009;Parker et al, 2012;Parker & Ollerton, 2013), numerous studies in experimental animal models (Elliott et al, 2004;Imai & Fujita, 2004;Wohlleben et al, 2004;Williamson et al, 2016) and two prospective studies in humans (Summers et al, 2005b;Correale & Farez, 2007). Based on this wide range of evidence, it is clear that helminth therapy (known as 'helminthic therapy' to most self-treaters, helminth providers and to many scientists) has the potential to deal with underlying causes of inflammation in Western society, and may offer benefits not achievable with pharmaceutical intervention.…”

Section: Introductionmentioning

confidence: 99%

Practices and outcomes of self-treatment with helminths based on physicians' observations

et al. 2016

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The successful use of helminths as therapeutic agents to resolve inflammatory disease was first recorded 40 years ago. Subsequent work in animal models and in humans has demonstrated that the organisms might effectively treat a wide range of inflammatory diseases, including allergies, autoimmune disorders and inflammation-associated neuropsychiatric disorders. However, available information regarding the therapeutic uses and effects of helminths in humans is limited. This study probes the practices and experiences of individuals ‘self-treating’ with helminths through the eyes of their physicians. Five physicians monitoring more than 700 self-treating patients were interviewed. The results strongly support previous indications that helminth therapy can effectively treat a wide range of allergies, autoimmune conditions and neuropsychiatric disorders, such as major depression and anxiety disorders. Approximately 57% of the self-treating patients observed by physicians in the study had autism. Physicians reported that the majority of patients with autism and inflammation-associated co-morbidities responded favourably to therapy with either of the two most popular organisms currently used by self-treaters, Hymenolepis diminuta and Trichuris suis. However, approximately 1% of paediatric patients experienced severe gastrointestinal pains with the use of H. diminuta, although the symptoms were resolved with an anti-helminthic drug. Further, exposure to helminths apparently did not affect the impaired comprehension of social situations that is the hallmark of autism. These observations point toward potential starting points for clinical trials, and provide further support for the importance of such trials and for concerted efforts aimed at probing the potential of helminths, and perhaps other biologicals, for therapeutic use.

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Got worms? Perinatal exposure to helminths prevents persistent immune sensitization and cognitive dysfunction induced by early-life infection

Cited by 71 publications

References 75 publications

Better with your parasites? Lessons for behavioural ecology from evolved dependence and conditionally helpful parasites

Better with your parasites? Lessons for behavioural ecology from evolved dependence and conditionally helpful parasites

Therapeutic Implications of Brain–Immune Interactions: Treatment in Translation

Practices and outcomes of self-treatment with helminths based on physicians' observations

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