Strongyloidiasis is a disease caused by infection with the soil-transmitted helminth Strongyloides stercoralis. The infection can become life threatening if it progresses to complicated strongyloidiasis. S. stercoralis infection is a concern primarily in developing countries with tropical or subtropical climates. In Australia, the disease is significant for Indigenous people in rural and remote communities in these climates. Conditions that facilitate infection with S. stercoralis overlap considerably with the conditions found in rural and remote Australian Indigenous communities.  These conditions include the physical and social context of the people living in these communities. Of particular emphasis in this review are their hygiene beliefs and behaviours. These beliefs and behaviours, which include beliefs surrounding defecation and general hygiene, as well as behaviours such as toilet use versus open-defecation, and use of footwear in areas with fecally contaminated soil, provide a focal point for intervention. Addressing harmful hygiene beliefs and behaviours through health education as a means of primary prevention of strongyloidiasis is considered, and a framework for implementing an educative programme is provided. There are considerable gaps in the research relating to the risk factors for and prevention of strongyloidiasis, as well as the role of the social determinants of health in facilitating infection with S. stercoralis. Furthermore, more research is required to consider the value of educative strategies versus anthelminthic chemotherapy in combatting this disease. The significance of strongyloidiasis in rural and remote Australian Indigenous communities must be recognized, and culturally safe, evidence-based means of preventing it need to be investigated.

Introduction

“We know that this parasite kills; we know that the infection can be lifelong in the absence of effective treatment; we know that the prevalence is probably much higher than previously estimated…we know enough to call for action now [1].”

Strongyloidiasis is a soil-transmitted helminthiasis caused by infection with the intestinal parasite Strongyloides stercoralis, a nematode that is endemic to tropical and subtropical regions [2–4]. Though under-recognised and poorly represented in the literature, strongyloidiasis is an important health issue in Australia.

Estimates have suggested that up to 100 million people are infected worldwide [5]. Poor disease surveillance has made it challenging to determine the prevalence of strongyloidiasis however, and the number of infected people is thought to be much higher [1]. In Australia, the infection is of particular significance for Indigenous people living in rural and remote communities (RRCs) in the northern parts of the country [6] who are by far the most affected population group [7,8]. Recent research indicates that the prevalence of the disease in these communities is as high as 60% [9,10]. With a prevalence rivaling that of the world’s most destitute countries, and an estimated fatality rate of over 80% in complicated cases [11], it is time for strongyloidiasis in Australia to be given due attention. This article addresses the underlying factors that have permitted and perpetuated the success of S. stercoralis in rural and remote Australian Indigenous communities. Additionally, it discusses existing and potential approaches to manage or eliminate these factors.

Clinical presentation of S. stercoralis infection

Uncomplicated cases can present asymptomatically or with non-specific symptoms. The exception is when the patient presents with larva currens.

Infection with S. stercoralis has manifestations of varying severity. It has the potential to become a life threatening illness if it progresses to complicated strongyloidiasis [11,12]. Uncomplicated cases can present asymptomatically or with mild, non-specific gastrointestinal, respiratory, and dermatologic symptoms. The ambiguous and subdued clinical presentation can make it difficult to diagnose the disease. The exception is when the patient presents with larva currens, a unique rash that is pathognomonic to S. stercoralis infection [6,12,13]. Complicated strongyloidiasis, which refers to either hyperinfective syndrome or disseminated strongyloidiasis, manifests less obscurely and more severely [5]. Occurring in 2.5% of cases, most often due to a compromise in the patient’s immune status, complicated strongyloidiasis may present with potentially life-threatening complications. These complications include shock, disseminated intravascular coagulation, meningitis, renal or respiratory failure, and septicemia, all of which contribute to its 50-86% case fatality rate [6,11,12,14].

Risk factors for strongyloidiasis infection

Understanding of the risk factors for developing strongyloidiasis is important for developing effective interventions in rural and remote Australian Indigenous communities (RRAICs). These risk factors stem from the interaction between factors pertaining to the individual (the host), the pathogen (S. stercoralis), and the sociocultural and physical environment. Many of these individual and contextual factors are present in RRAICs, explaining the high prevalence of the disease in this population.

Pathogen factors refer to the characteristics of S. stercoralis that allow it to infect humans. These include its mode of transmission, life cycle, and reservoir of infection. S. stercoralis may be transmitted through penetration of exposed skin (through contact with the faeces of an infected individual) or via the faecal-oral route. The parasite also has a unique ability to propagate itself via an auto-infective lifecycle [14]. Infected humans are the primary reservoir of infection, however the environment may also act as a reservoir in the case of continual habitation and contamination by infected humans [10,15].

Individual determinants of infection risk include the person’s health behaviours and beliefs, while environmental determinants refer to the individual’s social context and physical environment [16]. Individual and environmental risk factors that are particularly relevant to RRAICs include: contact of bare skin with infectious faeces and transport of faeces to the mouth via contaminated hands or food [14]; close living quarters; living in a warm climate [8,17]; and being socioeconomically disadvantaged [15]. Individual conditions seen in RRAICs that facilitate either skin or oral contact with infectious faeces are: limited use of appropriate footwear [18,19], the practice of open-defecation among children, the belief that open-defecation and the faeces of young children pose no health risk, not appreciating the health risks associated with faecally contaminated soil, poor general hygiene, and the unsafe disposal of nappies and faecal material [20]. Further contributing to the risk of contact with faeces is the lack of adequate sanitation hardware, as there is a high level of non-functional sanitation facilities in RRAICs [20–22]. Overcrowding is a significant issue in RRAICs, with 20% of remote and 53% of very remote Indigenous households thought to be overcrowded, exacerbated by the marked socioeconomic disadvantage faced by Indigenous people living in RRCs [23].

Clearly, the risk factors for S. stercoralis infection overlap significantly with the determinants of health of Indigenous Australians in RRCs. It is this overlap that has ensured that the insidious presence of strongyloidiasis in these communities has endured for so long.

Barriers to effective strongyloidiasis management in Australia

A number of barriers to effective management of strongyloidiasis in Australia have been identified. Firstly, there is sparse literature on the topic: among the soil-transmitted helminthiases (STHs), strongyloidiasis is the least well-researched [24]. Secondly, clinicians in RRAICs often lack adequate knowledge about the disease and its presentation, which may result in a delayed or missed diagnosis. Thirdly, there is poor knowledge surrounding appropriate treatment, as well as a lack of follow-up on unconfirmed cases [6]. Fourthly, the cost of screening and treatment has also been an obstacle to control, as has the lack of a coordinated public health strategy [4,7]. To aid in the management of S. stercoralis, effective primary prevention of should be employed to prevent infection.

Primary prevention of strongyloidiasis

The interplay of the risk factors for infection, determinants of health of Indigenous Australians in RRCs, barriers to control, and characteristics of RRAICs is reflected in the variety of strategies suggested. Here strategies are presented in isolation, but it should be emphasised that a homogenous approach would be ineffective in controlling a disease that has such a multifaceted foundation. Furthermore due to the scarcity of research on controlling strongyloidiasis in Australia, evidence must be drawn from studies undertaken in other countries, as well as those relating to hygiene-associated diarrhoeal diseases (HADDs) and STHs other than strongyloidiasis.

Strategies to break the transmission of S. stercoralis have the most published evidence, including reducing skin contact with faecally-contaminated soil and preventing faecal-oral transmission. These include wearing appropriate footwear, possessing and utilising adequate sanitation facilities, and improving hygiene beliefs and behaviours (HBBs). A systematic review found that wearing shoes was found to strongly lower the odds of infection with hookworm (OR 0.29, 95% CI 0.18-0.47), a soil-transmitted helminth that also penetrates exposed skin [24]. The results of a study conducted in Cambodia are also supportive of this intervention, as the authors found a negative association with possession of shoes and S. stercoralis infection (OR 0.4, 95% CI 0.2-0.9, P = 0.031) [25]. Possession and use of adequate sanitation facilities to be negatively linked to S. stercoralis infection (OR 0.3, 95% CI 0.1-0.5, P < 0.001) [25,26]. The possession and use of functional sanitation hardware also reduced the number of cases of soil-transmitted helminthiases (OR 0.46-0.58) [27,28]. Contrary to this however, a study conducted in Zanzibar, found no significant association between new strongyloidiasis cases and having access to a latrine at home (OR 0.97, 95% CI 0.51-1.86, P = 0.987) [29]. It is worth mentioning that, though not very well represented in the literature, there is yet another possible avenue for primary prevention of the disease through environmental control strategies. Unfortunately, limited research on such strategies precludes meaningful evaluation of this approach [15].

Studies evaluating the effect of improving HBBs on the incidence of strongyloidiasis, other STHs, or HADDs have validated the use of HBBs as a target for strongyloidiasis prevention programs. A review evaluating the effectiveness of hygiene interventions for improving general health outcomes in RRAICs found that encouraging hand washing with soap was effective in reducing STHs and HADDs in children [30]. Though the review did not pertain to strongyloidiasis, its supportive findings encourage the utilisation of hygiene interventions as a possible strategy for controlling the disease. One study evaluated in this review specifically addressed STHs, supporting the validity of improving HBBs as a control measure for strongyloidiasis [31].^. The usefulness of a strategy targeting HBBs is dependent not only on the degree of protection from infection that it would afford, but also on the practicality of implementation. Previous methods used to promote healthy hygiene behaviours in RRAICs have, unfortunately, been neither comprehensive nor long lasting, confirming the need for alternative, evidence-based approaches [30].

Approaching strongyloidiasis through health promotion

Health promotion to improve HBBs surrounding defecation may represent a viable strategy in the primary prevention of S. stercoralis infection. There are numerous avenues through which HBBs in RRAICs could be improved, though the suggested strategy discussed in this review focuses on improvement through health promotion. Health education is an essential component of any program to control STHs. The World Health Organization (WHO) recommends that health education be the starting point for preventing STHs because it ensures an environment in which the success of other methods of prevention will be facilitated [32,33]. The foundational nature of health education and the absence of current programs in Australia that utilise health promotion bespeak the urgency with which such an approach should be evaluated [4].  Strategies employing chemotherapeutic deworming strategies provide only short term benefit, and cannot prevent re-infection [27]. Addressing the disease through the lens of health promotion provides a long-term strategy to eradicate S. stercoralis infection through behavior change [27].

Here we propose a strategy focused on health education and based on two of the five tenets of the Ottawa Charter for Health Promotion: creating supportive environments and developing personal skills [34].

We propose a strategy focused on health education, based on the Ottawa Charter for Health Promotion
The primary focus of the strategy is to achieve the following objectives through health education. The first objective of this approach is to educate community members about S. stercoralis, and to ensure that they understand how it causes disease. When educating about S. stercoralis, it would be necessary to establish microscopic literacy, so as to create awareness of the microscopic world, and to facilitate an understanding of the concept that microorganisms can cause disease [35]. This would contextualise and give meaning to the remaining objectives [36]. The second objective is to encourage the use of toilets, if available, and to educate about alternative means of hygienic waste management. The third objective is to make community members aware of the health risks associated with faeces, with an emphasis on the importance of ensuring appropriate disposal of the faeces of S. stercoralis-infected individuals. The fourth objective is to educate community members about the importance of discouraging open-defecation by young children, and to enable caretakers to potty-train young children. The final objective is to educate individuals about the rationale behind hand washing, particularly after defecating, disposing of children’s faeces, or contact with soil. The components of this approach have been synthesised based on strategies for preventing strongyloidiasis, STHs, or other HADDs that have been suggested or evaluated in the existing literature. Additionally, the evidence from which this strategy was synthesised was derived primarily from studies in communities with similar socioeconomic contexts and sanitation infrastructure to RRAICs.

A suitable framework would be required in order to implement a program focusing on improving HBBs. The WHO has outlined one such framework that could be modified to increase its relevance to strongyloidiasis in RRAICs [32,33]. The action plan they have developed relates to hygiene behaviours beyond those surrounding defecation, but the principles are still applicable. Briefly, the framework details the need to: ascertain and understand local hygiene beliefs and traditional defecation behaviours, learn about the dynamics and the perceived needs of the target community, involve community members and build on or establish community organisations, direct the hygiene education at children and their caretakers, utilise a variety of participatory learning activities, and capitalise on human resources by involving community elders and other respected members of the community, as well as health professionals. It is emphasised that the educational strategies should be used alongside the provision of functional hand-washing and defecation facilities [32,33]. In order for the hygiene education framework to be applied to RRAICs, the principles of effective Aboriginal health promotion, as outlined in the 2002 Sydney Consensus Statement on Principles for Better Practice in Aboriginal Health Promotion, would need to be considered [37]. These principles include: acknowledging the social, economic, and cultural contexts of the target communities, ensuring continued community participation and evaluation, and maintaining transparency when designing and implementing any interventions [37]. Ensuring that the education program is culturally appropriate and acceptable by involving community members in its design and application is paramount to the efficacy of the intervention [20].

There are a number of limitations and barriers to this strategy. The scarcity of evidence for the effectiveness of health promotion and educative strategies to control strongyloidiasis is striking. Additionally, the cost of implementing a comprehensive behavioural intervention strategy could prove to be prohibitive. Research on the control of hookworm has suggested that the influence of health education would be negligible without first improving the economic status of the people living in these communities [38]. Additionally relevant is the sensitive nature of the topic of hygiene: indicating that there is a need for ‘better’ HBBs implies that the current practices are ‘bad’ or ‘wrong’[30]. This is a damaging sentiment that could hinder the implementation of this strategy. Another limitation of this strategy is the dependence on adequate sanitation infrastructure – a significant limitation when considering the previously discussed low levels of functioning sanitation hardware in RRAICs. Lastly, hygiene interventions for the control of strongyloidiasis have not been unanimously supported in the literature, as at least one study reported that there was no significant link between hand washing and S. stercoralis infection [24].

The strengths of this strategy lie in its capacity to lay the foundation for long-lasting control of the disease. As mentioned previously, health education is needed to set a facilitative stage for further control measures. This strategy also addresses the underlying factors that contribute to the hyperendemicity of strongyloidiasis in RRAICs. Most promising is the potential for long-lasting prevention that can come from educating children and their caretakers or elders about healthy hygiene behaviours. Improving the HBBs of caretakers and elders establishes a home environment in which said HBBs will be taught to children. Without this education and reinforcement in the home environment, it would be unlikely for the children to adopt these new behaviours [35]. Thus, by educating elders, the education of children is ensured. The effective education of children is critical, as children can apply the learnt behaviours in their adult lives and pass them on to the next generation [32,33]. This multigenerational education could ensure that the improved HBBs become ingrained in the norms of the community. Additionally, although the initial cost of implementing such a comprehensive intervention may be significant, there is the potential for a greater cost-effectiveness in the long run. This long-term reduction in cost could arise if the more permanent educative solution negates the need for regular use of screening and anti-helminthic chemotherapy in the future. The strategy’s final strength is its potential to empower target communities. By focusing on educating community members about S. stercoralis, the strategy would enable them to take the initiative to reduce their risk of infection, as opposed to cultivating a paternalistic situation in which they are exclusively reliant on the instructions of external parties.

Regular evaluation of outcomes of the strategy is essential to ensure its effectiveness.

This could be achieved by: regularly screening for infection, frequently discussing the perceived efficacy of the strategy with community members, and continually reassessing the hygiene needs of the community. However, it has been reported that measuring the success of hygiene interventions can be a complex and difficult undertaking [30].

Conclusions

The enduring presence of strongyloidiasis in RRAICs is appalling: a disease that is otherwise almost entirely restricted to impoverished countries thrives in the wealthy nation of Australia. Without addressing the social, cultural, and economic factors that underlie the health disparity seen in RRAICs, effectively controlling this disease will prove to be challenging. Health promotion and health education as a means of controlling strongyloidiasis should be further investigated, as the role of such strategies has, for the most part, only been incidentally discussed to date. There are a considerable number of gaps in the research relating to strongyloidiasis and health promotion strategies for improving hygiene in RRAICs. Areas that require more research include: culturally acceptable, non-confrontational methods of hygiene education, the short- and long-term cost-effectiveness of anthelminthic chemotherapy and screening, with or without health promotion programs, the role of the social determinants of health in strongyloidiasis in RRAICs, the role of overcrowding in the transmission of strongyloidiasis, strategies to reduce overcrowding in RRAICs; the influence of rurality on the prevalence of the disease, the role of the faecal-oral route of transmission and its significance to preventative strategies, and the potential role of the environmental stages of S. stercoralis as a target for control strategies.

The medical community of Australia must recognise the significance of strongyloidiasis in rural and remote Australian Indigenous populations. Furthermore, the need for comprehensive, coordinated control strategies – that prevent not only initial infection but also the potentially fatal complications of existing infection – must be made a priority when the health of Indigenous Australians is discussed.

Glossary of abbreviations

Acknowledgements

None.

Conflicts of interest

None declared.

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