Parasitic diseases of remote Indigenous communities in Australia

International Journal for Parasitology 40 (2010) 1119–1126

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International Journal for Parasitology journal homepage: www.elsevier.com/locate/ijpara

Invited Review

Parasitic diseases of remote Indigenous communities in Australia Deborah C. Holt a, James S. McCarthy b,c, Jonathan R. Carapetis a,* a

Menzies School of Health Research, Charles Darwin University, Casuarina, Northern Territory 0811, Australia Queensland Institute of Medical Research, Herston, Queensland 4006, Australia c University of Queensland, Herston, Queensland 4006, Australia b

a r t i c l e

i n f o

Article history: Received 14 March 2010 Received in revised form 12 April 2010 Accepted 12 April 2010

Keywords: Parasite Parasitic disease Indigenous Australia

a b s t r a c t Indigenous Australians suffer significant disadvantage in health outcomes and have a life expectancy well below that of non-Indigenous Australians. Mortality rates of Indigenous Australians are higher than that of Indigenous populations in developed countries elsewhere in the world. A number of parasitic diseases which are uncommon in the rest of the Australian population contribute to the high burden of disease in many remote Indigenous communities. High rates of infection with enteric parasites such as Strongyloides stercoralis, hookworm and Trichuris have been recorded and infection of the skin with the ecto-parasitic mite Sarcoptes scabiei is also a substantial problem. Secondary infection of scabies lesions, including with Staphylococcus aureus and group A Streptococcus, can produce serious sequelae such as rheumatic fever and post-streptococcal glomerulonephritis. Transmission of many parasites in many remote communities is facilitated by overcrowded living conditions and infrastructure problems which result in poor sanitation and hygiene. Improvements in environmental health conditions must accompany medical initiatives to achieve sustainable improvement in the health of Indigenous Australians. Ó 2010 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved.

1. Introduction Indigenous people in Australia suffer significant disadvantage in health outcomes compared with non-Indigenous Australians (Australian Bureau of Statistics, 2004–2005). Despite some improvements, life expectancy for Indigenous Australians born in 2006 remains 16–17 years below that of the non-Indigenous population (Trewin and Madden, 2008). Diseases all but eradicated in the major population centres continue to cause significant morbidity and mortality in remote Indigenous communities. Mortality rates for Indigenous Australians are higher than those of Indigenous populations in developed countries elsewhere in the world such as New Zealand, the US and Canada (Australian Bureau of Statistics, 2004–2005). Childhood illnesses are of particular importance as more than 40% of the Australian Indigenous population is under 14 years of age, more than twice the proportion in the total Australian population (Trewin and Madden, 2008). Indigenous children are particularly affected by failure to thrive, faltering and stunted growth, and nutritional microcephaly is common (Ruben and Walker, 1995; Skull et al., 1997). Indigenous Australians face a high burden of chronic diseases such as chronic renal disease, cardiovascular disease and diabetes. However as is the situation in many developing countries and Indigenous populations in other developed countries, infectious

* Corresponding author. Address: Menzies School of Health Research, Charles Darwin University, P.O. Box 41096, Casuarina, Northern Territory 0811, Australia. E-mail address: [email protected] (J.R. Carapetis).

parasitic diseases remain an important cause of morbidity. Many parasitic diseases were likely introduced to the Australian Indigenous population relatively recently, through contact with Macassan traders and subsequently European settlers. Others, such as malaria, are considered to have been successfully eradicated from Australia. Of note, however, the last significant outbreak of malaria occurred in 1962 among indigenous Australians on Roper River Mission in the Northern Territory (Black, 1981). Availability and accuracy of prevalence data for parasitic diseases in Indigenous Australians varies widely and is dependent on many factors such as: the availability, sensitivity and specificity of diagnostic techniques; the status of the disease as notifiable in some or all jurisdictions within Australia; and research studies conducted in the area. Even when accurate recent prevalence data is available, concurrent infection with multiple pathogens can mean that attribution of the specific contribution of individual pathogens to morbidity is difficult to assess. Despite these limitations, it is clear that several parasitic diseases contribute significantly to the overall burden of disease in Indigenous Australians, the most important of which are associated with gastrointestinal diseases and skin disorders (Table 1). 2. Gastrointestinal disease and diarrhoea Diarrhoea is an important cause of morbidity and hospitalisation for Indigenous children in Australia. Traditional semi-nomadic, hunter-gatherer lifestyles and low population densities are likely to have offered some level of protection against gastrointestinal

0020-7519/$36.00 Ó 2010 Australian Society for Parasitology Inc. Published by Elsevier Ltd. All rights reserved. doi:10.1016/j.ijpara.2010.04.002

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Table 1 Important parasites in remote Australian Indigenous communities. Types of parasite

Class

Enteric parasites Protozoa Helminths

Nematodes

Cestodes Skin parasites

Important pathogens Cryptosporidium parvum Giardia duodenalis Strongyloides stercoralis Ancylostoma duodenale Trichuris trichiura Hymenolepis nana Sarcoptes scabiei

infection (Gracey, 1992). In contrast, the overcrowded living conditions and sanitation and hygiene problems currently present in many remote communities mean that diarrhoeal disease is now common, particularly in children (Currie and Brewster, 2001; Grimwood and Forbes, 2009). High rates of childhood diarrhoea are also seen in Indigenous populations in industrialised countries elsewhere in the world, reflecting a similar effect of socio-economic disadvantage on disease prevalence (Grimwood and Forbes, 2009). The pattern of diarrhoeal disease in the tropical north of Australia is similar to that in many developing countries, with rotavirus most common in the cooler dry season and a peak prevalence of parasitic infections in the hot and humid wet season (Grimwood and Forbes, 2009). A study of Indigenous children hospitalised with diarrhoea in tropical Northern Territory between 1998 and 2000 demonstrated that rotavirus (27%) and enteroaggregative Escherichia coli (29%) were the most commonly isolated pathogens, with Strongyloides (7%) and Cryptosporidium (7%) the most commonly isolated parasites (Kukuruzovic et al., 2002). In the absence of acute or persistent diarrhoea, healthy Indigenous children may still suffer abnormal intestinal function, nutritional insufficiency and failure to thrive. Increased intestinal permeability ratios consistent with tropical–environmental enteropathy syndrome were found in 36% (27/75) of Indigenous children admitted to hospital in the Northern Territory without diarrhoea compared with none of the non-Indigenous children (Kukuruzovic and Brewster, 2002). This is likely the result of prolonged exposure to enteric pathogens, and is common in developing countries where similar problems with sanitation and hygiene exist and infection with intestinal parasites is common (Dickson et al., 2000; Hesham et al., 2004). High rates of wasting have been reported in the Northern Territory (Ruben and Walker, 1995; Skull et al., 1997; Department of Health and Families, 2008) although recent data suggest rates may be reducing (Department of Health and Families, 2008). It is likely that parasitic infection is one of a number of important contributors to this problem. Poor sanitation and hygiene, including unsafe disposal of nappies and other faecal material, results in high levels of infection with intestinal protozoa and soil transmitted intestinal nematodes in many remote Indigenous communities. Concurrent infection with more than one intestinal pathogen is likely to be common with one study in a remote community in Western Australia documenting that 57% of participants carried more than one intestinal parasite (Reynoldson et al., 1997). Of children hospitalised with diarrhoea in a Northern Territory study, 8.5% had more than one pathogen identified in routine stool microscopy (Kukuruzovic et al., 2002). The health impacts of gastrointestinal infection are likely to be exacerbated by multiple concurrent infections.

2.1. Intestinal protozoa 2.1.1. Cryptosporidium Cryptosporidiosis in humans is predominantly caused by infection with the coccidian protozoans Cryptosporidium parvum and

Cryptosporidium hominis. Infection occurs via direct faecal-oral transmission or by the ingestion of water, or rarely food, contaminated with human or domesticated animal (C. parvum only) faeces. Cryptosporidium oocysts can survive adverse environmental conditions and are highly resistant to chemical disinfectants used to treat water such as chlorine (Heymann, 2004). Infection can be asymptomatic but symptoms can include watery diarrhoea, abdominal pain, nausea and vomiting. Infection is generally selflimiting however individuals can excrete oocysts for several weeks after symptoms resolve and the oocysts can survive many months in moist environments (Heymann, 2004). Cryptosporidium parvum can cause severe mucosal damage which can continue after clinical recovery (Kukuruzovic and Brewster, 2002). Infection is associated with high levels of nitric oxide, as measured by urine nitrate plus nitrite excretion on a low nitrate diet, which is indicative of gut inflammation (Kukuruzovic et al., 2002). Infants and children are at particular risk of infection. Indigenous children were disproportionately infected with C. parvum among hospitalised children in Australia (Cruickshank et al., 1988; Assadamongkol et al., 1992) and high rates of asymptomatic carriage have also been documented (Assadamongkol et al., 1992). Among Indigenous children hospitalised with diarrhoea in the Northern Territory, 7% had C. parvum isolated from stool specimens (Kukuruzovic et al., 2002) while other studies identified a similar level of C. parvum in children with diarrhoea in the community setting (Gracey, 1992; Gunzburg et al., 1992). It is not clear how often Cryptosporidium causes diarrhoea or abdominal pain in Indigenous children from northern or central Australia. Cryptosporidiosis in the wider Australian population is largely due to outbreaks resulting from exposure to contaminated drinking water or swimming pools. Infection is generally self-limiting and treatment is often not necessary. Of available drugs, nitazoxanide appears to be the drug of choice for treatment (Anderson and Curran, 2007). 2.1.2. Giardia duodenalis Infection with the flagellated intestinal protozoan Giardia duodenalis occurs via ingestion of the cyst form through the consumption of contaminated water or food, or by direct person-to-person contact. Excystation occurs in the small intestine and the resulting trophozoites may cause gastrointestinal symptoms such as diarrhoea, nausea, abdominal pain and distension. The trophozoites encyst as they travel towards the colon, with cysts shed by both symptomatic and asymptomatic individuals. Both domesticated and native animals are also thought to contribute to contamination of surface water which can result in zoonotic infection. Diagnosis is usually made by the microscopic examination of stool for trophozoites or cysts, or by detection of antigens in stools using commercially available ELISA or direct fluorescent antibody methods. As infections are commonly asymptomatic, the presence of G. duodenalis does not necessarily infer the cause of illness (Heymann, 2004). High rates of Giardia infection have been documented in Indigenous communities in Western Australia, with studies finding prevalence rates of: 15.2% overall with 49% in 3 year olds (Jones, 1980); 32% in children and 12.5% in adults (Meloni et al., 1993); and 36% overall (Thompson et al., 2001). A similar prevalence of 34% was found in Indigenous children attending an urban child care centre in South Australia which was significantly higher than the prevalence rate in non-Indigenous children in the same setting (Grimmond et al., 1988). Data from hospitalised children in the Northern Territory found Giardia in only 3% of cases of diarrhoea and in almost 7% of controls. While prevalence may be underestimated due to the low sensitivity of stool microscopy, it was concluded that giardiasis was unlikely to be an important contributor to severe disease in these children (Kukuruzovic et al., 2002). Nevertheless, the identification of Giardia in the stools of children with diarrhoea or other

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symptoms warrants treatment with tinidazole or metronidazole (Antibiotic Expert Group, 2006). 2.2. Intestinal helminths 2.2.1. Strongyloides stercoralis Strongyloidiasis caused by the roundworm Strongyloides stercoralis, occurs widely in the tropical and subtropical areas of the world, with the highest prevalence associated with rural locations, living in institutional settings and low socio-economic status (Sheorey et al., 2000). Filariform larvae penetrate intact skin and migrate to the lungs where they penetrate the alveolar spaces, are carried through the bronchial tree to the pharynx and are swallowed. Maturation into adult worms occurs in the intestine and eggs hatch in the bowel. Auto-infection can occur when rhabditiform larvae in the bowel invade the enteric mucosa or perianal skin. Rhabditiform larvae pass out in the faeces and can develop directly into infective filariform larvae. Uniquely among human infecting helminths, S. stercoralis also has a free living cycle in which males and females persist in the soil and mate to produce further rhabditiform larvae. Disseminated strongyloidiasis (hyper-infection) can develop particularly in immunosuppressed individuals and has been associated with Human T-cell Lymphotrophic Virus 1 (HTLV-1) co-infection in central Australia (Einsiedel and Fernandes, 2008). Disseminated disease can lead to massive numbers of larvae in the lungs and intestines and has a high case fatality rate, often due to sepsis. Treatment with corticosteroids and immunosuppressants can precipitate disseminated infection (Cruz et al., 1966). Therefore it is recommended that infection with S. stercoralis should be excluded prior to commencing immunosuppressive therapy in patients from endemic areas, or alternatively that immunosuppressed patients in endemic areas receive regular treatment courses for S. stercoralis (Johnston et al., 2005). Symptoms of strongyloidiasis are varied but intestinal symptoms include abdominal pain, nausea, diarrhoea and weight loss. Recurrent urticaria and a rash known as larva currens can occur, the latter of which is associated with the migration of larvae under the skin. Patients may experience pulmonary symptoms including Loefflers syndrome as the larvae penetrate the alveolar spaces (Sheorey et al., 2000). Disseminated strongyloidiasis causes abdominal pain and distension and can result in pulmonary and neurological complications, and septicaemia. Eosinophilia is commonly present during acute and chronic infection but is often absent in disseminated disease. A study of children hospitalised with and without diarrhoea in the Northern Territory demonstrated that infection with S. stercoralis was associated with children of older age (Kukuruzovic et al., 2002). Significantly, Indigenous children with nutritional wasting (n = 87) were more likely to have strongyloidiasis than well nourished Indigenous children (n = 181) (Odds Ratio 6.5, 95% Confidence Interval 1.6–26.7). Strongyloides stercoralis infection was also associated with worse nutritional status, more severe hypokalemia and longer hospital stays (Kukuruzovic et al., 2002). Diagnosis of strongyloidiasis by detection of parasites can be difficult due to erratic excretion of larvae (Dreyer et al., 1996). Microscopic examination of stool samples has low sensitivity which can be improved by concentration of the sample and by examination of multiple samples (Uparanukraw et al., 1999). Detection of parasites in other body fluids such as duodenal aspirate and sputum is sometimes possible in disseminated disease. Culture of parasites on agar plates has higher sensitivity but requires viable larvae. An ELISA is available at reference laboratories for the serological diagnosis of strongyloidiasis. The time to seroconversion is unknown for humans and individuals with acute or hyper-infection can be stool-positive but sero-negative. The reported sensitivity and specificity values for the ELISA vary and it has not been evaluated for the Australian Indigenous population

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(reviewed in Johnston et al. (2005)). However the ELISA is considered to be a useful tool for individual diagnosis and monitoring of Indigenous patients (Speare and Durrheim, 2004; Page et al., 2006). While it does not discriminate between viable and non-viable larvae, molecular detection of S. stercoralis DNA in stool samples is reported to be highly sensitive and specific and may prove a useful and cost effective option in the future (Verweij et al., 2009). Due to the problems with diagnosis, accurate prevalence rates are difficult to determine. Approximately 30% of infected individuals are thought to be asymptomatic, maintaining disease by autoinfection (Sheorey et al., 2000). The very limited number of surveys of the prevalence of S. stercoralis in Indigenous communities in tropical northern Australia used a range of diagnostic methods and reported prevalence rates from 0% to 60% (reviewed in Johnston et al. (2005)). In one remote community, a study of 300 individuals indicated a prevalence of 15% by stool microscopy (Aland et al., 1996) while 7% of 291 Indigenous children hospitalised with diarrhoea had S. stercoralis identified using the same method (Kukuruzovic et al., 2002). Ivermectin is the drug of choice for treatment of this infection, except in pregnant women and children under 15 kg (Marti et al., 1996). In 2010 a population-based control program using these drugs commenced in a remote Indigenous community in Australia, at the instigation of community members (Kearns et al., 2009). This program will provide important information regarding the effectiveness of this approach compared with reliance on identification and clinical management of individual cases to reduce overall prevalence. By evaluating the clinical status of children in this community before and after treatment, this study will also hopefully clarify the contribution of Strongyloides infection to a range of health problems in Aboriginal children, such as anaemia, malnutrition and gastrointestinal symptoms (Kearns et al., 2009). 2.2.2. Hookworm Hookworm infections, caused by the human infecting species Necator americanus and Ancylostoma duodenale, occur throughout the world, particularly in poor and rural communities. Infection is commonly via larval penetration of intact skin although direct faecal-oral transmission can occur with A. duodenale. Repeated exposure can result in ground itch, a papular and erythematous rash at the site of larval skin penetration. Zoonotic infection with the animal hookworms Ancylostoma caninum and Ancylostoma braziliense can cause cutaneous larva migrans, a creeping, elevated, pruritic rash which results from the migration of the larvae under the skin. Eosinophilic inflammation of the intestinal tract can also occur, however these zoonotic infections are largely self-limiting. Recently Ancylostoma ceylanicum has also been identified in dogs and cats in Australia. This species may also be of public health significance as they are known to be capable of causing patent infection in humans (Palmer et al., 2007) although there are no reports to date of its detection in Aboriginal communities. In humans, adult worms live in the small intestine attached to the mucosal wall causing chronic blood loss. Hookworm has been endemic in Indigenous communities in northern Western Australia and the Northern Territory with A. duodenale the predominant species (Prociv and Luke, 1995; Hopkins et al., 1997; Thompson et al., 2001). High rates of hookworm infection were reported for many years, with a survey in an Indigenous community in northern Western Australia reporting a prevalence of 93% in children aged 5– 14 years and 77% overall (Hopkins et al., 1997). Iron-deficiency anaemia was correlated with the presence of hookworms in the stool of those over 14 years of age, however anaemia was highly prevalent regardless of the presence of hookworm in children aged 5–14 years (Hopkins et al., 1997). This can be attributed to a low nutritional intake and/or absorption of iron and an overall high burden of infectious diseases (Ali and Thomson, 2003).

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In studies carried out in a remote Indigenous community in Western Australia, likely resistance of A. duodenale to pyrantel was demonstrated (Reynoldson et al., 1997), however albendazole was shown to be an effective treatment (Reynoldson et al., 1998). Hookworm as a public health problem has been virtually eliminated in Queensland (Prociv and Luke, 1993) and the success of mass drug administration has been documented in a remote Indigenous community in Western Australia (Thompson et al., 2001) using albendazole. Australian Therapeutic Guidelines recommend a protocol of routine deworming of children aged 6 months to 12 years using a single dose of albendazole every 4 to 6 months, in regions of high helminth prevalence (Antibiotic Expert Group, 2006). While recent detailed epidemiological studies have not been undertaken, anecdotal data suggest that the prevalence of infection with this parasite is now very low. 2.2.3. Trichuris trichiura Infection with the whipworm Trichuris trichiura is by the ingestion of eggs from soil-contaminated food or hands. In most cases the worm burden remains low and patients are asymptomatic or have mild abdominal discomfort. In cases of heavy infection individuals are likely to experience epigastric pain, diarrhoea and weight loss and may develop dysentery with bloody diarrhoea and rectal prolapse (Sheorey et al., 2000). Infection rates were reported to be 80% in a survey of a remote Indigenous community in the East Arnhem region of the Northern Territory in the mid 1990s (Aland et al., 1996). While single dose albendazole (as used in deworming programs) reduces the intensity of T. trichiura infection, in contrast to hookworm it is relatively ineffective at clearing infection (Currie, 1997; Keiser and Utzinger, 2008). For treatment of diagnosed T. trichiura infection, daily albendazole for 3 days is recommended (Antibiotic Expert Group, 2006). More recently, infection rates have been reported to be much lower than previously, with T. trichiura isolated from only 3% of Indigenous children hospitalised with diarrhoea and not considered to be a cause of diarrhoea or bowel damage in these cases (Kukuruzovic et al., 2002). Given that housing and other environmental health infrastructure in these communities did not appear to improve substantially during the 1990s, it is possible that the single dose albendazole deworming strategy may have had an impact on Trichuris transmission in addition to the effect on hookworm. 2.2.4. Hymenolepis nana The cestode Hymenolepis nana is transmitted by the faecal-oral route and can be spread directly between humans without the need for an intermediate host (Sheorey et al., 2000). Adult worms develop in the small intestine where they produce eggs which are infective when passed in the faeces. However auto-infection can also occur when eggs develop into larvae and then adults directly within the small intestine. Infection with H. nana is often asymptomatic, but heavier infections can result in symptoms including abdominal cramps, diarrhoea and anorexia. Persisting infections can be treated with a single dose of praziquantel (Antibiotic Expert Group, 2006). High rates of infection with H. nana have been documented in Indigenous communities in Western Australia over many years, with prevalence ranging from 20% (Jones, 1980; Meloni et al., 1993) to as high as 55% (Reynoldson et al., 1997). Concurrent infection with H. nana and Giardia in remote communities was shown to be common (Jones, 1980; Reynoldson et al., 1997), with children aged less than 3 years more likely to be concurrently infected with Giardia than older children (Jones, 1980). A sustained community control program using albendazole in one community failed to have an ongoing effect on the prevalence of H. nana or Giardia (Thompson et al., 2001). The first report of the detection of Hymenolepis microstoma in humans was also documented as part of

these studies, using DNA sequence analysis for species identification as eggs of H. nana and H. microstoma are morphologically very similar (Macnish et al., 2002). Hymenolepis microstoma has definitive hosts which include mice, rats and hamsters, raising the possibility that zoonotic infection with H. microstoma occurs. Transmission of H. microstoma could be via an arthropod intermediate host or by direct human to human transmission (Macnish et al., 2002). 2.3. Other intestinal parasites The contribution of other organisms, such as Blastocystis spp., to gastrointestinal disease in Indigenous communities is unclear. Diagnosis of Blastocystis can be difficult as the cysts can be difficult to distinguish in wet mount preparations and can lyse in water (for instance during concentration procedures). While the exact involvement of Blastocystis in symptomatic gastrointestinal disease remains controversial, its worldwide distribution means it is likely to be present in remote Indigenous communities. For poorly understood reasons a number of intestinal nematodes which are widespread in developing populations in other tropical regions of the world are not significant problems for Indigenous Australians. Despite their proximity to Australia in neighbouring countries in South East Asia, the round worm Ascaris lumbricoides and the pork tapeworm Taenia solium for which humans are a definitive host, are rarely acquired in Australian Indigenous communities (Currie and Brewster, 2001; Grimwood and Forbes, 2009). 3. Skin infections It is likely that the skin disorders now prevalent in the Indigenous population in northern and central Australia were not present in traditional hunter-gatherer populations. Tinea is thought to have been introduced to Indigenous Australians via contact with Macassans on the north Australian coast (Green and Kaminski, 1973). Scabies is a far more recent introduction, having only become endemic in remote Indigenous communities in the last half century (reviewed in Currie and Carapetis (2000)). Despite the potential seriousness of these skin conditions, it was noted by Green and Kaminski (1977), that other diseases ‘‘. . .attracted more political interest, treasury funds and medical staff than diseases of the skin” (Green and Kaminski, 1977). Scabies, pyoderma and tinea are now common skin disorders in Indigenous communities (reviewed in Andrews et al. (2009b)). 3.1. Sarcoptes scabiei Scabies is an infection of the skin by the ecto-parasitic mite Sarcoptes scabiei. Female scabies mites (Fig. 1) burrow into the upper epidermis and lay eggs in the burrows, from which larvae emerge after 50–53 h. The larvae moult into protonymphs, then tritonymphs from which adults develop, with the full lifecycle taking 10–13 days. Transfer of mites is via direct person-to-person contact and fomites are thought not to contribute significantly to transmission (Mellanby, 1941; Taplin et al., 1983; Carapetis et al., 1997). Mites survive off the body for approximately 24–36 h in ambient conditions although lower temperatures and high humidity can enhance survival (Arlian et al., 1984). Scabies is a disease of worldwide significance with over 300 million people estimated to be affected at any one time (Taplin and Meinking, 1990), predominantly in disadvantaged communities. Scabies is associated with overcrowded living conditions and poverty, and is endemic in many remote Indigenous communities in central and northern Australia (Walton et al., 2004b). Prevalence

D.C. Holt et al. / International Journal for Parasitology 40 (2010) 1119–1126

Fig. 1. Female Sarcoptes scabiei mite (200) (courtesy of S. Pizzutto). Ó Menzies School of Health Research

rates of up to 50% in children and 25% in adults have been reported in the Northern Territory (Carapetis et al., 1997; Currie et al., 1997). A more recent study involving five remote Indigenous communities over 3 years reported an average monthly prevalence of scabies of 13.4% overall (Andrews et al., 2009a). This reduced prevalence compared to earlier studies in the same region may reflect the success of community-wide treatment programs (see below). Children still carried the major burden of disease with average monthly prevalence rates of 22.7% for children under 3 years of age (Andrews et al., 2009a) and 63% of children presenting to the community medical clinic with scabies by 12 months of age (Clucas et al., 2008). Classical or ordinary scabies presents as an allergic type skin reaction with generalised pruritis. The mite burden in ordinary scabies is around 11 mites per person (Mellanby, 1944) but this number reduces with subsequent infections (Mellanby, 1944; Arlian et al., 1994a, 1994b). Diagnosis of scabies is difficult as the clinical signs vary and can be confused with those of other skin conditions. Confirmation of clinical diagnosis can be made by microscopic examination of skin scrapings, however given the low mite burden in cases of ordinary scabies, the sensitivity of this technique is low (Walton and Currie, 2007). While there are commercially available assays for the serological diagnosis of scabies in animals, these assays have low sensitivity for diagnosis of the disease in humans (Haas et al., 2005). Therefore, the diagnosis is usually made clinically, relying on the presence of papules and marks of pruritis in the typical distributions (distally, particularly on wrists and hands, with preference for webspaces, in older children and adults, and more widespread disease, including around axillae, groin, neck and scalp in infants and babies). In the Northern Territory, a range of training materials and short-course educational programs have been developed to improve awareness and accuracy of scabies diagnosis in remote communities (available at http://www.crcah.org.au/research/east_ arnhem_healthy_skin_project.html). A rare form of the disease is crusted (‘‘Norwegian”) scabies which is characterised by hyper-infection with individuals reported as having over 4000 mites per gram of skin (Currie et al., 1995). The mechanism for progression from ordinary to crusted scabies is not well understood. It is clear that crusted scabies is caused by the same variety of mites which causes ordinary scabies. Outbreaks caused by an index case of crusted scabies result in ordinary scabies in contacts (Moberg et al., 1984; Estes and Estes, 1993), suggesting host factors are important in disease status. While many crusted scabies patients have underlying immunosuppressive conditions such as diabetes, HTVL-1 infection, substance

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misuse or pulmonary tuberculosis, some patients have no overt immunological deficit (Gogna et al., 1985; Mollison et al., 1993; Currie et al., 1995; Roberts et al., 2005). Crusted scabies is characterised by the development of hyperkeratotic skin crusts and severe fissuring of the skin. Secondary sepsis is common in crusted scabies patients and 5 year mortality rates of 50% were previously documented (Currie et al., 1997). Considerable effort has been made to improve outcomes for Indigenous patients with crusted scabies. The introduction of multiple dose ivermectin therapy for crusted scabies in the Northern Territory in 1996 was reflected in a significant drop in the annual death rate from crusted scabies from 4.3% from 1991–1996 to 1.1% from 1997–2000 (Roberts et al., 2005). However the first cases of clinical failure accompanied by in vitro resistance to ivermectin were reported in 2004 (Currie et al., 2004) and longitudinal analysis provided further evidence of emerging resistance, raising serious concerns for continuing effective treatment (Mounsey et al., 2009). Although crusted scabies is a rare form of the disease, affected individuals often remain infectious for long periods of time due to the difficulty in eradicating mites from their hyper-keratotic and crusted skin (Currie and Carapetis, 2000) and they can be important sources of transmission in their communities (Currie et al., 1997; Huffam and Currie, 1998). While scabies also affects many other animals, limited genetic exchange between different host-associated mite populations has been demonstrated (Walton et al., 1999, 2004a; Alasaad et al., 2008). Infections of humans with dog scabies mites differ clinically to infection with human mites, and are usually temporary in nature (Walton et al., 2004b). These data indicate that animals are not a significant source of infection in humans. This evidence was supported by the success of a community-based intervention which reduced the prevalence of human scabies in the absence of any concurrent dog health initiatives (Carapetis et al., 1997; Wong et al., 2002). This had important implications for control programs which focused on treating dog scabies with the aim of impacting on human disease (Walton et al., 1999). Work such as this highlights how cutting edge laboratory science can interface with clinical and laboratory research, and lead directly to important public health interventions. Secondary bacterial infection of scabies lesions is common, with scabies thought to underlie up to 50–70% of streptococcal pyoderma in remote Indigenous communities (Van Buynder et al., 1992; Carapetis et al., 1997). Skin infection with Group A Streptococcus can led to significant sequelae including acute post-streptococcal glomerulonephritis and potentially acute rheumatic fever, which occurs in Indigenous Australians at among the highest rates in the world (Carapetis et al., 1996). There are a number of treatments currently used for scabies which vary in efficacy, toxicity and cost (reviewed in Mounsey et al. (2008)). Sulphur compounds and 1% gammabenzene hexachloride (Lindane) have been widely used in the past however side effects, including neurotoxicity, limit their acceptability and availability. Permethrin as a 5% cream has replaced Lindane as the treatment of choice in many regions. Crotamiton is commonly used for treatment of infants under 2 years of age (Ewald, 2004). Although the acaricidal efficacy of crotamiton has been demonstrated in vitro (Mounsey et al., 2008), clinical trials indicate low efficacy in vivo (Taplin et al., 1990; Amer and el-Gharib, 1992). Of concern is the reported resistance of scabies mites to lindane, crotamiton and permethrin (Hernandez-Perez, 1983; Purvis and Tyring, 1991; Roth, 1991; Fraser, 1994). Benzyl benzoate is an extremely effective treatment but can cause severe skin irritation at therapeutic concentrations (25%) and treatment guidelines vary. Tea tree oil (Walton et al., 2004c) and aloe vera (Oyelami et al., 2009) have also been suggested as effective alternative treatments for scabies. Ivermectin is widely used as a treatment for other parasitic diseases of humans

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including the filarial worms Onchocerca volvulus, Wuchereria bancrofti and Brugia malaya, with few side effects. It is an effective drug for the treatment of scabies in animals and is used for treatment of crusted scabies in some parts of the world, including northern Australia. Both permethrin and ivermectin have been utilised in community control programs for scabies (see below). 3.2. Community-based control programs A number of community-based scabies and skin health programs have been conducted in Australian Indigenous communities based on topical treatment with permethrin, with variable results (Carapetis et al., 1997; Wong et al., 2001, 2002; Andrews et al., 2009a). A program carried out in one of the largest remote communities in the Northern Territory combined active screening regimens and annual treatment days with health education initiatives and environmental interventions (Wong et al., 2001). A reduction in both scabies and group A Streptococcus skin infection was sustained when analysed 15 months post-intervention (Wong et al., 2002). Another program which offered treatment to all residents followed by active screening and retreatment as necessary showed a reduction in prevalence of scabies from 29% before the program to less than 10%. Pyoderma was also reduced to approximately half that of the original prevalence, was less severe and no longer associated with scabies (Carapetis et al., 1997). More recently the East Arnhem Healthy Skin Project included active surveillance of children under 15 years of age and annual community-wide (unsupervised) treatment, in five remote communities over a 3 year period (Andrews et al., 2009a). The baseline prevalence of scabies across these communities was considerably lower than previously reported at 16.1% in children less than 15 years of age (Andrews et al., 2009a). This may reflect the success of the earlier community-based approaches with local guidelines recommending community-wide treatment (Carapetis et al., 1997; Wong et al., 2001, 2002). The East Arnhem Healthy Skin Project successfully reduced the prevalence of infected scabies from 3.7% to 1.5%, however the overall rate of scabies infection remained unchanged (Andrews et al., 2009a). This was due to poor compliance with treatment, particularly among household contacts of people with diagnosed scabies (La Vincente et al., 2009) and highlights the need for community-based programs to use treatments that do not rely on whole-body application of creams or lotions, and which can be administered in a supervised fashion (such as once-off oral medications). A mass community intervention for scabies in the Solomon Islands was successful in reducing the prevalence of scabies from 25% to less than 1%. Almost all community members were treated with ivermectin, or permethrin for pregnant women or children less than 15 kg. In addition all returning residents and visitors were treated regardless of the presence of symptoms (Lawrence et al., 2005). This raises the possibility that community-based control programs using ivermectin may be effective in Australian Indigenous communities, where they would likely reduce on the prevalence of a number of parasites including S. scabiei and S. stercoralis, and a trial in one remote community recently commenced (Kearns et al., 2009). 4. Environmental factors Indigenous Australians are disproportionately affected by both parasitic and non-parasitic diseases, with substantial impacts on their health. While improvements in health service resources and delivery are critical, they should be considered in the broader context of interdependent environmental factors which also affect health, such as crowding, adequate and safe water supply, hygiene and sanitation (Currie and Brewster, 2001).

Research in three remote communities demonstrated that residents of houses which had functioning facilities for the removal of faeces and tiled floors had far lower rates of skin infection than residents of houses without these facilities in the same communities (Bailie et al., 2005). Such improvements in infrastructure and hygiene would also be expected to reduce the transmission of enteric pathogens. Analysis of strategies aimed at preventing faltering growth in Indigenous children living in remote communities concluded that deworming programs should be conducted in populations with high rates of infection but should be used in conjunction with environmental interventions that would likely reduce the rate of re-infection, such as hand-washing and improved sanitation (McDonald et al., 2008b). Evidence from developing countries also indicates that multifaceted approaches which include improvements in sanitation and water supply, as well as hygiene promotion, were likely to have the greatest chance of improving health outcomes for children in remote Indigenous communities (McDonald et al., 2008a). Additional housing with robust essential health hardware is urgently required to reduce levels of overcrowding and infection rates (McDonald et al., 2009).

5. Conclusion Parasitic diseases are responsible for significant morbidity in the Australian Indigenous population, with those living in remote communities most affected. It is fundamental that issues of environmental health are addressed concurrently with health service initiatives if long-term and sustainable improvements are to be made in the control of both infectious parasitic and non-parasitic diseases in remote Indigenous communities in Australia. Acknowledgements We thank Susan Pizzutto for providing the micrograph of the scabies mite and Annette Dougall and Robyn Marsh for critical review of the manuscript. References Aland, K., Provic, P., Currie, B., Jones, H., 1996. Worm project at Galiwin’ku. Working Together 6, 10. Alasaad, S., Soglia, D., Sarasa, M., Soriguer, R.C., Perez, J.M., Granados, J.E., Rasero, R., Zhu, X.Q., Rossi, L., 2008. Skin-scale genetic structure of Sarcoptes scabiei populations from individual hosts: empirical evidence from Iberian ibexderived mites. Parasitol. Res. 104, 101–105. Ali, M., Thomson, N., 2003. Gastrointestinal disorders. In: Thomson, N. (Ed.), The Health of Indigenous Australians. Oxford University Press, Melbourne, pp. 290– 312. Amer, M., el-Gharib, I., 1992. Permethrin versus crotamiton and lindane in the treatment of scabies. Int. J. Dermatol. 31, 357–358. Anderson, V.R., Curran, M.P., 2007. Nitazoxanide: a review of its use in the treatment of gastrointestinal infections. Drugs 67, 1947–1967. Andrews, R.M., Kearns, T., Connors, C., Parker, C., Carville, K., Currie, B.J., Carapetis, J.R., 2009a. A regional initiative to reduce skin infections amongst aboriginal children living in remote communities of the Northern Territory, Australia. PLoS Negl. Trop. Dis. 3, e554. Andrews, R.M., McCarthy, J., Carapetis, J.R., Currie, B.J., 2009b. Skin disorders, including pyoderma, scabies, and tinea infections. Pediatr. Clin. North Am. 56, 1421–1440. Antibiotic Expert Group, 2006. Therapeutic Guidelines: Antibiotic. Therapeutic Guidelines Ltd., Melbourne. Arlian, L.G., Runyan, R.A., Achar, S., Estes, S.A., 1984. Survival and infestivity of Sarcoptes scabiei var. canis and var. hominis. J. Am. Acad. Dermatol. 11, 210–215. Arlian, L.G., Morgan, M.S., Vyszenski-Moher, D.L., Stemmer, B.L., 1994a. Sarcoptes scabiei: the circulating antibody response and induced immunity to scabies. Exp. Parasitol. 78, 37–50. Arlian, L.G., Rapp, C.M., Vyszenski-Moher, D.L., Morgan, M.S., 1994b. Sarcoptes scabiei: histopathological changes associated with acquisition and expression of host immunity to scabies. Exp. Parasitol. 78, 51–63. Assadamongkol, K., Gracey, M., Forbes, D., Varavithya, W., 1992. Cryptosporidium in 100 Australian children. Southeast Asian. J. Trop. Med. Public Health 23, 132– 137.

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