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The History of Bancroftian Lymphatic Filariasis in Australasia and Oceania: Is There a Threat of Re-Occurrence in Mainland Australia?

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The History of Bancroftian Lymphatic Filariasis in Australasia and Oceania: Is There a Threat of Re-Occurrence in Mainland Australia? Tropical Medicine and Infectious Disease Review The History of Bancroftian Lymphatic Filariasis in Australasia and Oceania: Is There a Threat of Re-Occurrence in Mainland Australia? Catherine A. Gordon 1,* ID , Malcolm K. Jones 2 and Donald P. McManus 1 1 Molecular Parasitology Laboratory, QIMR Berghofer Medical Research Institute, Brisbane, QLD 4006, Australia; [email protected] 2 School of Veterinary Science, University of Queensland, Brisbane, QLD 4072, Australia; [email protected] * Correspondence: [email protected]; Tel.: +61-7-3845-3069 Received: 26 April 2018; Accepted: 31 May 2018; Published: 4 June 2018 Abstract: Lymphatic filariasis (LF) infects an estimated 120 million people worldwide, with a further 856 million considered at risk of infection and requiring preventative chemotherapy. The majority of LF infections are caused by Wuchereria bancrofti, named in honour of the Australian physician Joseph Bancroft, with the remainder due to Brugia malayi and B. timori. Infection with LF through the bite of an infected mosquito, can lead to the development of the condition known as elephantiasis, where swelling due to oedema leads to loss of function in the affected area and thickening of the skin, ‘like an elephant’. LF has previously been endemic in Australia, although currently, no autochthonous cases occur there. Human immigration to Australia from LF-endemic countries, including those close to Australia, and the presence of susceptible mosquitoes that can act as suitable vectors, heighten the possibility of the reintroduction of LF into this country. In this review, we examine the history of LF in Australia and Oceania and weigh up the potential risk of its re-occurrence on mainland Australia. Keywords: Wuchereria bancrofti; lymphatic filariasis; elephantiasis 1. Introduction Lymphatic filariasis (LF), also known as Bancroftian filariasis or elephantiasis—due to swelling often in the lower limbs and genitals, upper limbs, and other areas of the body—is part of Australian history, with father and son, Dr. Joseph and Dr. Thomas Bancroft, two pre-eminent physicians and parasitologists, integral to the elucidation of the life-cycle of the human parasitic roundworm causing the disease. The causative agent of Bancroftian filariasis is a spirurid nematode Wuchereria bancrofti, named in honour of Joseph Bancroft and of Dr. Otto Wucherer, who was based in Brazil [1]. The earliest evidence of LF comes from Egypt, with a statue of Pharaoh Mentuhotep II (2055–2004 BC) depicting swollen limbs, which are characteristic of the disease (Figure1) [ 2], while artefacts from around 500 AD in West Africa also display scrotal swelling. The earliest written record of elephantiasis comes from the Ebers Papyrus (1550 BC) in Egypt [3]. The Greek medical writer, Celsus (30 BC–50 AD), also wrote about elephantiasis [3], the term as used then referring to both LF and leprosy [2], which can also present as elephantiasis due to the thickening of skin ‘like an elephant’. In later times, ancient Greek and Roman writers began referring to leprosy as ‘elephantiasis graecorum’ and LF as ‘elephantiasis arabum’ [2]. Similar descriptions of LF were provided by Chinese, Indian, Persian, and Arabian physicians from this time (500–600 AD). A Dutch merchant, Jan Huyghen van Linschoten, wrote of individuals in the Indian state of Goa (1588–1592) having ‘one of their legs and one foot from the knee downwards as thick as an elephant’s leg’, almost certainly describing LF [2]. Trop. Med. Infect. Dis. 2018, 3, 58; doi:10.3390/tropicalmed3020058 www.mdpi.com/journal/tropicalmed Trop. Med. Infect. Dis. 2018, 3, 58 2 of 25 Trop. Med. Infect. Dis. 2018, 3, x FOR PEER REVIEW 2 of 25 Figure 1. Timeline of Bancroftian filariasisfilariasis showing the earliest known record in the form of a statue of Pharaoh Mentuhotep II (2055–2004) and through to the elucidation of the lifecycle finalisedfinalised in 19041904 byby Dr.Dr. ThomasThomas Bancroft.Bancroft. Trop. Med. Infect. Dis. 2018, 3, 58 3 of 25 Trop. Med. Infect. Dis. 2018, 3, x FOR PEER REVIEW 3 of 25 Currently,Currently, therethere areare 856856 millionmillion peoplepeople inin 5252 countriescountries worldwideworldwide thatthat areare atat riskrisk ofof infectioninfection withwith the the three three species species of of nematodes nematodes which which cause cause LF, LF, including includingW. W. bancrofti bancrofti, which, which accounts accounts for for 90% 90% of LFof LF cases cases [4], [4], and andBrugia Brugia malayi malayiand andB. B. timori timori, which, which are are responsible responsible for for the the remainder remainder [ 5[5]].. There There areare aa numbernumber ofof otherother filarialfilarial nematodes,nematodes, includingincluding zoonoticzoonotic species,species, whichwhich cancan alsoalso causecause infectionsinfections inin humanshumans but but dodo notnot presentpresent asas LFLF [[6].6]. In this review, we will be concentrating primarily on W. bancroftibancrofti onlyonly due due to to our our focus focus on on Oceania Oceania and and the Pacific,the Pacific, where whereBrugia Brugiaspecies species are less are common. less common.Brugia species Brugia willspecies only will be referredonly be referred to in areas to wherein areas they where are they co-endemic are co‐endemic with W. bancroftiwith W.. bancrofti. InIn Australia,Australia, LFLF hashas beenbeen recordedrecorded historicallyhistorically alongalong thethe easterneastern coast,coast, extendingextending fromfrom thethe NorthernNorthern RiversRivers areaarea ofof NewNew SouthSouth WalesWales toto FarFar NorthNorth QueenslandQueensland andand thethe islandsislands ofof thethe TorresTorres StraitStrait (Figure(Figure2 2).). A A focus focus was was recorded recorded for for Brisbane, Brisbane, the the capital capital city city of of the the state state of of Queensland, Queensland, where where BancroftBancroft practicedpracticed medicinemedicine [[7].7]. Autochthonous cases have not been described since 19561956 [[8]8] inin Australia,Australia, butbut returnedreturned travelerstravelers andand serviceservice personnel,personnel, asas wellwell asas immigrantsimmigrants andand refugees,refugees, areare aa potentialpotential source source of of LFLF [[6,9].6,9]. Our closest PacificPacific neighbours, Papua New Guinea (PNG) and Indonesia, remainremain endemicendemic andand couldcould bebe thethe sourcesource ofof potentialpotential newnew casescases andand newnew invasiveinvasive mosquitomosquito speciesspecies capablecapable ofof transmittingtransmitting thethe disease.disease. Figure 2. Location of the Islands present in Oceania andand thethe PacificPacific referredreferred toto inin thisthis review.review. ThereThere are are an an estimatedestimated 2.7 2.7 millionmillion cases cases of of LFLF inin Oceania,Oceania, accountingaccounting forfor 2%2% ofof thethe globalglobal diseasedisease burdenburden due due to to this this disease, disease, although although this this figure figure comes comes from from only only one one report report of national of national data data in PNG in PNG [10]. However,[10]. However, this maythis may be an be overestimate an overestimate as prevalenceas prevalence varies varies greatly greatly by by village village and and provinceprovince [[11].11]. UtilisingUtilising thethe GlobalGlobal ProgramProgram forfor EliminationElimination ofof LymphaticLymphatic FilariasisFilariasis (GPELF)(GPELF) criteria,criteria, 4.814.81 millionmillion individualsindividuals inin PNGPNG livelive inin endemicendemic districtsdistricts [[11].11]. InIn thethe 20162016 progressprogress report,report, thethe numbernumber ofof peoplepeople requiringrequiring preventative preventative chemotherapy chemotherapy was was 14.7 14.7 million million in 11 in countries 11 countries of the of Western the Western Pacific Pacific [12]. While [12]. autochthonousWhile autochthonous cases of cases LF no of longer LF no occur longer in occur Australia, in Australia, research research has continued has continued at Australian at Australian research institutesresearch institutes and Universities, and Universities, notably at notably James at Cook James University, Cook University, where the where late Professorthe late Professor Rick Speare, Rick whomSpeare, this whom special this issue special is commemorating, issue is commemorating, was heavily was involved heavily in filariasis involved studies. in filariasis Primarily studies. this workPrimarily revolved this aroundwork revolved diagnostics around and the diagnostics status of LF and in PNG, the status which of will LF be in considered PNG, which further will later. be consideredThe GPELF further elimination later. strategy has two components. The first is to achieve transmission interruption,The GPELF whereby elimination the infection strategy is nothas spread two components. to new individuals, The first and is to the achieve second transmission is to control interruption, whereby the infection is not spread to new individuals, and the second is to control Trop. Med. Infect. Dis. 2018, 3, 58 4 of 25 Trop. Med. Infect. Dis. 2018, 3, x FOR PEER REVIEW 4 of 25 morbidity by alleviating the suffering of those who are oror havehave previouslypreviously beenbeen infected.infected. When we talk of elimination inin thisthis paper, wewe referrefer toto thisthis definitiondefinition byby the the WHO WHO GPELF GPELF program program [ [13].13]. 2. Lifecycle Although explored explored more more fully fully below, below, the the life life-cycle‐cycle is ispresented presented here.
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