Tropical Medicine and Infectious Disease Case Report Cluster of Angiostrongyliasis Cases Following Consumption of Raw Monitor Lizard in the Lao People’s Democratic Republic and Review of the Literature Leeyounjera Yang 1, Chirapha Darasavath 1, Ko Chang 1, Vilayvanh Vilay 2, Amphonesavanh Sengduangphachanh 3, Aphaphone Adsamouth 4, Manivanh Vongsouvath 3, Valy Keolouangkhot 1 and Matthew T. Robinson 4,5,* 1 Adult Infectious Disease Ward, Mahosot Hospital, Vientiane 01000, Laos; [email protected] (L.Y.); [email protected] (C.D.); [email protected] (K.C.); [email protected] (V.K.) 2 Infectious Disease Ward, 103 Military Hospital, Vientiane 01000, Laos; [email protected] 3 Microbiology Laboratory, Mahosot Hospital, Vientiane 01000, Laos; [email protected] (A.S.); [email protected] (M.V.) 4 Lao-Oxford-Mahosot Hospital-Wellcome Trust Research Unit (LOMWRU), Mahosot Hospital, Vientiane 01000, Laos; [email protected] 5 Centre for Tropical Medicine & Global Health, Nuffield Department of Medicine, University of Oxford, Oxford OX3 7LG, UK * Citation: Yang, L.; Darasavath, C.; Correspondence: [email protected] Chang, K.; Vilay, V.; Sengduangphachanh, A.; Adsamouth, Abstract: Angiostrongyliasis in humans causes a range of symptoms from mild headache and A.; Vongsouvath, M.; Keolouangkhot, myalgia to neurological complications, coma and death. Infection is caused by the consumption V.; Robinson, M.T. Cluster of of raw or undercooked intermediate or paratenic hosts infected with Angiostrongylus cantonensis or Angiostrongyliasis Cases Following via contaminated vegetables or water. We describe a cluster of cases involved in the shared meal Consumption of Raw Monitor Lizard of wild raw monitor lizard in the Lao PDR. Seven males, aged 22–36 years, reported headaches, in the Lao People’s Democratic abdominal pain, arthralgia, myalgia, nausea/vomiting, diarrhea, neurological effects and loss of Republic and Review of the appetite. Five were admitted to hospital. The final diagnosis was made by clinical presentation and Literature. Trop. Med. Infect. Dis. 2021, case history, and positive A. cantonensis PCR for two cases. All hospitalized patients recovered fully 6, 107. https://doi.org/10.3390/ following supportive treatment. The remaining two individuals sought local home remedies and tropicalmed6030107 made full recovery. Whilst most published reports concern infections via consumption of molluscs, Academic Editors: Johanna Lindahl, few detailed reports exist on infections that result from the consumption of reptiles and there exists Fred Unger and Jiaxin Ling little awareness in Lao PDR. This case cluster, which originates from a single meal, highlights the potential public health risk of the consumption of raw and wild-caught meat in Lao PDR and the Received: 21 May 2021 Southeast Asia region. Without specific diagnostics, clinical history and the consideration of recent Accepted: 11 June 2021 food consumption are important when evaluating patients. Published: 22 June 2021 Keywords: angiostrongyliasis; Angiostrongylus cantonensis; eosinophilic meningitis; Laos; zoonosis Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction Angiostrongylus cantonensis, also known as the rat lungworm, is a nematode responsible for human angiostrongyliasis. It is an emerging zoonotic pathogen and, while it is endemic in East Asia and Southeast Asia, it has become established globally. By 2012, over 2904 cases Copyright: © 2021 by the authors. had been recorded globally [1,2]. In Hawai’i cases have steadily climbed, with an average Licensee MDPI, Basel, Switzerland. of 2.4 cases/year between 2010 and 2014 increasing to 9 cases in 2015, and 21 cases occurred This article is an open access article in 2016 [3]. In China, outbreaks involving between 8 and 160 individuals [4] have occurred distributed under the terms and in addition to sporadic cases and seroprevalence studies suggest a prevalence of 0.8% conditions of the Creative Commons sero-positivity in the general population, which raises to 7.4% in those directly involved in Attribution (CC BY) license (https:// aquaculture or the processing of snails [5]. In Lao People’s Democratic Republic (Lao PDR), creativecommons.org/licenses/by/ A. cantonensis has been identified in cases of eosinophilic meningitis (EM), with 11% of 4.0/). Trop. Med. Infect. Dis. 2021, 6, 107. https://doi.org/10.3390/tropicalmed6030107 https://www.mdpi.com/journal/tropicalmed Trop. Med. Infect. Dis. 2021, 6, x FOR PEER REVIEW 2 of 9 (EM), with 11% of 35 patients possessing >10% eosinophils in cerebrospinal fluid (CSF) Trop. Med. Infect. Dis. 2021, 6, 107 obtained by diagnostic lumbar puncture, and being qPCR positive for A. cantonensis 2[6]. of 9 The life cycle of A. cantonensis is well documented [1,2,7] and cycles through rats, who are the definitive hosts, and molluscs (notably slugs and snails), which are interme- diate hosts. Humans become infected by consuming the intermediate or paratenic hosts 35 patients possessing >10% eosinophils in cerebrospinal fluid (CSF) obtained by diagnostic or via water or vegetation contaminated by larvae [8]. In humans, the worms are unable lumbar puncture, and being qPCR positive for A. cantonensis [6]. to complete the lifecycle and remain in the CNS. While the worms may remain in either The life cycle of A. cantonensis is well documented [1,2,7] and cycles through rats, who the subarachnoid spaces or meninges, further migration may occur in the brain, including are the definitive hosts, and molluscs (notably slugs and snails), which are intermediate hosts.migration Humans to the becomeeye. Damage infected resulting by consuming from migration the intermediate and the death or of paratenic the worms hosts them- or viaselves water can or result vegetation in an inflammatory contaminated respon by larvaese and [8 ].the In development humans, the of worms a meningo-enceph- are unable to completealitis syndrome the lifecycle [9]. This and is remain typified in theby a CNS. CSF Whileeosinophilia the worms constituting may remain >10% in of either the total the subarachnoidCSF leukocyte spaces count [6]. or meninges, further migration may occur in the brain, including migrationThe history to the (consumption eye. Damage of resulting host species) from usually migration suggests and thethe diagnosis death of thein a wormspatient themselveswith compatible can result symptoms. in an inflammatory Visualization responseof the worms and thein CSF development is the gold of standard, a meningo- but encephalitisit is rare. The syndrome majority [of9]. patients This is typifiedpresent with by a CSFheadache eosinophilia (95%); neck constituting stiffness >10% (46%), of par- the totalesthesia CSF (44%), leukocyte vomiting count (38%) [6]. and nausea (28%) are also reported [1]. In addition, neuro- logicalThe symptoms history (consumption include face of or host limb species) paralysis, usually photophobia suggests the and diagnosis diplopia in (resulting a patient withfrom compatible migration symptoms.of the worms Visualization to the eye). of theIn severe worms cases, in CSF continuous is the gold standard,high intracranial but it is rare.pressure The majoritymay occur of patients(from the present inflammatory with headache response) (95%); and neck may stiffness result in (46%), coma paresthesia and death (44%),[10,11]. vomiting Treatment (38%) is usually and nausea supportive. (28%) are also reported [1]. In addition, neurological symptomsInfection include of A. facecantonensis or limb is paralysis, typicallyphotophobia associated with and the diplopia consumption (resulting of an from under- mi- grationcooked ofor theuncooked worms to(raw) the host eye). species, In severe predominantly cases, continuous molluscs, high intracranialbut also frogs, pressure centi- maypedes, occur crustaceans, (from the fish inflammatory and lizards response)[6,12–15]. Consumption and may result of inraw coma protein and dishes death [is10 com-,11]. Treatmentmon in the is Lao usually PDR supportive. and not only include fish [16] but also snails (in a dish called ‘koi hoi’)Infection and lizard. of A.Monitor cantonensis lizardsis typicallycan routinel associatedy be observed with the being consumption sold at wet of markets an under- in cookedthe Lao or PDR uncooked (Figure (raw) 1), with host estimates species,predominantly putting typical molluscs, yearly trade but alsoat 4536 frogs, individual centipedes, liz- crustaceans,ards per market fish [17,18]. and lizards Monitor [6,12 lizards–15]. Consumptionof the genus Varanus of raw have protein been dishes well documented is common inas theparatenic Lao PDR hosts and for not A. cantonensis only include. Yellow fish [ tree16] butmonitors also snails (V. bengalensis (in a dish) from called across ‘koi Thai- hoi’) andland lizard. have been Monitor shown lizards to be can infected, routinely with be 95.5% observed of those being sampled sold at wetpositive markets for A. in can- the Laotonensis PDR [19]. (Figure 1), with estimates putting typical yearly trade at 4536 individual lizards per marketWe describe [17,18]. a Monitorcluster of lizards angiostrongyliasis of the genus Varanuscases in haveseven been individuals well documented related to the as paratenicconsumption hosts of for a A.single cantonensis meal of. Yellowraw monitor tree monitors lizard meat. (V. bengalensis In addition,) from we across review Thailand all the havereported been