Parasitol Res (2007) 101:1417–1423 DOI 10.1007/s00436-007-0659-8

ORIGINAL PAPER

Forensic entomology cases in Thailand: a review of cases from 2000 to 2006

Kom Sukontason & Paitoon Narongchai & Chaturong Kanchai & Karnda Vichairat & Pongruk Sribanditmongkol & Tanin Bhoopat & Hiromu Kurahashi & Manoch Chockjamsai & Somsak Piangjai & Nophawan Bunchu & Somsak Vongvivach & Wirachai Samai & Tarinee Chaiwong & Rungkanta Methanitikorn & Rachadawan Ngern-Klun & Duanghatai Sripakdee & Worachote Boonsriwong & Sirisuda Siriwattanarungsee & Chaowakit Srimuangwong & Boonsak Hanterdsith & Khankam Chaiwan & Chalard Srisuwan & Surasak Upakut & Kittikhun Moopayak & Roy C. Vogtsberger & Jimmy K. Olson & Kabkaew L. Sukontason

Received: 22 May 2007 /Revised: 23 June 2007 /Accepted: 27 June 2007 /Published online: 24 July 2007 # Springer-Verlag 2007

Abstract This paper presents and discusses 30 cases of tin, bezziana Villeneuve, Chrysomya chani cadavers that had been transferred for Kurahashi, Lucilia cuprina (Wiedemann), Hemipyrellia investigations to the Department of Forensic Medicine, ligurriens (Wiedemann), and two unknown species. Faculty of Medicine, Chiang Mai University, northern of the family [Hydrotaea spinigera Stein, Thailand, from 2000 to 2006. Variable death scenes were nudiseta (Wulp)], Piophilidae [Piophila determined, including forested area and suburban and urban casei (L.)], Phoridae [Megaselia scalaris (Loew)], Sarcoph- outdoor and indoor environments. The specimens found agidae [Parasarcophaga ruficornis (F.) and three unknown in the corpses obtained were the most commonly of the species], and Stratiomyiidae ( sp.) were also col- blow fly of family , and consisted of Chrys- lected from these human remains. Larvae and adults of the omya megacephala (F.), (Macquart) beetle, Dermestes maculatus DeGeer (Coleoptera: Dermes- Chrysomya villeneuvi Patton, Chrysomya nigripes Auber- tidae), were also found in some cases. Chrysomya mega-

K. Sukontason (*) : S. Piangjai : N. Bunchu : T. Chaiwong : H. Kurahashi R. Methanitikorn : R. Ngern-Klun : D. Sripakdee : Department of Medical Entomology, W. Boonsriwong : S. Siriwattanarungsee : S. Upakut : National Institute of Infectious Diseases, K. Moopayak : K. L. Sukontason Tokyo 162-8640, Japan Department of Parasitology, Faculty of Medicine, Chiang Mai University, R. C. Vogtsberger Chiang Mai 50200, Thailand Department of Biology, Midwestern State University, e-mail: [email protected] Wichita Falls, TX 76308, USA

P. Narongchai : C. Kanchai : K. Vichairat : P. Sribanditmongkol : J. K. Olson T. Bhoopat : M. Chockjamsai : S. Vongvivach : W. Samai : Department of Entomology, Texas A&M University, C. Srimuangwong : B. Hanterdsith : K. Chaiwan : C. Srisuwan College Station, TX 77845-2543, USA Department of Forensic Medicine, Faculty of Medicine, Chiang Mai University, Chiang Mai 50200, Thailand 1418 Parasitol Res (2007) 101:1417–1423 cephala and C. rufifacies were the most common species Materials and methods found in the ecologically varied death scene habitats associated with both urban and forested areas, while C. All forensic cases infested with specimens and nigripes was commonly discovered in forested places. S. transferred for investigation to the Department of Forensic nudiseta was collected only from corpses found in an Medicine, Faculty of Medicine, Chiang Mai University, indoor death scene. were received from 2000 to 2006. The personal data (age, sex, location of where the corpses were found, possible cause of death, etc.), if available, were recorded. Photo- Introduction graphs of the corpses and or fly specimens were taken. In cases where there were numerous fly larvae or Forensic entomology—the use of insects and in , collections of each species were made by forensic investigations—has been increasingly gaining assessing different morphological characters (such as hairy international recognition in medico-legal discipline world- or nonhairy and very large maggot) or behavioral wide. Although insects have been used primarily for features (such as skipping). Approximate 80 of the largest- estimating the time elapsed since death or postmortem sized larvae representing each type of maggot were interval, they have also been used for drug verification (Catts collected using long forceps, placed into clean plastic and Goff 1992), determination of antemortem trauma, and boxes, and immediately transported to the Department of verification of the relocation of corpses (Smith 1986;Hall Parasitology, Faculty of Medicine, Chiang Mai University. 1990; Catts and Goff 1992; Benecke 2004). When used to If only a small number of certain fly larvae were collected, estimate the minimum time since death, two basic steps as many as possible were kept as representative specimens. should be taken. The first step is to make the correct The resulting larval specimens were separated into three collection and identifications of the insects and/or arthropods groups. The first one contained about 20 larvae of each type feeding on the corpse, both at the death scene and at autopsy. of maggot, which were killed immediately by immersing in The second step is to apply knowledge of the arthropods’ life a beaker of hot water (≈70°C) for 30 s. In the cases of the cycle in indigenous fauna to determine the age of the third instar larvae, ten were processed using the procedure specimens collected (Erzinclioglu 1983; Introna et al. 1998). of Sukontason et al. (2004) and identified under optics of a Forensic entomology cases have been extensively light microscope to species using the taxonomic keys documented in several regions of the world. Examples of of Ishijima (1967), Greenberg and Kunich (2002), and this are provided for North America by Lord (1990) and Sukontason et al. (2004). Any eggs (first or second instar) Greenberg and Wells (1998) for the USA and by Anderson present were matured, and the resulting larvae were reared (1997) for Canada. In Europe, cases have been documented in rearing boxes until they reached the third instar and later by Introna et al. (1998), by Turchetto et al. (2001) for Italy, by identified as both the third instar larvae and adults. After Starkeby (2001) for Norway, by Benecke (1998), Amendt et identification, about 20 specimens of the second group were al. (2000), Benecke and Lessig (2001), Schroeder et al. kept as entomological evidence in 70% ethanol. The third (2003), Benecke et al. (2004), and Klotzbach et al. (2004)for group of maggots was used to confirm identification by Germany, and by Arnaldos et al. (2005) for Spain. Doc- rearing them to adulthood in the laboratory. The procedure umented cases in Colombia include those by Barreto et al. of fly rearing was previously described by Sukontason et al. (2002) and in Asia by Kulshrestha and Satpathy (2001)for (2004). Adult flies were identified according to the IndiaandLeeetal.(2004) for Malaysia. In Thailand, taxonomic keys of Tumrasvin et al. (1979) and Greenberg Sukontason et al. (2001, 2003, 2005a, b, 2006)havereported and Kunich (2002), and any peculiar fly or insect specimens individual cases of cadavers with insect infestation from the found was confirmed by specialists. northern part of the country since 2001. Although individual case reports are valuable in this subject, a composite review of such cases from one region of Results the world can introduce more understanding concerning their nature and the type entomological evidence that occurs. In Thirty corpses (6 females and 24 males) infested with insect Thailand, many forensic entomological cases have already specimens were included into this study. Geographical been reported; however, there is no paper that reviews them distribution of where corpses were found is shown in all together. Hence, this paper reviews the entomological Fig. 1. Eighteen cases originated in forested area, and specimens collected thus far from 30 human cases trans- another 12 were found in urban and suburban areas ferred for forensic investigation to Chiang Mai University, (outdoor=5, indoor=7; Table 1). Most corpses were in Chiang Mai, Thailand, to provide a more account of the type bloating stage (n=24) when they reached the Faculty of of forensic entomology cases that occur in this country. Medicine, Chiang Mai University, while another four cases Parasitol Res (2007) 101:1417–1423 1419

causes (four cases). The cause of death could not be clarified in the other ten cases (Table 2). Blow flies (family Calliphoridae) of the genera Chrys- omya were predominant in these investigations. They were found infesting in the corpses of 28 cases (93.3%), with the eight known species collected being Chrysomya megace- phala, C. rufifacies, C. nigripes, C. chani, C. villeneuvi, C. bezziana, Lucilia cuprina, and Hemipyrellia ligurriens. Two unknown blow fly species were obtained (Figs. 2 and 3). Species identification of these two specimens could not be performed, as their morphologies did not appear in the taxonomic keys used in our study and they could not be reared to adulthood. C. megacephala and C. rufifacies were the two most common species found in all locations (in 20 and 17 corpses, respectively). In addition, these two species were collected from the same body in 14 cases. More cases found in forested area were infested with C. megacephala (n=11) than C. rufifacies (n=8; Table 3). A similar number of cases (n=9) collected from the urban and/or suburban areas (either outdoor or indoor) was infested with C. megacephala or C. rufifacies (Table 3). Synthesiomyia nudiseta (Family Muscidae) and Parasarcophaga ruficor- nis (Family Sarcophagidae) were observed only for the indoor cases, while C. bezziana, C. chani, C. nigripes, Piophila casei (Family Piophilidae), Dermestes maculatus (Coleoptera: Dermestidae), and Sargus sp. (Family Strat- iomyiidae) were collected only in cases from forested regions (Table 3). Two muscid flies of the family Muscidae, Hydrotaea Fig. 1 Geographical distribution of 30 forensic corpses included in spinigera and S. nudiseta, were retrieved from ten bodies the forensic entomology study of human corpses in northern Thailand (Table 3). Other groups of flies or beetles included two (16°14′–19°56′N; 97°56′–101°21′E) from 2000 to 2006 were mummified. One case was skeletonized, and another was still fresh after being found within 1 day after the Table 2 Cause of death in cases infested with insects in northern disappearance of the victim. The cause of death could be Thailand from 2000 to 2006 clarified in 20 cases (66.7%), with the most common case being hanging (six cases), while gunshot wounds and Cause of death Location homicide by stabbing were the second most common Forest Outdoor urban/ Indoor urban/ suburban suburban

Homicide 9 0 0 Gunshot wound 4 0 0 Table 1 Number of cases found in different areas and seasons in Stabbed with a 40 0 northern Thailand from 2000 to 2006 sharp object Strangulation 1 0 0 Season Location Total Suicide 5 2 Forest Outdoor urban/ Indoor urban/ Hanging 4 1 1 suburban suburban Jumping from a cliff 1 0 0 Poison 0 1 0 Rainy 5 2 3 10 Transportation injury 1 0 0 Winter 7 0 4 11 Underlining disease 0 1 5 Summer 6 3 0 9 Unknown cause 3 2 5 Total 18 5 7 30 Total 18 5 7 1420 Parasitol Res (2007) 101:1417–1423

Fig. 2 Light micrograph of fly collected from human corpses. Caudal view of the third instar of L. cuprina displaying numerous dark Unknown blow fly larva with more or less hairy appearance spots (arrows) in the integument Fig. 3 Light micrograph of fly larva collected from human corpses. Fig. 5 Light micrograph of fly larva collected from human corpses. Enlargement of the caudal view of unknown fly in Fig. 2 showing six Anterior spiracle of unknown fresh fly larva having 28 lobes arranged prominent tubercles along the margin (arrows) in two irregular rows Fig. 4 Light micrograph of fly larva collected from human corpses.

cases having Megaselia scalaris (Family Phoridae), three methyl parathion and carbamate, methomyl). Toxicological having P. casei, two having P. ruficornis, two having analysis, using the cholinesterase inhibitor test, affirmed the Sargus sp., four having D. maculatus, and eight having cause of death in this particular case, and the hypothesis three unidentified species (Table 3). that dark spots in the maggot’s integument associates with In our study, nine cases contained three species, while toxic substance merits further investigation. In the same another eight and seven cases were inhabited by two and case, as shown in Fig. 4, an unknown species of four species, respectively. There was a significantly higher larvae was detected, with an anterior spiracle possessing 28 number of fly species in cases found in the forest rather lobes arranged in two irregular rows (Fig. 5). than urban and/or suburban areas (P=0.26; Mann–Whitney This paper recorded the first occurrence of S. nudiseta in U test). Two to six species of fly maggot (median=3.5) Thailand and under the optics of a light microscope. The were found in each of the cases found in the forest, while cephalic segment was tapering anteriorly, and the body was only one to four species (median=2.5) were found in each bluntly rounded and smooth posteriorly (Fig. 6), resembling body from urban and suburban areas. the third instar of the house fly, Musca domestica L. The A peculiar characteristic of maggots collected from one anterior spiracle was composed of six lobes arranged in a of these cases occurred. Dark spots were observed in the single row. The intersegmental spines between the protho- integument of the third instar of C. megacephala, C. rax and mesothorax were triangular with a pigmented, rufifacies, and L. cuprina in one corpse, with the most pointed tip. These spines were arranged as a group in a row obvious and numerous spots found in L. cuprina (Fig. 4). (Fig. 7). At the caudal end, a pair of posterior spiracles was Association of these dark spots with the cause of death in pronounced (Fig. 8). Each spiracle had a complete this particular case was unknown; however, the presence of peritreme, which was highly chitinized. Each spiracle numerous dark spots was almost the same as in a previous contained three “S-shaped” spiracular slits, radiating from case involving toxic substances (the organophosphate, the prominent button or ecdysial scar (Fig. 9). Parasitol Res (2007) 101:1417–1423 1421

Table 3 List of taxa collected from thirty human cadavers in northern Thailand from 2000 to 2006

Family Species Location Total

Forest Outdoor urban/suburban Indoor urban/suburban

Diptera Calliphoridae (n=28) Chrysomya megacephala 11 3 6 20 Chrysomya rufifacies 84 5 17 10 0 1 Chrysomya chani 10 0 1 Chrysomya nigripes 30 0 3 Chrysomya villeneuvi 60 1 7 Hemipyrellia ligurriens 10 0 1 Lucilia cuprina 21 0 3 Two unidentified 7 1 1 9 Muscidae (n=10) Hydrotaea spinigera 70 0 7 Synthesiomyia nudiseta 00 3 3 Sarcophagidae (n=8) Parasarcophaga ruficornis 00 2 2 Three unidentified larvaea 31 3 7 Phoridae (n=2) Megaselia scalaris 20 0 2 Piophilidae (n=3) Piophila casei 30 0 3 Stratiomyiidae (n=2) Sargus sp. 2 0 0 2 Coleoptera Dermestidae (n=5) Dermestes maculates 40 0 4 One unidentified 3 0 0 3 Hymenoptera Formicidae (n=1) One unidentified 1 0 0 1 a The first species had an anterior spiracle with 24 lobes arranged in two regular rows. The second species had 16 lobes arranged in three irregular rows, while the third species had 28 lobes arranged in two irregular rows.

Discussion Entomological evidence from two cases indicated that P. ruficornis was a flesh fly of forensic importance in northern This study summarized forensic entomology cases investi- Thailand. It has also been reported that this flesh fly species gated in northern Thailand from 2000 to 2006. More has being frequently encountered on the island of Oahu, incidences of C. megacephala and C. rufifacies occurred in Hawaii, and regarded as an early invader of remains (Nolte human cadavers in Thailand when compared to those et al. 1992). Likewise, it has also been included as one of previously reported in Malaysia (Cheong et al. 1973; Lee the necrophagous arthropods collected from domestic swine et al. 2004), Colombia (Barreto et al. 2002), or the USA (Sus scrofa L.), an model in forensic entomology on and Canada, where these two fly species are regarded as Oahu Island (Davis and Goff 2000). Investigation of the forensically important (Byrd and Castner 2001). Of the effects of the drug, phencyclidine, on the development rate eight species of puparial blow flies observed, only C. of P. ruficornis in decomposing rabbit tissue was conducted nigripes represented the unusual behavior of adhering by Goff et al. (1994). Geographically, this flesh fly has been together side by side on the exposed bone. Greenberg and recorded in many regions to include Thailand, India, Sri Kunich (2002) cited the biology of some blow flies in Lanka, Nepal, China, Malaysia, Taiwan, the Philippines, Malaysia and found that C. nigripes pupariated on twigs, Indonesia, Japan, Africa, Brazil, Hawaii (USA), Madagas- leaves, and wire mesh above the ground or near a car, Mariana Islands, Moluccas, Samoa, Socotra, and Papua decomposing animal, while C. chani pupariated on exposed New Guinea (Kano and Shinonaga 1994). bones and skin. It is interesting that the calliphorid flies found A recent case from Malaysia demonstrated that C. in corpses in northern Thailand were similar to those found in bezziana was a forensically important fly species but of cadavers in Malaysia, despite these two locations being about minimal consequence (Lee et al. 2004). The presence of 1,500 km apart (Lee et al. 2004). From these results, it is this species in human cadavers in Thailand corresponded surmised that the forensically important flies located between with events in Malaysia, although C. bezziana has been the central and southern parts of Thailand should be the same generally claimed as -producing flies in many parts of those found in the northern part of the country. of the world. Regarding this, C. bezziana should not be 1422 Parasitol Res (2007) 101:1417–1423

Fig. 6 Light micrograph of S. nudiseta larva collected from a human Fig. 8 Light micrograph of S. nudiseta larva collected from a human corpse. Anterior end showing internal cephalopharyngeal skeleton (C), corpse. Posterior spiracles (PS) at the caudal segment showing a anterior spiracle (as), with six lobes arranged in a single row, and highly chitinized, complete peritreme intersegmental spines (s) between the prothorax and mesothorax Fig. 9 Light micrograph of S. nudiseta larva collected from human Fig. 7 Light micrograph of S. nudiseta larva collected from a human corpse. Left spiracle illustrating three “S-shaped” spiracular slits (S), corpse. Intersegmental spines grouped in a row between the prothorax and radiating from the prominent button (B) or ecdysial scar mesothorax, each showing triangular shape with a pigmented, pointed tip

excluded from the list of forensically important flies, (Goff 2000). Geographically, S. nudiseta prevails in especially in tropical regions. tropicopolitan regions, at temperatures between the 20°C The investigation of flies in the corpses of this study annual isotherms (Skidmore 1985). It has also been clearly showed the forensic importance of P. casei, known recorded in the Ishigaki Island of Japan (Kano et al. as cheese skipper or jumping maggot. During the entomol- 1964), Norfolk Island (Smithers 1998), subtropical regions, ogical collection from these three cases, the P. casei larva’s and the USA (Byrd and Castner 2001). Accordingly, larvae skipping habit of 2 to 3 in. was obvious. Occurrence of this of S. nudiseta may be found to associate with human fly maggot in cases in Thailand was observed during both corpsesinsuchareaandmaybeusefulinforensic skeletonization phase of succession and of investigations, as previously documented in Hawaii (Goff the corpse. Benecke (1998) also recorded an entomological 2000). analysis using the presence of P. casei in the decomposed To gain full use of the potential of insects as entomol- corpse of a heroin user, who had been missing for about ogical evidence in forensic investigations, more biological 4 months. aspects (e.g., morphology, biology, life table, insect This paper gives the first recording of the forensic succession, developmental rate) of these insect species, importance of S. nudiseta in Thailand, but this species was especially C. megacephala and C. rufifacies, merits further found in cadavers from indoor death scenes. This phenom- investigation. enon was also associated with S. nudiseta’s indoor occurrence in Malaysia (Lee et al. 2004) and Hawaii (Goff 2000). Investigation of the case in Hawaii indicated that Acknowledgments This work received support from the Faculty of Medicine Research Fund and the Thailand Research Fund larval specimens of S. nudiseta provided an estimated time (RMU4980007). We thank the Chiang Mai University for funding of death as well as an indication of the death scene location reprint costs. Parasitol Res (2007) 101:1417–1423 1423

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