Parasitology Research

, 101:1417

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

Authors

    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Paitoon Narongchai
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Chaturong Kanchai
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Karnda Vichairat
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Pongruk Sribanditmongkol
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Tanin Bhoopat
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Hiromu Kurahashi
    • Department of Medical EntomologyNational Institute of Infectious Diseases
  • Manoch Chockjamsai
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Somsak Piangjai
    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Nophawan Bunchu
    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Somsak Vongvivach
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Wirachai Samai
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Tarinee Chaiwong
    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Rungkanta Methanitikorn
    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Rachadawan Ngern-Klun
    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Duanghatai Sripakdee
    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Worachote Boonsriwong
    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Sirisuda Siriwattanarungsee
    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Chaowakit Srimuangwong
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Boonsak Hanterdsith
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Khankam Chaiwan
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Chalard Srisuwan
    • Department of Forensic Medicine, Faculty of MedicineChiang Mai University
  • Surasak Upakut
    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Kittikhun Moopayak
    • Department of Parasitology, Faculty of MedicineChiang Mai University
  • Roy C. Vogtsberger
    • Department of BiologyMidwestern State University
  • Jimmy K. Olson
    • Department of EntomologyTexas A&M University
  • Kabkaew L. Sukontason
    • Department of Parasitology, Faculty of MedicineChiang Mai University
Original Paper

DOI: 10.1007/s00436-007-0659-8

Cite this article as:
Sukontason, K., Narongchai, P., Kanchai, C. et al. Parasitol Res (2007) 101: 1417. doi:10.1007/s00436-007-0659-8

Abstract

This paper presents and discusses 30 cases of cadavers that had been transferred for forensic entomology investigations to the Department of Forensic Medicine, Faculty of Medicine, Chiang Mai University, northern Thailand, from 2000 to 2006. Variable death scenes were determined, including forested area and suburban and urban outdoor and indoor environments. The fly specimens found in the corpses obtained were the most commonly of the blow fly of family Calliphoridae, and consisted of Chrysomya megacephala (F.), Chrysomya rufifacies (Macquart) Chrysomya villeneuvi Patton, Chrysomya nigripes Aubertin, Chrysomya bezziana Villeneuve, Chrysomya chani Kurahashi, Lucilia cuprina (Wiedemann), Hemipyrellia ligurriens (Wiedemann), and two unknown species. Flies of the family Muscidae [Hydrotaea spinigera Stein, Synthesiomyia nudiseta (Wulp)], Piophilidae [Piophila casei (L.)], Phoridae [Megaselia scalaris (Loew)], Sarcophagidae [Parasarcophaga ruficornis (F.) and three unknown species], and Stratiomyiidae (Sargus sp.) were also collected from these human remains. Larvae and adults of the beetle, Dermestes maculatus DeGeer (Coleoptera: Dermestidae), were also found in some cases. Chrysomya megacephala and C. rufifacies were the most common species found in the ecologically varied death scene habitats associated with both urban and forested areas, while C. nigripes was commonly discovered in forested places. S. nudiseta was collected only from corpses found in an indoor death scene.

Introduction

Forensic entomology—the use of insects and arthropods in forensic investigations—has been increasingly gaining international recognition in medico-legal discipline worldwide. Although insects have been used primarily for estimating the time elapsed since death or postmortem interval, they have also been used for drug verification (Catts and Goff 1992), determination of antemortem trauma, and verification of the relocation of corpses (Smith 1986; Hall 1990; Catts and Goff 1992; Benecke 2004). When used to estimate the minimum time since death, two basic steps should be taken. The first step is to make the correct collection and identifications of the insects and/or arthropods feeding on the corpse, both at the death scene and at autopsy. The second step is to apply knowledge of the arthropods’ life cycle in indigenous fauna to determine the age of the specimens collected (Erzinclioglu 1983; Introna et al. 1998).

Forensic entomology cases have been extensively documented in several regions of the world. Examples of this are provided for North America by Lord (1990) and Greenberg and Wells (1998) for the USA and by Anderson (1997) for Canada. In Europe, cases have been documented by Introna et al. (1998), by Turchetto et al. (2001) for Italy, by Starkeby (2001) for Norway, by Benecke (1998), Amendt et al. (2000), Benecke and Lessig (2001), Schroeder et al. (2003), Benecke et al. (2004), and Klotzbach et al. (2004) for Germany, and by Arnaldos et al. (2005) for Spain. Documented cases in Colombia include those by Barreto et al. (2002) and in Asia by Kulshrestha and Satpathy (2001) for India and Lee et al. (2004) for Malaysia. In Thailand, Sukontason et al. (2001, 2003, 2005a, b, 2006) have reported individual cases of cadavers with insect infestation from the 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 the world can introduce more understanding concerning their nature and the type entomological evidence that occurs. In Thailand, many forensic entomological cases have already been reported; however, there is no paper that reviews them all together. Hence, this paper reviews the entomological specimens collected thus far from 30 human cases transferred for forensic investigation to Chiang Mai University, Chiang Mai, Thailand, to provide a more account of the type of forensic entomology cases that occur in this country.

Materials and methods

All forensic cases infested with insect specimens and transferred for investigation to the Department of Forensic Medicine, Faculty of Medicine, Chiang Mai University, 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. Photographs of the corpses and insects or fly specimens were taken. In cases where there were numerous fly larvae or maggots, collections of each species were made by assessing different morphological characters (such as hairy or nonhairy maggot and very large maggot) or behavioral features (such as skipping). Approximate 80 of the largest-sized larvae representing each type of maggot were collected using long forceps, placed into clean plastic boxes, and immediately transported to the Department of Parasitology, Faculty of Medicine, Chiang Mai University. If only a small number of certain fly larvae were collected, as many as possible were kept as representative specimens. The resulting larval specimens were separated into three groups. The first one contained about 20 larvae of each type of maggot, which were killed immediately by immersing in a beaker of hot water (≈70°C) for 30 s. In the cases of the third instar larvae, ten were processed using the procedure of Sukontason et al. (2004) and identified under optics of a light microscope to species using the taxonomic keys of Ishijima (1967), Greenberg and Kunich (2002), and Sukontason et al. (2004). Any eggs (first or second instar) present were matured, and the resulting larvae were reared in rearing boxes until they reached the third instar and later identified as both the third instar larvae and adults. After identification, about 20 specimens of the second group were kept as entomological evidence in 70% ethanol. The third group of maggots was used to confirm identification by rearing them to adulthood in the laboratory. The procedure of fly rearing was previously described by Sukontason et al. (2004). Adult flies were identified according to the taxonomic keys of Tumrasvin et al. (1979) and Greenberg and Kunich (2002), and any peculiar fly or insect specimens found was confirmed by specialists.

Results

Thirty corpses (6 females and 24 males) infested with insect specimens were included into this study. Geographical distribution of where corpses were found is shown in Fig. 1. Eighteen cases originated in forested area, and another 12 were found in urban and suburban areas (outdoor = 5, indoor = 7; Table 1). Most corpses were in bloating stage (n = 24) when they reached the Faculty of Medicine, Chiang Mai University, while another four cases were mummified. One case was skeletonized, and another was still fresh after being found within 1 day after the disappearance of the victim. The cause of death could be clarified in 20 cases (66.7%), with the most common case being hanging (six cases), while gunshot wounds and homicide by stabbing were the second most common causes (four cases). The cause of death could not be clarified in the other ten cases (Table 2).
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Fig. 1

Geographical distribution of 30 forensic corpses included in the forensic entomology study of human corpses in northern Thailand (16°14′–19°56′N; 97°56′–101°21′E) from 2000 to 2006

Table 1

Number of cases found in different areas and seasons in northern Thailand from 2000 to 2006

Season

Location

Total

Forest

Outdoor urban/suburban

Indoor urban/suburban

Rainy

5

2

3

10

Winter

7

0

4

11

Summer

6

3

0

9

Total

18

5

7

30

Table 2

Cause of death in cases infested with insects in northern Thailand from 2000 to 2006

Cause of death

Location

Forest

Outdoor urban/suburban

Indoor urban/suburban

Homicide

9

0

0

 Gunshot wound

4

0

0

 Stabbed with a sharp object

4

0

0

 Strangulation

1

0

0

Suicide

 

5

2

 Hanging

4

1

1

 Jumping from a cliff

1

0

0

 Poison

0

1

0

Transportation injury

1

0

0

Underlining disease

0

1

5

Unknown cause

3

2

5

Total

18

5

7

Blow flies (family Calliphoridae) of the genera Chrysomya 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 megacephala, 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 ruficornis (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 Stratiomyiidae) were collected only in cases from forested regions (Table 3).
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Fig. 2

Light micrograph of fly larva collected from human corpses. Unknown blow fly larva with more or less hairy appearance

Fig. 3

Light micrograph of fly larva collected from human corpses. Enlargement of the caudal view of unknown fly in Fig. 2 showing six prominent tubercles along the margin (arrows)

Fig. 4

Light micrograph of fly larva collected from human corpses. Caudal view of the third instar of L. cuprina displaying numerous dark spots (arrows) in the integument

Fig. 5

Light micrograph of fly larva collected from human corpses. Anterior spiracle of unknown fresh fly larva having 28 lobes arranged in two irregular rows

Table 3

List of arthropod 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

8

4

5

17

Chrysomya bezziana

1

 

0

0

 

1

Chrysomya chani

1

 

0

0

 

1

Chrysomya nigripes

3

 

0

0

 

3

Chrysomya villeneuvi

6

0

1

7

Hemipyrellia ligurriens

1

 

0

0

 

1

Lucilia cuprina

2

1

0

3

Two unidentified

7

 

1

1

 

9

Muscidae (n = 10)

Hydrotaea spinigera

7

0

0

7

Synthesiomyia nudiseta

0

0

3

3

Sarcophagidae (n = 8)

Parasarcophaga ruficornis

0

0

2

2

Three unidentified larvaea

3

1

3

7

Phoridae (n = 2)

Megaselia scalaris

2

0

0

2

Piophilidae (n = 3)

Piophila casei

3

0

0

3

Stratiomyiidae (n = 2)

Sargus sp.

2

0

0

2

Coleoptera

Dermestidae (n = 5)

Dermestes maculates

4

0

0

4

One unidentified

3

0

0

3

Hymenoptera

Formicidae (n = 1)

One unidentified

1

0

0

1

aThe 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.

Two muscid flies of the family Muscidae, Hydrotaea spinigera and S. nudiseta, were retrieved from ten bodies (Table 3). Other groups of flies or beetles included two cases having Megaselia scalaris (Family Phoridae), three having P. casei, two having P. ruficornis, two having Sargus sp., four having D. maculatus, and eight having three unidentified species (Table 3).

In our study, nine cases contained three species, while another eight and seven cases were inhabited by two and four species, respectively. There was a significantly higher number of fly species in cases found in the forest rather than urban and/or suburban areas (P = 0.26; Mann–Whitney U test). Two to six species of fly maggot (median = 3.5) were found in each of the cases found in the forest, while only one to four species (median = 2.5) were found in each body from urban and suburban areas.

A peculiar characteristic of maggots collected from one of these cases occurred. Dark spots were observed in the integument of the third instar of C. megacephala, C. rufifacies, and L. cuprina in one corpse, with the most obvious and numerous spots found in L. cuprina (Fig. 4). Association of these dark spots with the cause of death in this particular case was unknown; however, the presence of numerous dark spots was almost the same as in a previous case involving toxic substances (the organophosphate, methyl parathion and carbamate, methomyl). Toxicological analysis, using the cholinesterase inhibitor test, affirmed the cause of death in this particular case, and the hypothesis that dark spots in the maggot’s integument associates with toxic substance merits further investigation. In the same case, as shown in Fig. 4, an unknown species of flesh fly larvae was detected, with an anterior spiracle possessing 28 lobes arranged in two irregular rows (Fig. 5).

This paper recorded the first occurrence of S. nudiseta in Thailand and under the optics of a light microscope. The cephalic segment was tapering anteriorly, and the body was bluntly rounded and smooth posteriorly (Fig. 6), resembling the third instar of the house fly, Musca domestica L. The anterior spiracle was composed of six lobes arranged in a single row. The intersegmental spines between the prothorax and mesothorax were triangular with a pigmented, pointed tip. These spines were arranged as a group in a row (Fig. 7). At the caudal end, a pair of posterior spiracles was pronounced (Fig. 8). Each spiracle had a complete peritreme, which was highly chitinized. Each spiracle contained three “S-shaped” spiracular slits, radiating from the prominent button or ecdysial scar (Fig. 9).
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Fig. 6

Light micrograph of S. nudiseta larva collected from a human corpse. Anterior end showing internal cephalopharyngeal skeleton (C), anterior spiracle (as), with six lobes arranged in a single row, and intersegmental spines (s) between the prothorax and mesothorax

Fig. 7

Light micrograph of S. nudiseta larva collected from a human corpse. Intersegmental spines grouped in a row between the prothorax and mesothorax, each showing triangular shape with a pigmented, pointed tip

Fig. 8

Light micrograph of S. nudiseta larva collected from a human corpse. Posterior spiracles (PS) at the caudal segment showing a highly chitinized, complete peritreme

Fig. 9

Light micrograph of S. nudiseta larva collected from human corpse. Left spiracle illustrating three “S-shaped” spiracular slits (S), radiating from the prominent button (B) or ecdysial scar

Discussion

This study summarized forensic entomology cases investigated in northern Thailand from 2000 to 2006. More incidences of C. megacephala and C. rufifacies occurred in human cadavers in Thailand when compared to those previously reported in Malaysia (Cheong et al. 1973; Lee et al. 2004), Colombia (Barreto et al. 2002), or the USA and Canada, where these two fly species are regarded as forensically important (Byrd and Castner 2001). Of the eight species of puparial blow flies observed, only C. nigripes represented the unusual behavior of adhering together side by side on the exposed bone. Greenberg and Kunich (2002) cited the biology of some blow flies in Malaysia and found that C. nigripes pupariated on twigs, leaves, and wire mesh above the ground or near a decomposing animal, while C. chani pupariated on exposed bones and skin. It is interesting that the calliphorid flies found in corpses in northern Thailand were similar to those found in cadavers in Malaysia, despite these two locations being about 1,500 km apart (Lee et al. 2004). From these results, it is surmised that the forensically important flies located between the central and southern parts of Thailand should be the same of those found in the northern part of the country.

Entomological evidence from two cases indicated that P. ruficornis was a flesh fly of forensic importance in northern Thailand. It has also been reported that this flesh fly species has being frequently encountered on the island of Oahu, Hawaii, and regarded as an early invader of remains (Nolte et al. 1992). Likewise, it has also been included as one of the necrophagous arthropods collected from domestic swine (Sus scrofa L.), an animal model in forensic entomology on Oahu Island (Davis and Goff 2000). Investigation of the effects of the drug, phencyclidine, on the development rate of P. ruficornis in decomposing rabbit tissue was conducted by Goff et al. (1994). Geographically, this flesh fly has been recorded in many regions to include Thailand, India, Sri Lanka, Nepal, China, Malaysia, Taiwan, the Philippines, Indonesia, Japan, Africa, Brazil, Hawaii (USA), Madagascar, Mariana Islands, Moluccas, Samoa, Socotra, and Papua New Guinea (Kano and Shinonaga 1994).

A recent case from Malaysia demonstrated that C. bezziana was a forensically important fly species but of minimal consequence (Lee et al. 2004). The presence of this species in human cadavers in Thailand corresponded with events in Malaysia, although C. bezziana has been generally claimed as myiasis-producing flies in many parts of the world. Regarding this, C. bezziana should not be excluded from the list of forensically important flies, especially in tropical regions.

The investigation of flies in the corpses of this study clearly showed the forensic importance of P. casei, known as cheese skipper or jumping maggot. During the entomological collection from these three cases, the P. casei larva’s skipping habit of 2 to 3 in. was obvious. Occurrence of this fly maggot in cases in Thailand was observed during both skeletonization phase of succession and decomposition of the corpse. Benecke (1998) also recorded an entomological analysis using the presence of P. casei in the decomposed corpse of a heroin user, who had been missing for about 4 months.

This paper gives the first recording of the forensic importance of S. nudiseta in Thailand, but this species was found in cadavers from indoor death scenes. This phenomenon 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 larval specimens of S. nudiseta provided an estimated time of death as well as an indication of the death scene location (Goff 2000). Geographically, S. nudiseta prevails in tropicopolitan regions, at temperatures between the 20°C annual isotherms (Skidmore 1985). It has also been recorded in the Ishigaki Island of Japan (Kano et al. 1964), Norfolk Island (Smithers 1998), subtropical regions, and the USA (Byrd and Castner 2001). Accordingly, larvae of S. nudiseta may be found to associate with human corpses in such area and may be useful in forensic investigations, as previously documented in Hawaii (Goff 2000).

To gain full use of the potential of insects as entomological evidence in forensic investigations, more biological aspects (e.g., morphology, biology, life table, insect succession, developmental rate) of these insect species, especially C. megacephala and C. rufifacies, merits further investigation.

Acknowledgments

This work received support from the Faculty of Medicine Research Fund and the Thailand Research Fund (RMU4980007). We thank the Chiang Mai University for funding reprint costs.

Copyright information

© Springer-Verlag 2007