Forensic Science International 120 (2001) 4247

Entomotoxicology$
Francesco Intronaa,*, Carlo Pietro Campobassoa, Madison Lee Goffb
a

Section of Legal Medicine (D.I.M.I.M.P.), University of Bari, Piazza G. Cesare, Policlinico, Bari 70100, Italy
b
Department of Entomology, University of Hawaii at Manoa, 3050 Maile Way, Honolulu, HI 96822, USA

Abstract
Entomotoxicology is a relatively new branch of forensic entomology. The potential use of insects for detecting drugs and
other toxins in decomposing tissues has been widely demonstrated. In death investigations, Diptera and other arthropods can
be reliable alternate specimens for toxicological analyses in the absence of tissues and uids normally taken for such purposes.
Entomotoxicology also investigates the effects caused by drugs and toxins on arthropod development in order to assist the
forensic postmortem interval estimates. However, several remarks on the limitations of entomotoxicology have been
highlighted recently. In this paper, the implications for the practice of this forensic procedure are fully reviewed.
# 2001 Elsevier Science Ireland Ltd. All rights reserved.
Keywords: Forensic entomology; Forensic toxicology; Drug analysis; Insect development; Postmortem interval

1. Introduction
Entomotoxicology studies the application of toxicological analysis to carrion-feeding insects in order to identify
drugs and toxins present on intoxicated tissues. Entomotoxicology also investigates the effects caused by such substances on arthropod development in order to assist the
forensic PMI estimates [1]. The increase in drug-related
deaths (mainly heroin and cocaine) or deaths somehow
connected to accidental or suicidal consumption of poisoning and/or toxic substances justies the great interest
aroused by this discipline in forensic medicine.
In skeletonised bodies or bodies in advanced decomposition, where more traditional sources, such as blood, urine or
internal organs are not available, insects may serve as
reliable alternate specimens for toxicological analyses.
Insects can be analysed quite easily after homogenisation
of the most representative specimens by common toxicological procedures such as radio-immune analysis (RIA), gas
chromatography (GC), thin layer chromatography (TLC),
high pressure liquid chromatography (HPLCMS) and gas
mass analysis (GCMS). Diptera larvae-feeding on intoxicated human tissues introduce into their own metabolism
drugs and toxins taken by the person when still alive. The
$

Paper presented at the International Seminar in Forensic

Entomology (Bari, Italy, 1214 November 1998).
*
Corresponding author.

transfer of these substances from the human organism to

Diptera is not accomplished only at this level of the food
chain but continues also in beetles predating on blow y
larvae. Also Coleoptera can in their turn be submitted to
toxicological analysis for forensic purposes. A secondary
bioaccumulation has been noted in these predatory beetles.
2. Detection of drugs and toxicological analyses
Already in the late 1970s, Sohal and Lamb [2,3] demonstrated the accumulation of various metals including copper,
iron and zinc in adults of Musca domestica Linnaeus (Muscidae). Similarly, Nuorteva [4] reported the presence of
mercury in larvae, puparia and adults of Calliphoridae reared
on sh-containing mercury in methylated form. Mercury
was also detected in Staphylinidae predating on Diptera
larvae reared on sh. These entomotoxicological experiences were applied to the forensic case of a female cadaver
found in advanced decomposition in a rural area of Finland
and extensively colonised by Diptera larvae [5]. The low
concentration of mercury measured by the toxicological
analysis of adult ies made it possible to locate the geographical area where the victim came from, an area relatively free from mercury pollution.
Concerning the detection of poisons, as early as in 1958
Utsumi [6] observed that Diptera were attracted in a different
manner by rat carcasses depending on the poison causing

0379-0738/01/$ see front matter # 2001 Elsevier Science Ireland Ltd. All rights reserved.
PII: S 0 3 7 9 - 0 7 3 8 ( 0 1 ) 0 0 4 1 8 - 2

F. Introna et al. / Forensic Science International 120 (2001) 4247

death. In 1985, Leclercq and Brahy [7] rst demonstrated the

presence of arsenic in Diptera from the families of Piophilidae, Psychodidae and Fanniidae in a case of arsenic
poisoning occurred in France. In a suicidal poisoning,
Gunatilake and Goff [8] detected organophosphates
(malathion) in maggots of Chrysomya megacephala (Fabricius) (Calliphoridae) and Chrysomya rufacies (Macquart)
(Calliphoridae) submitted to toxicological analysis by using
GC.
Regarding the detection of prescription drugs, Beyer et al.
[9] illustrated the suicide with barbiturates of a 22-year-old
woman found in initial skeletonisation, 14 days after she had
last been seen alive. On account of the advanced decomposition, no organic uids and/or tissues were available for
toxicological analysis. The most representative Cochliomyia
macellaria (Fabricius) (Calliphoridae) larvae were analysed
by GC and TLC; the results revealed the presence of
phenobarbital. Other cases illustrating the potential of entomotoxicology in forensic cases are described by Kintz et al.
[10]. In a corpse, found approximatively 2 months after
death, toxicological analysis by liquid chromatography of
some organs (heart, lungs, liver and kidney) and of Calliphoridae larvae showed the presence of ve prescription
drugs among which benzodiazepines (triazolam, oxazepam), barbiturates (phenobarbital) and tricyclic antidepressants (alimemazine and clomipramine). Comparative
analysis of toxicological ndings showed greater sensitivity
of the method using Diptera larvae as samples rather than
cadaver tissues. Triazolam, in fact, was not detected in the
spleen and kidney but only in maggots. In other cases, Kintz
et al. [11] established a correlation between concentrations
of the drugs in maggots and human tissues. They detected
bromazepam and levomepromazine in cerebral material,
clavicle and Piophila casei (Linnaeus) (Piophilidae) larvae
found in completely decayed human remains. The same
authors [12] detected morphine and phenobarbital from
Calliphoridae larvae which had developed on the cadaver
of a chronic heroin abuser found putreed about 10 days
after death and from internal organs (blood, liver, heart,
kidney and brain). Both substances were analysed by using
liquid GC and uorescence polarisation immuno-assay
(FPIA). Always by FPIA, Introna et al. [13] obtained
positive results on empty puparia of Calliphora vicina
(Robineau-Desvoidy) (Calliphoridae) which had been
reared on substrates containing known concentrations of
morphine (greater than 10 mcg/g).
Wohlenberg et al. [14] identied by GCMS nortriptyline
from larvae found on the skeletonised remains of a 40-yearold man and on fragments of muscle, bone, skin and hair.
Similarly, Goff et al. [15] demonstrated amitriptyline and
nortriptyline from maggots and empty pupariae of Diptera
which had developed on rabbit carcasses administered with
different dosages of amitriptyline when still alive. On the
mummied remains of a woman whose death had occurred 2
years before the nding of the body, Miller et al. [16] showed
the presence of amitriptyline and nortriptyline in desiccated

43

cerebral fragments and from stomach contents as well as

from Phoridae puparial cases, cast beetle (Dermestidae)
skins and beetle fecal material; the frass was found
copiously near the corpse. In this study, the authors presented two extraction techniques (strong acid and strong
base) modifying the common extraction protocols from hair
[17,18] as these were applied to an analysis of material
having similar characteristics. Insect puparial cases consist
largely of chitin (a complex polysaccharide composed
essentially of n-acetylglucosamine and glucosamine), similar to that of human hair accounting for 2550% of exoskeleton dry weight; the other half being protein complexes.
Results showed that amitriptyline concentrations were
greater in puparia than exuviae or frass. This most likely
reects the food source preferences characteristic of the
carrion ies and beetles examined. Phoridae have a propensity for soft tissues where drug concentrations are likely to
be higher, while Dermestidae feed primarily on dried integument.
Regarding narcotic intoxications, Introna et al. [19]
demonstrated with the RIA, that the presence of opiates
(morphine) in larvae developed on liver collected from
bodies in which the cause of death was identied as opiate
intoxication. Regression analysis comparing the concentrations of opiates found in the larvae with those found in the
liver tissues resulted in a signicant correlation of
r 0:790. Similar results on opiates were also illustrated
by Goff et al. [20,21] who administered varied dosages of
cocaine and heroin to laboratory rabbits. Opiate toxicological analysis (codeine and morphine) yielded positive
results also on Calliphoridae larvae developed on a decomposed cadaver [22].
Although, several of these studies describe a correlation
between drug concentrations in larvae and in human tissues
on which they were feeding, other studies have not observed
any correlation or have found the concentrations in larvae to
be signicantly lower than those detected in tissues [10,20
23]. For instance, concentrations of morphine in larvae
reared on rabbit carcasses previously intoxicated were
30100 times lower than the concentrations found in the
tissues based on the results illustrated by Hedouin et al. [24].
Nolte et al. [23] used toxicological analysis of Diptera
larvae to determine cocaine intoxication in an almost completely skeletonised cadaver of a 29-year-old intravenous
drug abuser whose body was found 5 months after he had
last been seen alive. Although, cocaine is generally labile
and rapidly broken down by both enzymatic [25] and nonenzymatic [26] mechanisms, the authors were able to detect
cocaine and its major metabolite (benzoylecgonine) both in
larvae associated with human remains and in decomposing
skeletal muscle using GC and GCMS techniques. However,
quantitiuation by GC was not possible in muscle samples
because of interference by tissue-decomposition products.
As previously illustrated by Kintz et al. [12], the larvae in
this case too provided a more suitable specimen without any
decomposition interference.

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F. Introna et al. / Forensic Science International 120 (2001) 4247

Manhoff et al. [27] were able to detect by GCMS

cocaine in mummied tissues, in bloody decomposition
uids and also in Calliphoridae larvae and beetle faeces
collected from a set of decomposed human remains. Cocaine
and other drugs have been identied in the protein matrix of
human hair of drug abusers [17,18] and they may be
detectable for years following death (even in mummies
thousands of years old). These substances can be deposited
even in the protein matrix of the puparial cases. In our
experience (Introna et al., data not published) empty pupariae were also positive in cocaine analysis.
3. Effect of drugs on Diptera development
Previous studies focused on the potential use of insects as
alternate specimens for toxicological analyses; the results
demonstrate the usefulness of testing insects associated with
decomposed remains. A drug or toxin can be detected in the
larvae when its rate of absorption exceeds the rate of
elimination, but it is not yet known exactly how larvae
bioaccumulate or eliminate drugs, and how these affect
larval development.
The effects of drugs and toxins on the rate of Diptera
development is a paramount matter to solve before using
maggots for PMI determination. For instance, in the case of
malathion poisoning reported by Gunatilake and Goff [8],
the development stages of both C. megacephala and C.
rufacies were indicative of a minimum postmortem interval
of 5 days, whereas the victim had last been seen alive 8 days
prior to the discovery of the body. In outdoor Hawaiian
situations and for a postmortem interval of 1 week, many
more species of ies and predatory beetles (such as Staphylinidae and Histeridae) would have been expected in
association with human remains. The presence of only two
species of y larvae on the corpse supported the conclusions
of the authors that the malathion in the tissues delayed
invasion of the remains by various arthropod taxa and thus
oviposition for several days.
Goff et al. [15,20,21,2830] have investigated in detail
the effects of amitriptyline, cocaine, heroin, methamphetamine, phencyclidine and 3,4-methylendioxyamethamphetamine on the growth of Boettcherisca peregrina (RobineauDesvoidy) and Parasarcophaga rucornis (Fabricius), two
species of Sarcophagidae very common in Hawaii.
Studying the effects of cocaine on rate of development in
Sarcophagidae (B. peregrina) Goff et al. [20] demonstrated
that maggots develop more rapidly 36 h after hatching if
reared on liver and/or spleen of rabbits previously administered with a lethal dose of cocaine or twice such a dose. The
acceleration of larval development continued for the following 76 h after hatching. Total development times required for
pupariation and adult emergence were shortened correspondingly. Regarding the development of intoxicated larvae Lord [31] describes the case of a 20-year-old woman
found in the early bloated stage colonised by maggots of

Lucilia sericata (Meigen) (Calliphoridae) and Cynomyopsis

cadaverina (RobineauDesvoidy) (Calliphoridae) on the
face and upper torso. Most of the maggots were 69 mm
in total length or smaller indicating a PMI of 7 days, while
just a single maggot from the nasopharyngeal area measured
17.7 mm in total length indicating a period of 3 weeks. The
fast growth of this big larva appeared to be dependent on the
amount of cocaine in the nasal region. Subsequent investigation showed the victim was a cocaine abuser who had
snorted cocaine shortly before death.
Studying the effects of heroin on development of Sarcophagidae (B. peregrina) fed on intoxicated rabbit tissues
Goff et al. [21] observed that maggots grow at rates signicantly faster from 18 to 96 h, when larvae reached their
maximum length. The difference observed in the rates of
development were sufcient to alter postmortem interval
estimates, if the effect of heroin on the Diptera growth cycle
is not taken into consideration, based on larval development
by up to 29 h and estimates based on puparial development
by 1838 h.
Based on the results of Bourel et al. [32] if the presence of
morphine in the tissues is not considered then an underestimation of the postmortem interval of 24 h is possible for
larvae of L. sericata measuring from 8 to 14 mm total length.
The authors observed larvae of L. sericata developing at a
slower rate than those reared on rabbit carcass receiving less
than 50.0 mg/h of morphine.
Regarding the effects of methamphetamine (sympathomimetic substance active on the central system) on the
developmental patterns of P. rucornis, Goff et al. [28]
illustrated substantial analogies with the studies carried
out on heroin [21] and cocaine [20] as well as signicant
differences. An accelerated rate of development was
observed from 24 to 60 h only in maggots reared on rabbit
tissues containing lethal doses; following 60 h, the rate of
growth for the median lethal dosage colony slowed down.
Unlike the situation with heroin [21] and cocaine [20], larvae
from all colonies fed on rabbits receiving methamphetamine
were smaller at maximum length (attained earlier) than those
from the control colony. As observed for heroin [21], but not
for cocaine [20], there was a relationship between the
concentration of methamphetamine (and amphetamine) in
tissues and the duration of the puparial stage. Finally, it was
demonstrated that differences observed in the rates of development were sufcient to alter postmortem interval estimates based on larval development by up to 18 h and
estimates based on puparial development by up to 48 h.
The study carried out by Goff et al. [15] on the effects of
amitriptyline (a tricyclic antidepressant) always on the
Sarcophagid y P. rucornis showed no signicant differences among colonies in the rate of development to maximum size. Once maximum size had been attained, a
prolonged postfeeding period was recorded and thus duration of the larval stage was signicantly longer. In colonies
reared on tissues receiving the 600 and 1000 mg dosages of
amitriptyline (producing concentrations corresponding

F. Introna et al. / Forensic Science International 120 (2001) 4247

approximately to median lethal and 2.0 times median lethal

dosages based on body weight) puparia were signicantly
greater both in terms of length and weight. Results of this
study indicate that an estimate of PMI based on the duration
of the puparial stage could be in error by up to 47 h; when
this is combined with the error possibly resulting from the
increased duration of the larval stage, the total error could be
up to 77 h.
Goff et al. [29] also investigated the effects of another
commonly abused drug (phencyclidine) on the development
of the P. rucornis. Phencyclidine was introduced in the 70 s
as a smoking or snorting drug and is actually a tranquilizer,
easily found on the market mainly for veterinary use. Unlike
earlier studies dealing with cocaine [20], heroin [21] and
methamphetamine [28], there was not a direct relationship
between the dosage of phencyclidine administered and the
concentration of the drug detected in the tissues. As
observed with amitriptyline [15] no signicant differences
in larval growth rate were observed among the colonies,
although the duration of the postfeeding period was shorter
for larvae fed on tissues containing the drug. Mean differences
in duration of the larval stage in treated colonies ranged from
3 to 17 h less than required by the larvae in the control
colony. Similar to heroin, duration of the puparial stage was
longer for colonies fed on tissues containing the drug.
In 1997, Goff et al. [30] focused the effects of the 3,4methylendioxyamethamphetamine (MDMA, an hallucinatory substance derived from metamphetamine) on the rate of
development of P. rucornis reared on decomposing liver
tissues of intoxicated rabbits. Following base extraction,
analyses of the larvae and empty puparial cases detected by
liquid chromatography/mass spectrometry (LC/MS)
MDMA and its metabolite 3,4-methylendioxyamphethamine (MDA) in quantities directly related to the dosage
of the drug administered to the rabbits serving as a food
source. Larvae from colonies reared on tissues receiving the
67 mg (2.0 times the median lethal dosage) and the control
developed more rapidly from 24 h through 114 h. A maximum length of 20 mm was attained in the control colony at
84 h and in the 2.0 times median lethal dosage colony at
108 h of 19.1 mm. Pupariation was rst observed in this
latter colony at 190 h.
4. Discussion
All these investigations have demonstrated the possibility
of qualitative and quantitative correlations between drug
concentrations found in tissues, in developing Diptera larvae, in puparial cases and in insect fecal material since the
process of bioaccumulation is common in a wide variety of
insects [4]. However, although the use of arthropods as
alternate specimens for toxicological analyses is well documented in literature, there are also remarks on its limitations.
Pounder [33] found no correlation between the drug concentration in the larvae and in the tissues on which the larvae

45

were feeding. He also stated that although larvae are useful

as qualitative toxicological specimens, they appear to be of
limited quantitative value as the current state of research
does not allow for accurate quantitative assessments. In this
respect, Wilson et al. [34] analysed by HPLC C. vicina
larvae reared on human skeletal muscle obtained from cases
of suicidal overdose with co-proxamol (propoxyphene and
acetaminophen) and amitriptyline. Amitriptyline, nortriptyline and propoxyphene were all detected in third-instar
larvae in concentrations below that of the muscle food
source. Analyses on puparia and adults were totally negative. These results demonstrate that drugs do not bioaccumulate throughout larval life-cycle, suggesting an efcient
elimination through the Malpighian tubules and the
``nephrocytes'' of Diptera maggots [35]. A drug, indeed,
can be detected from larvae when its rate of absorption
exceeds the rate of elimination.
Similarly, Sadler et al. [36] focused on drug accumulation
and elimination in C. vicina larvae fed on drug-laden muscle
from three suicides involving amitriptyline, temazepam and
a combination of trazodone and trimipramine. The pattern
seen was a gradual rise in larval drug concentration to a peak
at about 78 days (associated with postfeeding stage and
pupariation) which then decreased to zero by pupariation at
16 days. These drugs were undetectable in puparia using
routine toxicological techniques. The authors observed that
larvae metabolise and eliminate drugs with varying levels of
efciency since larval drug concentrations vary considerably
throughout larval development with a clear decrease in drug
concentrations measured in non-feeding larvae and at pupariation. The precipitous decrease in drug concentrations
observed in non-feeding larvae and at pupariation also
suggested that only larvae actively feeding on a corpse
and fully developed should be sampled for toxicological
analysis because they represent the best source of drug
residues. In another experiment, Sadler et al. [37] investigated amitriptyline accumulation and elimination in C.
vicina larvae. The results showed a large degree of biological variation in larval drug concentrations indicating
unreliable quantitative extrapolation and unpredictable larval drug accumulation when maggots encounter more than
one drug or different concentrations of a single drug.
These studies provide very important information,
namely the absence of a drug from larvae does not necessarily indicative that a drug is not present in the food source. In
this respect, Sadler et al. [38] reared C. vicina larvae on a
substrate consisting of a mixture of aspirin (acetylsalicylic
acid), sodium salicylate, paracetamol, sodium aminohippurate, amphetamine sulphate and barbiturates (thiopentone,
phenobarbitone, amilobarbitone, barbitone and brallobarbitone) in concentrations equivalent to those accumulated in
skeletal muscle from fatal human overdoses. The toxicological analysis by HPLC of larvae developed on this food
source yielded a negative result for paracetamol, aspirin,
amilobarbitone and thiopentone (efciently eliminated by
C. vicina). For the other drugs, concentrations in larvae were

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F. Introna et al. / Forensic Science International 120 (2001) 4247

found to be signicantly lower than in their food source.

Barbiturates sharing the same basic chemical structure based
on a pyrimidine ring but differing in their side chain
structure were observed to be metabolised differently by
larvae. The authors' comments were that it is impossible to
predict which drugs are likely to be detected in maggots, on
the basis of the chemical structure. Furthermore, it was
conrmed that the absence of a drug in feeding larvae does
not necessarily imply its absence in the food source. In
another experiment, Sadler et al. [39] reared C. vicina larvae
on a substrate containing four common benzodiazepines
(bromazepan, diazepam, urazepam and loprazolam).
Results of the toxicological analysis by HPLC were negative
for loprazolam (rapidly eliminated by larvae) while both
bromazepam and diazepam were detectable but the relationship between larval drug concentration and foodstuff concentration differed. The authors demonstrated that the
benzodiazepine group of drugs show unpredictable patterns
of drug accumulation in larvae, as well as that of barbiturates.
Based on the results of these studies, Sadler et al. [37] also
found that drug concentrations in larval and pupal samples
which were left unwashed prior to analysis are signicantly
higher than in adequately washed samples due to surface
contamination. Consequently unwashed larvae can be useful
just for qualitative detection of drugs but adequate washing
of larval samples is required before any quantitative assumptions can be made.
On account of the above remarks, further entomotoxicological research should be carried out focusing on bioaccumulation, insect metabolism of drugs and test study data.
Much more has to be investigated even on the correlation
between drug concentrations in larvae and the human tissues
on which these larvae have fed. However, all the papers
reviewed show that prescription and illegal drugs and toxins
can be detected in arthropods. Diptera larvae, in particular,
those that are actively feeding on human bodies provide a
potentially valuable source of information in forensic investigations especially in the absence of tissues and uids
normally taken for toxicological analyses (see badly decomposed bodies or skeletonised human remains).
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