Int J Legal Med DOI 10.1007/s00414-014-1024-y

ORIGINAL ARTICLE

Inter-year repeatability study of volatile organic compounds from surface decomposition of human analogues Sonja Stadler & Jean-Paul Desaulniers & Shari L. Forbes

Received: 4 October 2013 / Accepted: 12 May 2014 # Springer-Verlag Berlin Heidelberg 2014

Abstract Decomposition odour and volatile organic compounds (VOCs) have gained considerable attention recently due to their use by insects and scent detection canines to locate remains. However, a comprehensive and accurate profile of decomposition odour is yet to be confirmed. This is, in part, due to the geographical diversity in the studies conducted and the variation in the methodology and compounds being reported. To date, no repeatability studies of decomposition odour have been conducted in the same environment. In order to address this current gap in the scientific literature, this study conducted three replicate trials in order to evaluate the interyear repeatability of the decomposition VOC profile in a southern Canadian environment. Surface decomposition trials were conducted during the spring and summer months and the VOCs were analysed by thermal desorption–gas chromatography–mass spectrometry (TD–GC–MS). This study was able to demonstrate that decomposition VOCs are produced consistently during their characteristic stages and that this relationship is maintained under varying environmental factors which influence the rate of decomposition. This consistent production of decomposition VOCs can lead to a better understanding of the mechanisms of soft tissue decomposition and their sources of variation, and it could potentially lead to improved applications of these compounds for the detection of decomposed remains. Keywords Forensic chemistry . Decomposition odour . Thermal desorption . Gas chromatography–mass spectrometry S. Stadler : J.800) and probability scores. A perfect spectral match has a match factor of 999 and spectra with no peaks in common receive a value of 0. The probability value indicates the uniqueness of the spectra as well as providing an indication that the library match is correct. The peak areas for all identified compounds were normalised against the area of the internal standard by calculating the peak area ratio. The peak area ratios for the experimental and control treatments for each experimental day were averaged, and a background subtraction was performed

Fig. 2 Average daily temperatures for the three spring/ summer outdoor trials utilising pig carcasses as human analogues. Trial 1 (2010) — average: 19.97 °C, minimum: 6.36 °C, maximum: 33.73 °C. Trial 2 (2011) — average: 21.26 °C, minimum: 5.15 °C, maximum: 41.91 °C. Trial 3 (2012) — average: 20.68 °C, minimum: 7.97 °C, maximum: 36.34 °C

for those compounds detected within the corresponding control samples.

Results Climatic conditions Trials 1, 2 and 3 all commenced the first week of June in 2010, 2011 and 2012, respectively, and continued until the remains had reached skeletonisation in late July. The temperature profiles of the three trials were similar with an average daily temperature of approximately 20 °C (Fig. 2). During Trial 1 (2010), the average daily temperature was 19.97 °C with an absolute minimum of 6.36 °C and an absolute maximum of 33.73 °C. Trial 2 (2011) had an average daily temperature of 21.26 °C, with an absolute minimum of 5.15 °C and an absolute maximum of 41.91 °C. Trial 3 (2012) had an average daily temperature of 20.68 °C, with an absolute minimum of 7.97 °C and an absolute maximum of 36.34 °C. The precipitation for Trials 1 and 3 were similar with 224 and 219 mm of total rainfall, respectively. However, Trial 2 experienced dryer conditions and received only 59.5 mm of total rainfall throughout the study. Carcass decomposition Observations on the stage of decomposition were carried out on each sampling day. Field notes and photos were used to record observations. Due to the short time between death and carcass deposition, all carcasses were classified as fresh

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at the time of deposition. No carcasses exhibited visual signs of autolysis or putrefaction at this time. The stages used to characterise decomposition are adapted from Refs. [22, 28]. Decomposition is not a discrete process and carcasses exhibited features of more than one stage at a time, termed as differential decomposition. Therefore carcasses were categorised based on the predominant features for a particular stage. In all studies, the carcasses followed the general progression of decomposition; however, there was some variability observed. Figure 3 depicts the onset and duration of the decomposition stages by experimental days for the decomposition trials carried out (ADD values are reported within each stage). The early stages of decomposition were comparable, with bloat first observed on experimental day 2 for Trials 1, 2 and 3. Deflation of the carcasses and onset of the active decay stage occurred by experimental day 6 for Trials 1 and 2; however, Trial 3 demonstrated an elongated bloat stage and did not reach active decay until day 10. It was during onset and progression of the active decay stage of decomposition that differential decomposition was generally observed. During differential decomposition, the head would progress to a more advanced stage of decomposition than the rest of the remains. Consequently, skeletal elements of the head and limbs would become visible when the torso was still observed to be in an active or advanced stage of decay. Advanced decay became apparent due to the overall lack of soft tissue on experimental day 11 for Trial 1 and experimental day 14 for Trial 3. Notably, the early onset of advanced decay occurred on experimental day 8 in Trial 2. This was attributed to a large number of maggots that migrated en masse from the carcasses in an east–south east direction on experimental day 7. This event occurred after a rainfall of approximately 2 mm. The carcasses were characterised as being in the dry remains stage

when no soft tissue remained and the carcasses only consisted of mummified skin and bones. This occurred on experimental days 22, 34 and 17 for Trials 1, 2 and 3, respectively. Decomposition VOCs The entire profile of decomposition odour was a complex mixture of hundreds of compounds; additionally, the levels of these compounds and the overall composition of the profile changed over time. In order to evaluate the detailed temporal trends observed during the three trials, compounds which were repeatedly detected with high mass spectral match factors across all three trials are reported herein. The predominant class of compounds within the VOC profile for all trials were the polysulphide compounds (DMDS, DMTS, and DMQS). DMDS was the most prevalent of the polysulphides and was first seen on experimental day 2 of the trials. This is representative of the other polysulphide compounds. The levels of polysulphides reach their apex during the bloat stage (Fig. 4) and represent over 90 % of the VOC profile during this stage. As decomposition progressed, DMQS persisted through to the advanced decay stage, DMTS remained part of the profile through advanced decay and into the dry remains stage, and DMDS remained detectable at low levels throughout the remainder of the trials. Indolic (indole and 1H-indole,3-methyl) and phenolic (phenol and phenol-4-methyl) compounds were the major aromatics detected in the replicate trials. The general trends for the aromatics varied over time; however, as a class, these compounds were predominant during the active and advanced decay stages (Fig. 5). Indole was present within the VOC profile during early decomposition, peaked at the end of the bloat stage and remained at elevated levels through to the end of the active decay stage. On average, indole represented over

Fig. 3 Onset and progression of the decomposition stages by experimental day for Trials 1, 2 and 3. Values within each stage indicate duration of the decomposition stage in ADD

Int J Legal Med Fig. 4 The total relative abundances for the sulphide compounds (DMDS, DMTS, and DMQS) across decomposition for Trials 1, 2 and 3. The x axis displays the experimental days for Trials 1, 2 and 3, respectively

55 % of the aromatics during the bloat stage. However, the levels of indole observed during Trial 3 were distinctly higher than those observed in the other trials, and during the bloat stage, it represented over 90 % of the aromatics. In comparison to the higher levels of indole, 1H-indole,3-methyl, also known as skatole, was present in lower amounts and was not observed during soft tissue decomposition in Trial 2. Overall, phenol was the most abundant of the aromatics and appears to have a two peak cyclic trend. The first peak occurred during active decay at the transition between the active and advanced decay stages. The second maxima for phenol occurred with the onset of the dry remains stage and represents over 90 % of the aromatics for this stage. However, this second peak was not detected in Trial 3. Although not present in the same concentrations as phenol, phenol-4-methyl also displayed maxima during the bloat and active decay stages for all three trials. Hexanal, heptanal and octanal were the dominant aldehydes detected, mostly during the later stages of decay. Although low levels of these compounds were detected in the earlier stages of decomposition particularly in Trials 1 and 3, the onset of their major trend occurred during the advanced decay stage (Fig. 6). During Trial 2, the aldehydes appeared in the advanced decay stage during transition to the dry remains stage (Fig. 6). The levels of the aldehydes Fig. 5 The total relative abundances for the aromatic compounds (indole, skatole, phenol, and phenol-4-methyl) across decomposition for Trials 1, 2 and 3. The x axis displays the experimental days for Trials 1, 2 and 3, respectively

during Trial 2 were also distinctly higher than those observed during Trials 1 and 3.

Discussion Soft tissue decomposition is a variable process from fresh remains to skeletonisation. The onset of the early stages, particularly the bloat stage, appears to be more consistent when investigated under similar environmental conditions. This was observed during the three trials as the carcasses all entered the bloat stage on experimental day 2. During these early stages, the intrinsic processes of early decomposition are likely to be less influenced by external factors [29]. However, as decomposition progresses, it becomes more variable, and during this research, the onset and duration of decomposition stages, even when standardised as ADD, were no longer consistent between trials. Temperature is not the only factor affecting decomposition, and the rate at which the biological process of decomposition occurs in relation to ADD may be accelerated due to the presence of a ‘catalyst’ such as insects [30] or the microbiological community. In the absence of such catalysts, decomposition may progress at a slower rate. This is the

Int J Legal Med Fig. 6 The total relative abundances for the aldehydes; hexanal, heptanal and octanal across decomposition for Trials 1, 2 and 3. The x axis displays the experimental days for Trials 1, 2 and 3, respectively. The figure legend has been inverted to allow visualisation of the smaller peaks in Trials 1 and 3 compared to the larger peak in Trial 2

hypothesised reason for the elongated bloat stage observed in Trial 3. Reduced insect activity was observed during the first few days likely due to the cooler temperatures (~13 °C). Anderson [31] identified a similar deceleration of decomposition when there was a delay in insect colonisation. Remains that were located indoors and experienced a delay in colonisation showed signs of bloat until day 10, whereas those that were readily colonised had entered the active decay stage by day 7 [31]. As decomposition progresses, the presence of catalysts, such as insects or bacteria, may have a greater influence on decomposition making characterisation in terms of ADD or qualitative stages difficult. Once blowfly larvae have completed feeding, they enter a migratory phase in preparation for their next life stage [31]. Typically, when they enter the migratory phase, individual larvae or small aggregates migrate outward from the remains in a 360 ° radius [32]. In rare instances, it has been reported that larvae can migrate in mass events as was observed in this study during Trial 2. Lewis and Benbow [32] defined an en mass dispersal as greater than 90 % of all larvae migrating in the same direction as one or two collective groups. This migratory pattern was observed in Trial 2 with the majority of the larvae migrating as a large group in one direction from all four replicate carcasses. A possible explanation for this rare migration pattern is the accumulation of rainfall and subsequent soil saturation. Additionally, the moist conditions following rainfall can improve larvae motility. The large numbers of maggots leaving the carcass prematurely resulted in excess soft tissue remaining on the carcasses. This soft tissue persisted for a considerable length of time and explains the elongated advanced decay stage observed in Trial 2. Decomposition VOCs The variety of VOCs found within decomposition headspace is the result of soft tissue degradation and the breakdown of macromolecules. These processes are facilitated by the intrinsic bacteria of the gastrointestinal and respiratory tract as well as by the microorganisms and entomological fauna that

colonise the remains [1, 3, 4, 10, 33]. However, the exact origin of these compounds within this complex system is unclear. The compounds may result from the metabolism of several bacteria or may be products of a sequential food chain with one organism degrading the products of the next [1, 4]. Additionally, many decomposition VOCs have also been identified within the headspace of isolated blowfly larvae and pupae [34]. As individual compounds, these VOCs are not unique to decomposition and can be found in a variety of environments and from numerous substrates [12]. The uniqueness of decomposition odour may be the result of the entire death assemblage; a combination of odourants from intrinsic soft tissue decomposition and those resulting from the microbial and entomological community that colonise the remains. As the study of decomposition odour develops, the entire profile of potential odourants needs to be further explored [8]. Although there is a large amount of variability in the number and type of compounds reported within the literature, the polysulphides (DMDS, DMTS and DMQS) are the most commonly reported compounds for decomposition VOC profiles [5–7, 9–12, 17–20]. This class of compounds is characteristic of the early decay stages, particularly the bloat stage [6, 7, 9, 10, 13]. During the three trials, DMDS was the most abundant compound identified and was consistently detected first during the early stages of decomposition at approximately 30 ADD. The polysulphides are believed to be the result of the putrefactive breakdown of the sulphur containing amino acids, cysteine and methionine [4, 11, 35]. However, the polysulphides are not likely a direct product of amino acid metabolism but rather the result of methanethiol (MeSH) oxidation [10, 35]. This reaction readily occurs in the presence of oxygen and, as a result, may decrease the amount of other thiols within the headspace of decomposition. The polysulphides, particularly DMDS, are potential markers for soft tissue decomposition [10]. Investigations of cadaveric VOCs have consistently identified these compounds as major components of decomposition odour. This class has been detected in a variety of decomposition scenarios from both human and porcine remains [5–7, 9–12, 17–20].

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These volatile sulphur compounds are known signalling molecules for carrion insects [10, 13, 15, 16], and a recent study showed that the early production of the sulphur VOCs played a role in the attractiveness of remains to carrion beetles during the early stages of decomposition [13]. The aromatic compounds in this study are also thought to be products of amino acid degradation. The indolic compounds, indole and skatole, are likely resulting from the amino acid tryptophan, whereas the phenolic compounds, phenol and phenol-4-methyl, are potentially produced during the breakdown of tyrosine [4, 36]. Of the aromatics, phenol is one of the more commonly reported compounds in decomposition VOC profiles [6, 7, 9, 10, 17, 18, 20]. Conversely, compounds such as indole and skatole that are reported breakdown products [2, 37] have been less frequently identified [9, 17, 19]. Skatole is the result of continuing proteolysis and is thought to be present during the active decay stage [2, 6, 9, 10, 37]. During Trials 1 and 3, skatole was detected at low concentrations during the active decay stage; however, during Trial 2, it was not detected. One possible explanation is the early onset of the advanced decay stage that occurred during Trial 2. The lower levels of skatole compared to indole in the other two trials indicate that it could be a secondary product and the rapid period of active decay during Trial 2 would have limited its production. Overall, in this study and within the literature, the aromatics have been found to be characteristic of the active and early stages of advanced decay [6, 7, 9]. Hexanal, heptanal and octanal identified in this study, along with additional short-chain aldehydes, have previously been identified within the headspace of decomposition [6, 9, 11, 19] and are likely the result of fatty acid degradation [1, 2, 4, 33]. Under aerobic conditions, the oxidation of the unsaturated free fatty acids by fungi, bacteria and atmospheric oxygen will produce a variety of aldehydes and ketones [2, 38]. The aerobic conditions necessary for oxidation would be typical of surface decomposition in contrast to a closed system [39] or burial where the anaerobic conditions would facilitate transformation of the fatty acids to adipocere [2]. Although volatile aldehydes have been identified throughout decomposition, they are characteristic of the later stages of decay [6, 7, 9]. Studies utilising porcine remains in surface decomposition have shown that free fatty acids including the unsaturated fatty acids are detectable in decomposition soil during the later stages of soft tissue decomposition [40, 41]. Upon release into the environment, likely through the purging of decomposition fluid, fatty acids become available as substrates for microbiological activity. Larizza and Forbes [41] identified peaks of unsaturated fatty acids from ADD 123.0–396.6 in a similar southern Ontario environment. Whereas Swann et al. [40] identified an increasing trend of free fatty acids with a maximum occurring at ADD 310–359 in the same environment as this study. Both sets of results correlate with the trend observed in this study where the aldehydes were seen to peak

during the transition from the advanced decay to dry remains stage (ADD of 395.1, 513.8 and 364.8 for Trials 1, 2 and 3, respectively). Trial 2 displayed distinctly higher levels of aldehydes compared to Trials 1 and 3 with a later peak at ADD 513.8. This later peak could be the result of the mass larval migration. The moist tissue and subsequent fatty acids that remained following the migration would not have been consumed by the larvae but rather degraded slowly by enzymatic or microbial action. This could have led to an increase in the oxidation of fatty acids, and the resultant increase in aldehydes present within the decomposition headspace. The decomposition VOCs reported in this study have been consistently detected within the headspace of both human and porcine remains [5–7, 9–12, 17–20]. These compounds are representative of the range of compounds found within the decomposition VOC profile and were detected throughout the research trials with an increasing trend through the bloat and active decay stage. For each trial (1, 2 and 3), this correlated with observations of the progressive degradation of soft tissue and the distinct decomposition odour associated with the remains during sampling. Recent studies that have investigated the production of VOCs across decomposition have shown that each stage has its own characteristic profile [6, 7, 9, 10], and although trends in the overall composition and progression of the decomposition VOC profile are emerging, no repeatability studies have been conducted until now. By conducting trials over 3 years, this work has demonstrated that representative components of the decomposition VOC profile are consistent within the same geographical location and under similar taphonomic conditions, i.e. surface deposition and seasonal variables. During the three trials, the rate and progression of decomposition was affected by environmental variables such as insect activity; however, the same change was reflected in the production of the characteristic decomposition VOCs. This is particularly evident during Trial 3, where the elongated bloat stage is mirrored in the production and subsequently delayed peak of the polysulphide compounds compared to Trials 1 and 2. This correlation of a chemical class with particular stages of soft tissue decomposition was also observed during Trial 2. Similar to the polysulphides, the aldehydes demonstrate a delayed peak compared to the other trials. However, this class was consistently produced during the later stages of soft tissue decomposition, and the effect of the mass maggot migration observed during this trial is mirrored in both the gross observations of decomposition and the detection of the aldehydes. The volatile signature responsible for the distinct odour of decomposition is not currently agreed upon by the scientific community. The commonalities that have been found between studies are generally limited to chemical classes, such as aromatics, sulphides, aldehydes and alcohols, with few

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compounds being reported in all studies [4, 7, 9, 18]. As more research is being conducted, the major compounds within these classes are being increasingly identified, i.e. DMDS, DMTS and phenol [7, 9, 10]. However, these individual VOCs are not unique to this odour source [12]. The differentiation of decomposition odour from other materials such as detritus and decaying matter will require researchers to incorporate these individual compounds into a dynamic profile that is unique to decomposing remains. In order to be effective, this set of VOCs must be consistently detected across geographical locations and in a range of forensic scenarios. This study has identified dominant decomposition VOCs which correlate well with the literature [5–7, 9–12, 17–20] and has conducted the analysis throughout soft-tissue decomposition over 3 years. Much of the analysis in this area has been conducted at discrete time points, particularly during the early post-mortem period. As a result, there is little information about the dynamic nature of these VOCs across the complete process of soft tissue decomposition. This study demonstrated the inter-year consistency of the decomposition VOCs and their temporal trends. The inclusion of these compounds in other published studies and the reproducibility of the temporal trends indicate that these VOCs could be agreed upon by most and form a preliminary signature of decomposition odour. Overall, this indicates that identification of the major VOCs consistently produced by decomposition is possible in various geographical locations and forensic scenarios. Additionally, this work has laid a foundation for the scientific validation of this potential evidence which can be furthered by the application of advanced instrumentation such as GC×GC–TOFMS to multi-year studies [7, 17]. These hyphenated techniques can generate more detailed profiles identifying minor compounds which are consistently present and further our goal of developing a comprehensive signature of human decomposition odour. Elucidation of this signature is important for enhancing forensic death investigations involving the search for and recovery of decomposed remains.

Conclusion This study analysed representative decomposition VOCs across 3 years from the surface decomposition of pig carcasses during the spring and summer months of southern Ontario, Canada and demonstrated that they are produced consistently during their characteristic stages. Additionally, it was shown that this correlation is maintained in the presence of environmental variables that influence the rate of decomposition. This is the first study to demonstrate the reproducibility of decomposition VOCs and serves to build the scientific foundation of this potential evidence. These findings can lead to a better understanding of the mechanisms of soft tissue decomposition

and the production of decomposition by-products such as VOCs. Elucidation of the VOC profile of decomposition odour can lead to improved applications of these compounds for the detection of decomposed remains.

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Inter-year repeatability study of volatile organic compounds from surface decomposition of human analogues.

Decomposition odour and volatile organic compounds (VOCs) have gained considerable attention recently due to their use by insects and scent detection ...
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