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Forensic studies A Scoping Review on Factors Affecting Cadaveric Decomposition Rates

Introduction: The importance of the determination of cadaveric decomposition rate is to enable the forensic pathologist and forensic scientist in estimating the time since death also known as post-mortem interval. There are many factors affecting the cadaveric decomposition rate including environmental factors and non-environmental factors. This scoping review is to explore the relationship between the delaying or accelerating factors and the decomposition rate. Methods: It was conducted using framework suggested by Arksey and O’Maley. Comprehensive search was performed to identify published works and literatures. Inclusion criteria for the search were articles in English published from 2007 to 2016 and related to taphonomic study as well as the decomposition process and/or rate. Results: A total of 2,893 titles were extracted from electronic databases and other resources and 41 articles were selected based on inclusion criteria. The variables and decomposition rates were generally varied between studies. Accelerating factors were mostly related to higher temperature including the summer season, rainy season, urban and desert area, sun-exposed on ground area, burning effect, enclosed vehicle as well as exposure to insects and scavenger activities. Decelerating factors often relied on the effect of the lower temperature such as winter season, deep coastal marine, underwater, highland and shaded area. It might also depend on the burial effect and other physical barriers by using heavy clothing, wrapping, lime and cement as well as the chemical barrier likewise the organophosphate (OP) pesticide etc. Conclusion: There were emerging evidences on the affecting factors of the decomposition rate, although it was still very limited in tropical countries including Malaysia. Findings of this scoping review demonstrated that insect activi-ties and temperature were the main factors affecting the overall decomposition rates except in the presence of physical barriers which might have contributed some variations to the decomposition rates.


Introduction
Post-mortem interval can be estimated using several methods such as entomological study, post mortem changes and taphonomic study, biochemistry of tissues or body fluids from the cadaver etc. The importance of the determination of cadaveric decomposition rate is to enable the forensic pathologist and forensic scientist in estimating the time since death also known as post-mortem interval. With estimation of postmortem interval, the investigating officer could narrow down the search of witness and suspects for a scene of crime or during the death investigation. There are many factors affecting the cadaveric decomposition rate including environmental factors and non-environmental factors. Environmental factors including weather (temperature, humidity etc.), indoor or outdoor, burial or underwater or above ground. Non-environmental factors DOI: 10.29011/FSTD-108. 100008 including body mass/size, wrapping or unwrapped, clothing or unclothed and entomological effects.
There are factors delaying decomposition indicated by M Lee Goff [1] in which divided into physical, chemical and climatic barriers. A body buried in the soil does not decompose as quickly as one exposed on the surface due to the physical barriers. In a similar manner, a body enclosed in a sealed casket or placed into some form of sealed container will also exhibit a delayed decomposition. Embalming process is specifically and chemically designed to prevent the decomposition of the body, with natural body fluids being drained and replaced with various preservative fluids. Insecticides will not permanently delay the colonization of the body by insects. With regards to the climatic factors, at temperatures below 6oC most insect activity ceases but may resume once temperatures rise above this threshold. Wind speed in excess of 16 km/h will inhibit insect flight. Rainfall may also serve as a temporary barrier. Under conditions unfavourable for the colonisation of insects, such as concealment, low temperature or mummification, mites might become the most important or even the only arthropods on a dead body. Zhou and Byard [2] have also describing the factors accelerating decomposition including exogenous and endogenous factors. Exogenous factors included exposure to elevated environmental temperatures, both outdoors and indoors, exacerbated by increased humidity or fires. Situations indoor involved exposure to central heating, hot water, saunas and electric blankets. Deaths within motor vehicles were also characterized by enhanced decomposition. Failure to quickly or adequately refrigerate bodies may also lead to early decomposition. Endogenous factors included fever, infections, illicit and prescription drugs, obesity and insulin-dependent diabetes mellitus. When these factors or conditions are identified at autopsy less significance should, therefore, be attached to changes of decomposition as markers of time since death. Therefore, the present review will explore the relationship between the delaying or accelerating factors and the decomposition rate. It is hoped that these findings will support future research on the decomposition changes and its affecting factors that might not been well-established to assist in the post-mortem interval estimation especially the homicidal cases.

Review Objectives
The authors declared that there was no competing conflict of interests involved in this review. The review objectives were: To identify significant factors affecting cadaveric decomposi-• tion rates To determine the common indicators used in computing the • cadaveric decomposition rates To study the relationship between the contributing factors and • decomposition rates

Methods
The design of the study is scoping review. Scoping review aims to map rapidly the key concepts underpinning a research area and the main sources and types of evidence available especially when an area is complex or has not been reviewed comprehensively before. For the purpose of this topic, the scoping review is performed to identify the affecting factors, determine the indicators for decomposition rates and study relationships between both factors and decomposition rates. In this review, cadaver refers to the dead human bodies or animal carcasses that are left to the decomposition process whilst decomposition rate is defined as the time relapse from the first decomposition stage (fresh) to the final decomposition stage (skeletonisation) which based on the TBS scoring system or any of the observational systems.
The 5 stages of the scoping review York Framework by Arskey and O'Maley include "Identifying the research questions", "identifying relevant studies", "study selection", "charting the data" and "collating, summarising and reporting the results". Consultation with reviewers from Ministry of Health (MOH), University of Science Islamic Malaysia (USIM) and Institute of Medical Research (IMR) are also conducted to enhance the review work undertaken by the research team members. The study was registered under the National Medical Research Registry Malaysia (NMRR) and the protocol was approved by the Medical Research and Ethics Committee (MREC) Malaysia (ID: NMRR-16-2310-33318).

Identifying the research questions the review questions were:
What are the major factors affecting cadaveric decomposition • rates How are the indicators used in computing the cadaveric de-• composition rates How the factors affecting the cadaveric decomposition rates •

Identifying the relevant studies
The purpose of performing the scoping review was to conduct a comprehensive search to identify primary studies (published work) and reviews. The research team members adopted a strategy for searching the evidence using different sources which included electronic databases and relevant research websites such as Pro-Quest, PubMed and Wiley. The searches also involved online journal articles and books focusing on taphonomic study in Forensic Science and Forensic Medicine.
The researchers decided to set the coverage of the review based on the time span and language of the articles. Inclusion criteria for the search were articles in English from year 2007 till 2016 and studies that are consistent with research questions related to taphonomic study as well as the decomposition process and/or rate are studied. The commencement date of 2007 was chosen in order to cover the recent 10 years findings and it was felt that the evidence on the decomposition rate was limited especially in Asian countries including Malaysia. Titles, abstracts and document text for eligibility were examined independently by the researchers. All type of studies were included in the search strategy. Unpublished articles or those written in the language other than English were excluded due to the cost and time that would be required to translate those documents. Studies that were irrelevant such as purely entomological methods and/or biochemical methods used were excluded. Key terms used in the search of articles were shown in (Table 1 and Table 2). decompos* OR postmortem change* OR postmortem interval* OR putrefact* OR decay* OR taphonom* AND cadaver* OR dead bod* OR carcass* OR animal* decompos* OR postmortem change* OR postmortem interval* OR putrefact* OR decay* OR taphonom* OR cadaver* OR dead bod* OR carcass* OR animal*

Study selection
The study selection is based on the objectives of the study. The review is focused on documents related to the factors including environmental and non-environmental factors affecting cadaveric decomposition rates. Based on the eligible abstracts, copies of full articles were retrieved. The full articles is checked by the researchers as to whether appeared to answer the research questions of the study. Selected full articles were then read by the researchers in order to select the final full articles for the review.

Charting the data
General and specific information about the studies is charted which include authors(s), year of publication, types of affecting factors, objectives or aims of the study, country of study location, study population/sample, sample size including comparison group (if any), methods/instruments and indicators used in the study and findings that were relevant to the objectives of the review.

Collating, summarising and reporting the results
The characteristics of the results from the selected articles from various countries are described based on the design, types and outcomes of each study. The findings of the review were presented in table. Table of evidence on the factors affecting the cadaveric decomposition rates and their relationships with measurements and indicators that are used to describe the various approaches or methods to determine the decomposition rate. Limitation of several studies and research gaps are also identified in order to generate useful knowledge on the taphonomy and post-mortem interval estimation. Table 3 shoed a total of 2,893 titles were extracted from the selected electronic databases and other resources using the search terms. As portrayed in Figure 1, 59 abstracts were included after the initial screening process and the rest were excluded as they were irrelevant with regards to the decomposition changes or rates, non-English articles, and duplicates. Among these 41 articles met the inclusion criteria in the review, environment factors and non-environmental factors were studied with total of 20 articles and 17 articles respectively. The rest of 4 articles were focus on mixed factors.  The studies in this review were equally focus on both environmental factors and non-environmental factors. Most of the environmental aspects surveyed the climate factors especially the temperate/tropical climate, dry and wet/rainy seasons, habitats/locations and burial effect. Additionally, researchers emphasize to explore the non-environment factors including the scavenger or insect effect, clothing, wrapping, lime or cement effect, burning effect. Countries of origin of the studies included Malaysia, Europe (United Kingdom, Italy, Germany, Poland, Romania, and Belgium), America (United States, Canada, Colombia and Brazil), Middle East (Saudi Arabia, Egypt, and Kuwait), South Africa, Australia and China. All the articles in this review were using animal carcasses as subjects except [3] using human cadavers to study on scavenger effects during summer season. Majority (26 articles) using swine / pig carcasses as subjects, followed by rabbit carcasses (10 articles) and minority were using monkey and other animal carcasses. The measurement of indicators for each studies were primarily on the comparison of time taken to different decomposition stages, however, some researchers were also using total body scoring (TBS) system in 6 articles as the decomposition scoring methods. Part of the studies utilised different approaches such as decomposition changes by observation, mass/weight loss, first colonisation of insects, insect richness, insect residency time, and insect succession patterns and taxa variation. In this review, there were 14 full text articles, out of the 41 selected articles, available online and free for open access. The lists of these articles were elucidated in a summary format as shown in the (Table 4).  The first colonizing wave, primarily Calliphoridae, was observed after 15 weeks when the temperature increased to 13°C. Families belonging to Coleoptera Order starting with Cleridae and Silphidae were observed at week 18 when temperatures raised above 18°C.

Results
Metabolic activity of anaerobic bacteria being inhibited by the low temperatures. Three cold-adapted environmental bacteria P. articus, P. cibarius, P. cryohalolentis which appeared at the beginning of the freezing period (weeks 1-5) may constitute putative microbial markers for investigations of post-mortem interval during the cold season. Indicators: Time taken to decomposition stages.
Methods: Sampling was done once a day during the first 18 days and then each 2 days until decomposition day 31. It was then carried out twice a week until day 49 and then once a week until decomposition day 97. Arthropods were collected from above, around and below the cadavers to analyse abundance of the all arthropods.
One factor analysis of variance shared that there were no statistically significant differences between the abundance of the all arthropods collected from the three pigs during the decomposition (ANOVA, F =0.13, df=2, n =5981, P >0.05). Fresh (in Spring days 0-1 for Sunlit and 0-2 for Shaded); (in Summer days 0 for both); (in Fall days 0-2 for Sunlit and 0-3 for Shaded) Bloated (in Spring days 2-12 for Sunlit and 3-15 for Shaded); (in Summer days 1-4 for both); (in Fall days 3-10 for Sunlit and 4-10 for Shaded) Active Decay (in Spring days 13-30 for Sunlit and 16-35 for Shaded); (in Summer days 5-11 for both); (in Fall days 11->54 for both) Advanced Decay (in Spring days 31-42 for Sunlit and 36-45 for Shaded); (in Summer days 12-25 for both) Dry (in Spring days 42->63 for Sunlit and 46->63 for Shaded); (in Summer days 26->43 for both) Results indicated that habitat was only a factor in the decompositional rate of carrion in the spring season. The ambient temperature was the chief factor determining the seasonal variations in decay rate. Carcasses placed in spring and fall attracted a more diverse assemblage of insects than summer-placed carrion. Sunexposed carrion had greater variation in fauna than shaded carrion in spring and fall. Carcass 1 was rapidly scavenged then dragged from view by Day 22. Carcass 2 was scavenged in a similar fashion. Exposed tissue became covered by Orchomenella obtusa (Family Lysianassidae) which removed all the internal tissues rapidly. Carcass 3 remaining intact, developing a thick filamentous sulphur bacterial mat, until Day 92, when it was skeletonized by crustacea. Carcass 3 was deployed when the water was already extremely anoxic, which prevented larger crustacea from accessing the carcass. The influence of insects on decomposition rate in buried and surface remains. Methods: (i) buried (35 cm depth) after exposure to insect activity, (ii) buried without exposure, (iii) kept above ground behind an insect screen, or (iv) continuously exposed above ground in a field experiment.
Results showed that dipteran oviposition occurred consistently in groups i and iv only. Decomposition rates of rabbits kept behind the screen and those buried without exposure showed no difference (p = 0.450). This was significantly slower than those buried after exposure (p = 0.0016) which was in turn significantly slower than those continuously exposed (p << 0.001). Insect presence is the primary agent affecting decomposition rate via tissue consumption and also the heat they generate. Results showed significant differences (p << 0.001) in decomposition rates between carcasses with and without insect access prior to burial. An approximately 30% enhanced decomposition rate with insects was observed. In the Winter part of the experiment, the first insect activity on the burnt carcass began in the Day 18 (Calliphora vomitoria). On Day 26, a clear reduction of the tissues in several body regions (head, thorax, and abdomen) was observed. Two months after the exposure (Day 60), the bones were clean and only a few remains of burnt skin and muscles were still present. Control pigs with initial putrefactive stage was detected at the end of the second week. In third week, a moderate emphysematic phase in the head region and discharge of decomposition fluids from the mouth was observed. In the abdominal region, the beginning of a colliquative phase was observed.
In the Summer part, adult flies and first instar maggots (Phormia regina) appeared a few minutes/hours. First colonization wave (Calliphoridae) appeared on burnt and control pigs at the same time. After one week (Day 6), the carrion showed some clear skeletonized areas (head, thorax). After the first week, the rate of skeletonisation and the exposure of bones slowed down. In the fourth week (Day 27), soft tissues were almost completely lost, except for large fragments of dry or burnt skin. After 6 weeks, the control pig showed about 40% skeletonisation.