Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Forensic Science, Medicine and Pathology
Published in: Forensic Science, Medicine and Pathology 1/2019

01-03-2019 | Review

An interdisciplinary review of the thanatomicrobiome in human decomposition

Authors: Gulnaz T. Javan, Sheree J. Finley, Sari Tuomisto, Ashley Hall, M. Eric Benbow, DeEtta Mills

Published in: Forensic Science, Medicine and Pathology | Issue 1/2019

Login to get access

Abstract

Death does not occur instantaneously and organs do not decompose at the same rate or in the same way. Nulligravid human uteri and prostate glands are the last internal organs to deteriorate during decomposition; however, the reason for this very important observation is still enigmatic. Recent studies have elucidated that the composition and abundance of microbes in the human thanatomicrobiome (microbiome of death) varies by organ and changes as a function of time and temperature. The ileocecal area has the largest absolute postmortem burden that spreads to the liver and spleen and continues to the heart and brain depending on the cause of death. To truly understand the mechanisms of microbial assembly during decomposition, a thorough examination of different strategies utilized by the trillions of microbes that colonize decaying tissues is needed from a multi-organ and multidisciplinary approach. In this review, we highlight interdisciplinary research and provide an overview of human decomposition investigations of thanatomicrobiomic changes in internal organs.
Literature
1.
Ford WW. On the bacteriology of normal organs. Epidemiol Infect. 1901;1:277–84.
2.
3.
4.
Can I, Javan GT, Pozhitkov AE, Noble PA. Distinctive thanatomicrobiome signatures found in the blood and internal organs of humans. J Microbiol Methods. 2014;106:1–7.PubMedCrossRef
5.
6.
7.
Adserias Garriga J, Quijada NM, Hernandez M, Lázaro DR, Steadman D, Garcia-Gil J. Dynamics of the oral microbiota as a tool to estimate time since death. Mol Oral Microbiol. 2017;32:511–6.PubMed
8.
9.
Vass AA. Beyond the grave-understanding human decomposition. Microbiol Today. 2001;28:190–3.
10.
Stefanuto PH, Perrault KA, Grabherr S, Varlet V, Focant JF. Postmortem internal gas reservoir monitoring using GC× GC-HRTOF-MS. Separations. 2016;3:24.CrossRef
11.
Carter DO, Tomberlin JK, Benbow ME, Metcalf JL. Perspectives on the future of forensic microbiology. In: Carter DO, Tomberlin JK, Benbow ME, Metcalf JL, editors. Forensic microbiology. New York City: Wiley; 2017. p. 376–8.CrossRef
12.
Pascual J, von Hoermann C, Rottler-Hoermann AM, et al. Function of bacterial community dynamics in the formation of cadaveric semiochemicals during in situ carcass decomposition. Environ Microbiol. 2017;9:3310–22.CrossRef
13.
Javan GT, Finley SJ, Smith T, Miller J, Wilkinson JE. Cadaver thanatomicrobiome signatures: the ubiquitous nature of Clostridium species in human decomposition. Front Microbiol. 2017;8:2096.PubMedPubMedCentralCrossRef
14.
Bell CR, Wilkinson JE, Robertson BK, Javan GT. Sex-related differences in the thanatomicrobiome in postmortem heart samples using bacterial gene regions V1-2 and V4. J Appl Microbiol. 2018;67:144–53.CrossRef
15.
Pechal JL, Schmidt CJ, Jordan HR, Benbow ME. A large-scale survey of the postmortem human microbiome, and its potential to provide insight into the living health condition. Sci Rep. 2018;8:5724.PubMedPubMedCentralCrossRef
16.
Tuomisto S, Pessi T, Collin P, Vuento R, Aittoniemi J, Karhunen PJ. Changes in gut bacterial populations and their translocation into liver and ascites in alcoholic liver cirrhotics. BMC Gastroenterol. 2014;14:40.PubMedPubMedCentralCrossRef
17.
Belk A, Xu ZZ, Carter DO, Lynne A, Bucheli S, Knight R, et al. Microbiome data accurately predicts the postmortem interval using random forest regression models. Genes. 2018;9:104.PubMedCentralCrossRef
18.
Zhou C, Byard RW. Factors and processes causing accelerated decomposition in human cadavers–an overview. J Forensic Legal Med. 2011;18:6–9.CrossRef
19.
20.
Matuszewski S, Konwerski S, Frątczak K, Szafałowicz M. Effect of body mass and clothing on decomposition of pig carcasses. Int J Legal Med. 2014;128:1039–48.PubMedPubMedCentralCrossRef
21.
Vass AA, Barshick SA, Sega G, et al. Decomposition chemistry of human remains: a new methodology for determining the postmortem interval. J For Sci. 2002;47:542–53.
22.
Olakanye AO, Nelson A, Ralebitso-Senior TK. A comparative in situ decomposition study using still born piglets and leaf litter from a deciduous forest. Forensic Sci Int. 2017;276:85–92.PubMedCrossRef
23.
Dent BB, Forbes SL, Stuart BH. Review of human decomposition processes in soil. Environ Geol. 2004;45:576–85.CrossRef
24.
Goff ML. Early post-mortem changes and stages of decomposition in exposed cadavers. Exp Appl Acarol. 2009;49:21–36.
25.
26.
DeVault TL, Rhodes OE Jr, Shivik JA. Scavenging by vertebrates: behavioral, ecological, and evolutionary perspectives on an important energy transfer pathway in terrestrial ecosystems. Oikos. 2003;102:225–34.CrossRef
27.
Wilson EE, Wolkovich EM. Scavenging: how carnivores and carrion structure communities. Trends Ecol Evol. 2011;26:129–35.PubMedCrossRef
28.
Benbow ME, Lewis AJ, Tomberlin JK, Pechal JL. Seasonal necrophagous insect community assembly during vertebrate carrion decomposition. J Med Entomol. 2013;50:440–50.PubMedCrossRef
29.
Damann FE, Williams DE, Layton AC. Potential use of bacterial community succession in decaying human bone for estimating postmortem interval. J Forensic Sci. 2015;60:844–50.PubMedCrossRef
30.
Molina DK, DiMaio VJ. Normal organ weights in men: part II—the brain, lungs, liver, spleen, and kidneys. Am J Forensic Med Pathol. 2012;33:368–72.PubMedCrossRef
31.
Gunn A, Pitt SJ. Microbes as forensic indicators. Trop Biomed. 2012;29:311–30.
32.
Huang C, Sloan EA, Boerkoel CF. Chromatin remodeling and human disease. Curr Opin Genet Dev. 2003;13:246–52.PubMedCrossRef
33.
Bär W, Kratzer A, Mächler M, Schmid W. Postmortem stability of DNA. Forensic Sci Int. 1988;39:59–70.PubMedCrossRef
34.
Hynd MR, Lewohl JM, Scott HL, Dodd PR. Biochemical and molecular studies using human autopsy brain tissue. J Neurochem. 2003;85:543–62.PubMedCrossRef
35.
Williams T, Soni S, White J, Can G, Javan GT. Evaluation of DNA degradation using flow cytometry: promising tool for postmortem interval determination. Am J Forensic Med Pathol. 2015;36:104–10.PubMedCrossRef
36.
Di Nunno NR, Costantinides F, Bernasconi P, Bottin C, Melato M. Is flow cytometric evaluation of DNA degradation a reliable method to investigate the early postmortem period? Am J Forensic Med Pathol. 1998;19:50–3.PubMedCrossRef
37.
Molina DK, DiMaio VJ. Normal organ weights in women: part I-the heart. Am J Forensic Med Pathol. 2015;36:176–81.PubMedCrossRef
38.
Payne-James J, Simpson K. Simpson’s forensic medicine. Boca Raton: CRC Press; 2011.
39.
Levy AD, Harcke HT Jr. Essentials of forensic imaging: a text-atlas. Boca Raton: CRC Press; 2010.CrossRef
40.
Trotter SA, Brill Ii LB, Bennett JP. Stability of gene expression in postmortem brain revealed by cDNA gene array analysis. Brain Res. 2002;942:120–3.PubMedCrossRef
41.
Yasojima K, McGeer EG, McGeer PL. High stability of mRNAs postmortem and protocols for their assessment by RT-PCR. Brain Res Protocol. 2001;8:212–8.CrossRef
42.
43.
Cocariu EA, Mageriu V, Stăniceanu F, Bastian A, Socoliuc C, Zurac S. Correlations between the autolytic changes and postmortem interval in refrigerated cadavers. Rom J Intern Med. 2016;54:105–12.PubMed
44.
Sibulesky L. Normal liver anatomy. Clin Liver Dis. 2013;2(S1).
45.
Tuomisto S, Karhunen PJ, Vuento R, Aittoniemi J, Pessi T. Evaluation of postmortem bacterial migration using culturing and real-time quantitative PCR. J Forensic Sci. 2013;58:910–6.PubMedCrossRef
46.
Carpenter HM, Wilkins RM. Autopsy bacteriology: review of 2,033 cases. Arch Pathol. 1964;77:73–81.PubMed
47.
Wilson SJ, Wilson ML, Reller LB. Diagnostic utility of postmortem blood cultures. Arch Pathol Lab Med. 1993;117:986–8.PubMed
48.
Boutin EL, Battle E, Cunha GR. The response of female urogenital tract epithelia to mesenchymal inductors is restricted by the germ layer origin of the epithelium: prostatic inductions. Differentiation. 1991;48:99–105.PubMedCrossRef
49.
50.
Casper JL. A handbook of the practice of forensic medicine: based upon personal experience. London: New Sydenham Society; 1861.
51.
Tolbert M, Finley SJ, Visonà SD, Soni S, Osculati A, Javan GT. The thanatotranscriptome: gene expression of male reproductive organs after death. Gene. 2018;675:191–6.PubMedCrossRef
52.
Lee CH, Akin-Olugbade O, Kirschenbaum A. Overview of prostate anatomy, histology, and pathology. Endocrinol Metab Clin N Am. 2011;40:565–75.CrossRef
53.
Suzuki Y, Tsujimoto Y, Matsui H, Watanabe K. Decomposition of extremely hard-to-degrade animal proteins by thermophilic bacteria. J Biosci Bioeng. 2006;102:73–81.PubMedCrossRef
54.
Hyde ER, Haarmann DP, Lynne AM, Bucheli SR, Petrosino JF. The living dead: bacterial community structure of a cadaver at the onset and end of the bloat stage of decomposition. PLoS One. 2013;8:e77733.PubMedPubMedCentralCrossRef
55.
Hyde E, Haarmann DP, Petrosino JF, Lynne AM, Bucheli SR. Initial insights into bacterial succession during human decomposition. Int J Legal Med. 2015;129:661–71.PubMedCrossRef
56.
Metcalf JL, Parfrey LW, Gonzalez A, et al. A microbial clock provides an accurate estimate of the postmortem interval in a mouse model system. elife. 2013;2:e01104.PubMedPubMedCentralCrossRef
57.
Thomas TB, Finley SJ, Wilkinson JE, Wescott DJ, Gorski A, Javan GT. Postmortem microbial communities in burial soil layers of skeletonized humans. J Forensic Legal Med. 2017;49:43–9.
58.
59.
Pechal JL, Crippen TL, Benbow ME, Tarone AM, Dowd S, Tomberlin JK. The potential use of bacterial community succession in forensics as described by high throughput metagenomic sequencing. Int J Legal Med. 2014;128:193–205.PubMedCrossRef
60.
Benbow ME, Pechal JL, Lang JM, Erb R, Wallace JR. The potential of high-throughput metagenomic sequencing of aquatic bacterial communities to estimate the postmortem submersion interval. J Forensic Sci. 2015;60:1500–10.PubMedCrossRef
61.
Fredette JW. Bacteremias in the agonal period. Transl Res. 1916;2:180–8.
62.
Fouts DE, Torralba M, Nelson KE, Brenner DA, Schnabl B. Bacterial translocation and changes in the intestinal microbiome in mouse models of liver disease. J Hepatol. 2012;56:1283–92.PubMedPubMedCentralCrossRef
63.
Heimesaat MM, Boelke S, Fischer A, et al. Comprehensive postmortem analyses of intestinal microbiota changes and bacterial translocation in human flora associated mice. PLoS One. 2012;7:e40758.PubMedPubMedCentralCrossRef
64.
Burcham ZM, Hood JA, Pechal JL, et al. Fluorescently labeled bacteria provide insight on post-mortem microbial transmigration. Forensic Sci Int. 2016;264:63–9.PubMedCrossRef
65.
Dix J, Graham M. Time of death, decomposition and identification: an atlas. Boca Raton: CRC press; 1999.CrossRef
66.
Latil M, Rocheteau P, Châtre L, et al. Skeletal muscle stem cells adopt a dormant cell state post mortem and retain regenerative capacity. Nat Commun. 2012;3:903.PubMedCrossRef
67.
Mostafa EM, El-Elemi AH, El-Beblawy MA, Dawood AE. Adult sex identification using digital radiographs of the proximal epiphysis of the femur at Suez Canal University Hospital in Ismailia, Egypt. Egypt J Forensic Sci. 2012;2:81–8.CrossRef
68.
Đurić M, Rakočević Z, Đonić D. The reliability of sex determination of skeletons from forensic context in the Balkans. Forensic Sci Int. 2005;147:159–64.PubMedCrossRef
69.
Campobasso CP, Introna F. The forensic entomologist in the context of the forensic pathologist’s role. Forensic Sci Int. 2001;120:132–9.PubMedCrossRef
Metadata
Title
An interdisciplinary review of the thanatomicrobiome in human decomposition
Authors
Gulnaz T. Javan
Sheree J. Finley
Sari Tuomisto
Ashley Hall
M. Eric Benbow
DeEtta Mills
Publication date
01-03-2019
Publisher
Springer US
Published in
Forensic Science, Medicine and Pathology / Issue 1/2019
Print ISSN: 1547-769X
Electronic ISSN: 1556-2891
DOI
https://doi.org/10.1007/s12024-018-0061-0

Other articles of this Issue 1/2019

Forensic Science, Medicine and Pathology 1/2019 Go to the issue

Original Article

Frequency and intensity of pulmonary bone marrow and fat embolism due to manual or automated chest compressions during cardiopulmonary resuscitation

Images in Forensics

Intestinal obstruction as a cause of death in the mentally disabled

Case Report

A lethal case of hoarding due to the combination of traumatic and confined space asphyxia

Images in Forensics

Melioidosis mimicking miliary tuberculosis

Original Article

Applying virtual reality in forensics – a virtual scene walkthrough

Case Report

Sodium nitrite food poisoning in one family