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Impact of The Human Microbiome in Forensic Sciences
Impact of The Human Microbiome in Forensic Sciences
Impact of The Human Microbiome in Forensic Sciences
crossm
Manuel G. García and María D. Pérez-Cárceles contributed equally, and the order is arbitrary.
communities that involve a health condition could differ from person to person (10). Editor Danilo Ercolini, University of Naples
Federico II
The human microbiota is a highly dynamic system that can be affected by a Copyright © 2020 American Society for
multitude of factors, including the spatial and temporal components, which are critical Microbiology. All Rights Reserved.
because they are associated with factors such as age, sex, life habits, geographical Address correspondence to Isabel Legaz,
location, occupation, or interaction with other people (11, 12). From the forensic point isalegaz@um.es.
Accepted manuscript posted online 4
of view, microorganisms are important for their role in the process of cadaveric
September 2020
decomposition (13–15). During the agonal period, for example, microorganisms may Published 28 October 2020
enter the body and subsequently be useful for diagnosis of the cause of death (16, 17).
November 2020 Volume 86 Issue 22 e01451-20 Applied and Environmental Microbiology aem.asm.org 1
Minireview Applied and Environmental Microbiology
However, on many occasions, the microorganisms that cause fatal infections are not
identified at the time of death (18).
On the other hand, there is increasing evidence that humans have an extremely
diverse microbiome that can be useful in determining ethnicity, country of origin, and
even personal identity (19, 20). Similarly, the composition of the microbiome present in
the environment can be a useful indicator of geographical origin or as a means to link
people, animals, or objects to each other or to a specific location (20, 21). Therefore,
microorganisms can provide evidence in many different forensic scenarios, including
investigations into sexual assault when there is no other type of evidence available (22).
Given the enormous forensic potential presented by microbial analysis, there is a
need to develop standardized operating procedures for the collection, analysis, and
interpretation of microbial evidence, as well as to create solid and complete databases
SYSTEMATIC REVIEW
The methods used for this systematic review (covering 2009 to June 2020) were
developed by reference to the Preferred Reporting Items for Systematic Reviews and
Meta-Analyses (PRISMA) statement (23) for studies published in accordance with the
methods detailed in the Cochrane Handbook for Systematic Reviews of Interventions (77),
such as reference 24. The protocol for this systematic review was registered with the
International Prospective Register of Systematic Reviews (PROSPERO) prior to com-
mencement.
Inclusion criteria. All studies exploring the human microbiota in human forensic
science in subjects aged 0 to 89 years old were included. The articles were chosen
according to two main inclusion criteria: (i) application of the microbiome in forensic
sciences and (ii) microbiome of human origin.
Search strategy. Literature search strategies were developed in collaboration with
a health sciences librarian using two scientific electronic databases (Medline and
Google Scholar) and keywords.
For the articles included in the review, the key characteristics of the studies were
identified: topic discussed, first author, and year. The following keywords and
subject heading terms were used: postmortem and/or microbiology, forensic
and/or microbiology, postmortem and/or microbiome, forensic and/or microbiome,
thanatomicrobiome, sudden death and/or microbiome, and drowning and/or mi-
crobiome. The search in the two scientific electronic databases (Medline and Google
Scholar) was limited to articles published in English and studies conducted in
humans. Two independent reviewers revised titles and abstracts and then full-text
publications with reference to the inclusion criteria. Study selection interrater
agreement between the two reviewers was calculated as the proportion of positive
agreement (25).
Data extraction. Two independent testers retrieved duplicate data using Microsoft
Excel. We checked and compared multiple reports from the same study and extracted
them where specific data existed. For all studies that met the inclusion criteria, the
following data were extracted: authors, year of publication, geographic location, study
population, study design, sample size, age range, gender, ethnicity, method of micro-
biota analysis, type of bacteria detected at each anatomical site, provenance of the
microbiome studied, and main microorganisms found.
Risk of bias assessment. The risk of bias was assessed for each sample by
comparison with the Cohort Research Checklist of the Critical Assessment Skills Pro-
gram (CASP) (26). The following confounding variables within the CASP checklist were
evaluated: sample size, age, gender, population analyzed, and location of the analyzed
microbiome. Based on the CASP checklist, study output was graded as “bad,” “fair,” or
“good.” The overall quality of the proof was rated as high, moderate, weak, or extremely
low (27).
DESCRIPTIVE STUDIES
A total of 4,150 studies were identified in the two scientific electronic databases,
PubMed (2,454) and Google Scholar (1,696) (Fig. 1). A total of 3,780 duplicates and
nonrelevant studies were eliminated, and 370 studies were reviewed to assess their
relevance. A total of 337 studies were excluded by these criteria: (i) reviews (n ⫽ 44); (ii)
based on nonhuman samples (n ⫽ 176); (iii) based on clinical research (n ⫽ 88); and (iv)
unspecific (n ⫽ 29).
Finally, this search strategy identified 33 descriptive studies of microbiome and
postmortem interval (n ⫽ 8), drowning (n ⫽ 4) and sudden death (n ⫽ 4), geolocation
(n ⫽ 4), skin and surrounding microbiome (n ⫽ 4), sexual contact (n ⫽ 2), and identifi-
cation (n ⫽ 7) that were included in this systematic review.
Risk of bias assessment. According to the CASP risk of bias assessment, most
studies (63.6%) were judged as “good” due to the considered variables, while 36.4%
were judged as “poor” or “moderate,” largely due to confounding variables not being
considered (Table 1).
Participants were recruited from few geographic regions, making it difficult to
generalize beyond these regions. Overall, the quality of the literature was good.
Laboratory methods. The methods used to evaluate the microbiome varied be-
tween studies (Table 2). Most studies (24/33) used 16S rRNA gene sequencing to detect
a wider range of bacteria. Five studies (18, 28–31) used culture for detection of the
microbiome. Seven studies used PCR (16–18, 28, 32–34), and two studies used only
whole-metagenome sequencing (20, 35).
focused cohort accurately accurately factors factors Precise Believable with other quality
Study issue recruitment measured measured identified accounted for results results available data score
Postmortem interval determination
Adserias-Garriga et al. (41) ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫹ Moderate
DeBruyn et al. (76) ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫹ Moderate
Bell et al. (45) ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫹ Moderate
Pechal et al. (43) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Pechal et al. (44) ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ? Moderate
Javan et al. (14) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Hauther et al. (46) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Can et al. (15) ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫹ Moderate
Hyde et al. (42) ⫹ ⫺ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Geolocation
Walker et al. 2019 (20) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Brinkac et al. (54) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Nagasawa et al. (33) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Escobar et al. (55) ⫹ ⫹ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫹ Moderate
Human identification
Richardson et al. (19) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Schmedes et al. (34) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Schmedes et al. (35) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Wilkins et al. (61) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Park et al. (31) ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ ⫹ Good
Leake et al. (32) ⫹ ⫺ ⫺ ⫺ ⫺ ⫺ ⫹ ⫹ ⫹ Moderate
aData based on CASP-based risk of bias assessment. ?, this variable was unable to be assessed.
aem.asm.org 4
Applied and Environmental Microbiology
Cause of SIDS
Leong et al. (51) ✓
Highet et al. (52) ✓
Praveen and Praveen (30) ✓
Prtak et al. (18) ✓ ✓
Geolocation
Walker et al. (20) ✓
Brinkac et al. (54) ✓
Nagasawa et al. (33) ✓
Escobar et al. (55) ✓
Human identification
Richardson et al. (19) ✓
Schmedes et al. (34) ✓
Schmedes et al. (35) ✓
Wilkins et al. (61) ✓
Park et al. (31) ✓ ✓
Leake et al. (32) ✓ ✓
Cause of SIDS
Leong et al. (51) 88 0–1 W/M Australia Fecal
Highet et al. (52) 154 0–1 W/M Australia Intestine
Praveen and Praveen (30) W/M USA Gut flora
Prtak et al. (18) 121 0–2 W/M UK Blood and cerebrospinal fluid
an, number of individuals or samples; n.i., not indicated; W/M, women/men; SIDS, sudden infant death syndrome.
FIG 2 Representative diagrams illustrating the relationship between the microbiome and the postmor-
tem interval (PMI). (A) Representative diagram of the changes in microbiota during the different stages
of human decomposition (13). (B) Representation of microbial communities present before and after the
bloat stage in human decomposition (76).
ence of spore-forming microorganisms, because their spores allow the rapid coloniza-
tion of the new ecological conditions.
One study analyzed the daily differences in the oral microbial composition (palate,
tongue, internal mucosa of the cheek, and dental surfaces) in the different stages of
human decomposition to estimate the PMI (Fig. 2A). Different bacterial communities
are observable in fresh, bloated, active, and advanced decay and also in the dry remains
(38). The entire fresh stage was characterized by indigenous oral microbiome repre-
sentatives. The predominant families in the bloat stage were Peptostreptococcaceae and
Bacteroidaceae, which are mostly oral indigenous representatives, and Enterococcaceae,
which is a gut microbiome representative. The translocation and proliferation of
Clostridium in postmortem human internal organs is observed in several studies (14,
39). Clostridium species are believed to advance decomposition by breaking down
Similarly, Bell et al. (45) examined the postmortem microbiomes of the cardiac
tissues of 10 cadavers with a postmortem interval of 6 to 58 h. The investigation
revealed that the cardiac microbiomes of male and female cadavers are different. The
genera Streptococcus and Lactobacillus were found exclusively in men. The study also
revealed a higher prevalence of Pseudomonas and Clostridium in women. Thus, this
study provides data demonstrating that the microbiome has a discriminatory power for
sex differences in postmortem heart samples.
Another study of changes in postmortem intestinal microbial populations con-
cluded that Bacteroides and Lactobacillus could be used as quantitative indicators of
PMI (46).
A study of the postmortem microbiome analyzed different tissues (blood, brain,
liver, and spleen) and blood. It concluded that facultative anaerobic bacteria predom-
inate in corpses with a short PMI and obligately anaerobic bacteria predominate in
corpses with a longer PMI (15). In another study carried out on the bacterial species
associated with human decomposition in the intestine and oral cavity, but focusing on
the initial and final time points of the swelling stage, the authors emphasized that no
definitive conclusion could be reached regarding changes in the structure of the
community over time with the data set they analyzed (42).
Death by drowning. Drowning is the usual cause of death for most victims
recovered from watery environments (47). Determination of this type of death is
normally based on pathological findings but is sometimes complicated when the
typical signs of drowning are not obvious (48).
Diatom analysis can provide useful information for estimating the type and amount
of water aspirated, as long as the diatom density is high enough (48). The presence of
diatoms in closed organs (or bone marrow) generally suggests that the victim had
entered the water while still alive. However, many diatoms aspirated into the lungs
cannot enter the bloodstream because they are larger than the diameter of the alveolar
capillaries (49). For this reason, several studies have explored the possibility of using the
smallest aquatic microbes that can easily enter the blood circulation and that are
detectable even in putrefied victims as markers that allow the detection of death by
drowning (Table 3).
In one study, a triple PCR method with TaqMan probes was used to simultaneously
detect eight species of bacterioplankton, which are dominant in the blood of drowned
bodies, with the aim of confirming or ruling out drowning as the cause of death (17).
The authors compared corpses drowned in different types of water, and the genus
Aeromonas (A. hydrophila and A. salmonicida) was mainly observed in victims who had
drowned in freshwater. They were found in lung samples (100%), blood (100%), and
closed organs (85%) (Fig. 3C). In all the lung samples taken from victims discovered near
estuaries, both seawater (Vibrio and Photobacterium) and freshwater bacteria were
detected. In victims drowned in saltwater, the genera Vibrio and Photobacterium were
detected in all lung samples, 90% of blood samples, and in 50% of the organ samples
taken.
Using the methodology developed by Uchiyama et al. (17), samples of brain, kidney,
spleen, and lungs from 20 bodies found in freshwater, brackish water, and salt water
were analyzed by Rutty et al. to confirm the diagnosis of death by drowning. In the
same study, a water sample from each of the places where the bodies had been found
positive correlation was observed between the species richness of the samples ana-
lyzed and age in both groups.
Highet et al. (52) analyzed the intestinal contents of 52 SIDS cases and 102 fecal
control samples similar in both age and gender. In all cases, Clostridium innocuum,
Clostridium perfringens, Clostridium difficile, Bacteroides thetaiotaomicron, and Staphylo-
coccus aureus were analyzed. The authors described a statistically significant increase in
Clostridium difficile, Clostridium innocuum, and Bacteroides thetaiotaomicron in samples
with SIDS compared with the controls when both groups were analyzed.
Furthermore, they observed that the SIDS samples showed a significantly more
frequent dual colonization by Clostridium perfringens and Clostridium difficile than the
healthy cases (17% versus 5%). Triple colonization by Clostridium innocuum, Clostridium
perfringens, and Clostridium difficile was also significantly more frequent in SIDS samples
Determination of sexual
contact
Williams et al. (60) 43 21–70 W/M USA Pubic hair
Williams et al. (60) 6 21–70 W/M USA Pubic hair
Human identification
Richardson et al. (19) 37 n.i. W/M USA Skin
Schmedes et al. (34) 72 n.i. W/M USA Skin
Schmedes et al. (35) 12 n.i. W/M USA Skin
Wilkins et al. (61) 19 n.i. n.i. China Skin and surfaces of objects
Park et al. (31) 15 n.i. W/M South Korea Hand
Leake et al. (32) 2 25–69 M Switzerland Saliva
an, number of individuals or samples analyzed; n.i., not indicated; W/M, women/men.
significant differences in the detection rate of H. pylori between the different sampling
points of the gastric mucosa, between the causes of death, or the ages of the subjects.
Finally, the authors amplified and sequenced the vacA gene from H. pylori, finding how
the different genotypes showed specificity for geographic origin. The authors con-
cluded that their results suggest that the H. pylori genome could provide valuable
additional information for tracing the geographic origin of unidentified bodies.
In another study (55), the intestinal microbiome of Colombian adults was compared
with that of North Americans, Europeans, Japanese, and South Koreans, and the results
confirmed that the composition of the intestinal microbiota differed significantly
among different populations. For example, the phylum Actinobacteria was present in a
higher proportion in Japan, Colombia, and Europe but was practically absent or not
found at all in South Korea and the United States. The phyla Firmicutes, Bacteroidetes,
and Proteobacteria predominated in the intestinal microbiome of people analyzed in
Colombia, while in the other analyzed regions there was a higher proportion of
Bacteroidetes and lower proportions of Firmicutes and Proteobacteria. Tenericutes was
more frequent in Europe but absent from Japan and in a very low proportion in the
other regions. Finally, the verrucomicrobia were not found in either Japan or South
Korea but were present in Colombia, Europe, and, to a lesser extent, the United States.
Based on these data, the authors concluded that the geographic origin in the studied
populations had an impact on the composition of the intestinal microbiota.
(n ⫽ 29), Washington, DC (n ⫽ 26), and California (n ⫽ 34). They observed how the
microbial communities on the telephones and the shoes were significantly different for
the different cities, so that the analysis of both made it possible to determine from
which of the three geographic regions the samples had come.
Determination of sexual contact. The human microbiome of different regions of
the body (intestine, oral, skin, and urogenital) differs in composition, although these
microbiome regions are more similar to each other than to the microbiome of other
people (11). This potential individuality of the human microbiome suggests that there
is some transfer during sexual contact that would allow the human microbiome to be
used in investigations of sexual assault when there is no other type of evidence (60).
However, before the microbiome can be used in such a forensic context, it is first
necessary to address issues such as the stability of the microbiome both on the
However, it was seen how the presence of a second individual in the same space can
interfere with the classification by acting as a confounding factor. The classification
error was linearly correlated with the number of individuals per shared space.
In another study (34), the authors used a targeted sequencing method based on skin
microbiome markers developed for human identification. The sequencing panel con-
sists of 286 specific markers for the detection of 22 species belonging to the genera
Corynebacterium, Propionibacterium, and Rothia. In this study, 72 samples of skin
microbiomes from three body sites were analyzed: foot, hand, and chest. All samples,
regardless of body site, were correctly assigned to their host with 92% accuracy, leading
the authors to propose that the skin microbiome could be used for human identifica-
tion in future studies.
Schmedes et al. (35) describe a novel approach to assigning skin microbiomes to
position ceases, and if the corpse is in the soil and there is vegetation, there is an
increase in carbon and nutrients in the soil, which is why this stage is characterized by
the appearance of microorganisms representing the soil. Finally, the dry remains stage
is mainly characterized by the presence of spore-forming microorganisms, because
their spores allow a rapid colonization of the new ecological conditions (40, 42).
However, bacterial succession depends not only on the organs, tissues, or fluids but
also on other variables, such as seasonal variations, temperature, or location of the
body, while some studies demonstrate there are also variations in colonization patterns
that depend on the sex of the individual (14). Some authors (44) also indicate the need
to study how the conditions under which bodies are kept (frozen, burned, or em-
balmed) affect the microbiome.
The studies published on estimating the PMI based on the microbiome represent an
ACKNOWLEDGMENTS
We have no conflict of interest to declare.
For the search strategy and data extraction, data were retrieved and revised by M. G.
Garcia and I. Legaz.
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