Geographic Diversity of Helicobacter Pylori in Cadavers

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Geographic diversity of Helicobacter pylori in cadavers: Forensic estimation of geographical origin

Sayaka Nagasawa *, Hisako Motani-Saitoh, Hiroyuki Inoue, Hirotaro IwaseDepartment of Legal Medicine, Graduate School of Medicine, Chiba University, Chiba 260-8670, Japan

1. Introduction

In many areas worldwide, increasing internationalization andthe occurrence of large-scale disasters has resulted in growingnumbers of unidentied cadavers. This is an important forensicproblem. In Japan, 1000 or more deceased individuals are notidentied upon death every year, giving a total of more than 16,000unidentied deceased individuals [1] . Following the Great East Japan Earthquake and tsunami in 2011, about 3000 people remainmissing and there are about 300 unidentied bodies as of June2012. In 8 European nationsDenmark, Finland, Greece, Ireland,Portugal, Luxembourg, Spain, and Germany, there were 3035unidentied deceased individuals during the 4-year period from

1994 to 1998, of which 2228 were subsequently identied and 807remain unidentied [2] .

As methods of personal identication, ngerprints, dentalrecords and human DNA typing are reliable methods. Othermethods targeting personal characteristics, such as facial appear-ance and personal belonging, are also used. However, when suchinformation is lacking, personal identication becomes difcultand results in the case remaining unsolved. Therefore, methodsthat can quickly and easily narrow down the possible geographicorigins of unidentied cadavers would be extremely valuable.However, there are no effective ways to estimate the geographicalorigins of humans based on human DNA or morphologicalcharacter analysis. Therefore, tests that utilize the distinctgeographical distributions of DNA polymorphisms of latent humanviruses have been developed in recent years.

Various methods targeting different viruses have been devel-oped by Ikegaya and colleagues: John Cunningham virus (JCV) inthe kidneys [3,4] , BK virus (BKV) in the tubular epithelium [5,6] ,and Epstein-Barr virus (EBV) in B-lymphocytes [4] . Furthermore,we reported the use of this method for the varicella-zoster virus(VZV) in trigeminal ganglia [7] . A DNA chip has already been

Forensic Science International 229 (2013) 712

A R T I C L E I N F O

Article history:Received 20 December 2011Received in revised form 11 January 2013Accepted 18 February 2013Available online 11 April 2013

Keywords:H. pyloriDNA polymorphismvacA

A B S T R A C T

A method for determining thegeographical originof unidentied cadavers by determining the genotypeof Helicobacter pylori , which is latent in one-half of the worlds population, was developed. In the rststage, DNA was extracted from samplings at 5 points in the gastric mucosa of 177 individuals randomlyselected from cadavers undergoing medico-legal autopsy. 16S-rDNA of H. pylori DNA was detected bypolymerase chain reaction (PCR) in 101 cadavers (57.0%); by sex, 74 of 123 (60.1%) males and 28 of 54(46.4%) females were positive.There wereno signicant differences in H. pylori detection rate among the5 sampling points of the gastric mucosa, cause of death, or age. In the second stage, amplied fragmentsof H. pylori vacA regions s and m from 17 individuals with the following ethnic backgrounds weresequenced: Japanese, 10; Chinese, 2; South Korean, 1; Taiwanese, 1; Thai, 1; Afghan, 1; and Filipino, 1. Aphylogenetic tree constructed with these and 28 previously reported H. pylori strain sequences revealed3 major gene clusters consisting of East Asian type I (Japanese, South Koreanand Chinese), Western typeII, and Southeast Asia type III. The Taiwanese and Filipino samples deviated from the clusters type III towhich they typically belong.

The ultimate aim of the present study was to develop a more accurate method of determining of geographic origin of unidentied cadavers through the combination of the present method with other,virus-based methods H. pylori DNA was detected from over hal f of the cadavers tested and vacAgenotypes showed specicity to geographical origin. Therefore, these results suggest that the H. pylori

genome provides valuable additional information for tracing the geographical origin of unidentiedcadavers.

2013 Elsevier Ireland Ltd. All rights reserved.

* Corresponding author at: Department of Legal Medicine, Graduate School of Medicine, Chiba University, 1-8-1 Inohana, Chuo-ku, Chiba 260-8670, Japan.Tel.: +81 43 226 2078; fax: +81 43 226 2079.

E-mail addresses: [email protected] , [email protected] ,[email protected] (S. Nagasawa).

Contents lists available at SciVerse ScienceDirect

Forensic Science International

j o u r na l h o m ep ag e: w ww.e l sev i e r . co m/ loc a t e / fo r sc i i n t

0379-0738/$ see front matter 2013 Elsevier Ireland Ltd. All rights reserved.

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2.6. Statistical methods

The relationship between the H. pylori -positive rate and age, the 5 gastricsampling positions, and cause of death were tested by the rank test usingSpearmans correlation coefcients.

3. Results

The cadavers included in this study were selected at random,regardless of age, sex, cause of death, postmortem interval andcondition. The distribution of age and sex of the cadavers is shownin Fig. 1. H. pylori 16S-rDNA was detected in 57%. The H. pyloripositive rate for males (60.1%, 74/123) was higher than that forfemales (46.4%, 28/56) as shown in Fig. 2. H. pylori DNA becamedetectable for individuals in their teens, and the positive rateincreased with increasing age; the youngest and oldest individualsto test positive for H. pylori were 18 (male) and 89 (female) yearsold, respectively. Infection rates were greater than 50% inindividuals over 40 years old and older, which is consistent witha previous nding of 50% rates reported in previous epidemio-logical studies. The inuence of cause of death and postmorteminterval on the detection of H. pylori DNA is shown in Table 2. H. pylori DNA was detected in 57.7% (71/123) of individuals who diedof external causes. Individuals who died of internal causes hadsimilar H. pylori DNA-positive rates (54.8%, 17/31). H. pylori DNAwas also detected in subjects who died of chemical poisoning by

overdose of herbicides and anti-psychotic drugs. Spearmanscorrelation coefcients showed no statistically signicant differ-ences in positive rate among the causes of death ( p < 0.05).Regarding postmortem interval, 153 cadavers were estimated tohave within 1 week of death, and H. pylori DNA was detected in52.9% (81/153) of these individuals. Furthermore, for postmorteminterval of 1 week to < 1 month, H. pylori DNA was detected in 15(less than 40 years old, 2 and older than 40 years old, 13) of 19cadavers (less than 40 years old, 4 and older than 40 years old, 15).For postmortem interval of 1 month, all 5 cadavers (unknownage, 2 and > 60 years old, 3) were positive, and 1 mummiedcadaver with an estimated postmortem interval of several months

to 2 years, the longest in this study, was H. pylori DNA-positive.These results suggest that neither the cause of death nor time afterdeath affects the detection of H. pylori DNA.

Next, we examined the relationship between samples that wereH. pylori DNA-positive and the presence or absence of gastricndings on autopsy. Gastric ndings comprised macroscopicndings during autopsy and overall ndings obtained frombiochemical, histopathological and other laboratory tests per-formed at autopsy. As shown in Table 3, samples were collectedfrom 28 individuals showing gastric ndings, and H. pylori DNAwas detected in 75.0% of these samples. Regarding gastricsubmucosal hemorrhage and discoloration, some were due topost mortem changes and could not be distinguished from diseasesof the stomach. Additionally, 1 of 2 samples that were H. pylori -negative were from cases with gastric perforation, the cause of perforation was based on an injury that was due to an externalcause. For the remaining 146 individuals with no gastric ndingson autopsy, the H. pylori DNA-positive rate was 54.7%. In 3individuals, a post-operative scar from the resection of stomachcancer was observed and but H. pylori DNA was not detected.Although the relevance of the presence of gastric ndings and H. pylori was not elucidated, it is obvious that H. pylori DNA wasdetectable in over 50% of samples that had no gastric ndings incadavers.

The H. pylori DNA-positive rate in each of 5 points of the gastric

mucosa taken to determine the most suitable source of tissuesamples was similar at 52.5% (93/177) in the cardiac part and lessergreater curvature, 53.1% (94/177) in the upper greater curvature,

Table 1Target amplication regions and primers for PCR and sequencing.

Gene PCR/sequencing Primers Primer sequence Reference

16S-rDNA PCR 16S rRNA-F 50-TAAGAGATCAGCCTATGTCC-3 0 Kumar et al. (2008)16S rRNA-R 50-TCCCACGCTTTAAGCGCAAT-30 Kumar et al. (2008)

vacA s-region Both LMVAS-F 50-AAAATCAATCGCCCTCTGGTTTCTC-30 This studyLMVAS-R 50-TTCCCCCAATCCCAACCTCCATCAAT-30 This study

vacA m-region Both LMVAM-F 50-GCCCCTTGGAATTATTTTGACGCTA-30 This study

LMVAM-R 50

-ATCCCGCATGCTTTAATGTC-30

This study

Fig. 2. Human gastric mucosa samples positive for H. pylori by age and sex. Theyoungest and oldest positive individuals were an 18-year-old male and an 89-year-old female, respectively. The PCR-positive rate increased with advanced age andexceeded 50% at the 40 s.

Table 2Detection rate by cause of death and postmortem time.

Numberof cases

Number of H. pylori -positivecases

(%)

Cause of death1. External cause 123 71 57.7

Burns 14 11 78.5Drowning 26 17 65.3Freezing 3 2 66.6Starvation 2 2 100Injury 61 29 47.5Asphyxia 7 6 85.7Poisoning 10 4 56.5

2. Internal cause 31 17 54.8Cardiac disease 14 8 50Cerebral disorder 5 4 80Other 12 5 41.6

3. Unknown 23 13 56.5

Postmortem interval1 week 153 81 52.9

About 1 month 19 15 78.91 year 5 5 100

16S-rDNAregions of DNA extracted from 5 gastric mucosal sites were amplied byPCR. Samples were designated as positive for H. pylori if the 16S-rDNA region was

detected

from

at

least

1

site.

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50.8% (90/177) in the lesser curvature, and 51% (92/177) in thepylorus. Spearmans correlation coefcient showed no statisticallysignicant differences in the detection rates of H. pylori DNA ateach of the 5 points of the gastric mucous membrane ( p < 0.05). In101 H. pylori DNA-positive samples, 75, 13, 5, 3 and 5 were positiveat all 5 points, 4, 3, 2 and 1 points, respectively.

Finally, vacA s- and m-region DNA segments were amplied byPCR and sequenced in samples from the randomly collected 10 Japanese and other foreigner cadavers of known geographic originand previously reported reference sequences from 28 samples. Asshown in Fig. 3, The sequenced vacA genes were classied into 3major clusters: (1) East Asian type I, consisting of Japan, China, andSouth Korea; (2) Western type II, consisting of Russia, theAmericas, and Europe; and (3) Southeast Asia type III, consistingof Thailand, Hong Kong, Taiwan, and Vietnam. Phylogenetic treeanalysis of the H. pylori vacA s- and m-regions from the cadaversexamined in this study and those described in previous studiesrevealed that all strains could be classied into one of thesegenotypes with high bootstrap values.

4. Discussion

Gastric H. pylori is common among middle-aged and elderly Japanese. A seroepidemiological study of H. pylori infection amongapparently healthy residents of Sapporo found a prevalence of 7080% in individuals born before 1950 [24] . For residents born after1950, the frequency of H. pylori infection increased by approxi-mately 1% with the birth year [24] . Overall, the prevalence of H.

pylori infection has decreased over the past few decades; based onserum samples from 1015 healthy people living in severalprefectures in central Japan [25] , overall H. pylori seropositivitywas 72.7% in 1974, 54.5% in 1984, and 39.3% in 1994. In a 2007study of 777 university students with a mean age of 19.6 years, H. pylori prevalence was only 14.7% [26] . Previous studies used serumsamples to detect H. pylori , but in forensic autopsies, it is difcult toextract blood due to decomposition of the cadavers and hemolysis.In 1994, Judice et al. found no difference in H. pylori detection ratesbased on PCR amplication and the anti- H. pylori IgG antigendetection methods. In this study, therefore, we used PCR amplication to detect H. pylori DNA from 5 points of the humangastric mucosa, which remains relatively intact even whendecomposition has progressed. Consequently, H. pylori DNA wasdetected in over 50% of forensic autopsy samples, despite thepurported decline in the prevalence of H. pylori infection.

External causes of death such as injury due to trafc accidents,burns, or drowning are often associated with severe damage anddecomposition, and various body parts are often damaged ormissing. In this study, except for one case in which the stomachwas carbonized by a burn, gastric mucosal samples could becollected from all cadavers with external causes as the cause of death. Among the present cases, the trigeminal nerve was lost as aresult of head injury in 2 cases and blood could not be extracted in26 cases due to coagulation and decomposition due to burns ordrowning, and H. pylori DNA was detected in 57.7% of cases.Additionally, H. pylori was detectable from the stomach, which canalso contain many medicines and agricultural chemicals. Regard-ing postmortem interval, Castillo-Rojas et al. [27] reporteddetecting H. pylori DNA in Mexican pre-Columbian mummiesdating to circa 1350 BC [27] . In this study, we also detected H. pyloriDNA from a mummied body, which was estimated to have diedseveral months to 2 years prior. There was no informationregarding the age, sex, or cause of death of this individual. Thedetection rate of H. pylori DNA increased with postmorteminterval, but since there were many elderly people among thesamples with long postmortem interval, it was considered that the

inuence of age was greater than the inuence of postmorteminterval. These ndings conrm that the condition of the cadaverhas only a minimal inuence on the ability to detect H. pylori DNAin the gastric mucosa.

A number of studies reporting the relationship betweenstomach disease and H. pylori infection based on the detectionof specimens according to presence or absence of symptoms andusing various study protocols indicate a prevalence of 90% amongthe gastric disease cohort [2831] . However, the present study isthe rst to review actual gastric ndings and H. pylori DNAdetection. Gastric ndings on autopsy were observed in 28individuals, and H. pylori DNA was detected in 21 (75%) of these.Gastric submucosal hemorrhage and discoloration among theseindividuals were likely due to post-mortem changes and, therefore,

should

not

be

considered

to

be

linked

to

gastric

diseases.Accordingly, individuals with gastric diseases, i.e., ulcers, perfora-tions, and tumors, showed a H. pylori DNA detection rate of approximately 75%. The present ndings corroborate previousreports that suggest that H. pylori colonization is related to gastricdisease. On the other hand, of the remaining 149 individuals withno gastric ndings, 80 (54.7%) were found to carry H. pylori DNA,while no gastric ndings were observed in 53.6% of individualscarrying H. pylori . These ndings show that H. pylori DNA isdetected at high rates, even in the absence of gastric ndings,which in turn suggests the importance of gastric mucosal samplingin the analysis of H. pylori DNA, irrespective of gastric ndings.

In 1990, a new system of classication, known as the SydneySystem, was announced at the World Congress of Gastroenterolo-

gy

in

Sydney,

Australia

[32] .

As

endoscopy

has

been

gaining

in

Table 3Comparison of H. pylori -positive status for cases with and without gastric ndings. a

Numberof cases

Numberof H. pylori -positive cases

(%)

Finding 28 21 75Submucosalhemorrhage orchange in color

15 10 66.6

Ulcer

8

8

100Perforation 3 1 33.3Tumor 2 2 100

No ndings 149 80 53.6Post-operation 3 0 0

a Gastric ndings comprised macroscopic ndings during autopsy and overallndings obtained from biochemical, histopathological and other laboratory testsperformed at autopsy.

Fig. 3. Phylogenetic tree of H. pylori strain types based on vacA s- and m-regionsfrom 17 cadavers (10 Japanese, 2 Chinese, 1 South Korean, 1 Taiwanese, 1 Thai, 1Afghan, and 1 Filipino) submitted for medico-legal autopsy which showed F and 32reference strains which showed R.vacA genes were classied into 3 major clasters:(1) East Asian type I, Western type II, and Southeast Asia type III.

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