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Maryam Bazargan

David J. R. Foster

Andrew K. Davey

Beverly S. Muhlhausler

Rosiglitazone Metabolism in Human Liver Microsomes Using a Substrate Depletion Method

Paweł Kaczmarek

Mateusz Hermyt

Weronika Rupik

Embryology of the VNO and associated structures in the grass snake Natrix natrix (Squamata: Natricinae): a 3D perspective

Neuroprotective effects of intravenous immunoglobulin are mediated through inhibition of complement activation and apoptosis in a rat model of sepsis

Bram G. Janssen

Wilfried Gyselaers

Hyang-Min Byun

Harry A. Roels

Ann Cuypers

Andrea A. Baccarelli

Tim S. Nawrot

Placental mitochondrial DNA and CYP1A1 gene methylation as molecular signatures for tobacco smoke exposure in pregnant women and the relevance for birth weight

A Vigàno

VB Bogdanov

Q Noirhomme

N Guy

R Dallel

S Laureys

C Phillips

J Schoenen

POSTER PRESENTATION Open Access
Mechanisms of individual differences in
heterotopic noxious analgesia (DNIC),
an fMRI study
A Vigàno1, VB Bogdanov2*, Q Noirhomme3, N Guy4, R Dallel4, S Laureys3, C Phillips3, J Schoenen3
From The European Headache and Migraine Trust International Congress
London, UK. 20-23 September 2012
Introduction
Pain responses can be suppressed by heterotopic contin-
uous noxious conditioning, e.g. continuous noxious cold
stimulation.
Objective
These diffuse noxious inhibitory controls (DNIC) may
be abnormal in migraine (Sandrini et al 2006,). DNIC
effects are modulated by a number of prefrontal cortical
areas (Piché et al 2009) that could be dysfunctioning in
migraine interictally.
Methods
We examined in healthy volunteers blood oxygenation
level dependent (BOLD) responses in prefrontal cortex
to repeated continuous noxious cold stimulation. The
relationships between those responses and degree of
inhibition of laser-induced pain during heterotopic cold
stimulation were analyzed.
Results
Our results show that cold-induced BOLD response in
anterior cingulate, orbitofrontal and lateral prefrontal cor-
tices predict cold-induced heterotopic analgesia and
attenuation of cerebral BOLD responses to laser stimula-
tion. Prefrontal responses to the onset of cold stimulation
were strongly related to the subsequent DNIC effect.
Conclusion
We conclude that early responses to noxious conditioning
are important for prediction of the analgesic DNIC effect.
We hypothesize that this predictive effect of frontal cor-
tices may be abnormal in chronic migraine.
Author details
1University of Rome La Sapienza, Italy. 2University of Utah, USA. 3University of
Liège, Belgium. 4Université d’Auvergne., France.
Published: 21 February 2013
References
1. Sandrini G, Rossi P, Milanov I, Serrao M, Cecchini AP, Nappi G: Abnormal
modulatory influence of diffuse noxious inhibitory controls in migraine
and chronic tension-type headache patients. Cephalalgia 2006,
26:782-789.
2. Piche M, Arsenault M, Rainville P: Cerebral and cerebrospinal processes
underlying counterirritation analgesia. J Neurosci 2009, 29:14236-14246,
Dnic.
doi:10.1186/1129-2377-14-S1-P94
Cite this article as: Vigàno et al.: Mechanisms of individual differences
in heterotopic noxious analgesia (DNIC), an fMRI study. The Journal of
Headache and Pain 2013 14(Suppl 1):P94.
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2University of Utah, USA
Full list of author information is available at the end of the article
Vigàno et al. The Journal of Headache and Pain 2013, 14(Suppl 1):P94
http://www.thejournalofheadacheandpain.com/content/14/S1/P94
© 2013 Vigàno et al; licensee Springer. This is an Open Access article distributed under the terms of the Creative Commons Attribution
License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium,
provided the original work is properly cited.


Mechanisms of individual differences in heterotopic noxious analgesia (DNIC), an fMRI study

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Antiarrhythmic drugs for out-of-hospital cardiac arrest with refractory ventricular fibrillation

Junyi Zhang

Congming Zhu

Rui Guan

Zhipeng Xiong

Wen Zhang

Junzhe Shi

Yi Sheng

Bingchuan Zhu

Jing Tu

Qinyu Ge

Ting Chen

Zuhong Lu

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Fábio Santiago

Simone Lima

Tayná Pinheiro

Rafaele Tavares Silvestre

Ubirani Barros Otero

Marianne Medeiros Tabalipa

Nadezda Kosyakova

Maria Helena Ornellas

Thomas Liehr

Gilda Alves

Santiago et al. BMC Res Notes  (2017) 10:52 
DOI 10.1186/s13104-016-2369-8
CASE REPORT
Benzene poisoning, clinical and blood 
abnormalities in two Brazilian female gas station 
attendants: two case reports
Fábio Santiago1,2,3, Simone Lima1, Tayná Pinheiro1, Rafaele Tavares Silvestre1,2,3, Ubirani Barros Otero4, 
Marianne Medeiros Tabalipa4, Nadezda Kosyakova5, Maria Helena Ornellas1,2,6*, Thomas Liehr5 and Gilda Alv
es1,2,3
Abstract 
Background: Brazilian gas station workers are chronically exposed to benzene, toluene, xylene (BTX) during their 
working time. Describe below two cases of latin female gas station workers with benzene poisoning symptoms and 
miscarriage history.
Case presentation: In both cases were identified complex chromosomal rearrangements (CCR) with fluorescence 
in situ hybridization, applied to whole chromosome paints by chromosomes 1, 2 and 4. The lower natural killer cell 
(NK) cells have also been observed in cases correspondents, especially the rare type of NK (NKbright) in their periph‑
eral blood cells.
Conclusions: It is known that acquired chromosomal aberrations are positively correlated with cancer and reproduc‑
tive risk. In concordance, lower NK cytotoxicity increases the risk for cancer, as well. Thus, this is the first study provid‑
ing hints on a possible causative relation of lower NK cytotoxicity and increase rates of chromosomal rearrangements 
including CCRs.
Keywords: Benzene, Toluene, Xylene, Cytogenetic, Painting chromosome, Natural killer
© The Author(s) 2017. This article is distributed under the terms of the Creative Commons Attribution 4.0 International License 
(http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, 
provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, 
and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/
publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
Background
Brazilian gas station workers are chronic exposed to ben-
zene, toluene and xylene (BTX), mainly benzene, during 
the working time [1]. Chronic exposure to benzene may 
lead to progressive degeneration of bone marrow, aplastic 
anemia and/or leukemia. According to the U.S. Depart-
ment of Labor only a detailed history and appropriate 
investigative procedures will enable a physician to rule 
out or confirm the benzene poisoning [2]. To assist the 
examining physician the cytogenetic tests with fluores-
cence in situ hybridization (FISH) shown to be a new and 
valuable tool to determine the workers in risk [3]. Genetic 
damages caused by benzene include sister chromatid 
exchanges, DNA cross linking agents, DNA adduct for-
mations, and impairment of DNA repair mechanisms [4].
Since 2010, 115 gas station attendants have been moni-
tored in Rio de Janeiro city, Brazil applying FISH, using 
whole chromosome painting (wcp) probes for chromo-
somes 1, 2 and 4. Among the study group, the medi-
cal inquiry identified two female gas station attendants 
with signs and symptoms of acute benzene intoxica-
tion, associated with history of abortions. Added to the 
cytogenetic tests an large hematological evaluation by 
cytometry were made and found a down regulation of the 
natural killer (NK) cells association an acquired complex 
chromosomal rearrangements (CCRs).
Case presentation
Case 1
A 25-year-old latin woman, working 8 h per day, 6 days 
a week, for the last 4  years as a gas station attendant 
Open Access
BMC Research Notes
*Correspondence:  mariahelenaornellas@gmail.com 
6 Departamento de Patologia Geral, Faculdade de Ciências Médicas, 
Universidade do Estado do Rio de Janeiro, Avenida Professor Manuel de 
Abreu 444, 4° andar, Vila Isabel, Rio de Janeiro 20551‑030, Brazil
Full list of author information is available at the end of the article
Page 2 of 5Santiago et al. BMC Res Notes  (2017) 10:52 
had one gestation with miscarriage in the first half of 
pregnancy. Headache, dizziness irritability, asthenia 
and normal menstrual cycle were reported. A physical 
examination showed changes in the thyroid gland, nod-
ules in the right lobe, and a nonspecific pulmonary aus-
cultation. The attendant also reported being a former 
smoker and not having a family history of cancer. Was 
found in 1/100 metaphases a CCR involving 8 chromo-
somal breakpoints described as: 46,XX,der(1)t(1;4),der(4)
t(1;4;?),ace(1),ace(1), (Fig.  1). Hemogram showed mild 
neutopenia (1470 cells/mm3) and biochemistry tests 
revealed no changes compared to normal values as 
described in Table  1. On the other hand, the immu-
nophenotypic analysis confirmed neutropenia (33.00%), 
with a lower NK cell count (2.28%), with all NK CD56+/
CD16− (Table 2; Fig. 1).
Case 2
A 40-year-old latin woman, who was not a smoker or 
drug addict, working 48 h a week for the last 9 years as 
a gas station attendant had a pathological history of one 
miscarriage in the first half of pregnancy. Anxiety, dizzi-
ness, cramps, asthenia and normal menstrual cycle were 
reported. No physical examination alteration and no 
family history of cancer were observed. For case 2, Fig. 1 
shows one CCR, which was found in 1/100 metaphases, 
described as der(4)ins(2;4), which was due to a 3 break-
point event. Complete hemogram and biochemistry tests 
Fig. 1 CCRs found in case 1 and 2 and flow cytometric analyses of NK cell subsets. Case 1: a CCR—der(1)t(1;4),der(4)t(1;4;?),ace(1),ace(1). b, flow 
cytometric analyses of NK cell of case 1. Show all NK cells (CD56 positive) are CD16 negative, thus all are sub‑sets of NKbright. Case 2: c CCR‑ ins(2;4). 
Chromosome 2 was folded and thus looks shorter due to preparation. d flow cytometric analyses of NK cell of case 1. Show all NK cells (CD56 
positive) are CD16 negative, thus all are sub‑sets of NKbright. a, b the probes were conjugated with TexasRed to label chromosome 1 (red), Diethyl‑
aminocoumarin (DEAC) for chromosome 2 (lightblue) and fluorescein isothiocyanate (FITC) for chromosome 4 (green). Other chromosomes were 
counterstained with DAPI (dark blue). c, d BD FACSCanto II cytometer was used in both cases and the data analyses were performed using the 
Infinicyt® software
Page 3 of 5Santiago et al. BMC Res Notes  (2017) 10:52 
showed no abnormalities in comparison with normal 
values, as described in Table I. Like case 1, the immu-
nophenotypic analysis of case 2 resulted in a lower NK 
cell count (1.51%), with all NK CD56+/CD16− (Table 2; 
Fig. 1).
Conclusions
We characterized cytogenetic, hematological, and immu-
nophenotypic status in two female gas station attendants, 
who working in gas station with a proved harmful envi-
romental concentration of BTX. The following abnor-
malities were found: CCRs, a decrease in NK cells with 
abnormal CD16 expression, and early pregnancy loss.
It is well known that gas station workers are exposed 
to potentially harmful chemicals including BTX. How-
ever, benzene is considered the main carcinogenic 
agent (group 1 according to IARC) and studies associ-
ate this compound with acquired cytogenetic altera-
tions [5–7]. Among various forms of benzene-induced 
genetic alterations, aneuploidy and chromosomal break-
age are the most studied [4]. Chromosomal aberrations 
in peripheral blood lymphocytes of chronically benzene-
exposed patients were previously documented [5–7]. 
Table 1 Biometrics data (clinical and  demographic) of  2 
female gas station attendants
Gamma GT Gamma glutamyl transpeptidase
a Marijuana
Biometrics data Case 1 Case 2
Smokers No No
Ex‑smokers Yes No
Illicit drug consumption Yesa No
Alcohol abuse Yes No
Family history of cancer No No
Blood test
 Erythrocytes (106/µL) 4.0 4.2
 Hemoglobin (g/dL) 12.0 12.5
 Hematocrit (%) 36.1 38.0
 Mean corpuscular volume (fl) 88.7 88.6
 Leukocytes (/uL) 4620 7410
 Neutrophils (%) 32.1 57.4
 Typical lymphocytes (%) 56.7 34.5
 Basophils (%) 0.6 0.4
 Eosinophils (%) 3.7 1.5
 Monocytes (%) 6.9 6.2
 Platelets (103/µL) 230 312
 Reticulocytes (%) 1.21 0.7
 Gamma‑GT (U/L) 31.0 14.0
 Oxaloacetic transaminase (U/L) 0.23 17.0
 Pyruvic transaminase (U/L) 15.0 11.0
 Creatinine (mg/dL) 0.6 0.7
 Total bilirubin (mg/dL) 0.23 0.38
 Lactate dehydrogenase (mg/dL) 252 320
 Rheumatoid factor (IU/mL) 9.6 9.5
 C reactive protein (mg/dL) 0.11 0.12
Table 2 Results of Immunophenotyping by flow cytometry
Monoclonal 
antibody
Lymphocyte Monocyte Granulocyte Eosinophil
Case 1
 Percent of 
total cells
54.1 6.7 33.00 3.03
 CD 4 28.56 – – –
 CD 8 13.75 – – –
 CD4 + CD 8 42.31 – – –
 CD5 44.20 – – –
 CD7 50.00 – – –
 CD2 46.60 – – –
 CD3 41.87 – – –
 CD16 0.00 0.00 36.5 0.00
 CD56 2.28 0.00 0.00 0.00
 CD16 + CD 
56 (NK)
2.28 0.00 0.00 0.00
 CD19 5.77 – – –
 CD20 6.10 – – –
 CD10 0.07 – 28.94 –
 CD27 0.00 0.00 0.00 3.52
 CD22 5.88 0.00 0.00 0.00
 HLA‑DR 7.23 6.42 0.00 4.00
 CD11c 3.08 7.06 32.4 3.52
 CD25 0.00 0.00 0.00 5.70
Case 2
 Percent of 
total cells
31.23 5.4 63.6 0.16
 CD 4 13.51 – – –
 CD 8 9.08 – – –
 CD4 + CD8 22.59 – – –
 CD5 30.85 – – –
 CD7 25.17 – – –
 CD2 24.36 – – –
 CD3 22.59 – – –
 CD16 0.00 0.00 55.06 0.00
 CD56 1.51 0.00 0.00 0.00
 CD16 + CD 
56 (NK)
1.51 0.00 0.00 0.00
 CD19 5.58 – – –
 CD20 5.59 – – –
 CD10 0.13 – 46.09 –
 CD27 0.00 0.00 0.00 0.00
 CD22 4.88 0.00 0.00 0.00
 HLA‑DR 4.89 7.12 0.00 0.00
 CD 11c 0.20 3.75 49.12 0.00
 CD25 0.00 0.00 0.00 0.00
Page 4 of 5Santiago et al. BMC Res Notes  (2017) 10:52 
Zhang et  al. [5] reported dose-dependent chromosomal 
aneuploidies (mono- and trisomies) in the peripheral 
blood lymphocytes of workers exposed to benzene. In 
our study, we analyzed CAs only in three pairs of chro-
mosomes, which make up 22.8% of the human genome. 
It’s a cheaper and faster test to estimate the DNA damage 
when compared to whole genome CA screening. Chro-
mosomal aberrations (CAs) of high complexities could 
be detected in 1 out of 100 metaphases per patient (i.e. 
1%). The rate of CCRs in normal controls lies between 
0 and 0.5%, determined in 1000 metaphases, each [8]. 
In the present study, only 100 metaphases could be ana-
lyzed per case. Thus, the finding of one meta- phase with 
a CCR among 100 cells is at least noteworthy.
Even though CCR detection in peripheral blood is not 
directly correlated with enhanced cancer risk, it should 
be kept in mind that such CAs may indicate increased 
radio- and/or chemosensitivity. As tumors may be 
induced by environmental factors in combination with a 
special genetic susceptibility, the two cases reported may 
be at risk of acquiring malignancies [8].
As is well known, meiosis is a complex process con-
trolled by different checkpoints, but males and females 
respond differently to meiotic disturbances [9]. Dur-
ing oogenesis, meiosis is generally pursued leading to 
the formation of aneuploid gametes or with single gene 
mutations.
Thus, in gametes, acquired genetic changes can be 
passed on to the next generation. Several epidemiological 
studies support the idea that genotoxic and nongenotoxic 
events following benzene exposure may be initiators 
of childhood leukemia in utero [10]. Another study on 
AML has shown that disease is usually initiated in utero 
because the leukemic translocations and other genetic 
changes are present in blood spots collected at birth [10, 
11]. Also interesting is the fact that the majority of the 
CCR cases are reported in females ascertained through 
repeated spontaneous abortions or the birth of a mal-
formed child [11].
Besides the detected CCRs pointing towards enhanced 
chemosensitivity, these two female workers had hemato-
logical and immunological abnormalities characterized 
by mild leukopenia (case 1) and NK abnormalities. There 
are some studies concerning benzene with hematologi-
cal and immunological abnormalities in humans [12–16]. 
The effects of immunotoxicity induced by benzene are 
depression and alteration of both the immune system 
mediated by cells and the humoral system [15]. Lan 
et al. [13] observed that leucocytes, B and CD4+-T cell 
counts, were significantly decreased in workers exposed 
to benzene compared to the controls. In another study, 
the number of T lymphocytes, lymphocytes T CD4 and 
T CD8, and NK cells was reduced in the percentages 
and absolute numbers, and an increase in the mono-
cyte count in workers during the period of exposure was 
found [15]. Thus, it was suggested that the depressive 
effect of benzene on the T and NK cells may be a factor 
of the probable carcinogenic activity of benzene through 
the immune system.
Natural killer (NK) cells are immune effector cells that 
recognize both virally infected and malignant target cells. 
Surprisingly, the results of the immunophenotypic analy-
sis revealed NK CD56 positive (normal fluorescence) and 
CD16 negative in both cases, suggesting the presence 
of the rare subtype NK bright in the peripheral blood, 
which has low cytotoxic action [15]. It is possible that the 
action of BTX on the immune system had blocked the 
transition of immature CD56 bright cells into CD56 dim 
cells. In agreement with this finding, an 11  year follow 
up study showed that low NK cytotoxicity of peripheral 
blood lymphocytes correlates with an increased risk for 
cancer [16].
The identifications of chromosomal abnormalities and 
NK downregulation in the blood may be a new indicator 
for effective follow up of workers exposed to BTX, pre-
venting diseases mainly important for females and their 
offspring. Further studies with a larger number of work-
ers are necessary to confirm the results found.
Abbreviations
AML: acute myeloid leukemia; BTX: benzene, toluene and xylene; CAs: 
chromosomal aberrations; CCR: complex chromosomal rearrangements; FISH: 
fluorescence in situ hybridization; NK: natural killer.
Authors’ contributions
GA, UBO and MHO designed the study and applied for Research Ethics Board 
approval. MMT, TP, RTS and FS recruited the workers. The cytogenetic and 
immunophenotypic data were analyzed by NK, SL and FS. FS prepared the 
manuscript draft with important intellectual input from TL and MHO. All 
authors approved the final manuscript and had complete access to the study 
data.
Author details
1 Laboratório de Marcadores Circulantes, Departamento de Patologia e Labo‑
ratórios, Faculdade de Ciências Médicas, Universidade do Estado do Rio de 
Janeiro, Rio de Janeiro, Brazil. 2 Pós‑graduação em Ciências Médicas (PGCM), 
Universidade do Estado do Rio de Janeiro, Rio de Janeiro, Brazil. 3 Coordenação 
de Pesquisa, Instituto Nacional de Câncer, Rio de Janeiro, Brazil. 4 Unidade 
Técnica de Exposição Ocupacional, Ambiental e Câncer, Coordenação de Pre‑
venção e Vigilância, Instituto Nacional de Câncer, Rio de Janeiro, Brazil. 5 Jena 
University Hospital, Friedrich Schiller University, Institute of Human Genetics, 
Kollegiengasse 10, D‑07743 Jena, Germany. 6 Departamento de Patologia 
Geral, Faculdade de Ciências Médicas, Universidade do Estado do Rio de 
Janeiro, Avenida Professor Manuel de Abreu 444, 4° andar, Vila Isabel, Rio de 
Janeiro 20551‑030, Brazil. 
Acknowledgements
We thank the subjects who volunteered in the study.
Competing interests
The authors declare that they have no competing interests.
Availability of data and materials
All the data supporting our findings is contained within the manuscript.
Page 5 of 5Santiago et al. BMC Res Notes  (2017) 10:52 
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This study was approved by the local ethics committees (Instituto Nacional de 
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Received: 18 September 2016   Accepted: 30 December 2016
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