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Evaluation of micronuclei in oral 
mucosa of individuals exposed to 
ionizing radiation: a pilot study 
from Celaya, México 
 
Nicolas Padilla-Raygoza1*, María 
del Rocio Adame Gutiérrez2, Itza 
Zelene Moreno Martínez3, Vicente 
Beltran-Campos4, Silvia del 
Carmen Delgado-Sandoval1, Maria 
de Lourdes Garcia-Campos4, 
Modesto Antonio Sosa-Aquino5, 
Teodoro Cordova-Fraga5, Rafael 
Guzman-Cabrera6 
 
1Department of Nursing and Obstetrics, 
Division of Health Sciences and 
Engineering, Universidad of Guanajuato 
Mutualismo, México;  
2Academic Unity of Nursing N°1, 
University Autonomous of Guerrero, 
México;  
3Division of Health Sciences and 
Engineering, University of Guanajuato, 
México; 
 

 

 

 

 

 

 

 

 

 

 

 

4Department of Clinical Nursing, Division 
of Health Sciences and Engineering, 
University of Guanajuato, México  
5Department oh Physical Engineering, 
Division of Sciences and Engineering, 
University of Guanajuato, México  
6Departmentof Electrical Engineering, 
Division of Engineerings, University of 
Guanajuato, México  
 

*Corresponding author. 

 
 

Vol. 8, No. 1 (2019)   |   ISSN 2166-7403 (online)  
DOI 10.5195/cajgh.2019.331 |   http://cajgh.pitt.edu 

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Central Asian Journal of Global Health 
Volume 8, No. 1 (2019) |  ISSN 2166-7403 (online) | DOI 10.5195/cajgh.2019.331|http://cajgh.pitt.edu 

 
 

Abstract 

Introduction: Occupational exposure to ionizing radiation can potentially lead to adverse health effects, including cancer and 
genetic defects. Genetic damage caused by radiation can be detected if micronuclei are observed. The objective of this pilot study 
was to detect the presence of micronuclei in cells of the oral mucosa in inidividuals occupationally exposed to ionizing radiation. 
Methods:  We implemented a pilot case-control study in which we compared oral mucosa micronuclei in 30 medical and nursing 
personnel in radiology centers in Celaya, Mexico, with 30 volunteers not exposed to ionizing radiation recruited from a public 
University. The oral mucosa was brushed and the amount of micronuclei was quantified. Chi-square test or t-test for two proportions 
were used to compared ionizing radiation and genetic damage between exposed and non-exposed groups. 
Results: The exposed group had an average of 5.37 ± 3.49 micronuclei and the non-exposed had 0.37 ± 0.61 (P<0.01). In the 
exposed group, 90% of participants exhibited genetic damage compared to 6.67% in the unexposed group (P<0.05).  
Conclusion: In this pilot study, medical and nursing staff from radiology centers presented with higher genetic damage compared 
to control group. Further studies are needed to identify the prevalence of genetic damage due to occupational radiation exposure in 
Mexico. 

Keywords: Ionizing Radiation; Micronuclei; Genetic Damage 

Evaluation of micronuclei in oral 
mucosa of individuals exposed to 
ionizing radiation: a pilot study from 
Celaya, México 
 
Nicolas Padilla-Raygoza1*, María del 
Rocio Adame Gutiérrez2, Itza Zelene 
Moreno Martínez3, Vicente Beltran-
Campos4, Silvia del Carmen Delgado-
Sandoval1, Maria de Lourdes Garcia-
Campos4, Modesto Antonio Sosa- 
Aquino7, Teodoro Cordova- Fraga7, 
Rafael Guzman-Cabrera9 
 
1Department of Nursing and Obstetrics, 
Division of Health Sciences and Engineering, 
Universidad of Guanajuato Mutualismo, 
México;  
2Academic Unity of Nursing N°1, University 
Autonomous of Guerrero, México;  
3Division of Health Sciences and 
Engineering, University of Guanajuato, 
México; 

 

4Department of Clinical Nursing, Division of 
Health Sciences and Engineering, University 
of Guanajuato, México  
7Department oh Physical Engineering, 
Division of Sciences and Engineering, 
University of Guanajuato, México  
9Departmentof Electrical Engineering, 
Division of Engineerings, University of 
Guanajuato, México 

Research 

Introduction 

Chronic exposure to ionizing radiation can 
potentially lead to significant negative health effects, 
including increased incidence of cancer as well as genetic 
and immunological defects1. Moreover, exposure to low 
doses of radiation (less than 50 mSv/year) early in life 
increases susceptibility to damage from high-dose 
radiation exposure later in life2.  Studies on ionizing 
radiation have been predominantly focused on the high-
dose radiation exposure, such as nuclear bombs and 
nuclear plant spills1. The effects of chronic occupational 
low-dose radiation exposure received little attention.  

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CENTRAL ASIAN JOURNAL OF GLOBAL HEALTH 
 

 

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Many countries have adopted the International 
Commission on Radiological Protection (ICRP) 
recommendations of a 20-mSv-per-year occupational 
effective dose limit with allowances to go as high as 50 
mSv per year, as long as the average annual dose over 
five years does not exceed 20 mSv3. However, workers 
may be exposed to much higher doses during routine 
operations due to the nature of their occupation. 

Micronuclei (MN) are one way of detecting 
genetic damage caused by radiation. Damage from the 
radiation leads to the incorrect incorporation of genetic 
material into the nuclei of the daughter cells, resulting in 
chromosomal losses and unequal distribution of the 
genetic material. These genetic aberrations cause the 
emergence of MN4,5, small extranuclear bodies that 
contain centric or acentric chromatid, chromosomal 
fragments, or complete chromosomes that are not 
included in the daughter nuclei during mitosis.  Thus, 
MN are cellular markers of chromosomal damage4,6-8. 

Since buccal epithelial cells reported to be sensitive to 
radiation, observing MN presence in these cells can be 
used to accurately monitor potential exposure9,10. The 
MN testing has been used to identify early genotoxic 
effects, as well as to evaluate occupational exposure to 
mutagenic substances11. Since the MN test is non-
invasive, individuals are more willing to be screened 
through this method. 

The Mexican Official Norm NOM-229-SSA1-
2002 Environmental health, establishes the dose limit for 
individuals working in the radiology centers at 50 mSv 
per year12. For individuals who do not work in the 
radiology centers, the annual limit is 5 mSv. Little 
research has been done on occupation radiation exposure 
in Mexico, a research gap this study is aiming to fill. The 
objective of this pilot study was to measure the presence 
of MN in personnel exposed to ionizing radiation 
compared to non-exposed personnel in Celaya, Mexico. 
The hypothesis was that personnel exposed to radiation 
will have higher MN compared to non-exposed 
individuals.  

 

Methods 

Participants 

This was a case-control pilot study in which 
subjects exposed to ionizing radiation were compared to 
a group of unexposed individuals.  Research participants 
were assessed at the Life Style Laboratory of the Division 
of Health Sciences and Engineering, Celaya Salvatierra 
Campus of the University of Guanajuato in Celaya, 
Mexico. The inclusion criteria for exposed group were 
full-time employment at public or private x-ray center 
who reported direct involvement with x-ray equipment. 
Research participantes included physicians, nurses, and 
secretaries). The unexposed group consisted of nursing 
students, nurses, and medical doctors recruited from the 
University of Guanjuato who did not have regular 
exposure to x-ray and lived in the same city as the 
exposed group. The exclusion criteria for both the 
exposed and unexposed groups were any history of 
cancer diagnosis and/or presence of acute infectious 
disease (such as influenza) at the time of oral scraping.  

The project was approved by the Bioethics 
Committee (registration CBDCSI-87141126) through 
the Division of Health Sciences and Engineering of the 
Celaya Salvatierra Campus, University of Guanajuato, 
Mexico. 

Data collection 

Information on demographic factors, including 
age, gender, residence, marital status, and education, was 
collected using interviewer administered survey. 
Detailed information about occupational history, 
including previous experience in x-ray rooms and 
duration of previous employment, was also collected. 
Smoking was assessed as a dichotomous categorical 
variable and was defined as smoking two or more 
cigarettes a day. Radiation was measured as 1-month 

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Table 1. Sociodemographic characteristics by group 

Variable Exposed group 
n       % 

Non-exposed group 
n       % 

P-value 

Gender 
   Male 
   Female 

 
14     46.67 
16     53.33 

 
8    26.67 
22  73.33 

>0.05 

Residence 
   Urban 
  Suburban 
   Rural 

 
26     86.67 
1        3.33 
3       10.00 

 
21   70.00 
6     20.00 
3      10.00 

>0.05 

Marital status 
   Single 
   Married 
   Separated 
   Widowed 
   Divorced 
   Free union 

 
9      30.00 
15    50.00 
1        3.33 
2        6.67 
1        3.33 
2        6.67 

 
25   93.33 

  5     16.67 
0      0.00 
0      0.00 
0      0.00 
0      0.00 

<0.01* 
 
 
 
 

Education 
   Elementary 
   Secondary 
   High School 
   Technical career 
   Bachelor degree 
   Postgraduate    

 
2        6.67 
1        3.33 
3      10.00 
15     50.00 
2         6.67 
7       23.33 

 
0       0.00 
1       3.33 
1       3.33 
0       0.00 
26   86.67 
2      6.67 

<0.01* 
 
 
 
 
 
 

Occupation 
   Receptionist 
   Assistant 
   Technician 
   Nurse 
   Medical Doctor 
   Support team 

 
2        6.67 
2        6.67 
15    50.00 
5      16.67 
4      13.33 
2       6.67 

 
1      3.33 
0      0.00 
2      6.67 
15   50.00 
7      23.33 
5     16.67 

<0.02* 
 
 
 
 

Smoking 
   Yes 
   No 

 
4     13.33 
26    86.67 

 
8     26.67 
22   73.33 

0.20 

Age(years) 
  Mean ± S 

 
37.80 ±11.59 

 
25.30 ± 7.09 

 
<.01¥ 

Time at the work (years) 
   Mean±S 

 
10.83±7.86 

 
2.08±2.49 

 
<.01¥ 

*Fisher’s Exact-Test 
¥Student’s t test  

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uptake of ionizing radiation using a dosimeter. The 
dosimeters used in this study consisted of one pair of 
thermoluminescent crystals chips (TLD-100, 
ThermoFisher Scientific, Waltham, MA, USA) were 
placed in appropriated badges as previously described13.  
Before use, TLDs were annealed to 400oC for one hour 
and to 100oC for two hours in a muffle in order to erase 
any environmental or spurious signals. The badges were 
worn by the participants on the upper left side of the chest 
during work hours as the highest radiation exposure is 
expected in this part of the body14. The dosimeter 
readings were performed using the Harshaw TLD 3500 
equipment with appropriated readings parameters. 

All participants were given a dosimeter to carry 
during work hours for a month to measure exposure to 
ionizing radiation. After a month, the dosimeters were 
collected and sent for analysis to the Medical Physics 
Academic Body and Biomedical Instrumentation (León, 
Mexico). Radiation was defined as high exposure ( ≥4.1 
mSv) or low exposure ( ≤4.0 mSv) based on the Official 
Mexican Norm standards12.  

  Genetic damage was determined as the 
number of micronuclei present in the oral samples.  Oral 
samples were taken during the study enrollment by 
brushing the cheek of the mouth and storing the samples 
in a neutral pH buffer at 10ºC until processing, fixation, 
staining with Giemsa, and second fixation according to 
the technique previously described by Thomas et al15. 
MN were then quantified by clear field microscopy at 
100x magnification and were defined as the number of 
cells with micronuclei per 1000 cells. Genetic damage 
was defined as ≥2 MN per 1000 cells and no genetic 
damage was defined as <2 MN per 1000 cells. 

Statistical analysis 

The distribution of categorical variables, 
including gender, residence, marital status, education, 
occupation, and smoking, was compared between 
exposed and non-exposed groups using Chi-square test 
or t-test for two proportions. The continuous age variable 

was compared between exposed and non-exposed groups 
using Student’s t-test. The frequency of high- and low-
radiation exposure (≥4.1/month or <4.1 mSv/month) and 
presence of genetic damage (≥2 or <2 MN per 1000 cells) 
were represented using percentages and compared 
between exposed and non-exposed radiation groups 
using Fisher’s exact test. A two-tailed P value of 0.05 or 
less was considered to be significant. All statistical 
analyses were performed using STATA 13.0® (Stata 
Corp., College Station, TX, USA). 

 

Results 

We recruited 30 participants who worked in the 
x-ray centers (exposed group) and 30 participants who 
did not work in the x-ray center (non-exposed group). 
The distribution of the sociodemographic variables for 
the exposed and non-exposed groups is shown in Table 
1. Both groups were predominantly female (53.33% vs 
73.30%, P >0.05), urban residents (86.67% vs 70.00%, P 
>0.05), smokers (86.67% vs 73,33%, P=0.2), and 
married (50% vs 16.67%, P=0.02). The mean age and 
time at work were higher in the exposed than non-
exposed group (P <0.01). In the exposed group, there was 
a mean of MN 5.37±3.49 and in the non-exposed group 
there was a mean 0.37±0.61 (t-test=-7.73, df 58, P<0.01). 

High radiation exposure (≥4.1mSv) was 
significantly more common among the exposed group 
compared to the non-exposed group (13.33% vs 0.00%, 
P<0.05) (Table 2). Genetic damage (≥2 MN per 1000 
cells) was more common among the exposed group 
compared to the non-exposed group (90.00% vs 6.67%, 
P<0.05) in this sample.  

 

Discussion 

We found a significant difference in MN count between 
radiation exposed and non-exposed groups in Celaya, 
Mexico. The exposed group had higher number of 
participants with 

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 Exposed group (n=30) 
f      % 

Non-exposed group (n=30) 
f    % 

P-value 

Exposure to radiation (mSv/month)* 
  High (≥4.1) 4     13.33 0      0.00  0.04* 
  Low (<4.1) 26      86.67 30   100.00  
Number of Micronuclei (per 1000 cells) 
  Genetic damage 
  Non-genetic damage 

27   90.00 
3    10.00 

2      6.67 
28  93.33 

<.01 

*Fisher Exact Test 
Table 2. Distribution of exposure to ionizing radiation and genetic damage by the exposure group

unsafe level of exposure (13% vs 0%) based on the 
Official Mexican Standard -SSA1-2002, Environmental 
Health12. 

Our results are consistent with previously 
published literature. Qian et al.,16 found that personnel 
working with x-rays have a higher MN count than the 
control group of healthy adults without history of expose 
to radiation, which similar to the results found in this 
study, where the exposed group had a higher MN number 
per 1000 cells compared to the non-exposed group (Table 
2). We have also found that individuals working in x-ray 
centers have been exposed to more radiation than 
permitted by national guidelines. 

Kanaragaj et al.,17 quantified the presence of 
MN in binucleated cells (lymphocytes from peripherical 
blood) in subjects before and after undergoing computed 
tomography and found a significant increase in MN after 
the procedure. Their findings demonstrate that acute 
exposure to ionizing radiation causes genetic damage. In 
our study, we measured chronic occupational radiation 
exposure and found the number of MN in oral cells was 
significantly higher (P<0.05) in those exposed 
occupationally to ionizing radiation compared with the 
non-exposed group.  

The key limitation of this study is its small 
sample size. However, this was a pilot study designed to 
inform future larger investigations. Another limitation is 
that there was an age difference between exposed and 
non-exposed group, which may have influenced findings. 

Also, the measurement of radiation exposure was 
performed over the course of one month, which may not 
be sufficient. Another limitation is that there are other 
methods to identify genetic damage that could provide 
more insight, such as screening for micronuclei in 
lymphocytes.  

The strength of our study is that the 
measurement of exposure to ionizing radiation was 
performed in a consistent way, using standard dosimetry 
techniques. 

The results of this study warrant careful 
interpretation. While our results show significant 
differences for markers of genetic damage, the exposed 
and non-exposed groups are somewhat different in terms 
of age and several other characteristics to make definitive 
conclusions. Future studies should concentrate on 
establishing more robust methodology, recruiting more 
comparable study populations, as well as improving the 
sample size. Exposure to ionizing radiation may have a 
significant effect on genetic damage in individuals, 
therefore it is important to implement protective 
measures. In Mexico and other countries, it is very 
important to provide concise guidelines on planning, 
performing, and interpreting studies to monitor groups or 
individuals exposed to genotoxic agents.  

 

Acknowledgments 

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Central Asian Journal of Global Health 

Volume 8, No. 1 (2019) |  ISSN 2166-7403 (online) | DOI 10.5195/cajgh.2019.331|http://cajgh.pitt.edu 

 
 

The authors thank all the participants, without 
their support the study would not have been carried out. 

 

Financial Support 

The Research and Postgraduate Support 
Department of the University of Guanajuato financed the 
study; they did not participate in design of the study, 
neither analysis 

 

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	Abstract
	Keywords: Ionizing Radiation; Micronuclei; Genetic Damage
	Research

