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Published in final edited form as: Mutat Res. 2022 Dec 31;826:111813. doi: 10.1016/j.mrfmmm.2022.111813

Association between DNA repair capacity and Body Mass Index in women

Ian Crespo-Orta 1, Carmen Ortiz 1, Jarline Encarnación 1, Erick Suárez 2, Jaime Matta 1
PMCID: PMC10200731  NIHMSID: NIHMS1863461  PMID: 36621052

Abstract

Objective –

Examine whether DNA repair capacity (DRC) levels are associated with body mass index (BMI) in adult women.

Design and participants-

A nested study composed of 539 women without breast cancer (BC) from a case-control BC study in addition to 104 that were recruited later for a total of 643.

Measurements-

DRC levels were measured in lymphocytes using a host-cell reactivation assay with a luciferase reporter gene damaged by UVC. This assay measures the efficiency of nucleotide excision repair (NER). Log-binomial regression model was used. The prevalence ratio (PR) was used to evaluate the magnitude of the association between the BMI and DRC levels. An assessment of interaction terms was performed with the likelihood ratio test. The confounding effect was assessed by comparing the point estimates of the crude and adjusted PR.

Results-

The 75th percentiles of DRC levels of the women with a BMI between 18-25 and >25 showed statistically significant differences. The prevalence of a DRC ≤ 5% among women with BMI > 25 is 1.24 (95% CI: 1.03, 1.48) times the prevalence of having a DRC ≤ 5% among the women with BMI ≤ 25 after adjustments for different covariates. This excess was statistically significant (p<0.05). Women with a family history of cancer had an estimated PR of 1.25 (95% CI, 0.87-1.39; P≥0.05); and women with no family history of cancer, the estimated PR was 1.6 (95% CI, 1.14-2.22; p ≤ 0.05).

Conclusions-

Women with BMI >25 tend to have lower DRC levels. When having a family history of cancer, the PR of low DRC levels in overweight/obese individuals was not statistically significant. However, the PR of low levels of DRC in overweight/obese individuals with no family history of cancer was statistically significant.

Keywords: DNA repair capacity, lymphocytes, body mass index, women

1. Introduction

Obesity is now considered a worldwide health problem; its rate has doubled since 1980 [1]Click or tap here to enter text.. Between 1980 and 2013, the frequency of overweight and obesity combined increased by 27.5% for adults and 47.1% for children [2]. It is well-established that obesity is the leading cause of morbidity and mortality associated with multiple conditions, such as metabolic syndrome, diabetes mellitus, and cardiovascular diseases among others [3]. In addition, obesity is now considered as a risk factor for several cancers by the International Agency Research Cancer (IARC). The World Cancer Research Fund (WCRF) recommends that the BMI for an adult should be 21-23 kg/m2. Studies have indicated that an increase of 5 kg/m2 in BMI, adjusted for all potential confounders, is associated with a significant increase in the risk of uterine cancer [4]. Having a high BMI has been associated with an increased incidence of BC in postmenopausal women [5].

Obesity consists of the accumulation of fat that results in a bodyweight that exceeds skeletal and physical requirements [6]. One of the hallmarks of obesity is the excess adipose tissue [7], which is reflected in the body mass index (BMI) [8]. Many studies have examined, at a molecular level, how obesity affects the body health. Excessive caloric intake and obesity are associated with an increased generation of reactive oxygen species (ROS), which can ultimately lead to DNA damage by creating oxidized bases [9]. Polo and Labbe (2021) hypothesized that the protumorigenic effect of certain diets, such as the Western diet, is partly caused by a diet-induced erosion of the DRC caused by altered epigenetic and epitranscriptomic landscapes. In contrast, the Mediterranean diet (and other diets) can have a protective effect due to its ability to sustain a proficient DNA repair [10].

DNA repair capacity (DRC) describes the host’s capacity to repair DNA damage [7, 11]. Humans vary in their inherent sensitivities to mutagens and carcinogens due to differences in their DRC levels [12-14]. Several studies using functional repair assays in lymphocytes have demonstrated that DRC varies significantly among individuals, whereas lower DRC is associated with a higher risk of several types of cancer [15-19]. Our research team was the first to report that low DRC levels, measured as the efficiency of the nucleotide excision repair (NER), is an important risk factor for BC [17, 18]. NER is the most versatile DNA repair pathway which is responsible for repairing bulky, helix-distorting lesions, such as those induced by crosslinking agents and base-damaging carcinogens [20, 21].

Obesity and aging can cause dysregulation of DNA repair pathways and are significant risk factors for the development of cancer and metabolic disorders [22]. Azzarà et al. (2016) compared the lymphocytes from obese and normal adolescents and concluded that obese individuals had lower DNA repair efficiency in terms of double-strand breaks repair [23]. Pan et. al. (2009), by analyzing the associations between functional polymorphisms in eight major NER genes and esophageal cancer risk, reported that NER pathway-based risk was more evident in smokers, overweight/obese individuals, men, and ever drinkers [24].

Setayesh et al. (2018) concluded that there is evidence that obesity may be influencing DNA repair by different means, but the tissue specificity and the underlying molecular mechanisms are only partly understood. The review by these authors reported the effect of obesity over organ-induced DNA damage in animal studies. In humans, inconsistent results regarding DNA damage have been reported when evaluating lymphocytes and sperm cells. This might have been a consequence of heterogeneous study designs and confounding factors (e.g., uncontrolled intake of vitamins and minerals and consumption of different food types [25].

This study aimed to examine whether DRC levels, measured in terms of NER and using lymphocytes as surrogate markers, is associated with BMI in adult women. Previous studies showed that BMI [4] and low DRC [17] are risks factors for BC. We hypothesized that a relationship exists between DRC and BMI. This study represents a secondary analysis of a cohort of 643 women, 539 of them were used as controls in a case-control breast cancer study controlling for factors such as demographic characteristics, lifestyle, and clinical history [17, 26, 27].

2. Methods

2.1. Patient recruitment and data collection

This study was approved by PHSU’s IRB (#120207-JM). Participants were consented by the study nurse and completed an epidemiological questionnaire regarding demographic variables. Participants were selected from a population-based case-control study [17]. This study represents a secondary analysis of 539 women without BC that served as controls in previously published studies and 104 more for a total of 643. The recruitment of the extra 104 control women and the analysis of their DRC levels ended in 2013 and thus these results were not included in the study by Matta et al. (2012) that reflects the recruitment of controls until the publication date. Participants included in this secondary analysis were required to have had: 1) a negative clinical breast examination done by a physician, and 2) a normal mammography. No additional experimental work was performed for this publication.

2.2. DNA repair capacity (DRC) measurements and calculation

DRC was assessed in the participants’ lymphocytes through the host-cell reactivation (HCR) assay with a luciferase reporter gene, as previously published [17, 18]. Gene expression of luciferase activity was measured using a luminometer (Turner Designs, model TD-20/20, Sunnyvale, CA). DRC was calculated as the percentage of luciferase activity present after damaged plasmid DNA repair, compared to the undamaged plasmid DNA repair (100%). Results were expressed as a percentage of residual luciferase reporter gene expression (percentage of luciferase activity in luminescence units).

2.3. Body mass index

BMI is a calculated using the weight in kilograms divided by the square of the height in meters (kg/m2) [1]. To calculate the BMI, the team used the National Institutes of Health’s (NIH) online BMI calculator [28]. The BMI was divided in five categories: underweight (<18.5 kg/m2), normal (18.5-24.9 kg/m2), overweight (25.0-29.0 kg/m2), and obese (≥ 30kg/m2) [29].

2.4. Statistical methods

To explore the relationship between DRC and BMI, the DRC was dichotomized using the overall median value as a cutoff point (≤5% vs. > 5%). Regarding the BMI, categories were defined as 18-25 kg/m2 (normal weight) and >25 kg/m2 (overweight). The number of women with DRC values below the median was calculated for each BMI category. To assess the magnitude of the association between BMI and DRC, the prevalence ratio (PR) was computed as follows:

PrevalenceRatio=PR=PrevalenceofhavingDRC≤5withBMI>25PrevalenceofhavingDRC≤5withBMI≤25

The log-binomial regression model was used to estimate the association between BMI and DRC, controlling for different demographic and clinical factors. An assessment of interaction terms in this model was performed with the likelihood ratio test [30]. In addition, the confounding effect was assessed by comparing the point estimates of the crude PR and adjusted PR.

3. Results

3.1. Demographic characteristics

In the study group, around 36.1% of the women had a BMI under 25, and 63.9% were classified as overweight (Table 1). Approximately 47.7% of women had DRC levels under 5%. The mean age of the study group was 52.2 years. Only 39% and 27.4% reported multivitamin and calcium consumption in the last five years, respectively. Smoking prevalence was low (8.7%), whereas alcohol consumption was twice as high (17.4%). Approximately 57.7 % of the women reported having a family history of cancer.

Table 1.

Demographic and epidemiological characteristics of 643 women in the study group without breast cancer.

Characteristics N %
DRC < 5% 307 47.7
BMI (> 25) 411 63.9
Age (mean ± se^) 52.2 (±0.5)
Consume Multivitamin 251 39.0
Consume Calcium 176 27.4
Smokers 56 8.7
Consume Alcohol 112 17.4
Pregnancy History 110 17.1
Family history of Cancer 371 57.7
Hysterectomy 163 25.4
Endometriosis 68 10.6
Hormone replacement therapy 241 37.5
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se^ = standard error

3.2. Distribution of DNA repair capacity (DRC) by weight

The 75th percentiles of the DRC levels of the two groups with BMI 18-25 and >25 were significantly different (8.2 and 6.9% respectively, p<0.05).

Table 2 shows that the prevalence of having a DRC ≤ 5% among women with BMI > 25 is 1.24 (95% CI: 1.03, 1.48) times the prevalence of having a DRC ≤ 5% among women with BMI ≤ 25. Similar results were obtained after adjusting for selected variables (p<0.05). These results also indicate that subjects with BMI > 25 are most likely to have a DRC ≤ 5%.

Table 2.

Association between DRC levels and BMI estimated using the Prevalence Ratio (PR) in 643 women without breast cancer.

BMI Total DRC PRcrude
(95% CI)		 PRadjusted
(95% CI)
> 5% ≤ 5%
18-25 232 (100%) 136 (58.6%) 96 (41.4%) Reference Reference
>25 411 (100%) 200 (48.7%) 211 (51.3%) 1.24 (1.03, 1.48)* 1.25 (1.03, 1.50)*
Total 643 (100%) 336 (52.3%) 307 (47.7%)
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Values presented as crude PR and adjusted PR after adjusting for age, calcium, multivitamin, hysterectomy, endometriosis, Hormone replacement therapy, pregnancy history, and family history of cancer.

Among the women with no family history of cancer, the prevalence of having a DRC ≤ 5% among the women with BMI > 25 is 1.6 (95% CI: 1.13, 2.25) times the prevalence of having a DRC ≤ 5% among the women with BMI ≤ 25 (Table 4). After adjustment, the PR was statistically significant (p<0.05). Therefore, this data indicates that not having a family history of cancer may increase the prevalence of having a DRC ≤ 5% with a BMI > 25.

Table 4.

Association between DRC levels and BMI estimated using the Prevalence Ratio (PR) in 272 women with no family history of cancer.

BMI Total DRC PRcrude
(95% CI)		 PRadjusted
(95% CI)
> 5% ≤ 5%
18-25 95 (100%) 64 (67.4%) 31 (32.6%) Reference Reference
>25 177 (100%) 85 (48.0%) 92 (52.0%) 1.6 (1.14, 2.22) * 1.6 (1.13, 2.25) *
Total 272 (100%) 149 (54.8%) 123 (45.2%)
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Values presented as crude PR and adjusted PR after adjusting for age, calcium, multivitamin, hysterectomy, endometriosis, Hormone replacement therapy, and pregnancy history.

Among women with a family history of cancer, as shown in Table 3, the prevalence of having a DRC ≤ 5% among the women with BMI > 25 is 1.25 (95% CI: .87, 1.39) times the prevalence of having a DRC ≤ 5% among the women with BMI ≤ 25. However, this finding was not significant (p>0.05). This suggests that having a family history of cancer does not influence the prevalence of having a DRC ≤ 5% with a BMI > 25.

Table 3.

Association between DRC levels and BMI estimated using the Prevalence Ratio (PR) in 371 women with a family history of cancer.

BMI Total DRC PRcrude
(95% CI)		 PRadjusted
(95% CI)
> 5% ≤ 5%
18-25 137 (100%) 72 (52.6%) 65 (47.4%) Reference Reference
>25 234 (100%) 115(49.1%) 119(50.9%) 1.07 (0.86, 1.33) 1.25 (0.87, 1.39)
Total 371 (100%) 187 (59.4%) 184 (49.6%)
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Values presented as crude PR and adjusted PR after adjusting for age, calcium, multivitamin, hysterectomy, endometriosis, Hormone replacement therapy, and pregnancy history.

4. Discussion

This study addresses the question of whether there is an association between BMI and DRC levels. Our results establish a link between DRC levels, measured in terms of NER, in lymphocytes and BMI in adult women. Also, we evaluated whether having a family history of cancer could have a contribution to this relationship. In our study, we found that women with lower DRC levels tend to have a higher BMI.

Obesity has been associated with more oxidative stress (OS) and higher levels of DNA damage through increased production of ROS [3]. Lymphocytes of obese and normal-weight adolescents were shown to repair DNA double-strand breaks with distinct temporal kinetics [23]. In addition, different types of diet have been reported to differentially affect DRC [10]. Therefore, it is biologically plausible that DNA repair levels can be associated with body weight. Our finding might be explained by a previous reported association between obesity with an elevated level of c-reactive protein, a marker of inflammation [31], and low-grade chronic systemic inflammation in adipose tissue [32, 33]. This condition is influenced by the activation of the innate immune system in the adipose tissue that promotes the pro-inflammatory status and increases OS, triggering a systemic acute-phase response [3]. Additionally, obesity can lead to DNA damage through the enhanced production of oxidized bases [9, 34]. The base excision repair (BER) of oxidative purine modifications is vulnerable to OS, while the NER of pyrimidine dimers is more resilient [35]. NER perform multiple functions, mainly when other repair pathways exhibit reduced functionality [36].

Obesity has been associated with increasing risk of several types of cancers, including gallbladder, kidney, and liver [4]. Obesity is also associated with an increase in risk for colon, cervical, thyroid, ovarian, postmenopausal breast cancers, and leukemia [4]. Our findings support the hypothesis that lower DNA repair in association with high BMI is an additional risk factor for cancer and suggest that it may contribute to increased BC risk in postmenopausal overweigh/obese women.

5. Limitations

A limitation of the study is that only the NER pathway, specifically Transcription-coupled repair, was evaluated using the HCR. As demonstrated by the study of Azzarà et al. 2016, it is suspected that other DNA repair pathways (e.g., homologous and non-homologous end joining) involved in double-strand breaks may also have an essential role in repairing DNA damage associated with increased body weight. In future studies, an analysis of BER pathway could be performed due to the link between obesity and oxidative damage [3]. Finally, the epidemiological design of our study and second data analysis, although establishes an association between DRC levels and obesity, cannot be utilized to establish causality. Rather, obesity can be visualized as a modifying factor of the DNA repair phenotype of an individual.

For future research, increasing the number of study participants will allow for a broader view and a deeper understanding of the general results, especially when comparing individuals with and without a family history of cancer. Another limitation of the study is that we did not had the required data to calculate relative fat mass, which has been established as a better measure to diagnose high adiposity [37]. Finally, since this was a secondary study, in the original study, we did not collect the metabolic profile and comorbidities of the patients. It will be interesting to assess how the metabolic profile and comorbidities will affect the results of the statistical analysis.

Figure 1.

Figure 1.

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DRC distribution by body mass index (BMI) strata. The left panel shows the distribution of DRC values in women with normal BMI. The right panel shows BMI values in overweight/obese women. Numbers in parenthesis represent the (25th percentile and 75th percentile) values, respectively.

Highlights.

  • DRC levels were measured in lymphocytes using a host-cell reactivation assay.

  • This study measures DNA repair via the nucleotide excision repair (NER).

  • Women with BMI >25 tend to have lower DRC levels.

Acknowledgments

This study was supported by grants from NIH-MBRS Program grants #S06GM008239-20 (JM, principal investigator), 9SC1CA182846-04 (JM, principal investigator), and 5SC1CA157250-02 to Ponce Health Sciences University (PHSU). Editorial assistance (Tacia Torres, Alina Cruz).

Footnotes

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Declaration of interests

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

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