ORIGINAL STUDY

Aspecte epidemiologice ale patologiei oncologice la pacienții cu diabet zaharat (2007-2017)

 Epidemiological aspects of oncological pathology in patients with diabetes (2007-2017)

First published: 04 aprilie 2017

Editorial Group: MEDICHUB MEDIA

DOI: 10.26416/OnHe.38.1.2017.587

Abstract

Introduction. Diabetes and cancer are the two most frequent pathologies and are responsible for 8%, respectively 13% of all deaths globally, with a significant impact on public health. According to the International Agency for Research on Cancer, in 2012, worldwide, there were 14.1 million new cases of cancer, 8.2 million deaths and 32.5 million people diagnosed with cancer in the last 5 years, still alive.
Material and methods. The authors have proposed a retrospective - longitudinal observational study, over a period of 10 years, respectively between 2007 and 2017, on a group of statistically significant patients, diagnosed with oncologic disease, having as comorbidity type 2 diabetes, patients who were hospitalized in the Oncology Medical Clinic of the Craiova County Emergency Hospital, with the purpose of detecting the incidence of diabetes associated with neoplastic disease.
Results. Lung cancer, female breast cancer, pancreas, liver and rectal cancer were most commonly associated with diabetes mellitus in patients included in the study, predominantly in men from urban areas.

Keywords
epidemiology, diabetes, cancer, treatment, diagnosis

Rezumat

Introducere. Diabetul şi cancerul sunt două dintre cel mai frecvent întâlnite patologii, fiind responsabile de 8%, respectiv 13% din numărul total al deceselor la nivel global, având un impact semnificativ asupra sănătății publice. Conform datelor Agenției Internaționale de Cercetare a Cancerului, în 2012 existau la nivel mondial 14,1 milioane de cazuri noi de cancer, 8,2 milioane de decese şi 32,5 milioane de persoane diagnosticate cu cancer, în ultimii 5 ani, aflate în viață.
Material şi metodă. Autorii şi-au propus realizarea unui studiu observațional, de tip retrospectiv - longitudinal, pe o perioadă de 10 ani, între anii 2007 şi 2017, pe un lot de pacienți statistic semnificativ numeric, diagnosticați cu boală oncologică, având diabet zaharat de tip 2 asociat, pacienți ce au fost internați în Clinica de Oncologie Medicală a Spitalului Clinic Județean de Urgenţă Craiova, cu scopul decelării incidenţei diabetului asociat bolii neoplazice.
Rezultate. Neoplasmul bronhopulmonar, al glandei mamare la femei, neoplasmul pancreasului, cel hepatic şi rectal au fost cel mai frecvent asociate cu diabetul zaharat în cazul pacienților incluși în studiu, predominant în cazul bărbaților din mediul urban.

I. Introduction

Diabetes and cancer are the two most frequent pathologies and are responsible for 8%, respectively 13% of all deaths globally, with a significant impact on public health. According to the International Agency for Research on Cancer, in 2012, worldwide, there were 14.1 million new cases of cancer, 8.2 million deaths and 32.5 million people diagnosed with cancer in the last 5 years, still alive.

As for type 2 diabetes, International Diabetes Federation data shows that in 2014, worldwide, there were 386.66 million patients diagnosed with this disease and, as estimated, their number will double by 2035. Seventy-seven percent of adults with diabetes live in countries with medium and low levels of development. The incidence of new cancer cases worldwide is about 3.5 million per year (Ferlay, Sterialova, 2013).

In Romania, at the beginning of 2016, the Ministry of Health records talked about 999,192 people diagnosed with diabetes, an increase of 73,740 persons (202 new cases per day) compared to 2015 (Fadri, 2017).

The incidence of cancer is continuously growing in our country. In 2013, there were 67.300 new cases of cancer reported, compared to the previous year, 35% more cases compared to 1990 (50,000 new cases of cancer). In terms of mortality, in 2013, there were recorded 41,000 deaths caused by cancer. The most common organs/target tissues affected by cancer in the new cases were the lungs, colorectal segment and breasts (Global Burden of Disease Cancer Collaboration, 2015).

Epidemiological data show that the presence of diabetes increases the risk of many forms of cancers, knowing that the two diseases have a number of common risk factors (age, sex, obesity, physical inactivity, smoking, drinking and diet).

Data available to date show a more frequent association of cancer with diabetes in the 6th decade of life, most commonly in men, considering the high incidence of developing both neoplasia and diabetes in this category of age (Giovannucci E, Harlan D, 2010).

Type 2 diabetes, accounting for 90-95% of all diabetes cases already diagnosed, is due to deterioration in blood sugar control caused by inadequate secretion of insulin due to damage of the function of b pancreatic cells; the main characteristics are hyperglycemia, hyperinsulinemia and dyslipidemia, all of which being involved in tumour transformation (Chen Li Deling Kong, 2014).

Epidemiological studies conducted so far have reported a strong correlation between the risk of developing cancer and diabetes, classifying diabetes as an independent risk factor for many types of cancers (Aljada & Mousa, 2012). The most common types of neoplasms in patients having as comorbidity type 2 diabetes were endometrial, cervical, ovarian, stomach, lung and kidney cancer, whereas for pancreas cancer and hepatocellular carcinoma was identified a lower correlation (Hemminki et al., 2010).

There is a close link between obesity and malignancy (Renehan et al., 2008; Key et al., 2010). Neoplasms such as of esophagus, colon, endometrium, kidney, pancreas and breast tumours in women of postmenopausal age were positively correlated with Body Mass Index. It has been shown that overexpression of leptin, adiponectin and other proinflammatory cytokines generated by the abdominal fat is a key promoter of neoplasm development.

II. Personal contributions

1. Purposes

The authors have proposed a retrospective - longitudinal observational study, over a period of 10 years, between 2007 and 2017, on a group of statistically significant patients diagnosed with oncologic disease, having as comorbidity type 2 diabetes, patients who were hospitalized in the Oncology Medical Clinic of the Emergency County Hospital Craiova (CECHC).

The study aimed to outline the epidemiological demographic trend characteristic to the group of patients already diagnosed with type 2 diabetes, insulin and non-insulin dependent, for which was established  the diagnosis of malignancy, as well as the correlations that exist between the main common risk factors in the development of the two diseases - patient age and sex, area of origin, Body Mass Index. A feature of the development of neoplasms in diabetic patients is represented by the type of diabetes therapy administered that may be correlated with certain localization of the tumours.

A better knowledge, from a clinical and etiopathogenetic point of view, of diabetes association with cancer, will allow for a proper medical approach in terms of diagnostic, therapy and prevention.

2. Material and method

Description of population group

The study group was represented by a total of 421 oncological patients already diagnosed with type 2 diabetes, including 224 men and 194 women, with ages between 26 and 89 years who were hospitalized in the Oncology Medical Clinic of the Emergency County Hospital Craiova (ECHC), in the period 2007-2017.

Patient data were collected from the patient records of oncology department (ONC 2) and from the medical records of patients hospitalized in the Oncology Medical Clinic of the ECHC.

Variables and sampling mode

  • Adults aged between 26 and 89 years old, men and women, from urban or rural areas.
  • Oral diabetes medication or insulin therapy.
  • Anthropometric parameters:
    •  waist measurement (T) with measuring tape;
    •  weight measurement (G) using scales;
    •  calculation of Body Mass Index (BMI) - formula: BMI=weight (kg)/height(m) (https://www.nhlbi.nih.gov/health/educational/lose_wt/BMI/bmicalc.htm) was compared with the normal values for age and gender growth curves specific to the BMI.

Statistical analysis

Statistical and graphical processing of the obtained data was performed using Microsoft Excel, 2016.

In terms of statistical indicators, there were used the mean, standard deviation and linear correlation coefficient (r). Regarding the correlation coefficient (r), its value between 0 and 0.2 means an absent correlation; between 0.2-0.4 means a weak correlation; between 0.4-0.7 means an average correlation; 0.7-0.9 means a strong correlation, and a 0.9-1 coefficient indicates a very strong correlation.
Figure 1. The distribution of diabetic patients who developed a malignancy by gender
Figure 2. Distribution of cancer patients by gender and area
Figure 3. Distribution of cancer patients diagnosed with type 2 diabetes by age
Figure 4 A. The distribution of diabetic patients by neoplastic localization
Figure 4 B. The distribution of diabetic patients by neoplastic localization
Figure 5. The most common localization of neoplasms by gender, for patients diagnosed with type 2 di

3. Results obtained

a) Epidemiological and demographic data

From the 421 patients examined, aged between 26 and 89 years (mean: 64.52 years; SD=9.4), who constituted the study group, patients diagnosed with neoplasm having as comorbidity type 2 diabetes, 227 were men (53%) and 194 were women (47%).

From the 421 patients who form the study group, depending on the area of origin, 229 patients (54%) come from urban areas, while 192 (46%) from rural areas.

In terms of gender and area of origin, patient distribution is as follows: 109 women (24%) come from urban areas, and 91 of them from rural areas (21%)
Figure 6. Type of diabetes therapy administered
Figure 7. The distribution of cancer patients with type 2 diabetes as associated comorbidity by Body
Figure 8. The incidence of lung cancer by patients gender and area of origin
Figure 9. The distribution of patients with lung cancer and type 2 diabetes by age group
The distribution of patients by Body Mass Index

As for men, out of a total of 227 patients, 126 of them come from urban areas and 101 from rural areas.

The most common association of type 2 diabetes with cancer, for patients included in the study, was for the category of 60-70 years old, with a total of 145 cases, representing 34.4% of the total.

An increased incidence of type 2 diabetes associated with cancer is observed from the 5th decade of life until the 7th, with a significant number of cases (105) for the category 50-60 years old (24.9%), respectively with 128 patients for the age group of 70-80 years old (30.4%).

b) Correlations between neoplasm, type of diabetes medication administered and Body Mass Index in the Oncology Medical Clinic of ECHC in the period 2007-2017

The most common association of cancer with type 2 diabetes in the Oncology Medical Clinic of ECHC was in patients with lung cancer - 82 cases, representing 19.47% of total cases studied, 61 of whom being men (14.48% of the total, 74.3% of patients diagnosed with lung cancer) and only 21 women (4.98% of the total, 25.7% of patients diagnosed with lung cancer). Lung cancer, breast cancer for women, cancer of the pancreas, liver, rectum, colon, stomach, ovary, bladder and cervix were most commonly associated with diabetes in the patients included in the study.

In terms of gender, the incidence of breast cancer in women with type 2 diabetes (53 cases; 12.58%) is comparable to the incidence of lung cancer for men with this comorbidity (61; 14.48%), reported to the total number of patients included in the study.

As for the type of diabetes therapy administered to patients at the moment of neoplasm diagnosis, 246 subjects received oral diabetes medication (58.43%), 144 were insulin-requiring (34.2%), and 31 patients had controlled blood sugar through diet (7.36%).

In terms of Body Mass Index, the distribution of patients included in the study is (presented in Figure 7).

Most of the oncological patients included in the study, with type 2 diabetes as associated comorbidity, had a Body Mass Index >24.9 (257 subjects), representing 61% of all patients, as follows:

  • 179 overweight patients (BMI between 24.9 and 29.9)
  • 48 patients with grade I obesity (BMI between 30 and 34.9)
  • 22 patients with grade II obesity (BMI between 35 and 39.9)
  • 8 patients with morbid obesity (BMI>40).

As for the remaining patients, 123 of them had normal weight at the time of diagnosis of the neoplasm (BMI between 19.5 and 24.9), 31 were underweight and 10 were cachexic.

c. Correlations between age, sex, area of origin and Body Mass Index for the first 5 neoplasm localizations

1. Lung cancer is the most common neoplastic localization registered at the Oncology Medical Clinic, between 2007-2017, being present in 82 cases, representing 19.47% of all cases, according to data resulting from the study conducted on a group that included 421 patients with type 2 diabetes as associated comorbidity.

In terms of gender, it was noticed a higher incidence of lung cancer concurrently with type 2 diabetes in men, in 61 cases (74%), compared to women, 21 cases (26%).

In terms of gender and area of origin, 39% of the patients with lung cancer included in the study were men from rural areas, and 35% from urban areas. As for women, reported to the total number of cases diagnosed with lung cancer, the incidence of this disease is much smaller, 15% being women from rural areas and 11% from urban areas.

Taking into account the patient’s age at diagnosis, lung cancer incidence peak was in the 6th decade of life, 34% of them (28 cases) aged between 60 and 70 years.

Depending on Body Mass Index, overweight and obesity were strongly associated with the occurrence of lung cancer, 45 patients, representing 54.9%, having a BMI>25 at diagnosis. Twenty-seven patients had normal weight (33%), 8 patients were underweight and 2 were cachexic.

2. Breast cancer was diagnosed for 53 of the patients who had type 2 diabetes as associated comorbidity, accounting for 12.6% of all patients included in the study.

The incidence depending on the area of origin indicates similar data, 28 patients coming from rural areas (52.8%), and 25 from urban areas (47.2%).

Regarding distribution by age, the highest incidence of diabetic patients who developed breast cancer was in the 6th decade of life (22 patients), representing 41.5% in this category.

The high Body Mass Index for women with diabetes is closely linked to breast cancer occurrence. Fourty-two women, representing 79.25% of the total number of patients at diagnosis, had a Body Mass Index greater than 25.

3. Pancreas neoplasm was diagnosed in 39 patients included in the study, representing 9.25% of the total number of patients included.

By gender, a higher incidence was observed in men (22 men; 56.41%), especially for men from urban areas (16 men; 41%). Regarding women, 17 diabetic women (43.58%) developed pancreas neoplasm, predominantly from urban areas (11 patients; 28.2%).

It was noticed a high incidence of pancreatic cancer patients from urban areas, both for women and men, 69% of patients included in the study living in urban areas.

The number of patients diagnosed with pancreatic cancer included in the study was comparable for the 6th (13 cases, 33.3%) and 7th (14 cases, 35.89%) decade of life.
Figure 10. The distribution of patients with breast cancer and type 2 diabetes by age groups
Figure 11. The distribution of patients by Body Mass Index
Figure 12. The incidence of pancreas cancer by patients’ gender and area of origin
Figure 13. The distribution of patients with pancreas cancer and type 2 diabetes by age groups
Figure 14. The distribution of diabetic patients diagnosed with pancreatic cancer by Body Mass Index

As for distribution of patients by Body Mass Index, more than half of patients with pancreatic neoplasm were overweight or obese, which reinforces the idea of obesity as a risk factor for developing pancreatic cancer.

4. Primitive liver cancer was diagnosed in 30 patients included in the study, representing 7.1% of the total number of patients included. By gender, the frequency of men diagnosed with primitive liver cancer was higher (21 men, representing 70% of the total number of cases, versus 9 women, representing 30% of the total number of diabetic patients diagnosed with liver cancer).

Depending on age, the highest incidence was in the 7th decade of life, where 33% of diabetic patients diagnosed with hepatocellular carcinoma were aged between 61 and 70 years.
Figure 15. The distribution of diabetic patients diagnosed with hepatocellular carcinoma by age
Figure 16. The distribution of diabetic patients diagnosed with hepatocellular carcinoma by Body Mas

The high Body Mass Index does not correlate directly with the occurrence of hepatocellular carcinoma, the incidence of normal weight patients (12 patients, accounting for 40% of diabetic patients with hepatocellular carcinoma) being equal to the number of patients with BMI>25.

5. Rectal cancer

The number of diabetic patients diagnosed with rectal cancer was 29, representing 6.8% of all patients included in the study. Men were most likely to develop such malignancies, representing 69% of diabetic patients diagnosed with rectal cancer.

Depending on the area of origin, the frequency of occurrence of rectal cancer in diabetic patients for rural areas was significantly higher (59%) than for those from rural areas.

Depending on age, 41.3% of subjects were aged between 60 and 70 years.

Depending on Body Mass Index, 68.96% of diabetic patients diagnosed with rectal cancer had a BMI>25, underlining the fact that overweight and obesity lead to the occurrence of such malignancies.

4. Discussions

The incidence of diabetes and cancer has reached alarming levels in the past decade, being in a continuous growth, which generates a real public health problem, involving high costs for the society.

Both cancer and diabetes are chronic diseases with a highly degree of complexity and multifactorial origin, being characterized by a high mortality worldwide (8% - diabetes mortality, cancer mortality - 13%, globally). Therefore, taking into account some risk factors common for the two comorbidities (age, sex, obesity, physical inactivity, smoking, drinking and diet), it is necessary the development of comprehensive prevention programs and prevention to include both cancer and diabetes.
Figure 17. The incidence of rectal cancer by patients gender and area of origin
Figure 18. The distribution of diabetic patients diagnosed with rectal cancer by age

According to World Health Organization (WHO), between 30-50% of cancer cases can be prevented. Prevention consists in developing national programs in order to raise awareness regarding this public health problem, in order to adopt a healthy lifestyle (WHO, 2017).

Physical activity, diet, obesity are particularly important factors in cancer and diabetes prevention.
Figure 19. The distribution of diabetic patients diagnosed with hepatocellular carcinoma by Body Mas

Given the increased interest for conducting comprehensive prevention programs, both by the European Community and the Romanian State, regarding the spread of both cancer and type 2 diabetes, and the fact that a large number of diabetics patients develop a malignancy during their lifetime, and diabetes is a comorbidity that can influence the therapeutic response of antineoplastic therapy, it was decided to study the influence that type 2 diabetes has on the oncological patient.

According to data from the clinical trial conducted in the group of 421 oncological patients already diagnosed with type 2 diabetes, aged between 26 and 89 years, all of them from the Oncology Medical Clinic of the Emergency County Hospital Craiova, in the period 2007-2017, it is possible to conclude that the major objectives of this study were achieved, having been highlighted the epidemiological demographic picture characteristic to the group of patients already diagnosed with type 2 diabetes, with or without requiring insulin, at which was established the malignancy diagnosis, as well as the correlations that exist between the main risk factors common to the development of the two diseases.

Thus, the study revealed a higher frequency of the type 2 diabetes associated to cancer in men (53%), with an increased incidence in the range of 50-80 years, with a peak incidence in the 6th decade of life - results comparable with data from specialty literature (Giovannucci et al., 2010).

As for the distribution of cases by area of origin, it was observed an increased incidence among patients from urban areas (54%) compared to rural areas, where common risk factors for diabetes and neoplasia (physical inactivity, unhealthy diet) are less common. Studies have confirmed the lower incidence in rural areas, but emphasized the fact that these patients consulted the doctor in a more advanced stage of the disease than those from urban areas because of the low accessibility to health care (Monroe AC et al., 1992). 

Lung cancer (19%), breast cancer for women (13%), cancer of the pancreas (9%), as well as other localizations (liver, rectal, colon, stomach, ovary, bladder and cervix) were most commonly associated with diabetes for patients included in the study. Specialty literature emphasizes, similarly, an increased incidence of diabetic patients who develop lung, cervical, ovarian, stomach cancer, while for pancreas cancer and hepatocellular carcinoma was identified a lower correlation (Hemminki et al., 2010).

Depending on the area of origin, for each of the neoplasia’s localizations studied it was observed their increased incidence, especially among males from urban areas, in the age group 60-70 years, results comparable with data from specialty literature.

Epidemiological studies conducted so far have reported a strong correlation between the risk of developing cancer and diabetes, classifying diabetes as an independent risk factor for many types of cancers (Aljada & Mousa, 2012). It has been demonstrated that the presence of type 2 diabetes increases the mortality in patients diagnosed with cancer (CJ Currie et al., 2012).

The mechanism involved in the association between diabetes and cancer is associated with hyperinsulinemia, as a result of insulin resistance characteristic to type 2 diabetes. The role of insulin in cell proliferation by the action of IGF1, responsible for the inhibition of apoptosis, is particularly important in the development of malignant tissues (Chen Li Deling Kong, 2014).

In the studied group, the number of men diagnosed with cancer who associated type 2 diabetes as a comorbidity is significantly higher than of women, predominantly from urban areas.

In terms of antidiabetic medications administered at the time of cancer diagnosis, most of the patients included in the study (58.43%) were undergoing treatment with oral antidiabetic agents, 34.2% were insulin-requiring and only 7.36% of those controlled the level of sugar blood through diet. It is important to continue the antidiabetic therapy accordingly, the correlation between uncontrolled diabetes and cancer being stronger than the correlation between antidiabetic and development of malignancies, but is not ruled out any hypothesis that supports the risk of having developed cancer following administration of certain anti-diabetic medicines (Quang T et al., 2012).

In the studied group, lung cancer has the highest frequency, followed by breast cancer, then pancreas and rectal cancer, for patients diagnosed with type 2 diabetes. These localizations are closely correlated with patients’ age, gender and Body Mass Index, the most common cases being found in urban men with a Body Mass Index greater than 25, data sustained by specialty literature as well.

The occurrence of lung, pancreatic and rectal cancer in patients diagnosed with type 2 diabetes is closely correlated with patients’ age, gender and Body Mass Index, the most common cases being found in men from urban areas, with BMI>25.

The correlation of overweight and obesity with the risk of developing both cancer and type 2 diabetes is strong, considering that 61% of all patients included in the study had a BMI>25. This hypothesis of the study is supported by specialty literature, which correlates closely with obesity the risk of developing diabetes, cancer and cardiovascular events.

Population awareness campaigns regarding the risk of developing these chronic diseases should be continued, in order to correct risk factors – a balanced diet and physical activity play a decisive role in preventing and treating type 2 diabetes. Moreover, countless studies have shown that physical exercises have a particularly important effect in reducing insulin resistance (WebMD Medical Reference, 2012).

5. Conclusions

1. The incidence of diabetes and cancer is in a continuous growth, both in Romania and worldwide, becoming a real public health problem.

2. In the studied group, the number of men diagnosed with cancer and type 2 diabetes as associated comorbidity is significantly higher than of women, predominantly from urban areas.

3. Lung cancer, breast cancer for women, cancer of the pancreas, liver, rectum, colon, stomach, ovary, bladder and cervix were most commonly associated with diabetes in the patients included in the study.

4. In terms of gender, the incidence of breast cancer for women with type 2 diabetes (53 cases; 12.58%) is comparable to the incidence of lung cancer for men with this comorbidity (61 cases; 14.48%), reported to the total number of patients included in the study.

5. The occurrence of lung, pancreatic, and rectal cancer in patients diagnosed with type 2 diabetes is closely correlated with patient age, gender and Body Mass Index, the most common cases being found in men from urban areas, with Body Mass Index higher than 25.

6. Most diabetic patients were being treated with oral antidiabetic agents at the moment of diagnosis with neoplasia, which can support the hypothesis involving such drugs in carcinogenesis.

7. 61% of the diabetic patients included in the study at the moment of diagnosis with neoplasia were overweight or obese, with a BMI>25, which is a evidence for the strong involvement of excess adipose tissue in cancer development.

8. The most common association of type 2 diabetes with cancer, for patients included in the study, was for the category of 60-70 years old, with a total of 145 cases, representing 34.4% of the total.

9. The study emphasizes the importance of national programs of public information and prevention for these two chronic diseases with a major impact on public health by modifying risk factors, most of them common in the pathophysiology of diabetes and cancer. 

Bibliografie

1. Aljada, A., & Mousa, S. A. (2012). Metformin and neoplasia: implications and indications, Pharmacol Ther 133, 108–115.
2. Bluher, M. (2012). Are there still healthy obese patients? Curr Opin Endocrinol Diabete Obes 19, 341–346.
3. Calle EE, Kaaks R. Overweight, obesity and cancer: epidemiological evidence and proposed mechanisms. Nat Rev Cancer. 2004 Aug; 4(8):579-91.
4. Chen Li, Deling Kong (2014). Cancer risks from diabetes therapies: Evaluating the evidence, Pharmacology & Therapeutics 144 (2014) 71–81.
5. Currie CJ, Poole CD, Jenkins-Jones S, Gale EA, Johnson JA, Morgan CL. Mortality after incident cancer in people with and without type 2 diabetes: impact of metformin on survival. Diabetes Care. 2012 Feb; 35(2):299-304.
6. Giovannucci E, Harlan DM, Archer MC, Bergenstal RM, Gapstur SM, Habel LA, Pollak M, Regensteiner JG, Yee D. (2010) Diabetes and cancer: a consensus report, CA Cancer J Clin. 2010 Jul-Aug; 60(4):207-21. doi: 10.3322/caac.20078. Epub 2010 Jun 16.
7. Hemminki K., Li X., Sundquist J., & Sundquist K. (2010). Risk of cancer following hospitalization for type 2 diabetes. Oncologist 15, 548–555.
8. IDF. International Diabetes Federation, Diabetes Atlas, 6th ed. http://www.idf.org/diabetesatlas/europe [accessed 17 Feb 2014].
9. Ferlay J, Steliarova-Foucher E, Lortet-Tieulent J, Rosso S, Coebergh JW, Comber H, 2012, Cancer incidence and mortality patterns in Europe: estimates for 40 countries in 2012. Eur J Cancer 2013; 49(6):1374–403.
10. FADR - http://fadr.ro/diabetul-in-romania/
11. Global Burden of Disease Cancer Collaboration, JAMA Oncol. 2015; 1(4):505-527. doi:10.1001/jamaoncol.2015.0735, July 2015.
12. Monroe AC, Ricketts TC, Savitz LA., Cancer in rural versus urban populations: a review, J Rural Health. 1992, Summer; 8(3):212-20.
13. Quang T. Nguyen, DO, FACE,  Lindsay Sanders, DO, MPH, Anu P. Michael, MD, Scott R. Anderson, MS IV, Loida D. Nguyen, PharmD, BCPS, and Zackary A. Johnson, MS II, Diabetes Medications and Cancer Risk: Review of the Literature, Am Health Drug Benefits. 2012 Jul; 5(4): 221–229.
14. Renehan, A. G., Tyson, M., Egger, M., Heller, R. F., & Zwahlen, M. (2008). Body-mass index and incidence of cancer: a systematic review andmeta-analysis of prospective observational studies. Lancet 371, 569–578.
15. WebMD Medical Reference, 2012, http://www.webmd.com/diabetes/guide/type-2-diabetes-in-children
16. WHO, 2017, http://www.who.int/cancer/prevention/en/

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