Association between demographic variables and cervical cancer staging in elderly women: a retrospective study

 

Ana Hélia de Lima Sardinha1, Pabline Medeiros Verzaro1, Nívya Carla de Oliveira Pereira Rolim1, Sara Maria Ferreira de Sousa1, Aida Patricia da Fonseca Dias Silva1, Alynne Radoyk Silva Lopes1

 

Federal University of Maranhão, MA, Brazil

 

ABSTRACT

Objective: To associate the sociodemographic variables of elderly women with cervical cancer and staging of an oncology reference hospital. Method: An observational, retrospective analytical study of 559 elderly women. Results: The variables that presented a statistically significant correlation with cervical cancer staging were: married elderly women, histopathological squamous cell carcinoma, radiotherapy + chemotherapy as the first treatment received in the hospital, complete remission of the disease at the end of the first treatment, without deaths from cancer and never having smoked. Conclusion: Although  some characteristics are related to higher prevalence, they were not associated with staging, such as older ages. Early treatment was also an aspect associated with less late staging. Thus, the study reaffirms the importance of knowing the epidemiological characteristics of these women, as it favors the planning and evaluation of effective programs in the control of cervical cancer. 

Keywords: Cancers of the cervix; Aging; Women's health.

 

 

INTRODUCTION

The process of population aging is accelerating rapidly around the world, it is one of humanity's greatest triumphs and also one of the great challenges to be faced by society, however, the aging process, most often comes accompanied by the appearance of chronic non-communicable diseases, such as cancer. Elderly people represent the majority of new cases and deaths due to the disease, indicating the need for specific attention to this group and its particularities (1). With the favoring of sexuality of this age group due to modern discoveries that increase sexual desire, there were changes in the old conception that the elderly were asexual people, however, some elderly women do not possess information about safe sex, disregarding the use of condoms because they can no longer become pregnant, and it is up to the health professional to identify this gap in view of the risk for the development of cancer (2).

Cervical cancer is considered a public health problem in Brazil, although it is preventable when low-grade lesions are identified early, yet it has high mortality, contributing significantly to the burden of the disease in women, being considered the fourth most common type of cancer in this population (3)

About 85% of cases of cervical cancer occur in less developed countries (4), being associated with poverty and low education levels. Recurrent infection by the human papilloma virus (HPV) virus is considered the main cause for the development of this type of cancer (5,6), transmitted mainly through unprotected sexual contact.

The early identification and treatment of early-stage lesions contribute to the good prognosis of the disease. The strategies for early detection/screening of CC (Cervical Cancer) are the collection of material for cervical-vaginal cytopathological examinations, being recommended for women between 25 and 64 years of age, who have already started their sexual life, with annual periodicity, initially, and after two consecutive negative tests, periodicity should be every three years (4).

In view of the above, knowing the most prevalent staging of this tumor and the variables that have a significant correlation with it, contributes with information to strengthen practices and policies to improve control actions for cervical cancer , aiming to minimize the incidence of cases. Thus, the aim of the present study is to associate the sociodemographic variables of cervical cancer victims and the staging in an oncology reference hospital.

 

METHOD

This is an observational, retrospective and analytical study. The data came from the Aldenora Bello Cancer Hospital, a philanthropic institution and reference for cancer treatment, located in São Luís, the capital of Maranhão State. The institution's Health Information System of Hospital Records (SIS-RHC) was used as a data source, by means of the Tumor Registration Forms.  A total of 553 elderly women were sampled, corresponding to 100% of the cases of cervical cancer treated by the institution from January 1, 2009 to December 31, 2013, and the temporal cut-off of these data refers to those that were available at the time they were collected, due to a discrepancy in the hospital registry, justified by the lack of professionals responsible for this work.

We included women diagnosed with cervical cancer, aged 60 years or older, who were registered and performing treatment at the institution. Those who started treatment in another institution or who lived in other States of the Federation were excluded.

Demographic variables were analyzed: age, race, education, occupation, origin, neighborhood, city, marital status, alcoholism, tobaccoism, family history; clinical and treatment characteristics, such as the location of the primary tumor, histopathological type, NMD, staging, location of distant metastasis, clinic at the beginning of treatment, main reason for not performing treatment, first treatment received in the hospital, stage of the disease at the end of the first treatment and death from cancer. The variables of risk factors (coitarche, age at first Papanicolaou examination, smoking and family history) could not be evaluated due to the low completeness of the data.

The data were input in Excel and exposed in descriptive tables for better visualization of them. For the statistical calculation, the statistical program SPSS v. 19 was used, considering a significance level of 0.05. To perform the staging analyses, two groups were formed using the variable staging as a parameter, where the cases diagnosed in stage 0, I, and II formed the "Early Staging Group" and the cases diagnosed in staging III and IV formed the "Late Staging Group".

Possible associations between staging and sociodemographic and clinical variables were tested using the Chi-square test. The variables that presented probability values lower than 0.05 were used in the Binary Logistic Regression model, calculating the odds ratio values for each category within the variables.  Regarding the adjustment of the regression model, late-staging type was adopted as a reference in all possible associations. 

The research is part of a project entitled: "Men and women with cancer: meanings, perceptions and implications", approved by the Ethics Committee on Research with Human Beings of the Presidente Dutra University Unit University Hospital (HUUPD) with opinion No. 1,749,940. The research followed all the recommendations of resolution number 466 of December 12, 2012 of the National Health Council - Ministry of Health for Scientific Research in Human Beings.

 

RESULTS

According to the p values presented in Table 1 of the sociodemographic, variables correlated with staging, a statistically significant difference was found (p< 0.05) in the race variable. However, according to the regression model, "race" and "smoking" were not independently associated with staging (p > 0.05), as shown in Table 3. 

The age group from 65 to 70 years was more prevalent in the total population (n=167; 30.2%) and in the late stage group (n=77; 32.1%). For the "Marital Status", married women were prevalent in both early and late staging (n = 236; 42.7% of the total). In the variable occupation, the elderly female farmers were the most frequent in both groups. 

 

Table 1 – Association between staging and sociodemographic variables of the victims with cervical cancer, from 2009 to 2013 in an oncology referral hospital.

 

Variable

Staging

Early

No. 313; 56.6%

late

No. 240; 434%

Total

No. 553; 100%

p-value*

 

Age group

n (%)

60 - 64

95 (30.4)

67 (27.9)

162 (29.3)

 

 

 

0.289

65 - 70

90 (28.8)

77 (32.1)

167 (30.2)

71 - 74

58 (18.5)

42 (17.5)

100 (18.1)

76 - 79

32 (10.2)

23 (9.6)

55 (9.9)

80 - 84

30 (9.6)

16 (6.7)

46 (8.3)

85 - 89

4 (13)

10 (4.2)

14 (2.5)

≥ 90

4 (1.3)

5 (2.1)

9 (1.6)

 

Race

n (%)

white

44 (14.1)

46 (19.2)

90 (16.3)

 

 

 

0.030

Black

19 (6.1)

16 (6.7)

35 (6.3)

yellow

72 (23.0)

39 (16.3)

111 (20.1)

Brown

151 (48.2)

104 (43.3)

255 (46.1)

indigenous

0 (0.0)

2 (0.8)

2 (0.4)

No information

27 (8.6)

33 (13.8)

60 (10.8)

 

Education

n (%)

No

61 (19.5)

54 (22.5)

115 (20.8)

 

 

 

0.123

Incomplete fundamental

140 (44.7)

96 (40.0)

236 (42.7)

Complete fundamental

39 (12.5)

20 (8.3)

59 (10.7)

Medium level

38 (12.1)

26 (10.8)

64 (11.6)

Full top level

3 (1.0)

3 (1.3)

6 (1.1)

No information

32 (10.2)

41 (17.1)

73 (13.2)

 

Marital status

n (%)

single

75 (24.0)

56 (23.3)

131 (23.7)

 

 

 

0.232

married

151 (48.2)

101 (42.1)

252 (45.6)

widower

73 (23.3)

70 (29.2)

143 (25.9)

Judicially separated

8 (2.6)

11 (4.6)

19 (3.4)

Consensual union

1 (0.3)

1 (0.4)

2 (0.4)

No information

5 (1.6)

1 (0.4)

6 (1.1)

 

Occupation

n (%)

Physician (61)

1 (0.3)

1 (0.4)

2 (0.4)

 

 

 

 

 

 

 

 

0.512

Prof. Ens. Superior (139)

0 (0.0)

1 (0.4)

1 (0.2)

Professor Ens. preschool (143)

0 (0.0)

1 (0.4)

1 (0.2)

Professor (149)

5 (1.6)

2 (0.8)

7 (1.3)

Adm. Agents (319)

1 (0.3)

4 (1.7)

5 (0.9)

Sellers (451)

0 (0.0)

2 (0.8)

2 (0.4)

Domestic (540)

12 (3.8)

5 (2.1)

17 (3.1)

Serv. cons./limp. (552)

1 (0.3)

3 (1.3)

4 (0.7)

Washer (560)

0 (0.0)

1 (0.4)

1 (0.2)

Farmer (621)

99 (31.6)

74 (30.8)

173 (31.3)

Farmer (639)

0 (0.0)

1 (0.4)

1 (0.2)

Extractivists (654)

0 (0.0)

2 (0.8)

2 (0.4)

Fishermen (669)

1 (0.3)

2 (0.8)

3 (0.5)

Seamstress (795)

2 (0.6)

4 (1.7)

6 (1.1)

Worker (969)

1 (0.3)

0 (0,0)

1 (0.2)

Unrated (999)

68 (21.7)

51 (21.3)

119 (21.5)

Does not apply (888)

59 (18.8)

40 (16.7)

99 (17.9)

No information (9999)

63 (20.1)

46 (19.2)

109 (19.7)

Source: Data collected by the researcher, São Luís, 2018. 

 

Regarding the p values presented in Table 2 of association between staging and clinical variables, statistically significant differences were found in the following variables (p< 0.05): histological type, first treatment received at the hospital, disease stage at the end of the first treatment. In the other variables, no associations with staging were detected.

Regarding the variable Histopathological type, squamous cell carcinoma was the most prevalent in both groups, representing 80.8% (n=447), the category "other" was considered as a reference value, and patients with grade 3 cervical intraepithelial cancer (CIN 3) have 0.06 times lower chance of being associated with late staging when compared to patients of other types (OR = 0.06; p = 0.02). 

 

Table 2 – Association between staging and clinical variables of elderly women with cervical cancer, from 2009 to 2013 in an oncology referral hospital.

 

Variable

Staging

 

 

Early

No. 313

56,6%

Late

No. 240

 43,4%

Total

No. 553

 100%

 

p-value*

Histopathological type

N (%)

Squamous cell carcinoma

239 (76.4)

208 (86.7)

447 (80.8)

 

 

 0.024

Cervical intraepithelial neoplasia grade 3 - CIN 3

37 (11.8)

1 (0.4)

38 (6.9)

Adenocarcinoma

27 (8.6)

22 (9.2)

49 (8.9)

other

10 (3.2)

9 (3.8)

19 (3.4)

Family history of cancer n(%)

yes

68 (21.7)

54 (22.5)

122 (22.1)

 

0.335

No

82 (26.2)

75 (31.3)

157 (28.4)

No information

163 (52.1)

111 (46.3)

274 (49.5)

 

Alcoholism

n (%)

never

184 (58.8)

141 (58.8)

325 (58.8)

 

 

0.089

Ex-consumer

14 (4.5)

10 (4.2)

24 (4.3)

yes

11 (3.5)

20 (8.3)

31 (5.6)

Not rated

104 (33.2)

69 (28.7)

173 (25.5)

 

Tobaccoism

n (%)

never

117 (37.4)

103 (42.9)

220 (39.8)

 

 

0.021

Ex-consumer

76 (24.3)

42 (17.5)

118 (21.3)

yes

32 (10.2)

42 (17.5)

74 (13.4)

Not rated

88 (28.1)

53 (22.1)

141 (25.5)

 

 

 

First treatment received in hospital

n (%)

none

14 (4.5)

29 (12.1)

43 (7.8)

 

 

 

 

 

0.000

surgery

65 (20.8)

9 (3.8)

74 (13.4)

Surgery + Radiotherapy

19 (6.1)

1 (0.4)

20 (3.6)

Surgery + Radiotherapy + Chemotherapy

12 (3,8)

14 (5.8)

26 (4.7)

Surgery + Chemotherapy

3 (1,0)

4 (1.7)

7 (1.3)

Surgery + Chemotherapy + Hormone Therapy

1 (0,3)

0 (0.0)

1 (0.2)

radiotherapy

27 (8,6)

42 (17.5)

69 (12.5)

Radiation Therapy + Chemotherapy

162 (51,8)

134 (55.8)

296 (53.5)

chemotherapy

7 (2,2)

6 (2.5)

13 (2.4)

Hormonotherapy + Radiotherapy

1 (0,3)

0 (0.0)

1 (0.2)

other

2 (0.6)

1 (0.4)

3 (0.5)

 

Disease stage at the end of the first treatment

n (%)

No evidence of disease (complete remission)

188 (60.1)

56 (23.3)

244 (44.1)

 

 

 

0.000

Partial remission

22 (7.0)

29 (12.1)

51 (9.2)

Stable disease

42 (13.4)

47 (19.6)

89 (16.1)

Disease in progress

9 (2.9)

25 (10.4)

34 (6.1)

Oncologic therapeutic support

2 (0.6)

10 (4.2)

12 (2.2)

Death

12 (3.8)

28 (11.7)

40 (7.2)

Does not apply

38 (12.1)

45 (18.8)

83 (15.0)

 

 

 

 

Relevant exams

n (%)

Clinical examination and clinical pathology + Pathological anatomy

50 (16.0)

33 (13.8)

83 (15.0)

 

 

 

 

0.508

Clinical examination and clinical pathology + Imaging + Tumor markers

0 (0.0)

1 (0.4)

1 (0.2)

Clinical examination and clinical pathology + Imaging + Pathological anatomy

262 (83.7)

206 (85.8)

468 (84.6)

Clinical examination and clinical pathology + Imaging + Endoscopy and exploratory surgery + Pathological anatomy

1 (0.3)

0 (0.0)

1 (0.2)

*Chi-Square Test; Source: Data collected by the researcher, São Luís, 2018. 

 

The variable "First treatment received in the hospital", Radiotherapy + Chemotherapy was the most frequent in both groups 53.5% (n=296), but patients who underwent "surgery" and "surgery + radiotherapy" and "chemotherapy" were less likely to be associated with late staging when compared to those who did not undergo any type of treatment (OR = 0.13; p = 0.001/ OR = 0.04; p = 0.005/ OR = 0.14; p = 0.013; respectively) , the variable "none" was the reference variable, as shown in Table 3.

The variable "Disease stage at the end of the first treatment" presented a higher prevalence of complete remission in both groups 44.1% (n=244). It was the reference category. The groups of "partial remission" (OR = 3.27; p = 0.001), "stable disease" (OR = 3.62; p = 0.000), "disease in progression" (OR = 8.69; p = 0.000), "oncologic therapeutic support (OR = 15.04; p = 0.001), "death" (OR = 8.22; p = 0.000) and "does not apply" (OR = 2.28; p = 0.046) had higher chances of association with late staging compared to patients with complete remission. Oncologic therapeutic support was the category that most demonstrated chances of relationships with late staging (OR = 15.04), as shown in Table 3.

 

Table 3 – Predictors of late staging of the victims with cervical cancer from 2009 to 2013 in an oncology referral hospital.

 

 

Variable

Staging

 

 

 

Early 

No. 313

 

late

No. 240

 

RC

 

IC (95%)

p-value

 

Histopathological type

n (%)

Squamous cell carcinoma

239 

208 

0.61

0.22 - 1.74

0.358

Cervical intraepithelial neoplasia grade 3 - CIN 3

37 

0.06

0.01 - 0.64

0.020*

Adenocarcinoma

27 

22 

0.78

0.23 - 2.66

0.685

other

10 

REF

-

-

 

First treatment received in hospital

n (%) 

none

14 

29 

REF

-

-

surgery

65 

0.13

0.04 - 0.47

0.001*

Surgery + Radiotherapy

19 

0.04

0.004 - 0.38

0.005*

Surgery + Radiotherapy + Chemotherapy

12 

14 

0.56

0.15 - 2.14

0.395

Surgery + Chemotherapy

0.33

0.04 - 2.53

0.287

Surgery + Chemotherapy + Hormone Therapy

0

0

1.000

radiotherapy

27 

42 

0.79

0.27 - 2.35

0.671

Radiation Therapy + Chemotherapy

162 

134 

0.36

0.13 - 1.02

0.054

chemotherapy

0.14

0.03 - 0.66

0.013*

Hormoniotherapy + Radiotherapy

0

0

1.000

other

0.13

0.01 - 1.78

0.126

 

Disease statge at the end of the first treatment

n (%)

No evidence of disease (complete remission)

188 

56 

REF

-

-

Partial remission

22 

29 

3.27

1.68 - 6.39

0.001*

Stable disease

42 

47 

3.62

2.08 - 6.30

0.000*

Disease in progress

25 

8.69

3.54 - 21.30

0.000*

Oncologic therapeutic support

10 

15.04

2.84 - 79.56

0.001*

Death

12 

28 

8.22

3.63 - 18.60

0.000*

Does not apply

38 

45 

2.28

1.02 - 5.11

0.046*

 

Race 

n (%)

white

44 

46 

REF

-

-

Black

19 

16 

0.70

0.28 - 1.78

0.453

yellow

72 

39 

0.95

0.49 - 1.84

0.875

Brown

151 

104 

0.79

0.45 - 1.37

0.392

indigenous

9.94

-

0.999

No information

27 

33 

1.41

0.66 - 3.02

0.372

 

Tobaccoism

n (%)

never

117 

103 

REF

-

-

Ex-consumer

76 

42 

0.71

0.42 - 1.20

0.194

yes

32 

42 

1.19

0.65 - 2.19

0.568

Not rated

88 

53 

0.98

0.55 - 1.73

0.945

Source: Data collected by the researcher, São Luís, 2018. 

 

DISCUSSION

The results show a higher prevalence for the age group from 65 to 70 years (30.2%). Age was not associated with late staging, although the literature indicates that in developed countries, older women are diagnosed more frequently in advanced stages than  younger women, where each additional year in age the chance of having the diagnosis in the late stage increases by 3 % (7).

In this study, low education levels were more prevalent, which corroborates with other studies (8,4). Women with a low level of education have a higher risk of developing cervical cancer and a higher chance of being diagnosed in advanced stages III and IV (9), suggesting that these women may not have the necessary knowledge to seek screening/treatment and not recognize the importance of performing the preventive examination  (4).

Regarding marital status, married elderly women formed the group with the highest prevalence, although not associated with late staging, as well as other studies in the literature (10). It is assumed that married women have only one sexual partner, reducing exposure to sexually transmitted infections, while single women may have a greater number of partners having more contact with sexual carcinogens, such as HPV, Human Immunodeficiency Virus (HIV), chlamydia, among others (11). Despite the multiplicity of partners being an important risk factor for the development of CC, marriage does not constitute immunity, therefore the relationship between and the disease and marital status are more related to sexual behavior (10)

The variable never smoked in relation to smoking habits was the most prevalent in both groups, although it is considered a risk factor for the development of any type of cancer. The risk for developing cervical cancer increases proportionally to the number of cigarettes smoked per day, especially when this habit is started early (5).

Regarding the histopathological type, this study demonstrates that women with grade 3 - CIN 3 cervical intraepithelial cancer, are 6 times less likely to be associated with late staging. This data is justified because cervical cancer usually begins as low-grade intraepithelial lesions (LSIL), a preinvasive condition limited to the cervical epithelium, and is less likely to progress to invasive carcinoma, unlike high-grade intraepithelial lesions (HSIL). These are predominantly caused by oncogenic HPV types, having precursor lesion behavior of invasive carcinoma. This data reinforces the need for real quality control practice in screening programs for cervical cancer, since the curability in this phase of the disease can reach 100%, often being solved even at the outpatient level (12)

 Invasive squamous cells cancers of the uterine cervix are preceded by a long phase of cervical intraepithelial neoplasia. In this study, this data is perceived by the high prevalence of squamous cell carcinoma (SCC), corroborating findings from the literature, which shows that these are responsible for approximately 70% of cases of cervical cancer, while adenocarcinomas represent 15% to 35% of cases (5).

The delay in diagnosis leads to more aggressive and less effective treatments,  increases hospitalization costs and mortality  (13)  and the survival rate is slightly higher in women diagnosed with CPB  (14).

The treatment "surgery" and "surgery + radiotherapy" and "chemotherapy" were less likely to be associated with late staging, given this fully justifiable, because for locally advanced disease there is no indication for surgical treatment and the standard treatment is the association of chemo-radiotherapy (teletherapy concomitant with chemotherapy followed by brachytherapy) (15), although this factor is directly related to social and economic factors because many patients do not have access to basic resources for cancer treatment (16).

The elderly women in this study obtained complete remission of the disease, although this is not the reality in the northeast region that has one of the highest mortality due to cervical cancer according to studies. Therefore, it is necessary to maintain the follow-up of these elderly women even after complete remission for the prevention of recurrences, or if the case is the early diagnosis of relapses (17)

This study has limitations such as the discrepancy of the database, the lack of information in the medical records related to important variables of risk factors, as well as the possibility of an information bias related to the clinical staging of cases.

 

CONCLUSION

The results of the study reaffirm the need to improve the knowledge of women, especially in the case of those at older ages who were identified in a greater proportion, demonstrating that these women when diagnosed were already in more advanced stages. The data also infers that early diagnosis decreases the range of later stages due to the treatment having positive results. The lack of information from the female population and the resistance to preventive examination of cervical cancer are one of the main causes for the evolution of the disease. Therefore, knowing the epidemiological characteristics of these women becomes significant for  to support the planning and evaluation of effective programs in the control of cervical cancer. Thus, it is concluded that health education  is the best strategy to be used in order to reach this population highlighted with encouragement to perform the cytopathological examination.  The need to intensify  campaigns and proposals aimed at minimizing the morbidity and mortality of this cancer in the state of Maranhão as well as in Brazil is also perceived, in addition to improving the structuring of the cervical cancer screening program, in order to ensure  early access to both consultations and diagnosis, thus providing a reduction in the high percentages of advanced cases. 

 

REFERENCES

  1. Fonseca MRC, Pontes AEL, Traldi MC, Morais SS, Galdeano J. Frequency and factors associated with the adeforestation of the cervix. Health Magazine – UNG [Internet]. 2016 [cited 2020 Aug 20];10(1-2). Available from:  http://revistas.ung.br/index.php/saude/article/view/2085.

  2. Paula VM, Rodrigues LS. Sexuality of the old women and nursing contributions. EnfermBras [Internet]. 2020;19(4);345-54. [cited 2021 Mar 10] Available from:  https://portalatlanticaeditora.com.br/index.php/enfermagembrasil/article/view/4281/html.doi:https://doi.org/10.33233/eb.v19i4.4281

  3. Brazilian Institute of Geography and Statistics. Studies and research: demographic and socioeconomic information: synthesis of social indicators. Rio de Janeiro: IBGE [Internet]; 2016 [cited 2017 Nov 20]. Available from:  https://biblioteca.ibge.gov.br/visualização/livros/liv98965.pdf

4. World health organization. International agency for research on cancer. Globocan. Cited: 2020 Ago 20.

5. Ministry of Health (BR). Control of cervical and breast cancers. 2nd ed. Brasília, DF: Ministry of Health; 2013. (Basic Care Book, n 13).

6. Brazilian Society of Cancerology. Gynecological cancer. Cervix [Internet]. 2016 [cited 2020 Aug 20]. Available from: http://www.sbcancer.org.br/wpcontent/uploads/2016/10/cancerginecologico.pdf 

7. Rozario S, Silva IF, Koifman RJ, Silva IF. Characterization of women with cervical cancer assisted at Inca by histological type.  Rev Saúde Pública [internet]. 2019 [cited 2020 Dez 19];53:88. Epub Oct 03 2019. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0034-89102019000100278&lng=en doi:https://doi.org/10.11606/s15188787.2019053001218

8. Melo WA, Pelloso SM, Alvarenga A, Carvalho MDB. Fatores associados a alterações do exame citopatológico cérvico-uterino no Sul do Brasil. Rev Bras Saúde Mater Infant [Internet].  2017 Dec [cited 2020 Ago 20];17(4): 637-643. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1519-38292017000400637&lng=en. doi:  https://doi.org/10.1590/1806-93042017000400002.

9. Silva RCG, Silva ACO, Peres AL, Oliveira SR. Profile of women with cervical cancer treated for treatment in an oncology center. Rev Bras Hail Mater Infant [Internet]. 2018 Dec [cited 2020 Aug 20]; 18(4): 695-702. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S1519-38292018000400695&lng=en. doi: http://dx.doi.org/10.1590/1806-93042018000400002.

10. Figueiredo T, Souza CQ, Castilho EN, Silva TMR, Silva EP, Siqueira LG et al. Profile analysis of women with precancerous lesions of the cervix. Health Rev [internet]. 2015 [cited 2020 Aug 18]; 15(41):3-13.  Avaiable from: https://www.metodista.br/revistas/revistas-unimep/index.php/sr/article/view/2728doi: https://doi.org/10.15600/2238-1244/sr.v15n41p3-13.

11. Almeida AF, Holmes ES, Lacerda CCC, Farias CF, Costa MBS, Santos SR. Methods of detecting cervical cancer among health professionals. Rev aide UFPE online [Internet]. 2015 [cited 2020 Aug 18];9(1):62-68. Available from:  https://periodicos.ufpe.br/revistas/revistaenfermagem/article/view/10307/10978. doi: https://doi.org/10.5205/reuol.6817-60679-1-ED.0901201509.

12. Cervical Intraepithelial Neoplasia. National Cancer Institute [Internet]. 2016 [cited 2020 Aug 21]. Available from:  http://www1.inca.gov.br/rbc/n_46/v04/pdf/normas_2.pdf

13. Padilha Cátia Martins Leite, Araújo Junior Mário Lúcio Cordeiro, Souza Sergio Augusto Lopes de. Cytopathologic evaluation of patients submitted to radiotherapy for uterine cervix cancer. Rev Assoc Med Bras [Internet]. 2017 Apr [cited 2020 Sep 11]; 63 (4): 379-385. Available from: http://www.scielo.br/scielo.php?script=sci_arttext&pid=S0104-42302017000400379&lng=en. doi:  http://dx.doi.org/10.1590/1806-9282.63.04.379

14. Chandeying N, Hanprasertpong J. The prognostic impact of histological type on lclinical outcomes of early-stage cervical cancer patients whom have been treated with radical surgery. J Obste Gynaecol. 2017 [cited 2020 Dez 21]; 37(3):347-354. Available from: https://pubmed.ncbi.nlm.nih.gov/28141947/. doi: http://dx.doi.org/10.1080/01443615.2016.1245279

15. Frigo L, Zambarda S. Cervical cancer: effects of treatment. Cinergis [internet magazine]. 2015 Dec 1; [cited 2020 Aug 21]; 16(3): [approx. 0 p.]. Available from: https://online.unisc.br/seer/index.php/cinergis/article/view/6211/4554. doi: http://dx.doi.org/10.17058/cinergis.v16i3.6211.

16. Alfonso DL, Sergio C. Global strategies for the treatment of early-stage and advanced cervical cancer.  Current Opinion in Obstetrics and Gynecology [Internet]. 2016 [cited 2020 Dez 19]; 28:11-17 (Issue 1). Available from: https://journals.lww.com/co-obgyn/Fulltext/2016/02000/Global_strategies_for_the_treatment_of_early_stage.4.aspx. Doi: http://dx.doi.org/10.1097/GCO.0000000000000234

17. Barbosa IR, Souza DLB, Bernal MM, Costa ICC. Regional inequalities in cervical cancer mortality in Brazil: trends and projections until the year 2030. Science. Collective health [online]. 2016; 21(1):253-262. ISSN 1678-4561. [cited 2020 Aug 19]. Available from: https://www.scielo.br/scielo.php?script=sci_abstract&pid=S1413-81232016000100253&lng=pt&nrm=iso. doi: http://dx.doi.org/10.1590/1413-81232015211.03662015

 

Received: 12/20/2020

Revised: 02/18/2021

Approved: 04/14/2021