Insurance status and access to cervical cancer treatment in a specialized cancer center in Mexico

Abstract

To describe access to complete treatment in women with cervical cancer and state-sponsored insurance versus no insurance. We conducted a retrospective observational study. The source population consisted of women treated for cervical cancer from January 2000 to December 2015 in a tertiary care hospital. We included 411 women with state–sponsored insurance and 400 without insurance. We defined access to cervical cancer treatment as complete treatment (according NCCN/ESMO (National Comprehensive Cancer Network/European Society for Medical Oncology) standards) and timely initiation of treatment (less than 4 weeks). Clinical and sociodemographic characteristics were described and analyzed with logistic regression using complete treatment as the main outcome. A total of 811 subjects were included, the median age was 46 (IQR (Interquartile range) 42–50) years. Most of them were married (36.1%), unemployed (50.4%), and had completed primary school (44.0%). The most common clinical stages at diagnosis were II (38.2%) and III (24.7%). In the adjusted regression model, being married (OR (odds ratio): 4.3, 95% CI (confidence interval): 1.74–10.61) and having paid employment (OR: 2.79, 95% CI: 1.59–4.90) or state-sponsored insurance (OR: 1.54, 95% CI: 1.04–2.26) were positively associated with the possibility of having a complete treatment. Women with insurance were likely to be younger and receive timely treatment compared with uninsured women. Complete treatment was associated to insurance status and advanced stages of cervical cancer. State-sponsored insurance improves access to complete treatment. Government policies are needed to avoid social and economic inequity and provide better management of cervical cancer in our country.

1. Introduction

In 2003 Mexico established the Social Protection System in Health, better known as Seguro Popular (SP), a national health insurance model aimed to provide universal access to health services for the uninsured. It comprised almost 50% of the Mexican population with informal jobs who had no access to other insurance schemes.^[1] In 2005 Seguro Popular created the Catastrophic Health Expenditure Fund (FPGC, after its name in Spanish) to cover diseases that incurred catastrophic expenses, such as cataracts, human immunodeficiency virus, and cervical and breast cancer. A specialized committee determined which diseases to include in the FPGC based on prevalence and economic viability. Cervical cancer was included to this fund since its creation.^[2]

Cervical cancer is the fourth most common cancer in women worldwide. In Mexico, in 2019 cervical cancer had an incidence rate of 23.3 cases per 100,000 women and a mortality rate of 11.2 per 100,000, thus making cervical cancer the second leading cause of cancer death in women.^[3] Generally, overall incidence, mortality, and burden of cervical cancer in high-income countries are drastically lower compared with low- and middle-income countries.^[4] According to the ESMO Guidelines, cervical cancer treatment depends, among other factors, on clinical stage, and ranges from simple surgical procedures, such as conization, to extensive hysterectomies and cytoreductions, sometimes followed by adjuvant chemo- or radiotherapy.^[5] Even though treatment guidelines are available, lack of access to treatment, treatment abandonment, and loss to follow-up in low- and middle-income countries have led to increased mortality in women with cervical cancer worldwide.^[6]

Several studies have reported multiple compounding factors contributing to the nonparticipation of women in cervical cancer screening, such as unemployment, lack of or low education level, poor language proficiency (e.g., information and education campaigns not provided in the native language of the women the programs are aimed at), being unmarried, lack of knowledge about screening, previous negative experiences during screening, cultural and traditional beliefs, inaccessible areas, lack of funding, community awareness, cost-effectiveness, complications of Pap smear, lack of public policy compliance, or ineffective public policies.^[6]

Before 2003 up to 58% of health expenses in Mexico came from out-of-pocket payments.^[7] Furthermore, in 2000 up to 4.1% of all Mexican households incurred catastrophic expenses. These expenses dropped to 2.7% a year after Seguro Popular was implemented.^[8] Although out-of-pocket expenses dropped drastically under the program, universal coverage was not reached. Inequity in access to health care still remains a problem. We designed a retrospective observational study to describe the access to complete treatment of women with cervical cancer who were recipients of Seguro Popular (state-sponsored insurance) and were treated with FPGC funding.

2. Methods

This was a retrospective observational study. The source population consisted of 1886 women treated for cervical cancer between January 2000 and December 2015 at the National Cancer Institute. The sample included the subgroup of the uninsured and recipients of SP (insured). Considering a 95% CI, 80% power, and 1:1 allocation ratio, we estimated a sample size of 370–437 patients for each group. We finally decided to select 400 subjects per group based on the availability of records. The study population comprised 811 subjects: 400 women without insurance treated between 2000 and 2005 were selected by simple random sampling and paired by clinical stage with 411 women with SP (state-sponsored insurance) treated between 2006 and 2015.

We collected demographic, clinical, pathological, treatment, and follow-up data from their electronic medical records. We defined time to treatment as the period between the date at diagnosis (defined by the attending physician using clinical, pathological, and imaging data) and the date when the patients started receiving any treatment modality. We defined time to treatment as adequate (less than 4 weeks), moderately adequate (4–8 weeks), or inadequate (over 8 weeks). Time in treatment was the period between treatment initiation and discharge, death, or censoring. Stage at diagnosis was determined before treatment initiation. Complete treatment was defined as having received all the necessary interventions corresponding to clinical stage at diagnosis as indicated by National Comprehensive Cancer Network® (NCCN®) Guidelines for cervical cancer and The ESMO Clinical Practice Guidelines. Abandonment was defined as patients who did not finish their treatment due to known or unknown causes (in such cases we recorded the reason for abandonment). All data were verified and validated by a team of epidemiologists and clinical oncologists.

For the statistical analysis we first performed descriptive and comparative analyses for clinical, pathological, and treatment variables of patients with or without SP. We used measures of central tendency and dispersion for quantitative variables and frequency counts for qualitative variables. We used chi-square test of independence, Mann–Whitney’s U test, or Fisher’s exact test, as necessary, to evaluate the differences among groups. Using complete treatment as the outcome variable and the rest as predictors, we performed univariate and multiple logistic regressions. All analyses were done using STATA (v14.2, College Station, TX) licensed to the author. A bilateral P value threshold < .05 was used for statistical significance.

The study protocol was reviewed by our Institutional Review Board. (Ref. Rev/31/16). Informed consent was not required as this retrospective study includes a chart review and does not represent a risk for patients.

3. Results

The study population included 811 women treated at our hospital between January 2000 and December 2015; of which 400 (49.3%) were treated before the implementation of Seguro Popular (SP) and 411 (50.7%) after it was implemented. The median age of the entire cohort was 46 years (Q1–Q3 42–50). Most patients (n = 293, 36.1%) were married and reported being unemployed (n = 409, 50.4%) or homemakers (n = 258, 31.8%). Additionally, most of them had completed primary school at most (n = 357, 44%) or had no education at all (n = 273, 33.7%). The median age at their first sexual intercourse was 17 (Q1–Q3 15–19), and the median number of pregnancies was 5 (Q1–Q3 3–7). Clinical stage of cervical cancer at diagnosis was I for 153 (18.9%) patients, II for 310 (38.2%), III for 201 (24.8%), and IV for 147 (18.1%). Overall, 622 (76.7%) patients received complete treatment.

After comparing patients treated without SP (uninsured) and with state-sponsored insurance (SP), we observed that the median age was higher in the uninsured group (50.5, Q1–Q3 42–62) than in the insured group (45, IQR 43–38, P < .001). The proportion of married women decreased from 42% in the uninsured group to 30.4% in the insured group, with corresponding increasing proportions of cohabitation and single motherhood (P = .01). Similarly, the proportion of women with no schooling dropped from 43.3% to 25.3%, and those who finished secondary school increased from 8.8% to 16.8% (P < .001). Women living in urban areas increased from 50.5% to 63.5% (P < .001).

Regarding clinical characteristics, stage at diagnosis was similar between groups; however, stage I at diagnosis increased from 15.5% to 22.2%, and stage IV remained unchanged (18–18.3%). The proportion of women with complete treatment differed significantly between pre-and insured. In the uninsured group, 73.3% received complete treatment compared with 80.1% in the insured group (P = .02). Similarly, patients who waited more than 120 days to receive treatment decreased from 29.8% to 12.2%, and more than half (57.7%) received treatment within 60 days, compared with just 35.3% in the uninsured group (P < .001) (Table 1).

Table 1.

Characteristics of women treated for cervical cancer.

Variable	All patients		Pre-SP (n = 400, 49.3%)		Post-SP (n = 411, 50.7%)		P
	Median	Q1–Q3	Median	Q1–Q3	Median	Q1–Q3
Age	46	22–91	51	22–91	45	39–50	<.001
Age at first intercourse	17	15–19	17	15–19	17	15–19	.56
Variable	n	%	n	%	n	%	P
Marital status
Single	25	3.08	11	2.75	14	3.41	.01
Married	293	36.13	168	42.00	125	30.41
Cohabitation	115	14.18	38	9.50	77	18.73
Divorced	123	15.17	61	15.25	62	15.09
Widowed	157	19.36	78	19.50	79	19.22
Single mother	96	11.84	42	10.50	54	13.14
Highest level of education
None	273	33.66	169	42.25	104	25.30	<.001
Primary	357	44.02	171	42.75	186	45.26
Secondary	104	12.82	35	8.75	69	16.79
High School	47	5.80	16	4.00	31	7.54
College or higher	30	3.70	9	2.25	21	5.11
Occupation
Unemployed	409	50.43	172	43.00	237	57.66	<.001
Homemaker	258	31.81	155	38.75	103	25.06
Other employments	144	17.76	73	18.25	71	17.27
Clinical stage at diagnosis
I	153	18.87	62	15.50	91	22.14	.098
II	310	38.22	162	40.50	148	36.01
III	201	24.78	104	26.00	97	23.60
IV	147	18.13	72	18.00	75	18.25
Complete Treatment
Yes	189	23.30	107	26.75	82	19.95	.022
No	622	76.70	293	73.25	329	80.05
Time interval from diagnosis to start of treatment
4 or less wk	131	16.15	32	8.00	99	24.09	<.001
4–8 wk	236	29.10	104	26.00	132	32.12
Over 8 wk	444	54.75	264	66.00	180	43.80
Urbanization
Urban	463	57.09	202	50.50	261	63.50	<.001
Rural	169	20.84	118	29.50	51	12.41
Suburban	179	22.07	80	20.00	99	24.09

Q1-Q3 = Quartile 1- Quartile 3, SP = Seguro Popular.

The median follow-up was 22.3 (Q1–Q3 0.7–195) months for the uninsured group and 40 (Q1–Q3 4.1–122.5) months for the insured group.

Table 2 shows the results of multiple logistic regression with complete treatment as the outcome variable. We observed that the insured group had 1.5 times the odds (95% CI 1.04–2.26, P = .02) of receiving complete treatment. We also found that, unlike single women (reference), the odds of receiving complete treatment were higher for married women (OR 4.30, 95% CI 1.74–161, P < .001), cohabiting women (OR 3.37, 95% CI 1.28–8.86, P = .01), divorcees (OR 3.12, 95% CI 1.21–8.01, P = .01), widows (OR 3.14, 95% CI 1.23–8.00, P = .01), and single mothers (OR 2.70, 95% CI 1.04–7.23, P = .04). Similarly, the odds were higher for employed women compared with the unemployed (OR 2.79, 95% CI 1.59–4.90, P < .001). By contrast, the odds of receiving complete treatment dropped as clinical stage at diagnosis decreased (0.31 for stage III, 0.43 for stage IV), but it was not statistically significant for stage II, compared to stage I.

Table 2.

Logistic regression for odds of complete treatment.

Variable	Odds ratio	95% CI	P
Edad	0.99	0.97–1.00	.358
Marital status
Single		Ref
Married	4.30	1.74–10.61	.001
Cohabitation	3.37	1.28–8.86	.014
Divorced	3.12	1.21–8.01	.018
Widowed	3.14	1.23–8.00	.016
Single mother	2.70	1.04–7.23	.040
Occupation
Unemployed		Ref
Homemaker	1.65	1.10–2.48	.016
Other employments	2.79	1.59–4.90	<.001
Treated with Seguro Popular
No		Ref
Yes	1.54	1.04–2.26	.027
Clinical stage at diagnosis
I		Ref
II	0.83	0.46–1.47	.528
III	0.31	0.17–0.56	<.001
IV	0.43	0.23–0.80	.008

CI = confidence interval.

4. Discussion

Our study found that having social protection system in health was associated with a higher likelihood to receive complete treatment, adjusted by age, marital status, occupation and clinical stage. Moreover, a greater proportion of insured patients who began treatment within 4 weeks after being diagnosed (26.5%), compared with uninsured patients (19.95%).

The mean age at diagnosis in the uninsured group was 50 years, whereas it was 5 years lower in the insured group. The most common clinical stage at diagnosis was stage II in both uninsured (40%) and insured (36%) groups. The mean age of the uninsured group was significantly higher than the insured group perhaps due to a delay in diagnosis. This is consistent with the literature that found a positive association between age and more advanced clinical stages of the disease as a consequence of late diagnosis.^[9,10]

In a population based study, the authors report the results of 7226 women in the United States; they observed that for each year that the age at diagnosis increased, the likelihood of receiving complete treatment in advanced stages of the disease decreased 0.98 times.^[10] After correcting for other factors, we did not find that age was an independent factor that increased the likelihood of receiving complete treatment; however, this could be because the mean age of our population was considerably lower (46 years), as opposed to the groups with and without standard treatment evaluated by the authors (52 and 55 years, respectively).

The lack of schooling or poor schooling are factors contributing to patients not being integrated into screening programs or even completing their treatment. In our analysis, 169 women (42%) of the uninsured group and 104 (25%) of the insured group had no schooling. Some studies have examined the relationship between the level of education of parents and the likelihood of their daughters taking part in human papillomavirus vaccination campaigns, but there are few studies evaluating the effect of the level of education in complete treatment.^[11] Other study described that patients living in areas with a higher proportion of residents without high school had longer delays in initiation of treatment (44.7 days), compared with women living where most residents had completed high school or more education (38.2 days). Schooling and other factors, such as occupation and geographical accessibility, can influence the timely initiation of treatment.^[12]

In our population, having employment or being a housemaker increased the likelihood of receiving complete treatment by 2.7 and 1.6 times, respectively. A positive association between the level of education, the level of knowledge about cervical cancer, and the level of awareness of the disease has been demonstrated.^[13] Education and occupation could be proxy variables of the level of health literacy, which improves prognosis by allowing for early detection and complete treatment.^[14]

The most relevant prognostic factors include staging, early diagnosis, and access to timely treatment.^[12,15,16] Evidence revealed that having stage III (OR: 0.82, 95% CI: 0.71–0.94, P = .00), Medicaid (OR: 0.80, 95% CI: 0.72–0.88, P < .001), or being uninsured (OR: 0.67, 95% CI: 0.57–0.80, P < .001) decreased the likelihood of receiving complete treatment. In our population, stages III and IV were independent factors that decreased the likelihood of receiving complete treatment (OR: 0.31, 95% CI: 0.17–0.56, P < .001).^[10] Even though complete treatment improves cancer outcomes, it is expensive, involves out-of-pocket and catastrophic expenses, or is inaccessible to many.^[17,18] Incomplete treatment has been associated with social and economic vulnerability,^[19,20] which our country has tried to reduce through financial protection in health.

One of the largest cohorts of women with stage IV cervical cancer in the United States analyzed the factors associated with treatment delay in. They found those women with Medicaid and the uninsured had longer delays (31.8 and 31.2 days, respectively) compared with women with private insurance (25.8 days).^[21] Similarly, other study revealed that Medicaid and uninsured patients were less likely to receive timely treatment and complete radiotherapy (79.5% and 81%, respectively), as opposed to women with private insurance (85.6%).^[22] In our study, insured patients were 1.6 times more likely to complete treatment, and the likelihood of receiving treatment within the first 4 weeks after diagnosis increased significantly. This disparity in medical care and prognosis among American women cannot be directly compared with our population. Since our hospital is a public institution, we did not include women with private insurance. However, the uninsured were the least likely to receive complete treatment in both studies.

Some of the strengths of the present study include the randomization of the study population, which allowed us to draw inferences about the women treated in our hospital between 2000 and 2015. Moreover, all cases were examined by epidemiologists and clinical oncologists who selected those cases with complete treatment based on the NCCN Guidelines for Cervical Cancer. This made the results comparable according to international standards and other populations. Finally, we believe the present study yielded relevant data that can be useful to design public programs and insurance policies in our country.

One of the limitations of the present study is the temporary nature of the results. In 2020 INSABI (Institute of Health for Welfare) replaced Seguro Popular in Mexico. INSABI is a decentralized organism, attached to the Ministry of Health, in charge of providing health services, free medicine, and materials to the uninsured.^[23] Since copayment is not required and the recipients are increasing, in the upcoming years INSABI will face the challenge of achieving universal coverage and providing effective services and enough materials. The per capita expenditure in 2021 was 20.3% lower than in 2019 when Seguro Popular was still in place.^[24] Subsequent analyses comparing both programs are needed to improve access to health services for women with cervical cancer and close the inequity gap.

Our study suggest a significant difference between the uninsured and stated-sponsored insured patients in achieving complete treatment for cervical cancer at a specialized cancer hospital, as the insured group was more likely to receive timely treatment. Financial protection from the state is essential to provide free services, ensure timely treatment, reduce barriers to access to health care, and lower excess mortality in women with cervical cancer.

Although current changes to our health care system allow women with cervical cancer to receive treatment with no out-of-pocket cost to them, it is necessary to design and implement strategies to improve access to screening tests and education programs to facilitate early diagnosis and impact in survival outcomes

Acknowledgments

The authors thank the Instituto Nacional de Cancerología (INCan) for their technical assistance and administrative support, and are indebted to all persons who agreed to participate in the study. The INCan gives permission to be named.

Author contributions

Conceptualization: Abelardo Meneses-García, Nancy Reynoso Noverón.

Data curation: Juan Alejandro Torres Domínguez, Hugo Jiménez-Barrera, Nancy Reynoso Noverón.

Formal analysis: Juan Alejandro Torres Domínguez, Nancy Reynoso Noverón.

Funding acquisition: Nancy Reynoso Noverón.

Investigation: Nancy Reynoso Noverón.

Methodology: Nancy Reynoso Noverón.

Project administration: Nancy Reynoso Noverón.

Resources: David Isla-Ortiz, Abelardo Meneses-García, Nancy Reynoso Noverón.

Supervision: David Isla-Ortiz, Nancy Reynoso Noverón.

Validation: David Isla-Ortiz, Antonio Bandala-Jacques, Nancy Reynoso Noverón.

Visualization: Liliana Pérez-Peralta, Nancy Reynoso Noverón.

Writing – original draft: David Isla-Ortiz, Juan Alejandro Torres Domínguez, Liliana Pérez-Peralta, Antonio Bandala-Jacques, Nancy Reynoso Noverón.

Writing – review & editing: David Isla-Ortiz, Liliana Pérez-Peralta, Antonio Bandala-Jacques, Abelardo Meneses-García, Nancy Reynoso Noverón.