Study design

An observational, cross-sectional, and stratified study was carried out in 2018. We created a closed voluntary survey for medical specialists in a branch of oncology, which consisted of questions about the resources and strategies for managing CC patients. Questions were structured by the principal investigator and her panel of experts. Before the launch of the survey, the adaptations of the model were made through the digital server Survey Monkey® platform. Internal tests were carried out for 8 weeks to confirm the proper operation and security of the data obtained in the survey. Cookies were used and were set on the first page. The IP address was used for the filters.

The survey could be accessed from the same IP address but 24 h later. Users could return to the survey if they did not complete it. They could not go back to previous questions already responded to; if they returned to the survey, the next unanswered question was automatically displayed. No duplicate individuals were analyzed; only the last survey completed was included in the analysis. The Sociedad Mexicana de Oncología (SMeO) (Mexican society of oncology, SMeO) emailed each specialist personal invitations. It clearly stated that no personal information would be collected from the participant. If they accepted to participate and opened the link to the survey, the header specified the approximate duration of 10 min to answer it, and personal information or identification of the participant was not collected. Each participant had to accept the survey terms and confidentiality data and check a box if they agreed to do the survey. In the email invitation, the participants were told the length of the survey availability and purpose of the study. The survey link was emailed to answer the survey anonymously, thus ensuring the confidentiality of the information of all participants. Each participant responded in 80 days maximum.

The survey comprised three sections: (1) Demographic information of the physician; (2) resources of the institution (equipment, personnel, and materials for the care of patients with CC); and (3) information related to diagnosis and treatment (Annex 1).

The survey had an initial section with 26 questions that were applied to all respondents:

Subsequently, the second part of each survey was configured with questions specifically focused on the area of specialty of the respondent, being as follows:

Where pertinent, items provided a non-response option such as “not applicable” or “I do not have that information,” and the selection of one response option was enforced. Once page 1 was completed, it was possible to advance to the next page without the opportunity to return to the previous one; at the end, the information was saved automatically, and the link was closed, being able to generate a certificate of gratitude for having participated later. No summary was displayed.

To compare the interregional differences in the results, these were stratified into four geographic regions of the Mexican Republic, North, Center-North, Center, and South, following the classification of the Banco de México¹² (Fig. 1).

Figure 1 Distribution of medical specialists according to region. Top. Map of the Mexican Republic divided into four geographic regions, North, North-Center, Center, and South, following the classification of the Banco de México¹². The states that comprise each region are specified. The percentage of participation of each region is described for each specialty. Bottom. The proportion of participants from each public institution included in the survey is shown. 

The Ethics and Research Committees approved this study (018/002/ICI)-(CEI/1192/17). Because this was a voluntary survey with no risk involved, the study was approved without informed consent.

Participants

A list of the members from the SMeO¹³ and the Sociedad Mexicana de Radio-oncología (Mexican Society of Radio-oncology, SOMERA)¹⁴ was obtained. The survey was sent to medical oncologists, gynecologic oncologists, surgical oncologists, and radiation oncologists, assigned to public institutions, such as Instituto Mexicano del Seguro Social (IMSS), Instituto de Seguridad y Servicios Sociales de los Trabajadores del Estado (ISSSTE), Secretaría de Salud (SS), Secretaría de la Defensa Nacional, Secretaría de Marina, Petróleos Mexicanos, and University Hospitals (UH). The inclusion criterion for the participation of specialist physicians was the care of CC patients in a Mexican public institution. Incomplete questionnaires were eliminated from the analysis.

Statistical analysis

Only completed surveys were analyzed. No duplicate individuals were analyzed. The descriptive analysis determined the frequencies and percentages of the responses to each question. Items were not weighed; all were analyzed equitably. The response rates were compared among public health services, specialists, and regions. The uncertainty coefficient was used for the nominal variables, and Kendall’s Tau-C was used for the ordinal variables. The statistical significance was established at p < 0.05. The statistical analysis was performed using SPSS version 23 (IBM Corp, USA, 2014).

Demographic characteristics of the respondents

The survey was sent to a total of 1810 specialists, of whom 653 responded (36%); 147 participants were excluded, and 506 (27.9%) were analyzed (Fig. 2). From the total surveys analyzed, according to the participants’ specialty, 20.9% were medical oncologists, 15.8% were gynecologic oncologists, 45.8% were surgical oncologists, and 17.4% were radiation oncologists (Fig. 2). Twenty-nine percentages were female; the most frequent age range was 35-45. Ninety-two percentages of the respondents kept their current Mexican Council of Oncology certification. Within the Mexican Republic, the Center region had the highest participation (Fig. 1). Sixty-eight percentages belonged to third-level hospitals, while 31.8% belonged to second-level hospitals. The public institution with the highest participation in this survey was the IMSS (40.6%), as described in figure 1.

Figure 2 Flow diagram of survey study participants. Surveys were sent electronically to members of the Mexican Society of Oncology¹³ and the Mexican Society of Radio-oncology¹⁴. *Response rate was 36%, and 27.9% were analyzed. The surveys’ participants analyzed included medical oncologists, gynecologic oncologists, surgical oncologists, and radiation oncologists assigned to public institutions. 

Care of CC patients

The specialists from the different institutions treated a different number of CC patients annually. About 35.4% of respondents attended up to 50 patients, 26.5% attended up to 100 patients, 21.1% up to 300 patients, and 17% cared for more than 300 patients. Regarding the time elapsed between diagnosis of the disease and the beginning of treatment, 50.1% of the respondents from the IMSS, Federal SS, and ISSSTE answered that starting treatment after diagnosis takes 5-8 weeks. On the other hand, 56% of specialists from State SS, PX-SD-SM, and UH began treatment after 1-4 weeks. About 69.4% of the respondents followed the National Comprehensive Cancer Network care guidelines for treating patients with CC.

Availability of equipment in public institutions

Regarding the resources for the diagnosis of CC patients, following the International Federation of Gynecology and Obstetrics (FIGO, 2018)¹⁵, 96.2% of the respondents answered that they had computed axial tomography (CAT), 2.2% had magnetic resonance imaging (MRI), and 1.5% had positron emission tomography (PET) or PET-CT (Table 1). From the participants with radiotherapy (RT) equipment in their institutions, 76.8% indicated that they had a linear accelerator, 7.8% had a cobalt pump, 13.7% had both, and 0.7% had TomoTherapy. The respondents that did not have RT equipment (39.5%) or brachytherapy (BT) equipment (44.7%) had to refer their patients to other institutions for treatment.

Availability of services in public institutions for the care of CC patients

Concerning other services necessary for the care of CC patients, 94.7% had a pathology service; the remaining 5.3% sent samples of patients’ tumors to other institutions. Psychology service was available for 71.1% of respondents, psychiatry service for 26.5%, algology service for 68.4%, nutrition service for 67.4%, and thanatology service for 26.9% (Table 1).

Early stages of CC treatment (FIGO IA-IIA)

Sixty-nine percentages of the specialists performed open surgery in their institutions, 19.9% performed laparoscopic surgery combined with open surgery, 7.1% used laparoscopic surgery, and 3.2% performed open and robotic laparoscopic surgery. Forty-seven percentages of the specialists indicated that 20% of the patients treated with radical hysterectomy receive adjuvant RT or chemo-RT (CT-RT) followed by BT. In contrast, 43.6% indicated that more than 40% of patients receive only adjuvant treatment with RT or CT-RT. The supplies for surgical treatment were sufficient in the institutions of 70.5% of the participants (Table 1). The main factor that affected the participants during surgical treatment was the lack of operating room equipment (58.3%) (Table 1).

Locally advanced stages of CC treatment (FIGO IB-IVA)

Most participants (93.5%) from the different public institutions responded that the treatment for locally advanced disease was concomitant CT-RT; the rest used neoadjuvant CT, followed by RT (4.5%), RT as single therapy (1.8%), and neoadjuvant CT with surgery (0.2%). Twenty-four percentages of the specialists referred more than 50% of their patients to another hospital to receive CT-RT. This situation was consistent in the four regions. Cisplatin was the most used radio sensitizer regardless of the institution or the region (98.1%). For bulky tumors (stages IB2 and IIA2), the most used treatment was RT or CT-RT (65.4%), followed by complementary hysterectomy (29.2%), surgery (4.5%), and other treatment modalities (0.8%).

Advanced (FIGO IVB), persistent, and recurrent stages of CC treatment

According to 89.6% of medical oncologists, first-line therapy for metastatic, persistent, or recurrent advanced disease consisted of cisplatin, carboplatin, or carboplatin in combination with paclitaxel (Table 2). The patients that received a second line of treatment, according to 55.6% of the oncologists, were < 40%, while patients that received three or more lines of treatment were < 20% (Table 2). Regarding the availability of drugs, most institutions had cisplatin, paclitaxel, carboplatin, and gemcitabine. Seventy-three percentages of respondents had vinorelbine, 26.4% had topotecan, and 41% had bevacizumab (Table 2). Regarding treatment adherence, 95.8% of the respondents stated that more than 20% of the patients abandoned the treatment. Oncologists believe that the reasons include financial problems (27.7%), patients’ personal decisions (27.7%), treatment toxicity (13.8%), and family decisions (3.2%).

The number of oncology specialists for CC care is limited

In this study, 106 Medical Oncologists participated, from 352 clinical oncologists reported nationwide (0.28/100,000 inhabitants for 2018)¹⁶. Globally, a median of 1.25 medical oncologists/100,000 population and 0.48/100 cancer patients is estimated¹⁷. Eighty-eight radio-oncologists participated, from 346 registered nationwide (0.26/100,000 inhabitants)¹⁸. Thus, we have insufficient oncology specialists. A limited number of oncology specialists generates more consultations for these medical professionals. The Global Survey of Clinical Oncology Workforce, which included 93 countries worldwide, identified that in 22 countries (24%), a medical oncologist provides care to < 150 newly diagnosed cancer patients; in 39 countries (42%), a medical oncologist offers medical care for more than 500 cancer patients. Of these, 26 countries were in Africa (81%), nine in Asia (47%), two in Europe (6%), and two in South America (29%). While in some countries, there is an extreme shortage of oncologists, where they attend to more than 1000 patients with this diagnosis, 25 countries are in Africa (78%), and two countries (11%) are in Asia¹⁶. This last piece of data is consistent with the results of our study, where 17% of those surveyed report attending more than 300 CC appointments per year, confirming the disparities in the workload of Mexican oncologists.

Deficiencies in patient care

For treatment success and a better prognosis of the life expectancy of patients with CC, the treatment must begin immediately¹⁹. In our study, half of the respondents answered that the treatment delay in their institutions was 5-8 weeks, and up to 5% reported more than 13 weeks delay. The impact caused by treatment delays in CC has been documented. A study suggests that waiting for pathology results to define the diagnosis can delay treatment²⁰. Furthermore, patients with longer delays before RT have a reduction in overall and disease-specific survival²¹. Finally, another study found that patients who received treatment between 90 and 180 days, or more than 180 days after diagnosis, had an increased risk of death (1.33 and 1.36, respectively, p < 0.05) when compared with those who received treatment within 90 days after diagnosis²². In addition, participants reported that more than 20% of patients discontinued treatment after establishing the therapeutic regimen. Previous studies have identified multiple factors that influence treatment refusal or discontinuation by cancer patients²³.

The adequacy of public hospitals

In our study, the most significant participation was carried out by IMSS physicians. Of the 246 IMSS second-level units, oncology patients are cared for in 111 (45.1%). In the third level of care, 19 hospitals (7 in Mexico City, 3 in Jalisco, 3 in Nuevo León, 2 in Guanajuato, 1 in Yucatán, 1 in Coahuila, 1 in Puebla, and 1 in Veracruz) offer services to cancer patients²⁴. This data denotes a high urban concentration, which reflects the inequalities in hospital availability between localities and regions in the country. The states with the lowest levels of development have the highest number of public health units/100,000 inhabitants: Oaxaca, Nayarit, Chiapas, Guerrero, and Hidalgo. However, when it comes to resources specifically for cancer treatment, Mexico City concentrates most of the resources²⁵. Thus, 96% of participants surveyed have access to CAT scanners, and only 2.2% have access to an MRI service, which is the method of choice recommended by FIGO for staging¹⁵.

Magos et al. surveyed to determine the country’s current infrastructure and RT capabilities. The total number of RT machines was 162, a median of three devices per state (ranging from 0 in Tlaxcala to 46 in Mexico City)¹⁸. These data are consistent with what was found in our study. The density of devices per million inhabitants in Mexico is the lowest among other OECD members²⁶.

Regarding treatments

Surgical treatment is essential in the early stages of CC²⁷. Respondents reported low equipment availability and insufficient surgical procedure supplies in this study. This lack of resources has been observed in low- and middle-income countries due to the cost of equipment, facilities, maintenance, and training time for qualified personnel and surgical specialists²⁸.

Access to CT-RT treatment is essential for locally advanced CC since it constitutes 80% of the diseased population²⁹. Several respondents reported that patients needed to move to another city or state to seek care, generating high costs, causing a lack of adherence and treatment abandonment, and conditioning a worse prognosis. Similar results were reported in the study by Torreglosa-Hernández et al. in the Mexican population with CC; 20.7% of women received medical care in a unit other than the habitual residence, with more significant displacement toward Mexico City³⁰. In addition, the impact on prognosis has been demonstrated. For example, Gong et al. found that patients who lived in an urban area had a more favorable prognosis than those who lived in a rural area³¹. In addition, it has been established that patients who do not access this treatment have a poor prognosis and a 4-year loss in overall survival³².

Regarding the advanced stage of the disease, few specialists had the resources to indicate a second or third line of treatment. The combination of chemotherapy plus the monoclonal antibody bevacizumab has been the standard of care since it improves the overall survival of this group of patients²⁷. However, the cost of this drug probably represents one of the main limitations of its use in Mexico. The survey reported that none of the patients treated in the participating institutions had access to this treatment in the country’s southern region. It is essential to add that Seguro Popular was replaced by the Instituto de Salud para el Bienestar (Institute of Health for Welfare, INSABI) in 2020. The results presented in this study correspond to the benefits provided by Seguro Popular, so the impact of the new policies established by INSABI on the current condition of CC care remains to be studied. We urge that guaranteeing women’s access to CC treatment, particularly for those with significant social disadvantages regarding access to and coverage of highly specialized medical services, is essential.