Cervical Cancer Trends in Mexico: Incidence, Mortality and Research Output

Currently, cervical cancer is the fourth leading cause of cancer death in women worldwide, causing more than 275,000 deaths annually (Arbyn et al., 2008). Cervical cytology screening has been proven to decrease the incidence and mortality of cervical squamous cell cancer and to increase the cure rate of cervical cancer (Andrae et al., 2012; Ito et al., 2013; Nessa et al., 2013). Despite this, it has been considered that the risk of developing invasive cervical cancer is much higher among lowincome populations (Parikh et al., 2003; Raychaudhuri and Mandal, 2012; Simayi et al., 2013). In Mexico, a high percentage of women of reproductive age have never had a Pap smear (Conde-Ferráez et al., 2012). On the other hand, research evaluation consists of monitoring of ongoing research initiatives to assess the efficiency and effectiveness with which they are being implemented, to determine the extent to which they are achieving their targeted objectives, and to recommend adjustments. Additionally, cervical cancer may well also be considered a neglected disease in terms of scientific research, considering the proportion of articles dealing with a particular type of cancer with respect to its impact (Fajardo-Ortiz et al., 2014).


Introduction
Currently, cervical cancer is the fourth leading cause of cancer death in women worldwide, causing more than 275,000 deaths annually (Arbyn et al., 2008). Cervical cytology screening has been proven to decrease the incidence and mortality of cervical squamous cell cancer and to increase the cure rate of cervical cancer (Andrae et al., 2012;Ito et al., 2013;Nessa et al., 2013). Despite this, it has been considered that the risk of developing invasive cervical cancer is much higher among lowincome populations (Parikh et al., 2003;Raychaudhuri and Mandal, 2012;Simayi et al., 2013). In Mexico, a high percentage of women of reproductive age have never had a Pap smear (Conde-Ferráez et al., 2012).
On the other hand, research evaluation consists of monitoring of ongoing research initiatives to assess the efficiency and effectiveness with which they are being implemented, to determine the extent to which they are achieving their targeted objectives, and to recommend adjustments. Additionally, cervical cancer may well also be considered a neglected disease in terms of scientific research, considering the proportion of articles dealing with a particular type of cancer with respect to its impact (Fajardo-Ortiz et al., 2014). In order to better gauge and interpret the changing cervical cancer incidence and mortality in Mexico, we studied the trends in incidence and mortality rates from 2000 to 2010. Additionally, a bibliometric method was used to analyze cervical cancer Mexican research trends and performances, from 1994 to 2013, in order for focus on areas of weaknesses and future avenues to improve cervical-cancer care in Mexico.

Materials and Methods
We obtained the incidence data on cervical cancer from Incidence Database of the Department of Epidemiology of the Ministry of Health. The mortality data on cervical cancer was obtained from Mortality Database of the International Agency for Research on Cancer (IARC) of World Health Organization. Registered cervical cancer new cancer cases and deaths were extracted on restricting the analysis from 2000 through 2010, in order to examine recent trends over the 11-year period. We excluded cases below 25 years because of paucity of new cancer cases and deaths. The incidence and mortality data was grouped in following age groups: women aged 25-44 years, 45-49 years, 50-59 years, 60-64 years, and 65 years and older. The data was exported to Microsoft Excel® for analysis.
We computed the number of new cancer cases and deaths, and presented together with age-standardized rates.
On the other hand, Web of Science was used to produce statistics on the scientific production of the Mexican researchers. Mexican papers (articles, research notes, and review articles) in the field of cervical cancer were downloaded for the 20 publication years, 1994-2013. In order to approximate the overall number of published items on cervical cancer, the following search strategy was employed; (1) CU=mexico, (2) TS= ((cervical) OR (cervix)), (3) TS= (cancer OR onco* OR carcino* OR tumor OR neopl*); (1) AND (2) AND (3). Document information included names of authors, titles, years of publication, source journals, contact addresses, and subject categories of journals. The records were downloaded using Microsoft Excel ® software, and additional coding was manually performed for the number of authors, origin countries and institutes of the collaborators.

Results
Analysis of cervical cancer absolute incidence and mortality in Mexico, registered between 2000 and 2010, shows that there were 82090 and 46173 new cases and deaths, respectively. The number of new cases has remained constant, with a slight peak in 2007, but with a decline starting in that year. Meanwhile, the number of deaths of cervical cancer has decreased substantially (Table 1).
Incidence rate has decreased throughout the last five years. Figure 1 shows the cervical cancer incidence and mortality rates. The incidence decreased by 8.15% from 2006 to 2010. In the other hand, mortality rates showed an annual decrease of 4.93% in the same period. Figure 2 shows annual percentage changes (APCs) to the incidence and mortality rates during 2000-2010, where a decrease is observed in both rates. Figure 3 shows the trends of age-stratified incidence and mortality rates of women over the 11-year period. The incidence was increased until 2002 in 45-49, 50-59 and >65 age groups (Figure 2A). For 25-44 and 60-64 age groups, the incidence peaked in the period 2004-2006. However, a decrease in incidence began in 2006 in all age groups. The lowest incidence was seen in the 20-44 age group (11.06 per 100,000 women in 2000) and the highest (60.27 per 100,000 women in 2002) in the 50-59 age group. Furthermore, in the time period analyzed, mortality in all age groups studied had a substantial decrease ( Figure  2B). Figure 3 shows annual percentage changes (APCs) to the incidence and mortality rates during 2006-2010, where a decrease is observed in both rates.
Regarding the Mexican research on cervical cancer, a total of 780 Mexican items published in Web of Science from 2003 to 2012 was counted (Figure 4). A development trend was found for all documents and articles, which increased from 4 in 1994 to 74 publications in 2013. The 780 indexed items have been cited 12,533 times since   Figure 4 demonstrates the parallel increase in the number of citations in conjunction with the increase in published items.
The contributions of Mexican different institutes were estimated by the affiliation of at least one author. The top 10 institutes were ranked by the number of items ( Table  2). The National Autonomous University of Mexico had the most total (34.87%), followed by The Social Security Mexican Institute (16.02 %), National Institute of Cancerology (15 %), National Institute of Public Health (10.89 %), and Center for Research and Advanced Studies (10.38 %).
In total, 780 articles were published in 309 journals. Salud Publica de Mexico published the most articles with 47 articles comprising 6.01% of all the articles, followed by Archives of Medical Research (4.35%), International Journal of Gynecological Cancer (2.94%), Revista de Investigación Clínica (2.94%), and BMC Cancer (2.69%) ( Table III). 89.5% of the publications were in English, followed the Spanish (10.3%), and one in Portuguese (data not shown) Finally, we examine the types of research. The main types of research are shown in Figure 5, treatment and diagnosis dominate with 41.66 % of the total output between them.

Discussion
Our study analyzes the trends in incidence and mortality rates of cervical cancer among women in Mexico from 2000 to 2010. The main finding of the study is that the incidence rate has decreased over the period of last five years. Similarly, several reports in countries of North America (Mosavi-Jarrahi and Kliewer, 2013; Adegoke et al., 2012), Latin America (Muñoz and Bravo, 2012), and Asia (Jung et al., 2014) show a decreasing incidence rate.
On the other hand, cervical cancer mortality was stable or slightly decrease during period analyzed. Mortality data were similar to other countries with a middle income, e.g. Korea (Kim et al., 2013), Chile (Vidal et al., 2013), and Brazil (Gonzaga et al., 2013). In this study, cervical cancer incidence and mortality trends remained at same level in all age groups. This decrease in both incidence and mortality rates is perhaps because to the development and implementation of policies and programs against cervical in Mexico (Ruiz- Moreno et al., 2011;Lazcano-Ponce et al., 2009;Lazcano-Ponce et al., 2006).
However, despite the decrease in incidence and mortality rates is necessary to establish new public health policies, including prioritization in certain areas of scientific research. In this study dealing with cervical cancer Web of Science journal papers, we obtained some significant points on Mexican cervical cancer research trends and performances from 1994 to 2013. Our findings suggest a growing interest in cervical cancer research in Mexico as shown by the increased number of items each   1 9 9 4 1 9 9 5 1 9 9 6 1 9 9 7 1 9 9 8 1 9 9 9 2 0 0 0 2 0 0 1 2 0 0 2 2 0 0 3 2 0 0 4 2 0 0 5 2 0 0 6 2 0 0 7 2 0 0 8 2 0 0 9 2 0 1 0 2 0 1 1 2 0 1 2 2 0 1 3 articles total citations Figure 4 year. With respect to scientific production, the National Autonomous University of Mexico was the leader in cervical cancer research in Mexico, distinctly followed by the Social Security Mexican Institute, and National Institute of Cancerology. However, a problem of cervical cancer scientific research is that over 90 percent of such research is concentrated in only three cities: Mexico, Monterrey and Guadalajara (data not shown). One of the crucial policy issues in Mexico is how to enhance cancer research across all union territories. On the other hand, studies of treatment, diagnosis and prevention are the dominant work in the Mexican cervical cancer research community and receive more than 55% of total research output. The range of research domains correlate with those noted worldwide.
Several papers have examined cancer research in individual countries: in Italy (Micheli et al., 2009), Peru (Mayta-Tristán et al., 2013, and Turkey (Dursun et al., 2011). However, this analysis represents the first bibliometric research of cervical cancer, and is consistent with other studies that have shown an increased interest in the countries in scientific research of certain cancers, such as breast (Perez-Santos and Anaya-Ruiz, 2013), lung (Ho et al., 2010), and ovary (Guler et al., 2013).
This work represents the first bibliometric assessment of Mexican cervical cancer research. Cervical cancer research in Mexico is still developing, although some research has attained an international level. The findings of this study should provide useful information for those who will be performing research and studying cervical cancer for Mexican.