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Epidemiological surveillance of febrile rash ill

How to cite this article: Pérez-Pérez GF, Rojas-Mendoza T, Cabrera-Gaytán DA, Grajales-Muñiz C, Maldonado-Burgos MA. Epidemiological surveillance of febrile rash illness. Rev Med Inst Mex Seguro Soc. 2015 Jul-Aug;53(4):444-52.



Received: April 14th 2014

Accepted: February 12th 2015

Epidemiological surveillance of febrile rash illness

Gabriela Fidela Pérez-Pérez,a Teresita Rojas-Mendoza,a David Alejandro Cabrera-Gaytán,a Concepción Grajales-Muñiz,a Martha Alejandra Maldonado-Burgosa

aCoordinación de Vigilancia Epidemiológica, Instituto Mexicano del Seguro Social, Distrito Federal, México

Communication with: David Alejandro Cabrera-Gaytán

Telephone: (55) 5536 8861


Background: Three imported cases of measles were detected in 2011, so the issue of surveillance with epidemiological alerts intensified. The aim of this article is to describe the phenomenon of intensified surveillance of febrile rash illness before the import of confirmed measles in the country at the Mexican Institute of Social Security cases.

Methods: The cases of epidemiological surveillance system 2011 were obtained was compared with the prior year It was determined t-Student mean difference and Wilson test for proportions, both with an alpha value of 0.05.

Results: 2786 cases of febrile rash illness were reported, 51.2 % more cases than the previous year were reported in 2011, the number of reported cases in relation to the expected increase in 29 of the 35 Delegations, an increase in the average number of cases reported from week 26. 67.4 % of reported cases are concentrated in children under 5 years of age. The average days to collect laboratory sample improved after issuing alerts from 3.4 to 2.6 days (p < 0.000000559).

Conclusions: A significant increase in reported cases of febrile rash illness compared with the prior year was appreciated. The Institute has a surveillance system for robust and febrile rash illness, which has identified risks to the population.

Keywords: Meales; Epidemiological surveillance; Exanthema

Europe has experienced a measles virus circulation since 2009.1,2 In 2010, 32,480 cases of measles were reported with an incidence rate of 5.87 per 100 000 inhabitants, with genotype G3.3-5 predominant. The following year 32,124 cases were reported with an incidence rate of 6.34; 43.1% were classified as confirmed. The highest incidence rates were reported in France (23.04 per 100 000 population), Romania (19.45), Italy (8.56) and Spain (7.62) 6. 81.9% of the cases reported in Europe in 2011 reported no measles vaccine history.6 The serotypes in circulation were D4, B3, G3, D8, D9 and H1.1,2,4 The genotype D4 was detected in 24 European countries during 2011.1,7,8 2.3% of all cases were considered cases imported from other countries.9 At the same time, the United States of America (USA), had confirmed measles cases in different states, mainly associated with imports from other countries, where 86% of them had unknown measles vaccination history or were not vaccinated.10

Given this, the Dirección General de Epidemiología (DGE) issued the first measles epidemic alert on June 16 2011,11 coupled with the potential risk of reintroduction of the virus by the regular transit of travelers to areas with outbreaks. On June 22, 2011 surveillance guidelines were issued by the Soccer World Cup Office Sub 17, where the teams and citizens of countries such as Germany, Denmark, France, Holland, England, Czech Republic and the Republic of Congo (among others) were expected to attend, where major outbreaks of measles were often present, which significantly increased the likelihood of virus introduction into Mexican territory.11 Nearly a month after sending out this early alert, the first imported case of measles occurred on July 21, 2011, in a female aged one year nine months, who visited Mexico from France,12,13 leading a broad measles epidemiological alert to be issued. Subsequently, on July 29, 2011 another epidemiological alert was issued due to the second case of imported measles not associated with the first, in a woman of 16 with a history of having traveled to England and Scotland.14 On August 5 a third case was reported, also imported, corresponding to a 45-year-old male, living in Guanajuato and with a history of travel to New York and Canada. That year, a total of three confirmed cases of imported measles were reported in Mexico.15 Finally, on September 12, 2011, in the absence of any further cases to date, the epidemiological alert on imported measles cases in our country was lifted, on the 50th day after the last reported case.16

The Instituto Mexicano del Seguro Social (IMSS) as a member of the Sistema Nacional de Vigilancia Epidemiológica (SINAVE), strengthened said epidemiological surveillance of FRI (febrile rash illness) in all medical units; such intensified surveillance refers to the idea "the more you look, the more you find",17 so that certain cases or patients are followed more closely or have specific diagnostic tests for them;18 this is a kind of selection or information bias produced when an exposure (eg, issuing an epidemiological alert) may result in a higher probability of detection (FRI or confirmed cases of measles) in patients exposed. In this situation, there is a special operating system based on case definitions, which include lab tests; so the aim was to describe the experience of the IMSS in the intensification of epidemiological surveillance of FRI in the face of confirmed imported measles cases in the country.


All cases of FRI reported and discussed in the 2011 IMSS special surveillance system were reviewed.

An endemic channel was created by weekly epidemiological notification of the special FRI epidemiological surveillance system, by determining the geometric mean of the historic rates.19

Overall incidence rates were calculated per 100,000 beneficiaries enrolled in the family medicine program. The population used was that calculated halfway through the year, taken from the publications of the Division of Health Information intranet portal.20 Rates were calculated specific to municipality.

By observing the effects of the issuance of the epidemiological alert, the sampling rate was determined before epidemiological week (EW) No. 24 and after. A Student’s test t was used for the mean difference, and a Wilson test for proportions; both with an alpha value of 0.05, which were done in OpenEpi: Open Source Epidemiologic Statistics for Public Health, version 3.01.


In 2010, 1,836 cases of FRI were reported and studied, while in 2011 there were 2,786, representing an increase of 51.2 percentage points. After the first epidemiological alert was issued on June 16, 2011 (epidemiological week No. 24), no change was seen in the number of reported cases of FRI between that week and week No. 25; from EW No. 26 onward reported cases increased from 39 in 2010 to 73 cases in 2011. The peak of reported cases was during epidemiological week No. 32 with 170 cases (Figure 1).

Figure 1 Epidemic curve of cases of febrile rash illness by epidemiological week at onset. IMSS, 2010- 2011

However, epidemiological week No. 24, according to the endemic channel for FRI cases reported in the special epidemiological surveillance system, was an "epidemic zone", which was to descend for one week to the "alarm zone"; and thereafter, to remain in "epidemic zone" (Figure 2).
From the epidemiological week that the epidemiological alert was issued, compared to the same period last year, the average number of cases reported per week between those years (36.2, 95% CI 19.4673, 52.9327, p = 0.0001063) increased.

Figure 2 Epidemic curve of cases of febrile rash illness by epidemiological week of onset at IMSS. IMSS 2010-2011

The incidence rate for 2011 was 7.7 (95% CI 7.43, 8.002) per 100,000 enrolled in the family medicine program (range 2.7-27.2); where the highest incidence rate was in San Luis Potosi (Figure 3), contrasting with the incidence rate of the previous year, which was 5.1 FRI cases per 100,000 family medicine enrollees.

Figure 3 Crude incidence rate of febrile rash illness by notifying municipality. IMSS, 2011

The first two imported cases were in Distrito Federal Sur (July 20 and 29) and one more in Celaya, Guanajuato on August 5, 2011; in the latter municipality, the incidence rate was above national, but the Distrito Federal Sur was the delegation with the second lowest incidence rate in the Institute. In breaking down the distribution of reported cases of FRI in the Distrito Federal Sur municipality by epidemiological week in 2011 by date of onset of symptoms, an increased number of reported cases (Figure 4) is evident.

Figure 4 Epidemic curve of cases of febrile rash illness by epidemiological week of onset. South Regional Municipality of Distrito Federal, 2010 - 2011

During that year, the number of cases of FRI expected based on reporting at least one case per 20 000 inhabitants, increased in 29 of the 35 municipalities, with an increase of 995 cases reported over the previous year (Figure 5). The weekly average of reported cases increased by 18 cases (p = 0.001208).

Figure 5 Cases of febrile rash illness relative to cases expected by municipality, 2011

By age group, 67.4% of cases of FRI focused on children under 5 years of age (95% CI 65.61, 69.09; p <0.0000001) (Figure 6). 159.5 cases were reported per 100,000 inhabitants among children under 1 year and 45.4 among children 1-4 years old. The incidence rate declined as age increased.

Figure 6 Cases of febrile rash illness by sex and five-year age group. IMSS, 2011

As for the collection of diagnostic samples to confirm the presence of measles virus, in 2011 the sample was 97.5%, while in the previous year it was 91.3%. The sampling rate before EW No. 24 was 98.7% and after this, 98.9%; although the percentage of sampling did not vary much, the average number of days for the sampling was lower after EW No. 24, from 3.4 days to 2.6 days, after the alerts were broadcast (0.8, 95% 0.487913, 1.11209, p <0.000000559).


In the Americas, the endemic transmission of the measles virus was interrupted in 2002; however, in recent years isolated cases and outbreaks associated with cases imported have been reported.21 In Mexico, the decrease in measles cases and deaths has been extremely noticeable, going from 68,782 cases in 1990 to two in 1996. From 1997 to 1999 no confirmed cases of measles were recorded, and from 2000 to date they have identified a total of 167 confirmed measles cases considered imported. Since 2007 there had been no cases of measles in the country. However, the observed increase in other countries increases the epidemiological risk of reintroduction of the virus into the country; 42% of measles cases in the last year in the Americas have been due to people visiting countries with active transmission, as in 2011, there were major cultural and sporting events involving population movements in the Americas; in Mexico there was the FIFA U-17 World Cup; the U-20 World Cup held in Colombia, and in Brazil, the Rock in Rio event,22 for which the Pan American Health Organization (PAHO) issued an epidemiological alert that urged international travelers to be vaccinated against measles and rubella before visiting the Americas, in an effort to reduce the risk of reintroduction of the virus to the region.21

Against this background, Mexico identified three laboratory-confirmed cases of imported measles, so it was necessary to increase the epidemiological surveillance of FRI and issue alerts. Mexico was not the only country to detect imported cases of measles that year, they were also detected in Argentina, Brazil, Canada, Colombia, Chile, Ecuador, USA and Panama.23 Other countries in the Americas also issued notices and / or epidemiological alerts such as Brazil, Peru,24 Argentina26,27 Venezuela,28 Ecuador29 as well as the PAHO recommendations for travellers.21

Maintaining surveillance of FRI has managed to identify cases and potential risks to the population in the countries of the continent; for example, Chile, after 18 years without measles transmission, in 2011 reported confirmed cases, all related to imported cases from Brazil and the United States, a similar situation to Mexico 25. However, there are other experiences like in Ecuador, where the first four cases of measles were recorded in Tungurahua in July with incomplete vaccination programs or without vaccination history, culminating in various measles outbreaks (197 laboratory-confirmed cases).23,29

As for the number of reported cases of FRI until week No. 52 in 2011 in Argentina, this figure was 348 cases with the identification of two measles outbreaks (one imported and the other related to imported cases), with three people affected.23 Genotype D430 was identified. This is similar to what happened in Mexico in that year, where there were confirmed imported measles cases.31

The dramatic increase in measles cases was due largely to a large outbreak in Bulgaria for 2009-2010 with over 24,000 reported cases with 24 deaths.32 Thereafter, several countries of the old world reported measles cases. In Italy, between July 2009 and September 2010, 2,151 probable cases were reported with a cumulative incidence of 3.6 per 100,000 inhabitants.2 Meanwhile, in the outbreak in Spain in 2011, a total of 1,759 suspected cases were reported and confirmed.8 In the present study the incidence rate of FRI ranged from 2.7 to 27.2 cases per 100 000 enrollees, which was similar to other countries, with the proviso that no indigenously confirmed cases were detected.

In the measles outbreak in Italy in 2009-2010, 52.3% of suspected cases were male patients; 2 similar to the FRI reported in 2011 cases, where men accounted for 54.5% of cases.

With respect to age, in Spain, in 2011, the average age was 16.5 years (range 2 weeks to 57 years) among all reported cases, 8 which contrasts with the findings in this study, where age average was 6.2 years (range 1 month to 73 years); and in which most of the afflicted were children 1-4 years of age (mean age 1.8 years).

In Italy, there was an increase in the incidence of measles in a population with consistently high coverage in the province of Ferrara, in northern Italy. During the first six months of 2010, 19 cases were confirmed, 10 of which were hospitalized; although most of the confirmed cases were without vaccine history.33 The same situation was reported in Genoa with the presence of several outbreaks of measles between 2003 and 2010, despite optimal vaccination coverage.34 But in Spain, 68.2% of cases reported had no vaccination history, 8 while in Europe 8 of 10 cases had unknown or no measles vaccination history.10

Given the magnitude of the reported cases, cases of measles were even reported among health staff.35,36 In 2011, no cases were reported among IMSS health personnel, reflecting the degree of training and implementation of standard precautions and transmission mechanism.

In 2011, there was large circulation of the measles virus in several countries. Serotypes circulating in America in 2011 were D4, B3 and G3. In Africa it was B3. In Europe had a wider range, with D4 most prevalent, followed by D8. The highest incidence rates were recorded in Europe and Africa. However, Canada and the United States had the highest incidence in the Americas, followed by Brazil, Argentina and Chile. During the previous year, Brazil reported B3 and D4, whilst the remainder of the serotypes were isolated in North America. In all outbreaks, except for the second outbreak in Spain and the outbreak in Turkey, the D4 genotype measles virus has been confirmed. Genotype B3 measles virus was isolated to cases in the second outbreak of measles in Spain, while the D9 genotype was in Southeast Asia.37 Given the effect on public health in Europe, a group of experts on that continent concluded that there are favorable conditions for the eradication of measles:


  • Humans are the only source for the measles virus.
  • There is a vaccine that is safe, inexpensive and produces lifelong immunity.
  • There are specific and sensitive diagnostics.
  • There are no chronic carriers,38 and what’s more there is a syndromic surveillance system in the countries of the American continent, including the social security of Mexico.


In that sense, it is well documented that the risk of error caused by the surveillance bias is likely to increase as you increase the use of sanctions and incentives for the performance of quality measures;18 in this case, the impetus was the issue of epidemic alert with successive ranges. It has been documented that surveillance bias also has the potential to have other effects; for example, a FRI case would be reported in the special surveillance system, but without the incentive of applying appropriate diagnostic tests to minimize the evidence of the movement of the agent, which reflects a deficiency in the quality of attention, so that cases would not normally be detected;17 another effect would be that, where you have more FRI cases detected, those places get associated with higher rates of incidence, so that the regions or medical units where higher rates of incidence were evident, may be falsely labeled to have diminished the quality of preventive care, or even clinical medical care.17

In the present study, FRI reports were systematically continued each epidemiological week, which were studied in laboratory samples where the sampling rate in cases of FRI reported during 2011 was 97.5%, which was higher than in the previous year (91.3%), so the diagnosis and epidemiological outcome depended partly on exposure (epidemiological alert), as this intensified the special surveillance of FRI,39 specifically in reducing the number of days to collect the confirmation sample(s).

The special FRI surveillance system in our country recorded an increase in the number of reported cases, so performance indicators improved for epidemiological surveillance of this disease,40 primarily the rate of reporting subsequent to the measles alert circulated in July 2011, which increased five times compared to the annual average of the past five years. While the various publications of the Ministerios de Salud and other journals documented in absolute or relative figures confirmed cases of measles, or in greater detail laboratory-confirmed cases, this phenomenon was not documented through issuing warnings and / or epidemiology alerts in cases of FRI, so this study is a contribution to the study of this phenomenon in the IMSS, where surveillance was intensified by issuing epidemiological alerts. It is noteworthy that the Institute that year had 36.1 million family medicine enrollees, 20 meaning that 31.5% of the country’s population was affiliated with IMSS social security,41 which accounts for a large part of the Mexican population studied, together with the cases reported to the surveillance system involving patients of all ages and without any excluding condition, so it was not necessary to calculate a sample size; this situation is a strength of the present study. Also, the risk of introduction of this disease is latent, given the recent epidemiological situation in Europe and America; the Secretaría de Salud Federal through the Servicio Mexicano de Inteligencia Epidemiológica issued an early travel warning on March 27, 2014 because of outbreaks of measles.42 Mexico's success has been no indigenous cases of measles for more than a decade, and the special FRI surveillance system has enabled timely identification of confirmed cases that were imported; against this background, it is essential that all doctors (mainly from recent generations) keep measles in their differential diagnosis, as it can happen in our country, despite good vaccine coverage34 or having a vaccine history.43

Therefore, it is concluded that the Institute has a robust FRI surveillance system, which systematically reports cases, studies samples collected for the detection of the measles virus, and responds to epidemiological alerts.

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Conflict of interest statement: The authors have completed and submitted the form translated into Spanish for the declaration of potential conflicts of interest of the International Committee of Medical Journal Editors, and none were reported in relation to this article.

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