How to cite this article: Pérez-Pérez GF, Rojas-Mendoza T, Cabrera-Gaytán DA, Grajales-Muñiz C. Pertussis in Mexico, an epidemiological overview. A study of 19 years at the Instituto Mexicano del Seguro Social. Rev Med Inst Mex Seg Soc. 2015 Mar-Apr;53(2):164-70.

PubMed: http://www.ncbi.nlm.nih.gov/pubmed/25760745

ORIGINAL CONTRIBUTIONS

Received: November 28^th 2013

Accepted: October 30^th 2014

Pertussis in Mexico, an epidemiological overview. A study of 19 years at the Instituto Mexicano del Seguro Social

Gabriela Fidela Pérez-Pérez,^a Teresita Rojas-Mendoza,^b David Alejandro Cabrera-Gaytán,^c Concepción Grajales-Muñiz^d

^aÁrea de Vigilancia Epidemiológica de Sistemas Especiales

^bÁrea de Vigilancia Epidemiológica de Sistemas Especiales

^cÁrea de Vigilancia Epidemiológica de Enfermedades Respiratorias

^dDivisión de Vigilancia Epidemiológica de Enfermedades Transmisibles

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

Communication with: David Alejandro Cabrera-Gaytán

Telephone: 01 (52) 5536 8861, extension 15713

Email: david.cabrerag@imss.gob.mx; dcpreventiva@gmail.com

Background: Bordetella pertussis infection remains a public health problem in several developed and developing we describe the epidemiological syndrome cases subsystem special surveillance of whooping cough from 1992 to 2011 at a population with social security.

Methods: We obtained special cases subsystem Pertussis surveillance of 1992-2011. Univariate analysis was made of rates, ratios and proportions. Wilson was determined test for proportions to an alpha of 0.05, t-test for mean difference.

Results: We appreciate epidemic cycles every three to five years, the average baseline incidence, excluding epidemic years, 0.1 is considered confirmed cases per 100 000 beneficiaries assigned to family medicine, the highest incidence was recorded in 1997 and 2009. The most affected were children under 1 year of age and in outbreaks, the disease occurred at older ages.

Conclusions: During the period observed intermediate epidemic cycles 5 and 3 years of age presentation is consistent in other countries.

Keywords: Bordetella pertussis; Whooping cough; Epidemiological surveillance

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Whooping cough (pertussis) is a contagious acute infectious disease caused by the bacterium Bordetella pertussis (B. pertussis). Its location is restricted to the cilia of the nasopharynx, trachea, bronchi, and bronchioles of the human being, who is the only reservoir and bacteria transmitter for the development of the disease. It is highly contagious, endemic in any season, and has worldwide distribution, affecting 80 to 90% of unimmunized people, especially children, in whom it is very common, especially children under one year of age.¹

Whooping cough clinically manifested as pertussis-like syndrome is a major cause of infant morbidity and mortality with an estimated 50 million cases and 300,000 deaths recorded annually worldwide. The fatality rate in developing countries is as high as 4% in children under 12 months.²

In the Americas region, the total number of cases registered annually has fluctuated between 15,000 and 34,000 in the last ten years.^3-5 Outbreaks and epidemics of whooping cough occur in cycles every three to five years.²

Recently, in the United States of America (USA), over 35,000 cases of whooping cough have been reported, which include deaths; most were in infants under 3 months of age. The incidence rate of whooping cough among children exceeds that of all other age groups, although rates have increased in adolescents 13 to 14 years. The states that had the most outbreaks were Wisconsin, Minnesota, Washington, Vermont, Montana, Maine, Iowa and North Dakota.⁶ In response to this event, Mexico issued its epidemiological warning for whooping cough in July 2012, which highlighted the behavior of cases of whooping cough between 2000-2011, showing an oscillatory pattern similar to that observed in other countries, with exacerbations every three to five years, most recently in 2009 with 579 cases of whooping cough. 2010 showed a decline, but 2011 had 455 cases, marking an increase of 19% over the previous year. However, this finding is conditional on the implementation of diagnosis by polymerase chain reaction (PCR) as the traditional method. Unfortunately 85% of cases occurred in infants under one year of age.⁷ The reemergence of whooping cough cases in the US and Latin America puts the spotlight on this condition. Therefore, the objective was to describe the epidemiological picture of cases of pertussis-like syndrome and whooping cough based on the Subsistema Especial de Vigilancia Epidemiológica of Instituto Mexicano del Seguro Social (IMSS) from 1992-2011.

Methods

A descriptive analysis was done of morbidity data from the system of Sistema Especial de Vigilancia Epidemiológica of whooping cough/pertussis-like syndrome from the period 1992-2011 in Mexico with patients enrolled in IMSS according to the operational definition, and who have been confirmed by: laboratory, clinic, or epidemiological association. Morbidity rates were calculated whose denominators were the populations assigned to family doctors by municipality per 100,000. For geographic distribution, ranges were created of very high, high, medium, and low according to quartiles (Q1, Q2 and Q3) by incidence rate. The low range was a value less than Q1; the midrange was between Q1 and Q2; the high range was a value between Q2 and Q3, and the very high range was a value above Q3. A calculation of sample size was not required, since all cases were included from the special surveillance subsystem database, and it is a population-based study.

The analysis was of descriptive statistics with univariate determination of rates, ratios, and proportions. Wilson’s test for proportions was determined at an alpha value of 0.05, Student's t-test for difference between means, and Hartley’s test for equality of variance, completed in Epi-Info.

Results

Between 1992 and 2011, 3132 pertussis-like syndrome cases and 950 confirmed cases (23.28%, 95% CI 22.00, 24.61%) of whooping cough were classified. In the IMSS, during the period studied, whooping cough epidemic cycles were presented every three to five years, the highest incidence was recorded in 1997 and 2009 (Figure 1); last year an outbreak occurred in the north, from week 48 of 2008 to week 22 of 2009, in which the states of Nuevo Leon, Sonora, Tamaulipas, and Jalisco were involved, accounting for 79.8% (95% CI: 72.27, 85.77) of cases. Eight deaths were reported among Tamaulipas (5), Sonora (2) and Nuevo Leon (1). In 2010, 64 cases of whooping cough were registered with a national incidence rate of 0.18 per 100,000 enrolled individuals assigned to a family doctor. In 2011, 524 cases of pertussis-like syndrome were reported, of which 101 were confirmed as whooping cough (19.2748%, 95% CI 16.07, 22.82%) with an incidence rate of 0.3 for all age groups, 51.4% confirmed by clinic, 37.6%  by laboratory, and the remaining 10.8% by epidemiological association.

Figure 1 Probable and confirmed cases, incidence rate of whooping cough in all age groups per 100,000 enrolled individuals assigned to a family doctor. IMSS, 1992-2011

By age group, displacement of the disease to older ages was observed, but in all the years of study individuals under 1 year were most affected, with the exception of 1992. In 2009, individuals less than 1 year accounted for 75.6% of cases (95% CI: 67.56, 82.13), and in 2011 91.1% (95% CI: 83.93, 95.24) (Figure 2).

Figure 2 Percentage distribution of pertussis cases by age group. IMSS, 1992-2011

For 1992, the average age of cases of pertussis-like syndrome in males was 1.2 and for females it was 1.3 years (t = 0.080302, p = 0.9368); for 1996, the mean ages increased for both sexes: 3.7 years for males and 3.5 for females (t = 0.16907, p = 0.8666), to decline again in 2002 to 1.3 and 1.7 years, respectively (t = -0.5404, p = 0.5893). In 2009, when there was a pertussis-like syndrome outbreak, mean age shifted towards older ages, in males it was 2.1 and in females 4.2 years (t = -2.0442, p = 0.04156); a similar situation to 2011 with 1.8 years for males and 3.2 years for females (t = -1.73633, p = 0.08316).

Upon descriptive analysis of confirmed cases of whooping cough in children under 1 year of age, it was observed that in 2009 the most affected were 1-3 months old, predominantly female (45 versus 38). The median of diagnosis for both sexes was 2 months, without statistical difference by age in months (t = -0.29226, p = 0.7731). For 2011 the number of confirmed cases was greater in females than in males, however, cases occurred from the first to the ninth month of life, so the median age of diagnosis for both sexes was 1 month with no mean difference for age (t = -0.393362, p = 0.6989) (Figure 3).

Figure 3 Confirmed cases of whooping cough in children under 1 year of age. IMSS, 2009 and 2011

Of the 3132 cases of pertussis-like syndrome, in 520 it was possible to find the whooping cough immunization status; of those, 78 were in children under 3 months. Meanwhile for confirmed cases of whooping cough, vaccination status was in 106 cases, with a range of percentage of whooping cough vaccination history of 27.3 to 61.5%.

By municipality, at the launch of the system, 11 municipalities reported probable cases and two reported confirmed cases. In 2011, 33 of the 35 municipalities reported probable cases and 20 reported confirmed cases. There are differences among municipalities on the incidence of pertussis-like syndrome per 100,000 enrolled individuals assigned to a family doctor. At system launch, in most cases, the highest incidence was 1 case; for 2002 the cases were concentrated in the center of the country, and for 2009 it was in the north and south, while the incidence rate of cases of pertussis-like syndrome increased for selected years by municipality (Figure 4).

Figure 4 Geographical distribution of incidence rate£ of cases of pertussis-like syndrome. IMSS. A) 1992, B) 2002, and C) 2011. ^£ 100,000 enrolled patient assigned to a family doctor

Discussion

During the period studied, epidemic cycles are seen every three to five years, but it should be considered that for the initial years of the nineties, the trend of whooping cough presented important variations at the expense of difficulty in clinical and confirmatory diagnosis. Although surveillance for whooping cough was performed through the special subsystem created for this purpose in 1990 and since then it was part of the system of active surveillance, there was a lack of guidelines and procedures to systematize and unify the criteria for identification, study, monitoring, and final classification of cases.^8,9

In this regard, at first there were no operational definitions for suspected or probable cases of whooping cough, it was not until 1994 with the publication of the Norma Oficial Mexicana NOM-017-SSA2-1994¹⁰ for epidemiological surveillance, that the definition of pertussis-like syndrome was included. The whooping cough cases included before that year were based on clinical diagnosis emitted by each attending physician.

Thus, in Latin America itself there are differences in the various surveillance systems, from periodicity of reporting, notification type, operational case definitions, and population subject to study for Mexico, where reporting should be mandatory and immediate, and should include various operational definitions that include population of any age.

The cyclical behavior characteristic of whooping cough/pertussis-like syndrome is consistent in other countries^11-14 and in Mexico.⁷ In our country in 1991 the Programa Nacional de Inmunizaciones was renamed, and since then it has been known as Programa de Vacunación Universal (PVU) which, given the epidemiological situation of some infectious diseases, has incorporated into the basic vaccination scheme new biological agents for disease prevention. In this regard, in 1996 the acellular whooping cough vaccine was approved for children; in 1999 the pentavalent whole-cell DPT + HB + HI vaccine was incorporated; in 2007 the pentavalent acellular DPAT / VIP + Hib vaccine was incorporated, and in 2009 due to the outbreak in the north and in order to reduce missed opportunities for vaccination, Consejo Nacional de Vacunación (CONAVA) approved the temporary application of an accelerated scheme of vaccination with pentavalent acellular (DPaT / VIP + Hib) with DPT booster in preschool age. Based on the fact that the largest number of cases have been in children under one year, more than half of whom are in fact outside the target vaccination group, the intervention of vaccination strategies starting from this year has been promoted.¹⁵

The incidence rate of pertussis-like syndrome remains low, most likely because the disease is underestimated compared to other countries such as Chile, whose rate in 2002 was 7.0 per 100,000 population and in 2009 4.1,¹³ it being at 0.9 in 2002 and 0.4 in 2009 in this study; in Peru it was 1.6 cases in 2002¹¹ and in Uruguay 12.63 cases in 2012.¹²

With regard to sex, more cases have been reported in females than in males with an overall ratio of 1: 1.2, which contrasts with the 0.87:1 in 2010 for the European Union¹⁶ in all age groups and in earlier reports for our country17 and Peru, where it was 1:1.08.¹¹

As for age at diagnosis, children under one year were the most affected, and categorically those under 2 months, who are the most vulnerable and susceptible group of the general population, since they are outside the target group for vaccination.^11,13,18,19 However, from the incidents registered in the whooping cough epidemiological surveillance subsystem it was not possible to determine cases of this disease over five years of age, as has been published by different Ministries of Health in the Americas, as it has traditionally been considered an disease exclusive to childhood and cases in other age groups are rarely studied, although the operational definitions state that it can affect anyone of any age.⁹ In that sense, asymptomatic adolescents and adults or those with moderate symptoms are rarely diagnosed, because no intentional search is made. Therefore, the possibility of identifying a case is usually only considered when the association with whooping cough occurs in children.^20,21

The present study found that the average age of diagnosis of pertussis-like syndrome has increased, the hypotheses are that this could be due to: a) a shift of the disease to other susceptible ages,¹⁴ and b) increased epidemiological surveillance of pertussis-like syndrome cases.^3,7

In recent years the number of cases of whooping cough / pertussis-like syndrome have increased due to:

• Strengthening epidemiological surveillance.⁷
• Changes in the operational definition of cases.
• Criteria for the clinical classification of cases (cases without sample, insufficient number of contacts studied, and untimely classification).
• The introduction of a new technique (PCR) with greater diagnostic accuracy.⁷
• Increase in diagnostic suspicion at the operational level.
• The reemergence of the disease in several countries.^3,6,11-13
• Changes in vaccination schedules in children under 1 year with DPAT.^3,6,7
• The probable decreased immunity in adolescents and young adults.^22-24

It is considered a re-emerging disease as its incidence has increased worldwide, even in countries with adequate vaccination coverage.²⁵ In recent years there has been an increase in cases of this disease in Mexico and several countries of the Americas and Europe.^3,12,26,27

The Centers for Disease Control and Prevention (CDC) reviewed the medical records of more than 4,000 children in 15 counties in California (USA) in 2010 when a whooping cough epidemic occurred; the results revealed that the diphtheria-pertussis-tetanus acellular whooping cough vaccine (DPAT) had an overall efficacy in children age 4-10 of 88.7%, which is similar to levels found in clinical trials before the vaccines were authorized. The results also endorsed the need for a booster dose of Tdap at 11 to 12 years old;²⁸ that's why the CDC recommended that infants and children receive DPAT vaccine at 2, 4, 6, 15, and 18 months old, and a booster DPAT vaccine between 4 and 6 years old. Because DPAT protection fades with time, another dose of pertussis vaccine, known as Tdap, is recommended for adolescents 11 to 12 years. Adults who did not receive the Tdap vaccine as preteens should receive a dose currently.²⁸ The increase in cases of reported whooping cough continued in 2012 in Argentina, Brazil, Colombia, Chile, Guatemala, Mexico, Paraguay, Venezuela, and USA, which it made it so that in March of that year, at a meeting convened by the Pan American Health Organization (PAHO), with the participation of experts from 12 countries, it was concluded that the disease continues appearing in children under 5 years without complete vaccination plans for their age. In September 2012, the World Health Organization (WHO) convened an informal meeting of experts, who concluded that the acellular pertussis vaccine (aP) has limitations and that the problem must still be better characterized. Here, Suarez-Idueta et al. recommended the use of accelerated vaccination to protect those under 6 months of age and a booster vaccination for adolescents; this situation has been suggested in other studies as well as the use of the nest or cocoon technique.²⁹ While the vaccination status of children was not analyzed in this article, it did become evident that the disease was diagnosed at older ages in recent years. It is noteworthy that Mexico, like Uruguay, has one of the world's most comprehensive vaccination schemes. In the Americas, our country is the only one with a nominal census of children under eight years of age whose vaccination universally began in 1991 with six vaccines and currently has 14,³⁰ plus being one of the most complete in the Americas.³¹ However, despite these great achievements in public health in the Americas, PAHO reported that vaccination coverage against diphtheria, tetanus, and whooping cough have reduced significantly in the region.³¹

IMSS, through Acuerdo Secretarial No. 130, participates in the Comité Nacional de Vigilancia Epidemiológica (CONAVE),³² and since then helps update the guidelines for surveillance of diseases preventable by vaccination.³³

It is important to maintain surveillance of pertussis-like syndrome in all age groups in order to identify chains of transmission. On the other hand, due to variations in the frequency of probable cases and whooping cough cases that have been identified in the various municipalities and in different years, we cannot consider a geographic characterization or the absence of cases in some of them, rather it may be due to greater or lesser diagnostic suspicion of the disease, and classification criteria that foster an underestimation in the actual disease burden of this disease, which is why the importance is highlighted once again of having a permanent system of epidemiological surveillance of suspected cases and whooping cough cases aimed at all age groups. In that sense, the enrolled population has benefited thanks to the active epidemiological surveillance system that the Instituto has, and the strengthening of epidemiological surveillance of this disease in recent years.

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