Epidemiology of pertussis among adolescents, adults, and older adults in selected countries of Latin American: a systematic review

Figures & data

Table 1. Summary of selected study characteristics, by country, and corresponding information on pertussis cases among adolescents, adults, and older adults

						Adolescents, adults, and older adults pertussis cases (% of all confirmed cases)
Author, year^Ref	Study period	Study design	Study’s data source	Study participants	Age group of interest*	overall	By age group**	Database†
Argentina
National level data
Hozbor et al., 2009^10	2004–2007	Surveillance	SINAVE	Confirmed cases, all country	> 16 y	2.1%‡	n.r.	PubMed
Romanin et al., 2014^39	2002–2011	Surveillance	SINAVE	All cases reported^§, country	> 15 y	2.7%	n.r.	PubMed
Regional level data
Kusznierz et al., 2014^20	2006–2010	Cross-sectional	One tertiary hospital	Suspected for pertussis children < 14 y and the family contacts of confirmed cases, Santa Fe (city)	> 10 y	5.2%‡	n.r.	PubMed
Lavayén et al., 2017^21	2011–2015	Cross-sectional	INE	Suspected cases, Mar del Plata (city)	> 7 y	5.7%‡	n.r.	Scopus
Brazil
National level data
Willemann et al., 2014^12	2007–2011	Case-control	SINAN	Cases: confirmed pertussis cases Controls: notified as suspected cases, but were not confirmed as such	> 15 y	6.6%‡	n.r.	SciELO
Falleiros Arlant et al., 2014^23	2011–2012	Cross-sectional	SINAN	Confirmed cases, all country	> 10 y	11.6%‡	10–19y: 5.5% 20–59y: 5.8% ≥60y: 0.3%	Pubmed
Guimarães et al., 2015^28	2007–2014	Surveillance	SINAN	All cases reported^§, all country	> 15 y	8.8%‡	n.r.	Pubmed
Castro and Milagres, 2017^13	2010-2014 2015	Surveillance	SINAN	Cases reported, whole country	> 15 y PW (3rd trimester)¶	15 y, 2010–2014: 10,1%‡	n.r.	LILACS
						PW, 2015: 167 cases¶
Silva et al., 2017^26	2001–2014	Cross-sectional	SINAN	All cases reported^§, all country	> 10 y	13.1%‡ (all study period) 13.8%‡ (2007–2014)	10–19y: 5.9% 20–59y: 6.9% ≥60y: 0.3%	Google Scholar
Regional level data
Druzian et al., 2014^22	1999–2008	Cross-sectional	SINAN, LACEN	All cases reported^§, Mato Grosso do Sul state	> 10 y	8.4%‡	n.r.	PubMed
Berezin et al., 2014^29	2011–2012	Cross-sectional	Adolfo Lutz Institute	Household contacts of children with pertussis	> 10 y	7.9%¶	n.r.	PubMed
Bellettini et al., 2014^31	2011–2013	Case series	One hospital clinic	Suspected cases, Santa Casa de Misericórdia Porto Alegre	> 10 y	9.3%‡	10–19y: 8.1% 40–59y: 1.2%	SciELO
Torres et al., 2015^25	2007–2013	Cross-sectional	SINAN	Confirmed cases, Paraná State	> 10 y	13.4%‡	10–19 y: 5.2% 20–49y: 7.7% ≥65 y: 0.5%	PubMed
Cunegundes et al., 2015^30	2011	Cross-sectional	Pediatric department of one tertiary hospital	Paediatric healthcare workers	> 21 y	6.4%¶	n.r.	PubMed
Pimentel et al., 2015^32	2010–2011	Cross-sectional	10 outpatient clinics	Suspected cases	> 10 y	5.2%^¶	n.r.	PubMed
Lima et al., 2016^11	2009–2013	Cross-sectional	Population of Vitória municipality	Confirmed cases, Vitória da Conquista (city)	> 10 y	10.3%‡	10–14 y: 2.9% (I case) 20–39 y:7.7% (3 cases)	Google Scholar
Verçosa and Pereira, 2017 ^27	2005–2015	Cross-sectional	SINAN	Confirmed cases, Alagoas state	> 10 y	14.0%‡	10–19 y: 9.0% 20–49 y:5.0%	Google Scholar
Fernandes et al., 2018^28	2001–2015	Surveillance	SINAN – CVE-SP	All cases reported^§, São Paulo state	> 10 y	13.6%‡ (all study period) 13.7%‡ (2007–2015)	10–20 y: 4.3% >20 y:9.3%	PubMed
Chile
National level data
Lima et al., 2015^33	1932–2010	Time series	National Epidemiological Surveillance System, Epidemiological Statistics Yearbooks	All cases reported^§, all country	> 10 y	0.16–0.41 (per 100,000) (incidence rate for the period 2001–2010)	incidence rates per 100,000 for the period 2001–2010: 10–19 y:0.41 20–44 y:0.30 >45 y:0.16	PubMed
Colombia
Regional level data
Villareal et al., 2008^15	2008	Cross-sectional	Clínica Integral Sincelejo	Suspected cases between community living people, Sincelejo (city)	≥ 15 y	60%‡ (3 out of 5 cases)	10–19 y: 20% (I case) 20–59 y:40% (2 cases)	LILACS
Astudillo et al., 2011^36	2006–2007	Cross-sectional	SIVIGILA for Cali	Suspected cases and household contacts of confirmed cases, Southeast Cali (city)	> 15 y	66.7%‡	15–24 y: 30.6% 25–64 y:33.3%	Scopus
Ulloa-Virgüez, 2015^35	2010–2012	Cross-sectional	SIVIGILA	All cases reported^§, Antioquia, Nariño, Bogotá cases	>15 y	15.0%‡	15–44 y: 11.6% >44 y:3.4%	Scopus
Montilla-Escudero et al., 2016^34	2013 (outbreak)	Cross-sectional	SIVIGILA	Suspected cases, Antioquia	> 10 y	15.7%‡	n.r.	Scopus
Mexico
National level data
Conde-Glez et al., 2014^37	2010	Cross-sectional	National Institute of Public Health	National Health and Nutrition Survey, participants	> 10 y	40.4%–46.3%	n.r.	PubMed
Aquino-Andrade et al., 2017^38	2011–2014	Cross-sectional	11 hospital clinics	Confirmed cases aged <1 y and their household contacts	> 16 y	19.6%	n.r.	PubMed

*only data corresponding to age groups >10 years old are presented, even if data for younger ages have been reported in the corresponding study; **preferably by the WHO age-group definitions [adolescents 10–19 years, adults 20–59 years, and older adults ≥60 years] or anything close to that;†the database from which the corresponding publication was retrieved; ‡(percentage) among confirmed pertussis cases; ^§includes suspected and confirmed pertussis cases; ¶(percentage) among all participants (includes suspected, confirmed, and non-confirmed cases)

Abbreviations: CVE-SP. Centro de Vigilância Epidemiológica – São Paulo [São Paulo Satte Epidemiological Surveillance Center]; INE, Instituto Nacional de Epidemiología [(Bacteriology Service of the) National Institute of Epidemiology]; LACEN, Laboratório Central do Mato Grosso do Sul [Central Laboratory for Public Health]; n.r. not reported PW, pregnant women; SINAN, Sistema de Informação de Agravos de Notificação [System for Notifiable Diseases]; SINAVE, Sistema Nacional de Vigilância Epidemiológica [Argentinean National Epidemiological Surveillance System]; SIVIGILA, Sistema Nacional de Vigilancia en Salud Pública [National Public Health Surveillance System]; y, year(s)

Figure 1. PRISMA Flow diagram of studies selection

Table 2. Definitions of pertussis cases, and diagnostic procedures reported in respective studies

Author, year^Ref	Disease definition	Diagnostic procedure (% of confirmed cases*)
Argentina
Hozbor et al., 2009^10	Clinical case Cough lasting ≥2 weeks with ≥1 of the symptoms: coughing paroxysms, inspiratory whoop, or post-tussive vomiting. Confirmed case a person with acute cough illness of any duration, and a positive culture for B. pertussis or a case that meets the clinical case definition and is confirmed by PCR, or a case that meets the clinical case definition and is confirmed by serology, if the last vaccine dose was received at least four years ago. A significant increase of overall antibody titer against B. pertussis whole cell (sonicated) in paired sera is used as criteria for serological confirmation or a case that meets the clinical case definition and is directly epidemiologically linked to a laboratory confirmed case.	n.r.
Kusznierz et al., 2014^20	Convulsive cough Cough of ≥7 days duration, paroxysmal or not, with inspiratory stridor or inducing vomiting. Confirmed case Clinically compatible patient with convulsive cough. Index case Patient with convulsive cough and confirmed pertussis by PCR. Symptomatic contact Patient with manifestations of convulsive cough. ‘Primary’ were if symptoms began ≥7 days before the index case, and ‘secondary’ if the onset of symptoms was at least 7 days after the index case. The primary cases were considered as the source of infection.	PCR (100%)
Romanin et al., 2014^39	Suspected case Cough lasting ≥2 weeks with ≥1 of the symptoms: coughing paroxysms, inspiratory whoop, or post-tussive vomiting Confirmed case Suspected case with laboratory isolation of B. pertussis	Culture (n.r.) PCR (n.r.) Serological (n.r.)
Lavayén et al., 2017^21	<6 months. All acute respiratory infections with ≥1 symptom of: apnea, cyanosis, inspiratory stridor, vomiting after coughing or paroxysmal cough 6 months–11 years. Cough lasting ≥14 days, accompanied by ≥1 symptom of: paroxysmal cough, inspiratory stridor or vomiting after cough without other apparent cause >11 years. persistent cough lasting ≥14 days without other accompanying symptomatology	PCR (79%) PCR + Culture (19%) PCR + Culture + ELISA (2%)
Brazil
Bellettini et al., 2014^31	n.r.	PCR (100%)
Berezin et al., 2014^29	n.r.	PCR (82.1%) Culture (7.1%) PCR + Culture (25.0%)
Druzian et al., 2014^22	Suspected case Dry cough lasting ≥2 weeks and ≥1 of: paroxysmal cough, inspiratory whoop, post-cough vomiting, having a history of contact with a pertussis case confirmed by clinical criteria. Confirmed case Laboratorial criteria: isolation of Bordetella pertussis Epidemiological criteria: suspected case which has had contact with a pertussis confirmed case by laboratory testing, between the beginning of the catarrhal period up to 3 weeks after onset of the paroxysmal period Clinical criteria: suspected case with leukocytosis (> 20,000 leukocytes/mm^3) and absolute lymphocytosis (> 10,000 leukocytes/mm^3) and negative or not performed culture; and absence of epidemiological linkage; and no confirmation of another etiology.	Laboratory criteria-Culture (7.6%) Epidemiological linkage (22.7%) Clinical criteria (68.1%)
Falleiros Arlant et al., 2014^23	WHO-CDC definition	Culture (n.r.) PCR (n.r.)
Willemann et al., 2014^12	Case Cough and ≥1 of: paroxysmal cough, winch inspiratory or vomiting.	Laboratory criteria (n.r.) Epidemiological (n.r.) Clinical criteria (n.r.)
Cunegundes et al., 2015^30	n.r.	ELISA (positive if Bordetella pertussis-IgG > 62.5 IU/mL)
Guimarães et al., 2015^24	Confirmed case Laboratorial criteria: isolation of Bordetella pertussis using culture of PCR Epidemiological criteria: suspected case which has had contact with a pertussis confirmed case by laboratory testing, between the beginning of the catarrhal period up to 3 weeks after onset of the paroxysmal period Clinical criteria: suspected case with leukocytosis (> 20,000 leukocytes/mm^3) and absolute lymphocytosis (> 10,000 leukocytes/mm^3) and negative or not performed culture; and absence of epidemiological linkage; and no confirmation of another etiology.	Laboratory criteria (36.6%) Epidemiological + clinical (15.5%) Clinical criteria (47.2%)
Pimentel et al., 2015^32	Confirmed case Cough and a positive culture, or Clinical case and positive PCR. Clinical case Dry cough lasting ≥2 weeks and ≥1 of: paroxysmal cough, inspiratory whoop, post-cough vomiting Epidemiological criteria A clinical case with negative culture and/or PCR who had contact with a pertussis confirmed case by culture and/or PCR	Culture (10%) PCR (70%) Epidemiological linkage (30%)
Torres et al., 2015^25	Confirmed case Clinical criteria: cough lasting ≥2 weeks and ≥1 of: paroxysmal cough, inspiratory, post-coughing vomiting Laboratory criteria: isolation of Bordetella pertussis using culture of PCR Epidemiological clinical criteria: suspected case which has had contact with a pertussis confirmed case by laboratory testing in the period of transmissibility.	Culture (n.r.) PCR (n.r.)
Lima et al., 2016^11	Suspected case^19,55 Dry cough lasting ≥2 weeks and ≥1 of: paroxysmal cough, inspiratory whoop, post-cough vomiting; or having a history of contact with a pertussis case confirmed by clinical criteria. Confirmed case Laboratorial criteria: isolation of Bordetella pertussis Clinical and epidemiological criteria: suspected case which has had contact with a pertussis confirmed case by laboratory testing, between the beginning of the catarrhal period up to 3 weeks after onset of the paroxysmal period Clinical criteria: suspected case with leukocytosis (> 20,000 leukocytes/mm^3) and absolute lymphocytosis (> 10,000 leukocytes/mm^3) and negative or not performed culture; and absence of epidemiological linkage; and no confirmation of another etiology.	Laboratory criteria – Culture (n.r.) Epidemiological (n.r.) Clinical criteria (n.r.)
Castro and Milagres, 2017^13	n.r.	n.r.
Silva et al., 2017^26	n.r.	n.r.
Verçosa and Pereira, 2017^27	n.r.	Culture (n.r.) PCR (n.r.)
Fernandes et al., 2018^28	Confirmed case Clinical criteria: cough lasting ≥2 weeks and ≥2 of: paroxysmal cough, inspiratory, post-coughing vomiting Laboratory criteria: isolation of Bordetella pertussis using culture of PCR Clinical and epidemiological criteria: suspected case which has had contact with a pertussis confirmed case by laboratory testing in the period of transmissibility.	2007–2015 Culture / PCR (79%) Epidemiological criteria (21%)
Chile
Lima et al., 2015^33	Suspected case Cough ≥2 weeks and ≥1: paroxysms of coughing, inspiratory whoop, post-tussive vomiting without other apparent cause, or cough of shorter duration if the features of the clinical case are depicted. And in <6 months, respiratory infection that causes apnea. Confirmed case A suspected case that is laboratory confirmed or epidemiologically linked by the laboratory. Compatible or clinical case Suspected case which could not be demonstrated or confirmed by epidemiological association or confirmed at the laboratory.	n.r.
Colombia
Villareal et al., 2008^15	Probable cases <3 months: presenting respiratory disease with repetitive episodes of paroxysmal cough or apneas accompanied or not of inspiratory stridor. 3 months–12 years: presenting respiratory disease with repeated episodes of sustained paroxysmal cough lasting ≥1 week or with repetitive episodes of intense paroxysmal cough accompanied by inspiratory stridor and cyanosis subsequent with any time of evolution. 12 years: presenting respiratory disease cough lasting ≥2 weeks accompanied or not by paroxysms, expectoration and vomiting. Confirmed case A probable case confirmed by PCR or DIF. Confirmed case by epidemiological link A probable case definition that is epidemiologically linked to a case confirmed by PCR or Direct Immunofluorescence.	Laboratory criteria (PCR or DIF) (1/5) Epidemiological linkage (4/5)
Astudillo et al., 2011^36	Suspected case Cough lasting ≥1 week and ≥1 symptom paroxysmal cough, inspiratory stridor, post-cough vomiting and no other apparent cause. Atypical case One of the following symptoms: respiratory infection picture without another symptom, paroxysm, coughing, prolonged cough followed by periods of apnea, cyanosis and inspiratory stridor.	PCR (33.8%) Culture (8.3%)
Ulloa-Virgüez., 2015^35	n.r.	PCR (n.r.) DIF (n.r.)
Montilla-Escudero et al., 2016^34	Confirmed case A probable case confirmed by Direct Immunofluorescence and subsequently verified by either PCR or ELISA.	PCR (n.a.†) DIF (n.a.†) ELISA (n.a.†)
Mexico
Conde-Glez et al., 2014^37	Positive cases Anti-pertussis toxin antibody concentrations ≥45 FDA U/ml were considered to be seropositive according to the manufacturer’s.	ELISA (100%)
Aquino-Andrade et al., 2017^38	Symptomatic contacts Cough lasting ≥ 1 week during the last 3 weeks before onset of the diagnosed case’s symptoms, regardless of the presence of fever and rhinorrhea.	PCR (100%)
WHO^1
	Clinical case Cough lasting ≥2 weeks and ≥1 of: paroxysmal cough, inspiratory whoop, post-cough vomiting. Laboratory criteria Isolation of B. pertussis from a clinical specimen Positive PCR assay for pertussis Positive paired serology
CDC^55
	Clinical case Cough lasting ≥2 weeks and ≥1 of: paroxysmal cough, inspiratory whoop, post-cough vomiting. Laboratory criteria Isolation of B. pertussis from a clinical specimen Positive PCR assay for pertussis Epidemiologic linkage Contact with a laboratory-confirmed case of pertussis

*the percentage of confirmed cases by respective diagnostic method, if reported in the corresponding publication; †not applicable because the confirmed cases were tested by >1 method (DIF, PCR, and/or ELISA)

Abbreviations: CDC, Centers for Disease Control; DIF, Direct Immunofluorescence; ELISA, Enzyme-Linked Immunosorbent Assay; n.a., not applicable; n.r. not reported; PCR, Polymerase Chain Reaction; WHO, World Health Organization; FDA, Federal Drug Administration

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