A systematic review of the burden of pertussis disease in infants and the effectiveness of maternal immunization against pertussis

Figures & data

Table 1. Recommendations for maternal immunization with tetanus toxoid, reduced diphtheria toxoid, and acellular pertussis vaccine (Tdap) for each pregnancy in countries with a Tdap maternal immunization program (accurate to our knowledge at the time of writing).

Country	Recommendation for Tdap maternal immunization	Year of introduction	Reference
Argentina*	From 20 weeks gestation	2012	[17]
Australia*	Between 28 and 32 weeks gestation	2014	[18]
Bahamas	Tdap during each pregnancy	No information	[19]
Belgium	Tdap during each pregnancy	2012	[20]
Brazil*	A 20 weeks gestation	2017	[17]
Canada	During each pregnancy	2012	[21]
Chile	Between 27 and 36 weeks gestation	2016	[22]
Colombia*	From 26 weeks gestation	2012	[17]
Costa Rica	From 20 weeks gestation	2012	[17]
Czech Republic	Between 28 and 36 weeks gestation	2015	[23]
Denmark	From 32 weeks gestation	2019	[24]
El Salvador	From 28 weeks gestation	Not known	[25]
England*	From 16 weeks gestational	2016	[26]
French Territories (Mayotte)	From 18 weeks and ideally before 39 weeks gestation	2018	[27]
Honduras	Between 26 and 37 weeks gestation	2012	[17]
Hong Kong	Anytime in the second or third trimester, preferably before 35 weeks gestation	2019	[28]
India	Between 27 and 36 weeks gestation	2013	[29]
Ireland*	Between 27 and 36 weeks gestation	2013	[30]
Israel*	Pregnant women	2015	[31]
Italy*	In the third trimester (ideally 28 weeks gestation)	2017	[20]
Korea*	Between 27 and 36 weeks gestation	2014	[32]
Mexico*	After 20 weeks gestation	2012	[17]
Netherlands*	At 22 weeks gestation	2018	[33]
New Zealand*	Between 28 and 38 weeks gestation	2013	[34]
Panama*	Pregnant women	2012	[17]
Paraguay	Pregnant women		[17]
Peru*	Between 26 and 37 weeks gestation		[35]
Philippines*	Pregnant women and post-partum	2015	[36]
Portugal	Between 20 and 36 weeks gestation		[37]
Qatar	Between 27 and 36 weeks gestation	2017	[38]
Singapore*	Between 16 and 32 weeks gestation)	2017	[39]
Slovenia	As soon as possible after 24 weeks gestation	2017	[40]
Spain*	Pregnant women	2014	[37]
Switzerland*	Pregnant women	2013	[41]
Taiwan	Between 28 and 36 weeks gestation	2012	[42]
UK*	Between 28 and 38 weeks gestation	2012	[43]
Uruguay	Pregnant women		[17]
USA*	Between 27 and 36 weeks gestation	2012	[44]

UK, United Kingdom; USA, United States of America.

* Countries for which this review presents burden of disease results.

Figure 1. PRISMA flow diagrams for the two systematic literature searches performed for this review.

Figure 2. Pertussis disease incidence and hospitalization rates in infants <6 months of age in studies reporting results by person-time [57–59,63,69,78,81,83].

Figure 4. Pertussis-related hospitalizations per 100,000 population in infants <6 months of age [71,72,75,76,86].

Figure 3. Annual pertussis disease incidence per 100,000 population in infants <6 months of age [60,64–70,72–77,81,84,86].

Table 2. Key design features and results of studies describing the effectiveness of maternal pertussis immunization.

						Vaccine effectiveness (95% CI)
Country, reference	Population	Maternal vaccination recommendation (vaccine)	Study design; period	Sample size (no. of mothers vaccinated)	Outcome	Unadjusted	Adjusted
Australia Saul, 2018 [90]	Cases notified through public health units in local health districts Controls were born in a public hospital in the same district	28–32 weeks (Boostrix)	1:1 matched case–control study 16 August 2015–17 August 2016	Cases: n = 117 (52) Controls: n = 117 (72)	Laboratory-confirmed pertussis: culture, PCR or seroconversion in paired sera in the absence of recent vaccination.	<6 months: 51% (16–72) <3 months: 64% (18–84)	<6 months: 39% (−12 – 66) <3 months: 69% (13–89)
					Pertussis requiring hospitalization	6 months: 84% (47–95)	<6 months: 94% (59–99)
Spain Bellido-Blasco, 2017 [92]	Notified cases Controls: 3 for each case with anage difference <15 days	28–36 weeks and 15–89 days before delivery (NR)	Prospective matched case–control study 1 March 2015–29 February 2016	Cases n = 22 (5) Controls n = 66 (41)	PCR confirmed pertussis	<3 months: 92% (63–98)	<3 months: 90.9% (56.6–98.1)
United Kingdom Amirthalingam, 2014 [9]	Infants <3 months born 1 October 2012–3 September 2013 with laboratory confirmed pertussis	28–38 weeks or at least 7 days before delivery (Repevax)	Observational study (screening method; CPRD, PHE enhanced pertussis surveillance program, HES)	Cases n = 82 (15% vs 62% nationally)	Laboratory-confirmed pertussis: culture, PCR or serology	<2 months: 90% (82–95) <3 months: 91% (84–95)	-
United Kingdom Dabrera, 2015 [89]	Cases: infants <2 months with pertussis born during the study period Controls: 2 for each case, born consecutively after the case, from the same practice	Median 31.5 wks (cases), 33 wks (controls) (NR)	Case-(unmatched) control study (country-level, multiple primary care centers); 22 October 2012–11 July 2013	Cases: n = 58 (10) Controls: n = 55 (39)	Laboratory-confirmed pertussis: PCR or culture	<2 months: 91% (77–97)	<2 months: 93% (81–97)
United Kingdom Amirthalingam, 2016 [10]	Infants <3 months born 1 October2012–3 September 2013 with laboratory confirmed pertussis	28–38 weeks or at least 7 days before delivery (Repevax until 1 July 2014 then Boostrix-IPV)	Cohort study (screening method Immform, CPRD, PHE enhanced pertussis surveillance program); 2008–2013	n = 243 infants with pertussis (35% vs Immform: 50–62% Jan 2013-Dec 2015; CPRD: 78% Jan 2013; 70% Aug 2015)	Laboratory-confirmed pertussis using culture or PCR	<2 months: 90% (86–93) <3 months: 91% (88–94)	-
					Pertussis-related deaths	<3 months: 95% (79%–100%)	-
					Laboratory-confirmed pertussis (mothers vaccinated ≥ 28 days before delivery)	91% (88–94)	-
					Laboratory-confirmed pertussis (mothers vaccinated 7–27 days before delivery)	91% (80–96)	-
United States Baxter, 2017 [93]	Full term infants born at KPNC hospitals 2010–2015 to wP-vaccinated mothers	≥20 weeks (NR)	Retrospective cohort study (Kaiser Permanente Northern California claims database)	2 months follow-up n = 17 cases (1) 12 month follow-up n = 103 cases (22)	PCR-positive pertussis	<2 months 92.0% (57–100) <12 months 65% (45–79)	<2 months: 91.4% (19.5–99.1) <12 months: 69.0% (43.6–82.9)
United States Skoff, 2017 [91]	Cases: Full term Infants at least 2 days old 1 January 2011–31 December 2014 Controls: infants born at the same hospital aged <2 months on the case infant’s cough onset date	77% in the 3^rd trimester (Adacel, Boostrix)	Case–control study (multiple hospitals at 6 Emerging Infection Program Network sites)	n = 240 cases (17 in the 3^rd trimester) n = 535 controls (90 in the 3rd trimester)	Pertussis confirmed by culture, PCR or epidemiological link to a laboratory-confirmed case, or clinically compatible illness	-	<2 months: 77.7% (48.3–90.4)
					Pertussishospitalizations	-	<2 months: 90.5% (65.2–97.4)
United States Winter, 2017 [94]	Infants born 1 January 2011–Dec 2015 with known maternal vaccination status	76% during the third trimester (NR)	Retrospective cohort study (California public health surveillance)	n = 420 infants (354 during the 3^rd trimester)	Pertussis hospitalizations using clinical definition or laboratory confirmed. Mothers vaccinated in the 3rd trimester	<2 months: 75.4 (49.8–88.0)	<2 months: 52.1% (−0.16–80.3)
					Mothers vaccinated at any time during pregnancy	<2 months: 72.3 (49.0–85.0)	<2 months: 58.3 (14.9–79.6)
United States Becker-Dreps, 2018 [95]	Singleton deliveries >26 weeks gestation Jun 2010-Dec 2014	pregnancy onset to 2 weeks prior to delivery (NR)	Cohort study (Truven Market-Scan claims databases) Follow-up until 18 months	n = 332 (22)	Either inpatient or outpatient diagnosis + appropriate antibiotic treatment within 7 days	<6 months: 55% (24–73)	<6 months: 46% (6–69)
				n = 151 (6)	Inpatient-only cases (95% CI)	<6 months: 81% (40%–94%)	<6 months: 75% (20%–92%)
				n = 449 (30)	Possible pertussis: also includes outpatients with a cough diagnosis + a claim for a pertussis laboratory test, + appropriate antibiotic treatment within 7 days	<6 months: 49% (21–66)	<6 months: 35% (−2–59)
Columbia Hincapie-Palacio, 2018 [96]	Mothers recruited prior to vaccination at 8 urban hospitals Dec 2015–Apr 2016	Mean 28.59 ± 3.51 weeks (NR)	Cohort study 6 months follow-up	n = 745 vaccinated mothers (2 cases) n = 260 non-vaccinated mothers (0 cases)	Confirmed pertussis: met the case definition and PCR positive, or epidemiology linked to a laboratory-confirmed case, or confirmed by clinical criteria	Unable to be calculated due to low attack rate

ACIP, Advisory Committee on Immunization Practices; CI, confidence interval; CPRD, Clinical Practice Research Datalink; PHE, Public Health England; HES, Hospital Episode Statistics; n, number of participants/cases; MI, maternal immunization; Tdap, reduced tetanus toxoid, diphtheria toxoid, and acellular pertussis vaccine; PCR, polymerase chain reaction; VE, vaccine effectiveness.

Adacel, reduced antigen content diphtheria-tetanus-acellular pertussis vaccine; Boostrix, reduced antigen content diphtheria-tetanus-acellular pertussis vaccine; Repevax, reduced antigen diphtheria-tetanus-acellular pertussis-inactivated poliovirus vaccine.

Table 3. Key design features and results of studies describing the impact of maternal pertussis immunization.

Country, reference	Maternal vaccination coverage	Study design; period	Sample size	Outcome	% Reduction (95% CI)
Argentina Vizzotti, 2016 [88]	High ≤50% Low = <50%	Surveillance study (Argentinean Health Surveillance System) Jan 2010–Dec 2013	5,657 cases	Confirmed pertussis: suspected illness positive by culture, PCR, or serology, or, an epidemiological link to a laboratory-confirmed case Suspected pertussis in infants <6: ARI and at least one of: apnea, cyanosis, stridor, post-tussive vomiting or paroxysmal cough	Reduction between high and low vaccination regions: <2 months: 51% (35%–67%; p = 0.001) 2–6 months: 44% (24%–66%)
				Deaths per 100,000 population	<12 months: 2.1 (year 2010); 9.8 (2011); 3.9 (2012) and 1.3 (2013).
				Case fatality rate	<12 months: 1.4 (year 2010); 2.7 (2011); 1.7 (2012) and 0.9 (2013).
United Kingdom Amirthalingam, 2014 [9]	64%	Observational study (screening method; CPRD, PHE enhanced pertussis surveillance program, HES) 1 January 2008–30 September 2013	90 cases	Percentage change in number of confirmed pertussis cases, 2013 vs 2012 (95% CI)	<1 month: −77% (−90% – −53%) 1 month: −77% (−84% – −67%) 2 months: −80% (−87% – −69%) 3–5 months: −65% (−79% – −41%) 6–1 months: −68% (−89% – −23%)
				Percentage in number of confirmed pertussis cases, 2013 vs 2011 (95% CI)	<1 month: −38% (−75 – 46) 1 month: −35% (−58 – 0) 2 months: −44% (−67 – 7) 3–5 months: 5% (−45 – 100) 6–11 months: 0% (−70 – 234%)
United Kingdom Amirthalingam, 2016 [10]	78% (Jan 2013) 70% (Aug 2015)	Cohort study (screening method; PHE); Oct 2012-Sept 2015	243 cases	Annual incidence (cases per 100,000 population) before maternal immunization (2009–2011) vs after (2013–2015)	<3 months: 62.5 (pre-vaccine) vs 60.4 (vaccine era) 3–5 months: 14.0 (pre-vaccine) vs 12.7 (vaccine era)

CPRD, Clinical Practice Research Datalink; PHE, Public Health England; HES, Hospital Episode Statistics.

Figure 5. Effectiveness of maternal Tdap vaccination against pertussis disease and hospitalizations in infants up to 6 months of age [9,10,89–95].

Figure 6. Plain language summary.

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