Immunogenicity and safety of the 13-valent pneumococcal conjugate vaccine in patients with immunocompromising conditions: a review of available evidence

Figures & data

Table 1. Underlying medical conditions for which both PCV13 and PPSV23 are currently recommended by ACIP for individuals ≥6 y of age.^14-16

Risk group	Underlying medical conditions
Immunocompetent	• Cerebrospinal fluid leak
	• Cochlear implant
Functional or anatomic asplenia	• Sickle cell disease/otherhemaglobinopathy
	• Congenital or acquired asplenia
Immunocompromised	• Congenital or acquired immunodeficiency
	• HIV infection
	• Chronic renal failure
	• Nephrotic syndrome
	• Leukemia
	• Lymphoma
	• Hodgkin disease
	• Generalized malignancy
	• Iatrogenic immunosuppression
	• Solid organ transplant
	• Multiple myeloma

ACIP = Advisory Committee on Immunization Practices; PCV13 = 13-valent pneumococcal conjugate vaccine; PPSV23 = 23-valent pneumococcal polysaccharide vaccine.

Table 2. Overview of studies

				Study population			Main outcomes
Reference	Purpose of study	Study design	Country/Setting	Vaccination history	N^a	Age,^b y	Immunogenicity	Safety
Asplenia/sickle cell disease
Papadatou et al.^Citation23	Immunogenicity (serotypes 3, 9V, 19A, 19F, and 23F only) of one dose of PCV13 in patients previously vaccinated with PPSV23	Prospective cohort; immunogenicity evaluated 7 and 28 d postvaccination	Greece/Academic hospital	PCV7 vaccination 7 y prior; 1–4 doses of PPSV23 1–11 y prior	39	36.5 (19–48)	PCV13 induced serotype-specific increases in IgG antibody GMCs in previously vaccinated subjects. Reduced immunogenicity among subjects previously vaccinated with PPSV23 was time and dose dependent.	NR
Rezai et al.^Citation24	Immunogenicity of one dose of PCV13 and one dose of PPSV23	Randomized crossover; immunogenicity evaluated 8 weeks after second vaccination	Iran/Academic hospital	Vaccination with any pneumococcal vaccine >5 y prior	47	29.6 (20–44)	Mean IgG concentrations were significantly higher in subjects receiving PCV13 before vs after PPSV23.	NR
Nived et al.^Citation25	Immunogenicity (12 serotypes common with PPSV23 only) of one dose of PCV13	Prospective cohort; immunogenicity evaluated 4–6 weeks postvaccination	Sweden/Community hospital	PCV13 naive and PPSV23 naïve or >1 y prior; or PPSV23 <1 y prior if two or more serotype-specific IgG concentrations were <0.35 μg/mL	33	52 (22–80)	Serotype-specific IgG GMCs were higher in subjects receiving prior PCV13 and PPSV23 vs PPSV23 alone. PCV13 induced a booster response in those with previous PPSV23 vaccination.	NR
De Montalembert et al.^Citation22	Immunogenicity and safety of two doses of PCV13	Open-label, single arm, phase 3; immunogenicity evaluated 1 month postvaccination	France, Lebanon, United Kingdom, United States, Egypt, Italy, Saudi Arabia/NR	one or more doses dose of PPSV23 administered ≥6 months prior	158	13.3 ± 3.08	PCV13 elicited serotype-specific increases in IgG GMCs and OPA GMTs against all vaccine serotypes after one dose. Responses were generally comparable after each dose.	PCV13 was well tolerated and safety events were consistent with those previously reported for PCV13; no new safety concerns emerged during the study. Most AEs and SAEs were vaso-occlusive crises.
HIV infection
Bhorat et al.^Citation27	Immunogenicity and safety of three doses of PCV13 followed by one dose of PPSV23	Open-label, single arm, phase 3 study; immunogenicity evaluated 1 month postvaccination	South Africa, Romania/NR	Pneumococcal vaccine-naive	301	25.8 ± 16.7	One dose of PCV13 elicited significant increases in serotype-specific IgG GMCs and OPA GMTs compared with prevaccination. For most serotypes, IgG GMCs modestly increased with subsequent doses of PCV13 and after PPSV23.	PCV13 and PPSV23 were well tolerated; no new safety concerns emerged during the study.
Glesby et al.^Citation26	Immunogenicity and safety of three doses of PCV13	Open-label, single arm, phase 3; immunogenicity evaluated 1 month postvaccination	United States/Medical centers	One or more doses of PPSV23 administered ≥6 months prior	329	47.3 (19–73)	One dose of PCV13 elicited significant increases in serotype-specific IgG GMCs and OPA GMTs in PPSV23-prevaccinated subjects. For certain serotypes, antibody responses modestly increased with subsequent doses.	Rates of injection site redness and swelling and headache, fatigue, and vomiting after dose 3 were slightly higher in subjects who received two or more vs one previous dose of PPSV23.
Lombardi^Citation30	Immunogenicity and safety of two doses of PCV13 vs one dose of PPSV23	Prospective cohort with control group; immunogenicity evaluated 8, 24, and 48 weeks postvaccination	Italy/Infectious disease clinical centers	Pneumococcal vaccine-naive	100	PCV13, 43.9 ± 9.05; PPSV23, 45.6 ± 10.5	At 48 weeks, serotype-specific IgG GMCs were comparable for PCV13 and PPSV23.	PCV13 and PPSV23 were well tolerated; no new safety concerns emerged during the study.
Sadlier et al.^Citation28	Immunogenicity (12 serotypes common with PPSV23 only) of prime-boost immunization with PCV13 followed by PPSV23 vs PPSV23 alone	Randomized; immunogenicity evaluated 8 and 28 weeks postvaccination	Ireland/Ambulatory HIV clinic	NR	60	37 ± 10	Serotype-specific IgG GMCs and OPA GMTs (for select serotypes) increased following a prime-booster strategy with PCV13/PPSV23 vs PPSV23 alone.	NR
Ohtola et al.^Citation31	Immunogenicity (serotypes 14 and 23F only) of one dose of PCV13 followed by PPSV23 8 weeks later vs PPSV23 alone	Prospective cohort; immunogenicity evaluated 1 month postvaccination	United States/Academic hospital	PPSV23 >5 y prior or vaccine-naive	51	PPSV23, 55.2 (50–64); PCV13/PPSV23/HIV+, 54.8 (49–63); PCV13/PPSV23/HIV–, 55.6 (50–64)	Serotype-specific increases in IgG GMCs after PCV13/PPSV23 vs PPSV23 alone were similar. Immunogenicity in HIV+ PCV13/PPSV23 recipients was decreased compared with HIV-negative–matched controls.	NR
Ohtola et al.^Citation32	Immunogenicity as measured by serotype-specific (serotypes 14 and 23F only), total, and switched memory B cells of one dose of PCV13 followed by PPSV23 8 weeks later vs PPSV23	Prospective cohort; immunogenicity evaluated 1 week postvaccination	United States/Academic hospital	PPSV23 >5 y prior or vaccine-naive	48	PPSV23, 55.0 (51–59)^c; PCV13/PPSV23/HIV+, 54.0 (52–58)^c; PCV13/PPSV23/HIV–, 55.5 (52–58)^c	For HIV+ subjects, serotype-specific B cell concentrations were significantly lower with PCV13/PPSV23 vs PPSV23 alone.	NR
Rossheim et al.^Citation29	Immunogenicity (serotypes 3, 6A, 7F, and 19A only) of one dose of PCV13 in subjects with PPSV23 vaccination 1–3 vs >3 y prior	Prospective observational cohort; immunogenicity evaluated 1 month postvaccination	United States/HIV clinic	PPSV23 1–3 y and ≥3 y prior	96	44 (20–65)	Fold rise in serotype-specific IgG GMCs (serotypes 3, 7F, 19A) increased in subjects with a longer interval since PPSV23 vaccination.	NR
Farmaki et al.^Citation13	Immunogenicity and immunologic memory (serotypes 3 and 14 only) of one dose of PCV13 followed by one dose of PPSV23 12 months later in patients taking antiretroviral therapy	Prospective study; immunogenicity evaluated 1 month after each vaccination	Greece/Community hospital	PCV13-naive, PPSV23 vaccination >1 y prior	40	50.6 ± 8.6	Significant increases in serotype-specific IgG antibody concentrations were observed after combined vaccination (2-fold rise-fold rise observed 1 month after PCV13 vaccination alone). Significant increases in serotype-specific memory B cells^d were observed after PCV13 vaccination.	NR
Hematologic malignancies (leukemia, lymphoma, multiple myeloma)
Pasiarski et al.^Citation33	Immunogenicity of one dose of PCV13 in treatment-naive patients with CLL vs healthy subjects	Prospective cohort with control group; immunogenicity evaluated 1 month postvaccination	Poland/Community hospital	Pneumococcal vaccine-naive	39	CLL, 66 (47–79); control, 68.5 (54–83)	Antibody response (≥2-fold increase in serotype-specific IgG antibody concentrations compared with prevaccination) was reported in 58.3% of patients with CLL and 100% of healthy subjects.	NR
Svensson et al.^Citation34	Immunogenicity and safety of one dose of PCV13 vs PPSV23 in treatment-naive patients with CLL	Two-arm, randomized; immunogenicity evaluated 1 month postvaccination	Sweden/Hematology units	Pneumococcal vaccine-naive or pneumococcal vaccination >5 y prior	128	69 (46‒87)	OPA GMTs elicited by PCV13 were higher than those elicited by PPSV23 for 10 of 12 serotypes common to both vaccines.	38% of patients reported AEs, all of which were grades I or II. No vaccine-related SAEs were reported.
Andrick et al.^Citation35	Immunogenicity of one dose of PCV13 in patients with CLL ± concomitant ibrutinib	Prospective cohort; immunogenicity evaluated 1 month postvaccination	United States/Academic hospital	Pneumococcal vaccination >2 y prior	8	69.5 (53–77)	Antibody responses (≥2-fold increase in postvaccination serotype-specific IgG antibody concentrations over baseline levels of three serotypes) were observed in all patients with CLL who were not treated with ibrutinib and none of those who were.	NR
Small et al.^Citation40	Immunogenicity (serotypes 1, 3, 4, 6B, 7F, 14, 18C, 19F, and 23F only) and safety of three doses of PCV13 in HSC recipients	Prospective cohort; immunogenicity evaluated after reaching pre-set immunologic milestones (T cell and Ig thresholds)	United States/Academic hospital	NR	59	39 (3–68)	Antibody response (seroconversion or 3-fold rise in serotype-specific IgG antibody concentrations) was 73%, including 87% of patients aged <21 y at HCT and 67% of patients aged >21 y. Response correlated with higher levels of circulating CD4+, CD45RA+ T cells and CD27+, IgM– memory B cells.	No SAEs were observed.
Bahuaud et al.^Citation37	Immunogenicity (serotypes 4, 6B, 9V, 14, 18C, 19F, 23F only) of one dose of PCV13 in patients with MM	Prospective cohort; immunogenicity evaluated 1, 6, and 12 months postvaccination	France/Community hospital	Pneumococcal vaccine-naive	20	62 (50‒74)	At 1 month post-vaccination,12 (60%) patients were responders by IgG GMCs (>2-fold increase from baseline and >1 µg/mL antibody concentration) and eight were responders by OPA (>4-fold increase from baseline and titer ≥LLOQ). At 6 and 12 months, only six and two responders, respectively, had persistent immunity by OPA responder criteria.	NR
Locke et al.^Citation36	Immunogenicity (serotypes 1, 3, 4, 5, 6B, 7F, 9V, 14, 18C, 19, and 23F only) and safety of up to three doses of PCV13 in patients with MM receiving autologous hematopoietic cell transplant	Prospective cohort; immunogenicity evaluated 3 months post-transplant	United States/Academic hospital	NR	6	Adults	All patients who received pre- and post-transplant vaccinations were responders by IgG levels (significantly greater fold changes in PCV13 serotype-specific IgG titers compared with non-PCV13 serotype IgG levels).	PCV13 was well tolerated and safety events were consistent with those previously reported for PCV13. No new safety concerns emerged during the study.
Cordonnier et al.^Citation39	Immunogenicity and safety of four doses of PCV13 followed by one dose of PPSV23 in HSC recipients	Prospective cohort; immunogenicity evaluated 1 month after each dose	Europe, Canada, United States/NR	No pneumococcal vaccination since HSC transplant	216	42.0 (2–71)	Serotype-specific IgG GMCs and OPA GMTs increased in all patients after dose 1. IgG GMCs and OPA GMTs increased after dose 4 compared with after dose 3 (except for serotype 3 IgG GMCs in the pediatric group). Immunity remained stable after PPSV23 administration. Pediatric patients tended to have numerically higher GMCs than adults after each PCV13 dose and after PPSV23.	Local and systemic reactions were more frequent after dose 4 vs dose 3 of PCV13. Six possible vaccine-related SAEs were reported: facial diplegia (14 d after PCV13 dose 1), injection site erythema and pyrexia (1 d after PCV13 dose 2), two episodes of autoimmune hemolytic anemia in a single patient (18 and 116 d after PCV13 dose 3), Guillain-Barré syndrome (29 d after PCV13 dose 4 and 1 d after PPSV23), and cellulitis (2 d after PPSV23).
Shah et al.^Citation38	Immunogenicity (serotypes 14, 19F, and 23F only), incidence, time to vaccination, and safety for three doses of PCV7/PCV13 with 1–2 booster doses (for nonresponders)	Retrospective cohort; immunogenicity evaluated after dose 3 and 1–2 booster dose(s) 1 month apart	United States/Academic hospital	NR	58	34 (0.9–64)	30 (53%) patients achieved a serotype-specific IgG response (seroconversion or ≥3-fold rise in GMCs) to all three serotypes (serotypes 14, 19F, 23F). Among initial nonresponders who were revaccinated one or more doses all evaluated subjects responded.	PCV13 was well tolerated; no new safety concerns emerged during the study.
Autoimmune/rheumatologic disorders
Kantso et al.^Citation41	Immunogenicity (12 serotypes common with PPSV23 only) and safety of one dose of PCV13 or PPSV23 in patients with Crohn disease ± concomitant immuno-suppressive drugs	Randomized clinical study; immunogenicity evaluated 1 month postvaccination	Denmark/Academic hospital	Pneumococcal vaccine-naive	151	44 ± 14	Serotype-specific IgG GMCs were higher for PCV13 compared with PPSV23 and highest in the untreated group. Immune responses were impaired for patients on azathioprine or mercaptopurine ± TNF-α antagonist therapy.	Safety events were consistent with those reported previously; no new safety concerns emerged during the study.
Rakoczi et al.^Citation42	Immunogenicity and safety of one dose of PCV13 in patients with RA ± concomitant DMARD therapy (ETA vs ETA+MTX)	Prospective cohort with control group; immunogenicity evaluated 1 and 2 months postvaccination	Hungary/Academic hospital	Pneumococcal vaccine-naive	46	RA, 55.1 ± 10.4; control, 63.9 ± 9.8	IgG antibody concentrations significantly increased from pre- to 1 and 2 months postvaccination in RA and control groups and remained higher than baseline levels at 8 weeks postvaccination. Immune responses were significantly higher in the control groups not receiving ETA or ETA/MTX.	No clinically relevant AEs were reported in any patients.
Kapetanovic et al.^Citation47	Immunogenicity (serotypes 6B and 23F only) of one dose PCV13 in patients with RA ± concomitant MTX	Prospective cohort; immunogenicity evaluated 4–6 weeks postvaccination	Sweden/Academic hospital	Pneumococcal vaccine-naive	20	MTX, 67.4 (39.1–78.6); no DMARD, 67.3 (38.6–86.7)	Antibody responses (≥2-fold increase in postvaccination serotype-specific IgG antibody concentrations over baseline levels) was significant for 6B in the MTX treated group (evident in one patient only) and both 6B and 23F in the non-treated group.	NR
Caporuscio^Citation45	Immunogenicity and safety of one dose of PCV13 in patients with RA on immunosuppressive therapy vs healthy controls	Prospective cohort with control; immunogenicity evaluated 1 and 6 months postvaccination	Italy/Academic hospital	NR	44	RA, 62.1 ± 11; control, 63.7 ± 2	Postvaccination, 61% of patients receiving DMARDs had an antibody response (≥2-fold increase in antibody titer); protection was maintained through 6 months.	Mild systemic and local AEs (redness and/or swelling of injection site) were reported by 44% of vaccinated patients with RA and by 16% of healthy subjects.
Nived et al.^Citation43	Immunogenicity (serotypes 6B and 23F only) and safety of one dose of PCV13 in patients with systemic vasculitis ± immunosuppressive therapy	Prospective cohort with control; immunogenicity was evaluated at 4–6 weeks postvaccination	Sweden/Academic hospital	Pneumococcal vaccine-naive or PPSV23 >1 y prior	98	Vasculitis, 65 (22–85); control, 57 (17–85)	Serotype-specific IgG GMCs and the proportion of patients with IgG concentrations ≥1 µg/mL increased in all groups postvaccination but were lower in the vasculitis group compared with the control. Pre- and postvaccination OPA titers were lower in vasculitis patients compared with controls.	PCV13 was well tolerated; no new safety concerns emerged during the study.
Nagel et al.^Citation44	Immunogenicity (12 serotypes common with PPSV23 only) and safety of one dose of PCV13 in patients with SLE ± belimumab and/or DMARD therapy vs healthy controls	Prospective cohort with control group; immunogenicity evaluated 4–6 weeks postvaccination	Sweden/Academic hospital	Pneumococcal vaccine-naive or pneumococcal vaccination >5 y prior	68	SLE, 50.8; control, 43.6	Serotype-specific IgG GMCs increased significantly in patients with SLE and controls postvaccination, but IgG titers and fold increases were significantly lower among patients. No significant differences in postvaccination IgG GMCs or in fold increases were observed in belimumab-treated patients.	PCV13 was well tolerated; no new safety concerns emerged during the study.
Winthrop et al.^Citation46	Immunogenicity and safety of one dose of PCV13 in patients with moderate to severe psoriasis using tofacitinib	Open label vaccine substudy; immunogenicity evaluated 4 weeks postvaccination	United States/Academic hospital	Pneumococcal vaccine-naive	60	52 (23‒70)	GMFRs from baseline in serotype-specific OPA titers ranged from 8.3 to 101.9. GMTs ranged from 4.9 to 99.5 at baseline and from 66.1 to 2782.2 at 4 weeks.	37.7% of patients reported treatment-emergent AEs; no severe AEs or SAEs were reported.
Solid organ transplant
Dendle et al.^Citation49	Immunogenicity and safety of one dose of PCV13 in kidney transplant recipients; measurement of donor-specific (anti-HLA) antibodies	Prospective cohort; immunogenicity evaluated 1 month postvaccination	Australia/Outpatient vaccination clinic	Pneumococcal conjugate vaccine-naive; 77% had prior PPSV23	45	56.1 (47.0‒63.9)	Median increases in IgG GMCs from baseline ranged from 1.1- to 1.7-fold across the 13 serotypes included in PCV13; all patients had OPA GMTs ≥1:8 for three of four serotypes tested by this method.	PCV13 was well tolerated; no new safety concerns emerged during the study. No anti-HLA antibodies or transplant rejections were reported.
Sun et al.^Citation48	Immunogenicity (serotypes 6B, 14, 19F, 23F only) and safety of one dose of PCV13 in solid organ transplant candidates and recipients	Prospective cohort; immunogenicity evaluated 1 month postvaccination	Taiwan/Aca-demic hospital	NR	21	NR	At 1 month postvaccination, 58.3–75.0% of 13 patients with follow-up had significant antibody responses (≥2-fold increase in antibody levels from baseline) to each of the individual serotypes.	PCV13 was well tolerated; no new safety concerns emerged during the study.
Renal failure
Mitra et al.^Citation50	Immunogenicity and safety of one dose of PCV13 in patients with ESRD receiving dialysis	Prospective cohort; immunogenicity evaluated 2 months and 1 y postvaccination	United States/Academic hospital	Pneumococcal vaccination naive or >5 y prior	17	62.6 ± 9.05	Serotype-specific IgG GMCs were significantly increased for all serotypes at 2 months postvaccination compared with prevaccination. By 1 y, significant increases were evident only for serotypes 5, 6B, 18C, and 19F. Vaccine responses (≥2-fold increase in antibody concentration and concentration ≥1 µg/mL) to >75% of serotypes was shown in 53% at 2 months and 23.5% at 12 months postvaccination.	PCV13 was well tolerated; no new safety concerns emerged during the study.

AE = adverse event; CLL = chronic lymphocytic leukemia; DMARD = disease-modifying anti-rheumatic drug; ESRD = end-stage renal disease; ETA = etanercept; GMC = geometric mean concentration; GMFR = geometric mean fold rise GMT = geometric mean titer; GVHD = graft vs host disease; HLA = human leukocyte antigen; HSC = hematopoietic stem cell; Ig = immunoglobulin; LLOQ = lower limit of quantitation; MM = multiple myeloma; MTX = methotrexate; N/A = not applicable; NR = not reported; OPA = opsonophagocytic assay; PCV7 = 7-valent pneumococcal conjugate vaccine; PCV13 = 13-valent pneumococcal conjugate vaccine; PPSV23 = 23-valent pneumococcal polysaccharide vaccine; RA = rheumatoid arthritis; SAE = serious adverse event; SLE = systemic lupus erythematosus; TNF = tumor necrosis factor

^aVaccinated subjects.

^bMedian (range) or mean ± SD, unless stated otherwise.

^cMedian (interquartile range).

^dRefers specifically to isotype-switched Ig memory B cells.

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