Original Studies
Effect of Macrolides and β-lactams on Clearance of
Bordetella pertussis in the Nasopharynx in Children With
Whooping Cough
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Yu-Mei Mi, MM,* Chun-Zhen Hua, MD,* Chao Fang, MM,† Juan-Juan Liu, MM,* Yong-Ping Xie, MM,*
Luo-Na Lin, MM,* and Gao-Liang Wang, MM*
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Objective: The purpose of the current study is to investigate the bactericidal
effect of macrolides and β-lactams on Bordetella pertussis (B. pertussis)
in the nasopharynx and provide guidance for treating macrolides-resistant
B. pertussis infections.
Methods: Patients with whooping cough was diagnosed by culture of naso-
pharynx swabs between January 2016 to December 2018. B. pertussis was
identified using specific antisera against pertussis and parapertussis. Drug
susceptibility test was carried out using the E-test method. The clearance
of B. pertussis in nasopharynx at 7 and 14 days into and posttreatment with
macrolides, and β-lactams was compared.
Results: A total of 125 B. pertussis samples were collected from patients
who received single antibiotic treatment. Among those isolates, 62.4%
(78/125) had high resistance with minimum inhibitory concentrations
greater than 256 mg/L for erythromycin and azithromycin. The MIC90 of
piperacillin, cefoperazone-sulbactam, meropenem, ampicillin, ceftriax-
one, ceftazidime and trimethoprim-sulfamethoxazole for these isolates
was <0.016, 0.094, 0.094, 0.19, 0.19, 0.25 and 0.75 mg/L, respectively.
The clearance rate with β-lactams treatment (68.8%, 44/64) was signifi-
cantly higher than that with macrolides treatment at 14 days posttreat-
ment (50.8%, 31/61) (χ2 = 4.18, P = 0.04). Macrolides had a better clear-
ance rate at 7 days posttreatment than β-lactams (χ2 = 4.49, P = 0.03) for
macrolides-sensitive isolates and a worse clearance rate for macrolides-
resistant isolates.
Conclusion: B. pertussis isolates had a high-resistant rate for macrolides
in our study. Macrolides are the first choice for treating pertussis caused
by macrolides-sensitive strains, and some β-lactams such as piperacillin
should be considered as alternative antibiotics for treatment of macrolides-
resistant B. pertussis infection.
Key Words: Bordetella pertussis, children, nasopharynx, β-lactams, mac-
rolides
(Pediatr Infect Dis J 2021;40:87–90)
Accepted for publication August 23, 2020.
From the *Division of Infectious Diseases, The Children’s Hospital, Zhejiang
University School of Medicine, National Clinical Research Center for Child
Health, Hangzhou, Zhejiang, P.R. China; †Department of Clinical Labora-
tory, The Children’s Hospital, Zhejiang University School of Medicine,
National Clinical Research Center for Child Health, Hangzhou, Zhejiang,
P.R. China.
Supported by Natural Science Foundation of Zhejiang Province, China (LGF
18H010001).
The authors have no conflicts of interest to disclose.
This study was approved by the Ethics Committee and the Institutional Board
of Privacy and Security at the hospital (2016-IRB-014) and was performed
under the institution’s opt-out passive consent policy.
This manuscript has not been published previously and is being submitted only
to The Pediatric Infectious Disease Journal.
Address for correspondence: Chun-Zhen Hua, MD, Division of Infectious Dis-
eases, The Children’s Hospital, Zhejiang University School of Medicine,
National Clinical Research Center for Child Health, 57 Zhugan Lane, Hang-
zhou 310003, P.R. China. E-mail: huachunzhen@zju.edu.cn.
Copyright © 2020 Wolters Kluwer Health, Inc. All rights reserved.
ISSN: 0891-3668/21/4002-0087
DOI: 10.1097/INF.0000000000002911
The Pediatric Infectious Disease Journal • Volume 40, Number 2, February 2021
Copyright © 2020 Wolters Kluwer Health, Inc. Unauthorized reproduction of this article is prohibited.
P ertussis (whooping cough) is a highly contagious respiratory
disease caused by Bordetella pertussis (B. pertussis). The inci-
dence of pertussis has reemerged in many countries despite the
high-vaccine coverage worldwide,1–3 which presents a great threat
to children’s health. Antibiotic treatment eliminates B. pertussis
from an infected child and thus controls the transmission between
contacts. In addition, antibiotics can reduce the duration of illness
and the severity of disease in children if treatment started early after
infection.4,5 The first choice of antibiotic for pertussis children is
macrolides;6,7 however, macrolides-resistant B. pertussis (MRBP)
has increased in recent years worldwide, especially in some regions
of China.8–10 Therefore, there is an urgent need to find an antibiotic
with bactericidal activity against B. pertussis. We have shown that
while cefuroxime has a relatively high minimum inhibitory con-
centration (MIC) against B. pertussis (12 mg/L), ampicillin, pipera-
cillin, ceftriaxone and cefoperazone-sulbactam have much lower
MICs, which are in the range of 0.047 to 0.38 mg/L.11 Thus, those
antibiotics with lower MICs could be bactericidal against B. pertus-
sis in vivo. In the current study, we compared the clearance rate of
β-lactams and macrolides against B. pertussis in the nasopharynx
and provided references for treatment and recommendations for the
quarantine period for pertussis children.
MATERIALS AND METHODS
Enrollment
Patients enrolled in this study were children receiving
treatment for pertussis in the Children’s Hospital of Zhe Jiang
University from January 2016 to December 2018. Inclusion cri-
teria included as follows: (1) Culture positive for B. pertussis in
nasopharynx during admission; (2) antibiotics (including those
received before admission) were only macrolides (erythromycin,
azithromycin or clarithromycin), and treatment had lasted 2 weeks
(2–3 curses of treatment when using azithromycin, and 3–4 days
treatment gap between courses) and (3) antibiotics (including those
used before admission) were only β-lactams (except the first and
second generation of cephalosporins).11 Exclusion criteria included
as follows: (1) The duration of antibiotics treatment was less than 2
weeks, or antibiotics treatment was not continuous even if the total
treatment period reached 2 weeks. (2) A combination of antibiotics
was used. (3) Patients did not finish once-a-week nasopharyngeal
swab culture during treatment. (4) Lost contact and unable to finish
follow-up swab culture after discharge from the hospital.
Bacterial Culture and Antibiotics Susceptibility Test
The collection of nasopharyngeal swab, inoculation and
bacteria culture was performed as described previously.11 B. per-
tussis strains were confirmed by positive slide agglutination with
specific antisera against B. pertussis and negative reaction with B.
parapertussis antiserum (Remel Europe Ltd., United Kingdom).
Samples that were positive for both sera were further analyzed by
high-throughput whole-genome sequencing.
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 Mi et al The Pediatric Infectious Disease Journal • Volume 40, Number 2, February 2021

Treatment
Nasopharyngeal swabs were taken from patients upon
admission. Antibiotics were prescribed before culture results were
obtained as follows: (1) For those patients who had been prescribed
with macrolides or β-lactams (except the first and second gener-
ation of cephalosporin) and had a short course of treatment (for
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treatment, and 5 were from the group of β-lactams treatment. There
was no significant difference for relapse rates between macrolides
group (11/61, 18.0%) and β-lactams group (9/64, 14.1%, χ2 = 0.37,
P = 0.55).
The clearance rate in these 125 patients and the drug resist-
ance of isolates is shown in Table 2. There was also no significant

erythromycin and β-lactams, shorter than 7 days; for azithromy-
cin, shorter than 5 days), or whose symptom was getting better, the
same antibiotics were prescribed. (2) For patients who have been on
macrolides and other β-lactams (except the first and second genera-
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difference in the clearance rate from the nasopharynx when treat-
ment started within 7 days or after 7 days of infection (χ2 = 0.89,
P = 0.34). The clearance rate in the group received macrolides for 14
days was significantly lower than that in group received β-lactams

tion of cephalosporin) for more than 7 days and symptoms have
not improved, cefoperazone-sulbactam or piperacillin-tazobactam
(if cefoperazone-sulbactam was not working) was prescribed. (3)
Erythromycin or azithromycin was prescribed if no antibiotics have
been prescribed before admission. Patients with positive bacte-
ria cultures were treated with antibiotics for 14 days,11 and naso-
pharyngeal swabs were taken at 7 and 14 days into treatment, and
7 and 14 days postdischarge from hospital during follow-up visits.
Statistical Analysis
Enumeration data were shown as number (percentage, %).
Comparisons of enumeration data between groups were analyzed
using χ2 test or Fisher’s exact test. Normal distribution data were
presented as mean ± standard deviation. A comparison of nor-
mal distribution data between groups was analyzed using t-test.
Abnormal distribution data were presented using the median with
interquartile range. A comparison of abnormally distributed data
between groups was analyzed using the Mann-Whitney U test.
P < 0.05 was considered as statistically different.
RESULTS
Demographic Information
We have recruited a total of 125 pertussis children that fit
our criteria in our study. There were 64 males (51.2%, 64/125).
Age distribution was between 15 days and 9 years, 1 month with a
median age of 4.4 months (3.03, 9.51). There were 48.8% (61/125)
of patients that received macrolides, which included 50 cases of
erythromycin and 11 cases of azithromycin. The other 51.2%
(64/125) of patients received β-lactams, which included 23 cases of
cefoperazone-sulbactam, 11 cases of piperacillin-tazobactam and
30 others that received ceftriaxone, cefodizime, cefdinir, cefixime,
amoxicillin-clavulanate or ampicillin-sulbactam. There were no
significant differences in age (z = 1.21, P = 0.23), sex (χ2 = 1.78,
P = 0.18) or period before admission (z = 1.85, P = 0.06) between
the 2 groups treated with macrolides and β-lactams.
(χ2 = 4.18, P = 0.04); treatment with macrolides had higher clear-
ance rate for macrolides-sensitive B. pertussis (MSBP) than MRBP
(7 days into treatment, χ2 = 9.35, P = 0.002; 14 days into treatment
χ2 = 20.11, P < 0.001; 7 days posttreatment χ2 = 15.99, P < 0.001;
14 days posttreatment χ2 = 6.79, P = 0.009). There was no differ-
ence for clearance rate against MSBP by β-lactams or macrolides
treatment (7 days starting treatment χ2 = 0.50, P = 0.48; 14 days
into treatment χ2 = 1.49, P = 0.22; 14 days posttreatment χ2 = 3.09,
P = 0.08) except β-lactams treatment has a lower clearance rate at 7
days posttreatment (χ2 = 4.49, P = 0.03). The clearance rate against
MRBP was significantly higher in the β-lactams group than that in
the macrolides group (7 days into treatment, χ2 = 7.57, P = 0.006;
14 days into treatment χ2 = 18.55. P < 0.001; 7 days posttreatment
χ2 = 16.12, P < 0.001; 14 days posttreatment χ2 = 5.95, P = 0.01).
DISCUSSIONS
There were increased reports on MRBP in recent years, espe-
cially in China that had the highest rate of resistant isolates with
the highest MICs.8–11 Our results showed that 62.4% of the isolates
had MICs greater than 256 mg/L, which was consistent with our
previous finding (75.4%) and a study from Shanghai (57.5%).9,11
Nonetheless, the current recommendation for treating B. pertussis
is still macrolides.6,7 Treatment with macrolides for MSBP infec-
tion could reduce symptoms and shorten disease duration if treat-
ment was started at an early stage after infection.5 Symptoms in
some patients with MRBP infection were improved by macrolides
treatment, probably by inhibiting toxin production from bacteria by
macrolides.12 However, relapse of infection was very common. We
also found that most bacteria colonies recovered from nasopharyn-
geal swabs appeared dusty like after antibiotics treatment, which
indicates that antibiotics treatment may have changed the physiol-
ogy of these bacteria.
Pertussis is a highly contagious respiratory disease and can
spread from respiratory droplets containing bacteria colonized in

Drug Susceptibility Tests TABLE 1. MIC Values for 10 Antibiotics in 125

As shown in Table 1, we determined MICs in these 125 iso- B. Pertussis Isolates
lates for 10 antibiotics. There were 62.4% (78/125) isolates that had
MIC Min MIC Max MIC50* MIC90†
MICs higher than 256 mg/L to erythromycin and azithromycin. On Antimicrobial Agent (mg/L) (mg/L) (mg/L) (mg/L)
the other hand, all isolates were sensitive to piperacillin and had
MICs lower than 0.016 mg/L. Erythromycin (125) 0.023 >256 >256 >256
Azithromycin (125) <0.016 >256 >256 >256
SXT (125) 0.002 1.5 0.19 0.75
Treatment Outcomes Ampicillin (94) 0.023 0.5 0.094 0.19
Symptoms, including paroxysmal cough, posttussive vomit- Piperacillin (125) <0.016 <0.016 <0.016 <0.016
ing, and apnea, became better in 80.0% (100/125) patients after Cefuroxime (33) 2 16 6 12
treatment for 2 weeks. There was no significant difference in the Ceftazidime (31) 0.023 0.5 0.094 0.25
rate of improvement between the group received macrolides (47/61, Ceftriaxone (125) 0.047 0.38 0.094 0.19
Cefoperazone-sulbactam (125) <0.016 0.38 0.032 0.094
77.0%) and those received β-lactams (53/64, 82.8%) (χ2 = 0.65, Meropenem (125) 0.006 0.25 0.047 0.094
P = 0.42). Twenty patients (20/125, 16.0%) had worse paroxysmal
*MIC50, MIC at which 50% of the isolates tested are inhibited.
cough within 1 week after finishing the first treatment and had been †MIC90, MIC at which 90% of the isolates tested are inhibited.
readmitted into the hospital. Fifteen of these 20 (75.0%) patients had MIC indicates minimum inhibitory concentration; SXT, trimethoprim-sulfameth-
MRBP infections, in which 10 were from the group of macrolides oxazole.

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 The Pediatric Infectious Disease Journal • Volume 40, Number 2, February 2021 Effect of Antibiotics Against B. pertussis

TABLE 2. Drug Resistance Rate and Clearance Rate of B. Pertussis by Treatment With Different Antibiotics

Clearance Rate in Nasopharynx % (n)

Antibiotics Age Median Days of History 7 d Into 14 d Into 7d 14 d

for Treatment Isolates (n) Male (n) (IQR), mo Median (IQR) Treatment Treatment Posttreatment Posttreatment
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Macrolides 61 28 4.0 (2.8, 6.3) 8 (6, 12) 18.0 (11) 50.8 (31) 73.7 (45) 86.9 (53)
Macrolides-sensitive (30)* 14 3.9 (2.8, 5.8) 8 (6, 11) 33.3 (10) 80.0 (24) 96.7 (29) 100 (30)
Macrolides-resistant (31)† 14 4.0 (2.7, 6.9) 9.5 (6.5, 25.3) 3.2 (1) 22.6 (7) 51.2 (16) 74.2 (23)
β-lactams 64 38 4.4 (3.0, 9.5) 8 (8, 14) 26.6 (17) 68.8 (44) 85.9 (55) 92.2 (59)
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Macrolides-sensitive (17)‡ 9 4.7 (3.4, 5.2) 10 (8, 11) 23.5 (4) 58.8 (10) 70.6 (12) 82.4 (14)
Macrolides-resistant (47)§ 29 4.8 (3.3, 10.24) 10 (8, 25) 27.7 (13) 72.3 (34) 91.5 (43) 95.7 (45)
*Longest carriage time 35 d.
†Longest carriage time 81 d.
‡Longest carriage time 49 d.
§Longest carriage time 56 d.
IQR indicates interquartile range; MSBP, macrolides-sensitive B. pertussis; MRBP, macrolides-resistant B. pertussis.

the nasopharynx. Thus, we have evaluated the outcome of treat-
ments by the clearance rate of B. pertussis in the nasopharynx. We
found that the clearance rate for MSBP by macrolides at 7 days
and 14 days into treatment was 33.3% and 80.0%, respectively. In
contrast, the clearance rate for MRBP was only 3.2% and 22.6%
at the same time points. It suggests that macrolides should not be
prescribed for pertussis caused by MRBP. For MSBP, macrolides
had better bactericidal activity than β-lactams in vivo; however, the
7-day course of macrolides is not enough to clear all B. pertussis
strains in the nasopharynx and will lead to relapse.13–15 Of the 20
patients whose symptoms relapsed after the first 14 days of treat-
ment, 3 were positive for B. pertussis again after the second admis-
sion, which also showed that adequate course of treatment is very
important for bacteria clearance. Therefore, a treatment plan for at
least 14 days is advised strongly.
There were very few β-lactams susceptibility tests against
B. pertussis worldwide. Our study showed that MICs of ampicillin,
ceftriaxone, ceftazidime, cefoperazone-sulbactam and meropenem
were lower than that of other antibiotics tested here. Piperacillin
had a MIC lower than 0.016 mg/L for all strains. Furthermore, we
showed that the clearance rate of the group received a combina-
tion of these β-lactams was higher against B. pertussis at 14 days
into treatment comparing to that of the group received macrolides,
suggesting that these β-lactams can be used to treat pertussis in
children in regions like China where MRBP is circulating. There
was no difference in the clearance rate for β-lactams against MSBP
and MRBP. Piperacillin, which had high antibacterial activity in
vitro, also cleared B. pertussis in nasopharynx very well.11 It is
worth considering a multicenter study to test whether piperacillin
should be used as the first choice of antibiotics in areas with a lot
of MRBP isolates. Trimethoprim-sulfamethoxazole is not suitable
for infants younger than 2 months.16 The MIC of trimethoprim-sul-
famethoxazole in our study was higher than that of other β-lactams.
Nevertheless, there is no reference for the MIC values of trimeth-
oprim-sulfamethoxazole in the Clinical and Laboratory Standards
Institute; thus, the effect of this antibiotic against B. pertussis still
needs to be studied.17
As shown in Table 2, the clearance rate of β-lactams was
lower against MSBP, but significant higher against MRBP than that
of macrolides. Thus, it is important to promote the effectiveness of
β-lactams, such as piperacillin against B. pertussis in China, where
there are many MRBP isolates. We have shown previously that a
96% (24/25) clearance rate against B. pertussis in nasopharynx at 2
weeks treatment can be achieved by using cefoperazone-sulbactam
or piperacillin, which was much higher than what we have observed
in the group that received β-lactams in the current study (68.8%,
44/64). The reason could be multiple β-lactams were used in the
present study, and only half of those were cefoperazone-sulbactam
and piperacillin. It also suggested that cefoperazone-sulbactam
and piperacillin might be better for clearing B. pertussis than other
β-lactams in nasopharynx. In addition, the limited sample number
might have also had an effect on our results.
It has been shown that the prescription of antibiotics at an
early stage of infection (less than 7 days) could significantly reduce
symptoms of pertussis patients and shorten disease duration.4,5
We tested whether early antibiotics prescription can eliminate
B. pertussis faster from colonization. It turned out that there was
no difference in the clearance rate when antibiotics were prescribed
within or after 7 days of disease onset. There were also patients
who had mild symptoms but were still positive for B. pertussis by
nasopharyngeal swab. Some patients even carried B. pertussis for
35 to 81 days. The presence of symptomless patients with coloniz-
ing B. pertussis suggested that antibiotics might have reduced the
toxin production in B. pertussis, which needs to be investigated in
future studies.
In conclusion, isolates of B. pertussis are highly resistant
to macrolides in our region. Treatment with macrolides is the first
choice for MSBP infection, and it needs to be used for at least 2
weeks to clear colonization of B. pertussis in the nasopharynx.
β-lactams, such as cefoperazone-sulbactam or piperacillin, should
be prescribed as alternative antibiotics for treating MRBP infec-
tion in regions with a high prevalence of MRBP isolates. B. pertus-
sis culture of nasopharyngeal swabs should be considered as one
of the standards to evaluate treatment outcomes. Limitations of our
study were that the research was only carried out in a single center,
the number of patients was small, and many types of β-lactams
have been used, which limited the analysis of the treatment effect
from a single antibiotic. Piperacillin showed the strongest in vitro
effect; however, we had to replace it with piperacillin-tazobactam
in our treatment due to a lack of piperacillin in the hospital. A
future study has been planned to investigate the effect of differ-
ent β-lactams on pertussis in children in multicenter with more
samples.
ACKNOWLEDGMENTS
We thank Ying-Jie Lu, Boston Children’s Hospital, for his
critical reading of this article.
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