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Clinical Efficacy of Doxycycline for Treatment of Macrolide-Resistant antibiotics Article Clinical Efficacy of Doxycycline for Treatment of Macrolide-Resistant Mycoplasma pneumoniae Pneumonia in Children Hyunju Lee 1,2, Youn Young Choi 3, Young Joo Sohn 3 , Ye Kyung Kim 3, Mi Seon Han 4 , Ki Wook Yun 1,3 , Kyungmin Kim 2 , Ji Young Park 5 , Jae Hong Choi 6, Eun Young Cho 7 and Eun Hwa Choi 1,3,* 1 Department of Pediatrics, Seoul National University College of Medicine, Seoul 03080, Korea; [email protected] (H.L.); [email protected] (K.W.Y.) 2 Department of Pediatrics, Seoul National University Bundang Hospital, Seongnam 13620, Korea; [email protected] 3 Department of Pediatrics, Seoul National University Children’s Hospital, Seoul 03080, Korea; [email protected] (Y.Y.C.); [email protected] (Y.J.S.); [email protected] (Y.K.K.) 4 Department of Pediatrics, Seoul Metropolitan Government-Seoul National University Boramae Medical Center, Seoul 07061, Korea; [email protected] 5 Department of Pediatrics, Chung-Ang University Hospital, Seoul 06973, Korea; [email protected] 6 Department of Pediatrics, Jeju National University School of Medicine, Jeju 63241, Korea; [email protected] 7 Department of Pediatrics, Chungnam National University Hospital, Daejeon 35015, Korea; [email protected] * Correspondence: [email protected] Abstract: In areas with high prevalence of macrolide-resistant Mycoplasma pneumoniae (MRMP) pneumonia, treatment in children has become challenging. This study aimed to analyze the efficacy Citation: Lee, H.; Choi, Y.Y.; Sohn, of macrolides and doxycycline with regard to the presence of macrolide resistance. We analyzed Y.J.; Kim, Y.K.; Han, M.S.; Yun, K.W.; children with MP pneumonia during the two recent epidemics of 2014–2015 and 2019–2020 from Kim, K.; Park, J.Y.; Choi, J.H.; Cho, four hospitals in Korea. Nasopharyngeal samples were obtained from children with pneumonia E.Y.; et al. Clinical Efficacy of Doxycycline for Treatment of for MP cultures and polymerase chain reaction (PCR). Macrolide resistance was determined by Macrolide-Resistant Mycoplasma the analysis of 23S rRNA gene transition. Time to defervescence and to chest X-ray improvement pneumoniae Pneumonia in Children. were analyzed. Of 145 cases, the median age was 5.0 years and MRMP accounted for 59 (40.7%). Antibiotics 2021, 10, 192. https:// Among macrolide-susceptible MP (MSMP), 78 (90.7%) were treated with macrolides and 21 (35.6%) doi.org/10.3390/antibiotics10020192 in the MRMP group with doxycycline. In MRMP pneumonia, shorter days to defervescence (2 vs. 5 days, p < 0.001) and to chest X-ray improvement (3 vs. 6 days, p < 0.001) in the doxycycline group Academic Editor: Owen B. Spiller than in the macrolide group was observed, whereas no differences were observed among children Received: 23 January 2021 with MSMP pneumonia. Compared to macrolides, treatment with doxycycline resulted in better Accepted: 15 February 2021 outcomes with a shorter time to defervescence and to chest X-ray improvement among children with Published: 17 February 2021 MRMP pneumonia. Publisher’s Note: MDPI stays neutral Keywords: Mycoplasma pneumoniae; macrolides; drug resistance; doxycycline with regard to jurisdictional claims in published maps and institutional affil- iations. 1. Introduction Mycoplasma pneumoniae (MP) is an important cause for community-acquired pneu- monia in children and adults [1,2]. MP infections in children are known as mild and Copyright: © 2021 by the authors. Licensee MDPI, Basel, Switzerland. self-limiting; however, antimicrobial treatment is recommended in children with moderate This article is an open access article to severe lower respiratory tract infections [1,3,4]. distributed under the terms and MP is distinguished from other bacteria due to unique microbiologic characteristics, conditions of the Creative Commons including lack of a cell wall, which attributes to being intrinsically resistant towards beta- Attribution (CC BY) license (https:// lactams [5]. Therefore, antibiotics that act on the bacterial ribosome and inhibit protein creativecommons.org/licenses/by/ synthesis such as macrolides or tetracyclines or agents that inhibit DNA replication such as 4.0/). fluoroquinolones are active against MP [6,7]. Among these, macrolides are recommended Antibiotics 2021, 10, 192. https://doi.org/10.3390/antibiotics10020192 https://www.mdpi.com/journal/antibiotics Antibiotics 2021, 10, x FOR PEER REVIEW 2 of 11 Antibiotics 2021, 10, 192 2 of 11 as fluoroquinolones are active against MP [6,7]. Among these, macrolides are recom- mended as first-line treatment for MP pneumonia in children due to the potential toxici- ties of other agentsas first-line in children. treatment However, for MP in pneumonia cases with delay in children in defervescence due to the potential and clinical toxicities of other deterioration, agentsmacrolide-resistance in children. However, should inbe cases considered. with delay Delayed in defervescence effective treatment and clinical is deterioration, associated withmacrolide-resistance prolonged and/or more should severe be considered.presentation Delayed[8]. Macrolide-resistance effective treatment has is associated emerged worldwidewith prolonged with a relatively and/or high more prev severealence presentation in Asia, ranging [8]. Macrolide-resistance from 23.3% to over has emerged 84.8% [7]. Therefore,worldwide treatment with a with relatively the increa highse prevalence in macrolide-resistance in Asia, ranging has from become 23.3% chal- to over 84.8% [7]. lenging. Therefore, treatment with the increase in macrolide-resistance has become challenging. In this study, Inwe this aimed study, to wecompare aimed the to ef compareficacy of the macrolides efficacy of and macrolides doxycycline and in doxycycline in children with MPchildren pneumonia with MP treated pneumonia in the context treated of in no the information context of no regarding information macrolide regarding macrolide resistance, whichresistance, were retrospectively which were retrospectively tested and classified tested and as macrolide-sensitive classified as macrolide-sensitive MP MP (MSMP) and macrolide-resistant(MSMP) and macrolide-resistant MP (MRMP). MP (MRMP). 2. Results 2. Results 2.1. Patient Characteristics2.1. Patient Characteristics During the twoDuring epidemics the two of 2014–2015 epidemics and of 2014–2015 2019–2020, and 173 2019–2020, cases were 173 positive cases werefor positive for MP PCR or cultureMP PCR and or diagnosed culture and with diagnosed MP pneumonia. with MP Among pneumonia. 173 cases, Among 21 cases 173 cases, were 21 cases were excluded due excludedto at least due one to of at the least following: one of the concomitant following: steroids concomitant (n = 14), steroids underlying (n = 14), underlying disease (n = 12),disease date of (n last= 12), fever date not of lastspecified fever ( notn = specified7), and follow (n = 7),up and to other follow institution up to other institution (n = 3) (Figure(n 1).= 3)Additionally, (Figure1). Additionally,children treated children for less treated than for5 days less (macrolide than 5 days n (macrolide= 5, n = 5, doxycycline ndoxycycline = 2) were alson = excluded. 2) were also Finally, excluded. 145 Finally,cases were 145 casesincluded were in included the analysis; in the analysis; 103 103 (71.0%) during(71.0%) the during 2014–2015 the 2014–2015 season and season 42 cases and (29.0%) 42 cases from (29.0%) the 2019–2020 from the 2019–2020 season. season. Figure 1. FlowFigure diagram 1. Flow of cases diagram included of cases in theincluded study forin the comparison study for ofcomparison antibiotic responseof antibiotic between response macrolides be- and doxy- cycline in childrentween withmacrolidesMycoplasma and doxycycline pneumoniae pneumoniain children accordingwith Mycoplasma to macrolide pneumoniae resistance. pneumonia MP, Mycoplasma according pneumoniae . to macrolide resistance. MP, Mycoplasma pneumoniae. The demographics and clinical characteristics of cases included in this study are shown The demographicsin Table1. Amongand clinical 145 cases, characteristics 59 (40.7%) wereof cases male included and the medianin this agestudy was are5.0 years. There shown in Tablewas 1. noAmong difference 145 cases, of median 59 (40.7%) age between were male MRMP and andthe MSMPmedian groups. age was Eight 5.0 cases (5.5%) years. There washad no underlying difference diseases of median (neurologic age between disease, MRMPn = and 1; hematologic MSMP groups. disease, Eightn = 3; cardiac cases (5.5%) haddisease, underlyingn = 1; endocrinediseases (neurologic disease, n =disease, 1; gastrointestinal n = 1; hematologic disease, disease,n = 2). Amongn = the cases 3; cardiac disease,tested, n = 92.0% 1; endocrine (127/138) disease, were n MP = 1; PCR gastrointestinal positive, 62.7% disease, (32/51) n = 2). were Among anti-mycoplasma the cases tested,IgM 92.0% positive, (127/138) 48.3% were (57/118) MP PCR showed positive, anti-mycoplasma 62.7% (32/51) IgG were≥ 1:640,anti-myco- and 94.6% (35/37) plasma IgM positive,showed a48.3% four-fold (57/118) increase. showed The anti-mycoplasma median duration ofIgG fever ≥ 1:640, was 7 and days 94.6% and children in the MRMP pneumonia group had significantly longer duration of fever (8 days vs. 7 days, p value = 0.003). Median duration of cough was 15 days and there was no significant Antibiotics 2021, 10, 192 3 of 11 difference according to macrolide resistance. More than one-third of the cases showed lobar consolidation and 11.0% had parapneumonic effusion. There was no difference in radiologic
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