Mycoplasma genitalium infection: current treatment options, therapeutic failure, and resistance-associated mutations

Figures & data

Table 1 Clinical efficacy studies of tetracycline/doxycycline, alone or versus macrolides, for treatment of Mycoplasma genitalium infection

Reference	Year	Study type	Population	M. genitalium cases (n)	Tetracycline regimen(s) and M. genitalium microbiological cure	Macrolide regimen and M. genitalium microbiological cure
Horner et al^Citation10	1993	Prospective case–control study	164 men with/without NGU attending an STI clinic, UK	27 men	DOXY 200 mg d 1, 100 mg d 2–d 9 10/14 cured (71.4%)	Not applicable
Johannisson et al^Citation18	2000	Uncontrolled observational study	233 men and 85 women attending STI clinics, Sweden	18 men 3 women	TET 500 mg 12 hourly ×10 d 5/13 men cured (38.5%) 0/1 women cured (0%)	Not applicable
Gambini et al^Citation19	2000	Prospective study with treatment varying by room	201 men with/without NGU attending an STI clinic, Italy	53 men	DOXY 200 mg/day ×7 d 33/35 cured (94.3%)	AZM 1 g stat 14/17 cured (82.4%)
Falk et al^Citation17	2003	Uncontrolled observational study	519 men and 464 women attending an STI clinic, Sweden	34 men 26 women	DOXY 200 mg d 1, 100 mg d 2–d 9 or LYME 300 mg 12 hourly ×10 d Men: 6/16 cured (37.5%) Women: 4/14 cured (28.6%)	AZM 500 mg d 1, 250 mg d 2–d 5 Men: 16/16 cured (100.0%) Women: 20/20 cured (100.0%)
Björnelius et al^Citation20	2008	Uncontrolled observational study	152 men with NGU and 60 women with cervicitis attending 6 STI clinics, Norway and Sweden	152 men 60 women	DOXY 200 mg (d 1), 100 mg (d 2–d 9) Men: 13/76 cured (17.1%) Women: 10/27 (37.0%)	AZM 1 g stat Men: 33/39 cured (84.6%) Women: 15/17 cured (88.2%)
Mena et al^Citation21	2009	Randomized controlled trial	398 men with NGU attending an STI clinic, USA	78 men	DOXY 100 mg 12 hourly ×7 d 14/31 cured (45.2%)	AZM 1 g stat 20/23 cured (87.0%)
Schwebke et al^Citation22	2011	Randomized controlled trial	305 men with NGU attending 4 STI clinics, USA	94 men	DOXY 100 mg 12 hourly ×7 d (± tinidazole 2 g stat) 12/39 cured (30.8%)	AZM 1 g stat (± tinidazole 2 g stat) 30/45 cured (66.7%)
Manhart et al^Citation23	2013	Randomized controlled trial	606 men with NGU attending an STI clinic, USA	80 men	DOXY 100 mg 12 hourly ×7 d (+ AZM placebo) 8/27 cured (29.6%, mITT)	AZM 1 g stat (+ DOXY placebo) 15/38 cured (39.5%, mITT)

Abbreviations: M. genitalium, Mycoplasma genitalium; NGU, non-gonococcal urethritis; STI, sexually transmitted infection; DOXY, doxycycline; TET, tetracycline; LYME, lymecycline; AZM, azithromycin; d, day/days; mITT, modified intention to treat population.

Table 2 Clinical efficacy studies of fluoroquinolones, alone or versus macrolides, for treatment of Mycoplasma genitalium infection

Reference	Year	Study type	Population	M. genitalium cases (n)	Fluoroquinolone regimen(s) and M. genitalium microbiological cure	Macrolide regimen(s) and M. genitalium microbiological cure
Yasuda et al^Citation45	2005	Uncontrolled observational study	97 men with NGU attending a urology clinic, Japan	97 men	LVFX 100 mg 8 hourly ×7 d or 14 d TFLX 150 mg 8 hourly ×14 d GFLX 200 mg 12 hourly ×7 d or 14 d LVFX (7 d): 5/16 cured (31.3%) LVFX (14 d): 9/18 cured (50.0%) TFLX: 5/7 cured (71.4%) GFLX (7 d): 22/24 cured (91.7%) GFLX (14 d): 6/6 cured (100.0%)	Not applicable
Jernberg et al^Citation24	2005	Uncontrolled observational study	5,423 men and 4,683 women attending an STI clinic, Norway Patients were either symptomatic for STIs or contacts of patients diagnosed with urethritis, cervicitis, or M. genitalium infection	234 men 218 women	OFX 200 mg 12 hourly ×10 d MXF 400 mg daily ×7 d OFX: 25/45 cured (55.6%) MXF: 27/27 cured (100.0%)	AZM 1 g stat AZM 1 g on d 1 and d 5–d 7 AZM 500 mg daily d 1, 250 mg daily d 2–d 5 AZM 1 g stat: 144/183 cured (78.7%) AZM 1 g + 1 g: 28/38 cured (73.7%) AZM 1.5 g (first-line): 76/98 cured (77.6%) AZM 1.5 g (second/third-line): 8/23 cured (37.8%)
Bradshaw et al^Citation28	2006	Prospective case–control study	636 men with/without NGU attending an STI clinic, Australia	34 men	MXF 400 mg daily ×10 d (following AZM 1 g stat on basis of persistent urethral symptoms) 9/9 cured (100.0%)	AZM 1 g stat or AZM 1 g per week ×3 weeks 23/32 cured (71.9%)
Bradshaw et al^Citation25	2008	Uncontrolled observational study	1,538 men and 313 women attending an STI clinic, Australia Patients had NGU/epididymo-orchitis, cervicitis/PID, or were contacts of patients infected with M. genitalium	161 men 30 women	MXF 400 mg daily ×10 d (following AZM 1 g stat on basis of persistent urethral symptoms) 11/11 cured (100.0%)	AZM 1 g stat 101/120 cured (84.2%)
Takahashi et al^Citation44	2011	Uncontrolled observational study	87 men with NGU attending a urology clinic, Japan	5 men	LVFX 500 mg daily ×7 d 3/5 cured (60.0%)	Not applicable
Hamasuna et al^Citation49	2011	Uncontrolled clinical trial	169 men with NGU attending urology clinics, Japan	18 men	GFLX 200 mg 12 hourly ×7 d 15/18 cured (83.3%)	Not applicable
Ito et al^Citation47	2012	Uncontrolled clinical trial	89 men with NGU attending a urology clinic, Japan	14 men	STFX 100 mg 12 hourly ×7 d 11/11 cured (100.0%)	Not applicable
Terada et al^Citation26	2012	Uncontrolled retrospective study	257 women with M. genitalium positive cervicitis attending a gynecology clinic, Japan	257 women	MXF 400 mg daily ×7 d MXF 400 mg daily ×14 d LVFX 500 mg daily ×7 d LVFX 500 mg daily ×14 d STFX 200 mg daily ×7 d STFX 200 mg daily ×14 d MXF (7 d): 38/42 cured (90.5%) MXF (14 d): 42/42 cured (100.0%) LVFX (7 d): 12/22 cured (54.5%) LVFX (14 d): 15/21 cured (71.4%) STFX (7 d): 11/14 cured (78.6%) STFX (14 d): 12/13 cured (92.3%)	AZM 1 g stat AZM SR 2 g CAM 400 mg daily ×7 d CAM 400 mg daily ×14 d AZM 1 g stat: 36/42 (85.7%) AZM SR 2 g stat: 19/21 (90.5%) CAM (7 d): 13/20 (65.0%) CAM (14 d): 17/20 (85.0%)
Takahashi et al^Citation48	2013	Uncontrolled clinical trial	208 men with NGU attending a urology clinic, Japan	16 men	STFX 100 mg 12 hourly ×7 d 15/16 cured (93.8%)	Not applicable
Bissessor et al^Citation27	2015	Prospective cohort study	160 patients with M. genitalium infections attending an STI clinic, Australia	112 men 43 women	MXF 400 mg daily ×10 d 53/60 cured (88.3%)a	AZM 1 g stat 95/155 cured (61.3%)

Notes:

a Six of the seven patients who failed MXF therapy were treated with pristinamycin at a dose of 1 g 6 hourly ×10 d; these six patients were M. genitalium polymerase chain reaction-negative at 28 d post-pristinamycin therapy.

Abbreviations: NGU, non-gonococcal urethritis; STI, sexually transmitted infection; PID, pelvic inflammatory disease; LVFX, levofloxacin; TFLX, tosufloxacin; GFLX, gatifloxacin; STFX, sitafloxacin; OFX, ofloxacin; MXF, moxifloxacin; AZM, azithromycin; CAM, clarithromycin; M. genitalium, Mycoplasma genitalium; SR, slow release; d, day/days.

Table 3 Laboratory studies of Mycoplasma genitalium antimicrobial susceptibility and genotypic resistance testing

Reference	Year	Study type	Population	M. genitalium DNA extracts or isolates examined (n)	Macrolide resistance (MIC data/resistance mutationsa)	Fluoroquinolone resistance (MIC data/resistance mutationsb)	Comments
Bradshaw et al^Citation28	2006	Prospective case–control study	9 men with NGU attending an STI clinic, Australia	4 isolates	All 4 isolates had raised MICs to macrolides (AZM >8 mg/L, ERY >32 mg/L, CAM >32 mg/L)	Not applicable	8/9 men experienced improvement/resolution of symptoms before NGU recurrence; one was persistently asymptomatic
Jensen et al^Citation32	2008	Laboratory analysis	M. genitalium DNA extracts and isolates from 12 men with NGU who failed AZM therapy in Australia, Norway, and Sweden 7 AZM^S genetically distinct control strains, Sweden	12 AZM^R DNA extracts 7 clinical isolates 7 control strains	7/7 isolates persisting after azithromycin therapy had raised MICs to macrolides (AZM ≥8 mg/L, ERY ≥16 mg/L, CAM ≥16 mg/L) 12 23S rRNA gene mutations reported: 5 at position 2059 (all A2059G); 5 at position 2058 (4 A2058G, one A2058C)	Not applicable	None
Chrisment et al^Citation40	2012	Uncontrolled retrospective study	136 patients with M. genitalium infection attending STI clinics, general practice clinics, and hospitals, France	115 DNA extracts	13 23S rRNA gene mutations reported: 9 at position 2059 (6 A2059G, 2 A2059T, 1 A2059C); 2 at position 2058 (2 A2058G); 1 at position A2062T; 1 at position C2038T	Not applicable	None
Shimada et al^Citation60	2010	Uncontrolled retrospective study	308 men with NGU attending a urology clinic, Japan	28 DNA extracts	Not applicable	Single substitutions reported in the gyrA gene at position 321 (T321A) in 2 specimens Single substitutions reported in the parC gene of 4 specimens: G248A, G259T, A260T, A290G	None
Shimada et al^Citation34	2011	Uncontrolled retrospective study	308 men with NGU attending a urology clinic, Japan	25 DNA extracts	4 23S rRNA gene mutations reported: 1 at position 2059 (A2059G); 3 at position 2185 (T2185G)	Not applicable	The A2158G mutation is not associated with macrolide resistance in other bacteria. Amino acid substitutions reported in the L4 and L22 ribosomal proteins of unknown significance. The strain with the A2059G mutation was cured with AZM 1 g
Ito et al^Citation7	2011	Laboratory analysis	7 men with M. genitalium related NGU which failed AZM therapy at a urology clinic, Japan	7 DNA extracts	4 23S rRNA gene mutations reported: 2 at position 2059 (A2059G); 2 at position 2058 (A2058G)	Not applicable	All 7 men had no AZM^R mutations in pretreatment M. genitalium DNA extracts. One of the M. genitalium strains with the A2058G mutation also had a L4 protein mutation
Walker et al^Citation35	2013	Longitudinal study	1,100 women attending 29 primary care clinics, Australia	33 DNA extracts	Unspecified 23S rRNA gene mutations were reported in 2/27 pretreatment samples from patients cured with AZM 1 g stat, and also in the test-of-cure samples of 3/3 patients who failed AZM 1 g stat therapy	Not applicable	Women were recruited in the Chlamydia Incidence and Re-infection Rates Study. There were 27 baseline, 14 follow-up, and 3 positive test-of-cure specimens
Twin et al^Citation31	2012	Laboratory analysis	82 pretreatment and 20 post-treatment samples from patients with clinical treatment failure attending an STI clinic, Australia	102 DNA extracts	16/82 pretreatment samples had 23S rRNA gene mutations (A2058G, A2059G, A2059C) 20/20 post-treatment samples from patients failing AZM therapy had 23S rRNA gene mutations (12 A2059G, 7 A2058G, 1 A2059C)	Not applicable	Mutations detected by high resolution melt analysis that may not have been able to detect the type 4 SNP (A-to-T) at position 2058
Gesink et al^Citation39	2012	Uncontrolled observational study	314 participants recruited through telephone and community initiatives, Greenland	26 DNA extracts	Single 23S rRNA gene mutations reported in 26/26 M. genitalium cases tested: 17 at position 2058 (A2058G); 9 at position 2059 (A2059G)	Not applicable	None
Tagg et al^Citation33	2013	Laboratory analysis	143 initial and 43 follow-up M. genitalium-positive samples from 167 patients attending STI clinics, Australia	186 DNA extracts	62/143 (43.4%) initial DNA extracts had 23S rRNA gene mutations at either position 2058 (21 A2058G, 2 A2058T, 1 A2058C), or 2059 (38 A2059G) Follow-up DNA extracts of 23/24 (95.8%) patients had 23S rRNA gene mutations	1/143 (0.7%) had gyrA mutations (G285C) resulting in an amino acid changes 22/143 (15.4%) initial DNA extracts had parC mutations (11 G248T, 3 G259A, 2 G259T, 1 G241T, 1 G244A, 1 A247C, 1 G259C, 1 A260G, 1 G307A) resulting in amino acid changes Follow-up DNA extracts from 3/24 (12.5%) patients had gyrA/parC mutations	The matched initial DNA extract for 8/23 follow-up specimens with 23S rRNA mutations did not have evidence of these same AZM^R mutations
Couldwell et al^Citation36	2013	Uncontrolled observational study	33 patients attending a STI clinic with M. genitalium infections, either as NGU cases (30 men) or their sexual partners (2 women, 1 man), Australia	32 DNA extracts	15/32 (46.9%) had 23S rRNA gene mutations at position 2058 (A2058G, A2058T) or position 2059 (A2059G)	6/32 (18.8%) had gyrA mutations (G285C) or parC mutations (G248T, G259A, A260G)	Transmitted macrolide resistance was reported in 4/20 (20.0%) of samples from patients who had not received AZM pretreatment. None of the study group reported prior fluoroquinolone use
Yew et al^Citation8	2011	Laboratory analysis	11 M. genitalium DNA extracts from men with recurrent NGU, New Zealand	9 DNA extracts	4/9 (44.4%) had A2059G mutations in the 23S rRNA gene	Not applicable	Unable to amplify 23S rRNA genes of 2/11 known M. genitalium-positive DNA extracts
Anagrius et al^Citation30	2013	Uncontrolled retrospective study	11 patients testing positive for M. genitalium after treatment with azithromycin 1 g single-dose (n=10) or extended azithromycin 1.5 g (n=1) therapy, Sweden	8 DNA extracts	1/8 (12.5%) pretreatment and 8/8 (100.0%) post-treatment samples had non-specified macrolide-associated 23S rRNA gene mutations	Not applicable	2/10 pretreatment samples were missing and 1/10 pretreatment samples had insufficient DNA for amplification. The patient failing the extended azithromycin had macrolide mutations in the pretreatment DNA extract
Pond et al^Citation41	2014	Uncontrolled observational study	217 men with urethritis-related symptoms, UK	22 DNA extracts	23S rRNA gene mutations reported in 9/22 (40.9%) samples: 5 at position 2058 (A2058G); 9 at position 2059 (3 A2059G, 1 A2059C)	1/22 (4.5%) had a parC mutation (A247C)	None
Kikuchi et al^Citation38	2014	Laboratory analysis	90 M. genitalium DNA extracts from men with NGU, Japan	68 DNA extracts (macrolide resistance testing) 51 DNA extracts (fluoroquinolone resistance testing)	23S rRNA gene mutations reported in 5/68 (7.4%) samples: 4 at position 2058 (A2058G); 1 at position 2059 (A2059G)	5/51 (9.8%) had gyrA mutations (4 C267T, 1 C270T); 18/51 (35.3%) had parC mutations (12 G248A, 3 G248T, 2 G259A, 1 C356A)	The significance of the reported C356A mutation is unclear as it is outside the fluoroquinolone resistance-determining region
Salado-Rasmussen and Jensen^Citation13	2014	Uncontrolled retrospective survey	1,008 patients from general practice, private specialists and hospitals with M. genitalium infection, Denmark	1,085 DNA extracts	385/1,008 (35.5%) patients had macrolide resistance; A2058G (61%) and A2059G (35%) were the most common mutations	Not applicable	None
Hay et al^Citation42	2015	Laboratory analysis	601 women attending primary health care clinics, South Africa	41 DNA extracts	A2058G mutations reported in the 23S rRNA gene of 4/41 (9.8%) DNA extracts tested	Not applicable	None

Notes:

a Mutation positions are according to Escherichia coli numbering;

b mutation positions are according to M. genitalium G37 genome (GenBank accession number NC000908.2).

Abbreviations: M. genitalium, Mycoplasma genitalium; NGU, non-gonococcal urethritis; STI, sexually transmitted infection; AZM, azithromycin; CAM, clarithromycin; ERY, erythromycin; AZM^S, azithromycin-susceptible; AZM^R, azithromycin-resistant; SNP, single nucleotide polymorphism; MIC, minimum inhibitory concentration.

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