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Vaginal Microbiome Transplantation in Women with Intractable Bacterial Vaginosis

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Vaginal Microbiome Transplantation in Women with Intractable Bacterial Vaginosis BRIEF COMMUNICATION https://doi.org/10.1038/s41591-019-0600-6 Vaginal microbiome transplantation in women with intractable bacterial vaginosis Ahinoam Lev-Sagie 1,6*, Debra Goldman-Wohl1,6, Yotam Cohen2,6, Mally Dori-Bachash2, Avner Leshem2,3, Uria Mor2, Jacob Strahilevitz4, Allon E. Moses4, Hagit Shapiro2, Simcha Yagel1 and Eran Elinav 2,5* We report the results of a first exploratory study testing the severe end of the BV spectrum. Fecal microbiome transplantation use of vaginal microbiome transplantation (VMT) from healthy (FMT), in which feces from healthy donors are introduced into donors as a therapeutic alternative for patients suffering from recipients’ intestines to replace their disease-associated micro- symptomatic, intractable and recurrent bacterial vaginosis biome, has recently been successfully used in treating severe and (ClinicalTrials.gov NCT02236429). In our case series, five recurrent Clostridium difficile infection23. Although gastrointestinal patients were treated, and in four of them VMT was associ- microbiome interventions may offer a different ecological scenario ated with full long-term remission until the end of follow-up than those related to a dysbiotic vaginal microbiome, we hypoth- at 5–21 months after VMT, defined as marked improvement of esized that a similar use of VMT might be beneficial in treating the symptoms, Amsel criteria, microscopic vaginal fluid appear- most severe cases of recurrent and antibiotics-nonresponsive BV. ance and reconstitution of a Lactobacillus-dominated vaginal Five patients were recruited (aged 27–47 years and referred to as microbiome. One patient presented with incomplete remis- patients A–E; Extended Data Fig. 1). All suffered from intractable BV, sion in clinical and laboratory features. No adverse effects defined as four or more symptomatic episodes of BV during the pre- were observed in any of the five women. Notably, remission vious year19, relapsing after repeated, prolonged and diverse antibi- in three patients necessitated repeated VMT, including a otic attempts requiring continuous maintenance antibiotic treatment donor change in one patient, to elicit a long-standing clini- to remain symptom free. All patients reported a substantial negative cal response. The therapeutic efficacy of VMT in women with impact of BV symptoms on their quality of life, including devastating intractable and recurrent bacterial vaginosis should be further consequences to their relationships, sexual intimacy and self-esteem. determined in randomized, placebo-controlled clinical trials. All five patients were otherwise healthy. Patient screening, exclusion Bacterial vaginosis (BV) is a form of vaginal microbial com- criteria and the consent process are described in the Methods. The munity alteration in which the microbiome normally dominated three donors were premenopausal, healthy volunteers, aged 35–48 by Lactobacillus species switches to one characterized by the emer- years (donors 1–3; Extended Data Fig. 1), who did not report having gence of anaerobes1–4. BV is prevalent in women of reproductive age, BV in the last 5 years or any history of recurrent BV. Donor selection affecting from one-fourth to one-third of women5. It ranges from and screening are detailed in the Methods. Repeated communication an asymptomatic finding in most cases to a clinically symptomatic between the lead physician and the donors ensured that the behav- entity characterized by an abnormal, often malodorous vaginal dis- ioral requirements (e.g., abstinence from sexual activity for 1 week charge in 16% of women diagnosed with BV, summing up to a prev- before donation in the sexually active donor) were strictly followed. alence of 4.4% for symptomatic BV in women aged 14–49 years5. BV Before transplantation, all patients were treated with an intra- may be associated with risk of upper genital tract infection6, compli- vaginal antibiotic regimen16 that previously resulted in a longer cations of pregnancy (particularly preterm birth and lower success symptom-free period, which consisted of 5 g clindamycin cream in fertility treatments7–10) and susceptibility to sexually transmitted (2%) for 7 d (recipients B, C and E) or 5 g metronidazole gel (0.75%) infections11. At the clinically severe end of the BV spectrum, treat- for 5 d (recipients A and D). VMT was performed 1 week after ment with antibiotics (either systemic or vaginal) is associated with completion of antibiotic treatment24. During the procedure, vagi- a 30% relapse rate within 3 months of initial treatment and a relapse nal fluid for transplantation was collected from the donors starting rate of up to 50–70% within 1 year12. Therapeutic options are very from the seventh day of the menstrual cycle (Methods) and taken limited in the subpopulation of women who experience persistent from the upper half of the vagina and cervical fornices, while avoid- or recurrent BV despite multiple antibiotic treatment attempts13–15. ing the cervix. The collected discharge was evaluated by pH and Maintenance antimicrobial treatment16,17 is often the treatment sug- microscopy, diluted with 1 ml of sterile saline and transferred to the gested in these cases, but it can predispose to vaginal candidiasis18 recipient’s posterior fornix, without the use of a speculum (Fig. 1a). and resistant infections19,20. Importantly, probiotic treatment of VMT was completed within no more than 60 min of sample col- symptomatic patients with oral and/or vaginal administration of lection and was performed at any stage during the recipient’s men- bacterial Lactobacillus strains has produced mixed results21,22, sug- strual cycle, except during menstruation. After the first VMT, gesting that the microbiome as a whole, rather than a single bacte- repeat VMTs were performed in cases of symptom recurrence or rial species, may be necessary for an effective cure at the clinically with reappearance of one or more positive Amsel criteria during 1Department of Obstetrics and Gynecology, Hadassah-Hebrew University Medical Center, Jerusalem, Israel. 2Immunology Department, Weizmann Institute of Science, Rehovot, Israel. 3Department of Surgery, Tel Aviv Sourasky Medical Center, Tel Aviv, Israel. 4Department of Clinical Microbiology and Infectious Diseases, Hadassah-Hebrew University Medical Center, Jerusalem, Israel. 5Division of Cancer–Microbiome Research, DKFZ, Heidelberg, Germany. 6These authors contributed equally: Ahinoam Lev-Sagie, Debra Goldman-Wohl, Yotam Cohen. *e-mail: [email protected]; [email protected] NATURE MEDICINE | www.nature.com/naturemedicine BRIEF COMMUNICATION NATURE MEDICINE a RecruitmentScreening Donation Medical Microscopic Next-generation assessment Whiff test pH evaluation sequencing Donors Recipients Months Diagnosis Vaginal antibiotics Transplantation Follow-up b c Before VMT After VMT 4 A B 3 C D 2 E Amsel criteria 1 0 0 100 200 300 400500 600700 Days from baseline A d A B B BV P C C D D E E IM BL Whiff test Microscopy N N 0 100 200 300 400 500600 700 0 100 200 300 400 500 600700 Days from baseline Days from baseline A A P B 5.00 B C 4.75 C D 4.50 D E pH E Discharge 4.25 N 4.00 0 100 200 300 400 500 600 700 0 100 200300 400 500 600 700 Days from baseline Days from baseline Fig. 1 | Clinical features of VMT. a, Schematic depiction of the VMT study. b, Amsel criteria. c, Wet-mount microscopy before VMT: clue cells (black arrow). The vaginal microbiome comprised of abnormal coccid bacteria (white arrow). Wet-mount microscopy after VMT: normal, mature vaginal squamous epithelial cells (black arrow) and Lactobacillus morphotypes (white arrow) are present. This wet mount represents normavaginal discharge (original magnification, ×400). d, Discrete clinical features during post-VMT follow-up. A–E are the individual VMT recipients. BL, borderline; BV, bacterial vaginosis; IM, intermediate; N, negative (whiff test, discharge), normal (microscopy); P, positive. follow-up examinations (Extended Data Fig. 2). At each follow-up Four patients (patients A–D) had long-lasting improvements appointment (weekly for the first month and monthly to bimonthly in their Amsel scores (Fig. 1b), microscopic vaginal fluid appear- thereafter), patients were interviewed and underwent a vaginal ance (Fig. 1c,d), whiff test, discharge and vaginal fluid pH (Fig. 1d) examination (including quantification of discharge, pH measure- after 1–3 VMT sessions (Extended Data Figs. 2 and 3). The fifth ment, whiff test and microscopy). Remission of BV was defined at patient (patient E) had partial remission, manifesting as a subjective each appointment as disappearance of symptoms, normalization reduction of symptoms, negative whiff test, cumulative Amsel scor- of all Amsel criteria and appearance of a normal Lactobacillus- ing of 0–1 and an intermediate microscopic vaginal fluid appear- dominated microbiome by light microscopy. ance. Patients A and B underwent a single VMT each from donors 1 NATURE MEDICINE | www.nature.com/naturemedicine NATURE MEDICINE BRIEF COMMUNICATION ab Donor 1 A C E Donor 2 1 4 15 Donor 3 BV, baseline 0.5 2 10 0 5 0250 0200 0200 BC Amsel Days Days Days 0 PC2 (14.1%) BD –5 1 4 –10 0.5 2 –15 0 –20–10 010 20 0100 0500 PC1 (66.1%) Days Days cd Donor 1 Distance from donors AU Donor 2 0 10 20 30 40 A C E Donor 3 0 4 20 BV, baseline Pre-VMT BV - post-VMT ** 0.5 2 Post-VMT 1 0 10 0 250 0 200 0 200 BC Amsel Days Days Days BD 0 4 PC2 (11.4%) 0 0.5 2 –10 1 0 0 100 0500 –20 –10 0 10 20 30 Days Days PC1 (61.9%) efA C E A C E 1.0 0.5 Abundance Antibiotics (pharyngitis) Antibiotics
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