Hostname: page-component-6bf8c574d5-xtvcr Total loading time: 0 Render date: 2025-02-23T22:06:07.696Z Has data issue: false hasContentIssue false

Vaginal Microbiota Transplantation: The Next Frontier

Published online by Cambridge University Press:  01 January 2021

Rights & Permissions [Opens in a new window]

Abstract

The success of fecal microbiota transplantation (FMT) as a treatment for Clostrioides difficile infection (CDI) has stirred excitement about the potential for microbiota transplantation as a therapy for a wide range of diseases and conditions. In this article, we discuss vaginal microbiota transplantation (VMT) as “the next frontier” in microbiota transplantation and identify the medical, regulatory, and ethical challenges related to this nascent field. We further discuss what we anticipate will be the first context for testing VMT in clinical trials, prevention of the recurrence of a condition referred to as bacterial vaginosis (BV). We also compare clinical aspects of VMT with FMT and comment on how VMT may be similar to or different from FMT in ways that may affect research design and regulatory decisions.

Type
Symposium 1 Articles
Copyright
Copyright © American Society of Law, Medicine and Ethics 2019

While fecal microbiota transplants (FMT) have received significant attention as a treatment for recurrent Clostridium difficile, a new area of microbiota transplantation is emerging: vaginal microbiota transplants (VMT) for treatment of bacterial vaginosis (BV). The recent use of high-throughput genetic sequencing approaches has led to much deeper understanding of the composition of vaginal microbiota communities and their influence on sexual and reproductive health.Reference Gajer, Brotman, Bai, Ravel, Gajer and Abdo1 For example, there has been significant research confirming clinically relevant differences between women with BV, also referred to as polymicrobial vaginal microbiota, and women with dominance by one of only a few lactobacillus species, the latter being considered “optimal.” Women with symptomatic BV typically experience abnormal malodor and increased vaginal discharge,Reference Bilardi, Walker and McNair2 although researchers estimate that as many as 50% of women with BV are asymptomatic.Reference Amsel, Totten and Spiegel3 There is evidence, however, that even asymptomatic women retain elevated risk of adverse health outcomes.Reference McKinnon, Achilles and Bradshaw4 The etiology of BV is not well understood, but a collection of excellent articles recently addressed the current understandingReference Martin and Marrazzo5 of its pathogenesis,Reference Muzny and Schwebke6 the interplay of its host immunity and environment,Reference Murphy and Mitchell7 and the limitations of its current treatments.Reference Bradshaw and Sobel8 There is significant evidence that BV can be sexually transmitted from men to women (i.e., when penile microbiota transferred during vaginal sex disrupt lactobacillus dominance in the vagina) and between female sex partners.9 There is also evidence that susceptibility to BV is driven in part by the host immune response, which may be altered by numerous environmental, genetic, and hormonal factors.10

Researchers have also observed that the prevalence of BV varies by race and ethnicity — demographic data that subjects self-reported. The prevalence of BV has been shown to vary between and within countries worldwide, reported to range from as low as 7% in Burkina Faso to as high as 68% in Mozambique.Reference Nugent, Krohn, Hillier, Bautista, Wurapa, Sateren, Kenyon, Colebunders and Crucitti11 A study of over 4,000 women conducted in the U.S. estimated the prevalence of BV at around 29%, with lower prevalence in non-Hispanic whites (23.2%) and higher prevalence in non-Hispanic blacks (51.4%).Reference Koumans, Sternber and McQuillan12 Whether this is due to biologic differences originating from genetic variation across racial groups or variation based on ethnicity (e.g. exposure to particular diets, behaviors, and lifestyle factors — whether cultural or socioeconomic) is unclear, given that research methods for collecting demographic data to date often conflate race and ethnicity rather than eliciting more nuanced information.Reference Bonham, Green and Perez-Stable13 Genetic and biological factors are likely intertwined with differences in socioeconomic status and behavioral factors.14 Chronic stress, smoking, and certain viral coinfections have all been correlated with increased susceptibility to BV, while hormonal contraceptive use has been correlated with decreased risk of incident, prevalent, and recurrent BV.15

Thus, it seems likely that only a bacterial “reset” to a more stable, beneficial lactobacillus-dominated community would have a long-term impact on a woman's sexual and reproductive health. We hypothesize that such a reset could be achieved via vaginal microbiota transplantation (VMT) using cervicovaginal secretions (CVS).

Incredibly, out of the ~180 known species of lacto-bacilli, only a few (i.e. L. crispatus, L. iners, L. jensenii, L. gasseri) have been found to typically dominate the human vagina.16 However, there is mounting evidence that not all species of lactobacilli found in the human vagina should be considered optimal or beneficial; namely, vaginal microbiota communities dominated by Lactobacillus iners have been observed to be less stable and more pro-inflammatory.17 This is particularly concerning because L. iners is the species of lactobacillus most commonly found after “successful” antibiotic treatment for BV, and was most commonly associated with transitions to diverse microbiota.Reference Ravel, Brotman and Gajer18 Thus, it seems likely that only a bacterial “reset” to a more stable, beneficial lactobacillus-dominated community would have a long-term impact on a woman's sexual and reproductive health. We hypothesize that such a reset could be achieved via vaginal microbiota transplantation (VMT) using cervicovaginal secretions (CVS).

Medical Considerations

The Clinical Need

The composition of a woman's vaginal microbiota has a profound impact on her sexual and reproductive health and on her susceptibility to disease.Reference Anahtar, Gootenberg, Mitchell, Kwon, Chen, Song, Wei, Smith and Ravel19 BV is a vaginal infection that is tied to the composition of the vaginal microbiota. It is typically identified using Amsel's criteria and Nugent score.20 BV can be a distressing and chronic condition for many women. For more than 50% of women with the condition, BV negatively affects their quality of life.Reference Bilardi, Walker and Temple-Smith21 BV often recurs and is frequently recalcitrant to antibiotic treatment. In addition to physical symptoms, BV can have an emotional impact on women who experience the condition. In one study, women frequently reported that their symptoms “made them feel embarrassed, ashamed, ‘dirty’ and concerned others [might] detect their malodour and abnormal discharge.”22 Their symptoms also affected their self-esteem and sex lives, making them reluctant to engage in sexual activity. Further, women with BV are more susceptible to sexually transmitted infections (STIs), including human immunodeficiency virus (HIV), gonococcal, chlamydial, and trichomonal infections.Reference Allsworth, Lewis, Peipert, Brotman, Klebanoff and Nansel23 STI transmission rates from women to men are also higher if the woman has BV.Reference Mastromarino, Vitali and Mosca24 Further, researchers have found evidence of a continuum of microbiota in the female reproductive tract linking the vaginal microbiota to the uterine microbiota,25 and thus women with BV are at higher risk for pelvic inflammatory disease, as well as miscarriage, premature delivery, and post-partum endometritis.Reference Reid, Bocking, Taylor, Darville and Haggerty26 Similar observations have also been made recently connecting vaginal and bladder microbiota,Reference Thomas-White, Forster and Kumar27 perhaps explaining increased risk of urinary tract infections associated with BV.Reference Stapleton, Sumati and Saritha28 Potential links have also been found between vaginal microbiota and cervical, ovarian, and urothelial cancers.Reference Kyrgiou, Mitra, Moscicki, Nené, Reisel, Leimbach and Xu29

Clearly, BV is a profound concern in women's health, and yet our current approaches for treatment have limited success.30 The current standard of care is use of antimicrobials with broad-spectrum anaerobic bacterial coverage, such as metronidazole and clindamycin. Short-term cure rates for first line treatments are typically 60-70% at four weeks after treatment, but recurrence rates in excess of 50% occur within the first year.Reference Larsson, Forsum, Bradshaw, Morton, Hocking, Sobel, Schmitt and Meriwether31 Other drugs based on different mechanisms of action for treatment of BV are in the FDA pipeline, but as of now, none have yet been approved.

VMT as a Potential Solution

The tremendous success of fecal microbiota transplantation (FMT) for treating Clostrioides difficile infection (CDI) has launched interest in microbiota transplantations and microbiota-based therapies for a wide range of conditions and diseases. Whereas FMT involves transfer of fecal matter, VMT would involve transplanting vaginal bacteria from one woman to another using CVS, a mixture of mucus secreted from the endocervix into the vagina, shed epithelial cells, bacteria, and other proteins, ions, and lipids. CVS can be self-collected using a non-absorptive menstrual fluid collection device, a method that is both quick and, unlike other absorptive collection methods such as swabs and cervicovaginal lavage, does not require dilution.Reference Boskey, Moench, Hees and Cone32 Herein, we refer to VMT as the process of obtaining CVS from a female donor, and after some minimal processing with the goal of maintaining viability of the bacteria, administering the donor CVS material into the vagina of a recipient.

To our knowledge, the first reported successful VMT procedures in humans were reported in 1955 by Gardner and Dukes as part of their efforts to identify the bacteria that was thought to cause the condition “nonspecific vaginitis.” They reported that they were able to induce Haemophilus vaginalis vaginitis (now called BV) in 11 out of 15 volunteers (73%) by directly inoculating material from the vaginas of infected women into the vaginas of the healthy volunteers.Reference Gardner and Dukes33 Further, in two of the successful inoculations, the donor material had been taken “from patients in whom the disease had been experimentally produced.” No details were given as to how the material was collected and transplanted. In contrast, using pure cultured bacteria, the researchers were able to infect only one out of 13 women.34

The use of VMT to treat or prevent recurrence of BV would require the transplantation of Lactobacillus species from the donor to the recipient. Although we are not aware of attempts to transplant lactobacillus bacteria from a donor to a recipient by VMT, there is significant epidemiological evidence that vaginal microbiota are transferred routinely between women who have sex with women (WSW) through sexual practice. In one study of 58 monogamous female couples, 95% had concordance for the absence or presence of BV.Reference Marrazzo, Koutsky and Eschenbach35 In another study of WSW, women with BV were more likely to report a sexual partner with BV, sharing of vaginally inserted sex toys, and vaginal lubricant use.Reference Marrazzo, Thomas, Agnew and Ringwood36 Another study suggested similar trends with the presence of Lactobacillus bacteria; of 31 couples monogamous for more than three months, 23 (77%) were found to possess identical strains of Lactobacillus.Reference Marrazzo, Antonio, Agnew and Hillier37 The likelihood of sharing identical lactobacilli was not related to age, lifetime male sex partners, or the practice, frequency, or timing of other sexual behaviors. The only practice that demonstrated a trend toward association with sharing identical lactobacilli strains was the reported use of shared vaginal sex toys.38 Another recent study, which was the largest and longest community-based prospective cohort study of WSW, provided additional data to support transmission of bacterial species between women. Co-enrolled largely monogamous couples had a low rate of incident BV, and had predominantly lactobacillus-dominated vaginal microbiota that remained closely aligned and stable over long periods of time.Reference Vodstrcil, Walker and Hocking39 These studies support the feasibility of transplanting lactobacillus bacteria from a donor to a recipient using CVS.

Comparison to Other Ongoing Microbiota Transplant Studies Practices

An analogous form of vaginal microbiota transfer, or vaginal seeding, is being tested as a way to expose babies born by Caesarean section (C-section) to their mother's vaginal secretions as would occur during vaginal birth.Reference Mueller40 Several studies implicate birth by C-section in increasing risk of obesity, asthma, allergies, and immune deficiencies.Reference Huh, Rifas-Shiman, Zera, Pistiner, Gold, Abdulkerim, Sevelsted, Stokholm, Bønnelykke, Bisgaard, Thavagnanam, Fleming, Bromley and Mueller41 The observation that the composition of the microbiota that colonizes the body of newborns differs between birth by C-section and vaginal birth suggests that this early exposure can play a role in educating the immune system.Reference Olszak, An and Zeissig42 In these studies, mothers with Lactobacillus dominated vaginal microbiota undergoing a scheduled C-section have sterile gauze inserted in their vagina to collect their CVS during the hour prior to surgery.Reference Dominguez-Bello, De Jesus-Laboy and Shen43 Within the first two minutes of birth, babies are exposed to their mother's CVS by swabbing the mouth, face, and body with the gauze. Early results suggest that the bacterial communities of newborns delivered by C-section could be partially restored to resemble that of vaginally delivered babies.44 By nature, vaginal seeding is not a true transplant, in that the donor material is not administered to the same site in the body in the recipient.45

Although there are clear parallels between VMT and FMT, there are also significant physiological and clinical differences that must be considered when developing treatment protocols, developing a regulatory framework, and measuring efficacy in clinical care and research. In the healthy intestines, the micro-biota composition is highly diverse, with roughly 160 bacterial species per person.Reference Lloyd-Price, Abu-Ali, Huttenhower, Qin, Li and Raes46 In the disease state, C. difficile is the single causative agent, and more likely to lead to disease in individuals with decreased bacterial diversity, such as those treated with antibiotics.Reference Theriot and Young47 Thus, the goal with FMT is to inhibit C. difficile proliferation in the intestines, which leads to a return to healthy bacterial diversity. In contrast, there is no single causative agent for BV, and it is the depletion of lactobacillus bacteria and resulting overgrowth of a polymicrobial community of anaerobes that is considered pathological.Reference Oakley, Fiedler, Marrazzo and Fredricks48 In the case of Lactobacillus-dominated vaginal microbiota, usually a single Lactobacillus species is highly abundant and desirous for VMT donors. Moreover, when FMT is used for treating CDI, complete microbiota engraftment is not essential for a clinical cure.Reference Staley, Kelly and Brandt49 While the subset of bacteria strains from the donor stool that initially engraft in the recipient wanes over time,Reference Smillie, Sauk and Gevers50 at the point where the transplanted strains are at their nadir, the CDI would be eradicated and recurrence less common. In the context of BV, the Lactobacillus species that repopulate after antibiotic treatment, commonly L. iners, typically do not provide protection from BV recurrence.Reference Mayer, Srinavasan, Fiedler, Petrova, Reid, Vaneechoutte and Lebeer51 Thus, the goal of VMT may be engraftment of the dominant Lactobacillus species in the donor sample as well as the minor bacterial species in the community. Although the dominant species may be the most obvious important player, the other minor species may play an important role in allowing the recovery of the dominant species after perturbations due to menses and sexual activity.52

Regulatory Considerations

Regulation and Oversight

For decades, the U.S. Department of Health and Human Services, through the Food and Drug Administration (FDA), has overseen the approval of drugs, biologics, and medical devices for commercial distribution by requiring demonstration of safety and efficacy through clinical trials research. However, such FDA oversight is contingent on the substance being tested, e.g., it must be a drug, biologic or medical device and it must have a connection to interstate commerce. In the early days of FMT, many physicians did not think that fecal matter was a drug, nor did they anticipate that it would be a product that would be marketed. Therefore, they believed FMT would not be subject to FDA oversight. Instead, they viewed FMT, with stool typically provided from a local donor known to the patient, as the practice of medicine. In fact, the first recorded use of FMT was documented in 1958,Reference Eiseman, Silen, Bascom and Kouvar53 but the first randomized clinical trial for treating recurrent CDI with FMT was reported in 2013.Reference van Nood, Vreize and Niewdown54 In the interim, FMT was conducted by physicians as part of clinical care. In 2013, FDA stated that it considered fecal material to be a “live biotherapeutic product” (LBP), a subcategory of drugs, and that physicians performing FMTs would need to submit an Investigational New Drug application (IND) to the agency. However, in response to a groundswell of opposition, FDA announced that it would exercise its “enforcement discretion” and not require an IND for physicians performing FMT for patients with recurrent CDI unresponsive to standard antibiotic therapy.

Although VMT is newer in the repertoire of micro-biota transplantations, many of the same initial regulatory questions apply to VMT as to FMT. An initial issue is whether the FDA has regulatory authority over VMT. As stated above, FDA jurisdiction is tied to products that have a connection to “interstate commerce” and, in addition, are “held for sale.”55 Prior to the 1997 Food and Drug Modernization Act (FDAMA), there might have been a successful argument that FDA does not have the authority to regulate VMT with vaginal secretions from a donor known to the patient and performed in a doctor's office. Rather, the procedure might have been the practice of medicine, regulated by state medical boards. However, FDAMA made clear that “the connection with interstate commerce required for [FDA] jurisdiction” is presumed to exist56 and case law since the passage of the act has expanded the domain of what counts as interstate commerce. This includes products that have never crossed state lines but include some ingredient or component part that has traveled in interstate commerce.57 In addition, the product need not be sold nor must there be an intent to sell the product. As long as the product is used by a physician in a procedure it can be considered “held for sale.”58 Thus, in the case of VMT, a court would likely find that although the CVS are not a part of interstate commerce, the collection device would be, as a component part of the VMT, and therefore the agency would be able to assert jurisdiction. While some would consider this regulatory overreaching, the federal courts in a number of circuits have embraced FDA's broader jurisdiction. Only if the procedure were to be performed for free would it possibly be considered outside of FDA's jurisdiction, but even then, courts have considered devices used by physicians in the course of a procedure “held for sale.”59

If CVS were to be sold, it clearly would be subject to FDA rules and regulations. In the context of FMT, this is being played out in FDA's efforts to regulate stool from a stool bank that is shipped across state lines and is sold to physicians and hospitals for treatment of recurrent C. difficile that is unresponsive to traditional antibiotic therapies. It is conceivable that CVS, like stool or blood, could be banked and sold to health care providers and patients. Similar to stool, CVS is self-collected, though the timing for collection is not dependent on unpredictable bodily functions and, thus, can be more flexible. While donors would have to avoid days like menstruation and ovulation (if not using hormonal contraceptives, as ovulation affects vaginal secretions), collection could occur at any time on eligible days. The basic eligible donor pool would be limited to women of reproductive age, and the stringency of the screening criteria would be at least as high for CVS collection as has been reported for stool. In contrast to blood collection, self-collection of CVS is minimally invasive, similar to tampon insertion and removal, and does not cause pain or have risks of side effects such as dizziness, fainting, etc.

In addition to having a connection to interstate commerce, FDA jurisdiction to regulate a substance as a drug or biologic is tied to whether it is to be used to cure, treat, mitigate or prevent symptoms of disease. Some researchers and clinicians believe that a vaginal microbiota not dominated by lactobacillus should be considered “diseased.”Reference Reid60 Under this definition, VMT to increase lactobacillus would be a treatment, and the regulatory path would be that for a drug or biologic. However, sometimes, women with BV are asymptomatic, which means a VMT might be used to “promote vaginal health.” There is also the possibility that VMT could be used with adolescent girls as a prophylactic to promote lactobacilli during the time where the vaginal microbiota starts to potentially shift toward lactobacillus dominance.Reference Hickey, Zhou and Settles61 Such claims, i.e., “promotion of vaginal health” and “promotion of lactobacillus,” would be considered structure/function claims in the world of dietary supplements, and the product would not be regulated as a drug, but because CVS via VMT is delivered vaginally rather than orally, CVS could not be considered a dietary supplement. The claims would be considered drug claims for prevention of BV. Alternatively, some women might seek out a VMT to reduce vaginal odor. This claim, “eliminating odor,” could have different regulatory implications than treatment claims. For example, a product claiming only to reduce odor would be regulated as a cosmetic rather than as a drug.

Under the Federal Food Drug and Cosmetic Act (FDCA), a cosmetic is a product (excluding soap) “intended to be applied to the human body for cleansing, beautifying, promoting attractiveness, or altering the appearance.”62 While cosmetics, under the law, may not be “adulterated” or “misbranded,” they do not require FDA approval prior to marketing. Products, such as vaginal douches, for example, that claim to cleanse or make a woman “feel fresh,” are regulated as cosmetics. However, as stated above, if the purpose of the substance/procedure is to treat, cure, prevent or mitigate the symptoms of a disease or to affect the structure/function of the body, the substance would come within the regulatory umbrella for drugs and biologics. Yet, as has been the case with fecal matter for FMT where a number of researchers and clinicians have questioned the “fit” of the drug/biologic pathway, CVS for VMT poses similar challenges to the drug and biologic regulatory scheme.

Finding the Right Regulatory Pathway

Although FDA has the authority to regulate CVS as a drug/biologic, the drug/biologic approval process assumes that the product can be standardized so that each therapeutic unit is the same in terms of composition, dose and potency. While the microbiota community in CVS may be relatively more homogeneous than stool, it will still differ from woman to woman and will fluctuate over time. Similar to stool, dosing and potency are likely to be difficult to determine. Although some of these challenges are addressed for biologics through the manufacturing process, obstacles still remain.Reference Khoruts, Hoffman and Palumbo63

Another concern with the drug pathway is that because of the expense to the drug manufacturer/sponsor of going through all of the required procedures and clinical trials, the price of the ultimate drug, if approved, is likely to be quite high. In addition, the approval process takes on average ten years. If during this timeframe women want access to the procedure, like the situation with FMT, women may engage in a “do-it-yourself (DIY)” VMT. The potential for “DIY” VMT exists as is evidenced by the fact that women who share sex toys share the same vaginal microbiome as a result of transfer of vaginal microorganisms. Given that the process of using a menstrual cup to collect CVS is as simple as tampon insertion and removal, the methods are publicly available, and the menstrual cups themselves can be obtained over the counter at most pharmacies, the potential for DIY treatment may be higher than with FMT. (Additional challenges to regulating CVS as a drug/biologic through the submission of an IND are described below in the section below entitled “Submitting an IND.”)

In the context of FMT, several authors have suggested that regulatory models based on other transferred/transplanted human body constituents, e.g., organs, blood or tissue, might be more appropriate for microbiota transplantations.Reference Sachs and Edelstein64 These other areas are regulated as a combination of the practice of medicine with FDA or the Public Health Service (PHS) oversight of the screening of donors and testing of transplanted material for infectious diseases and the regulation of any banks where such products are collected, packaged and stored for use. If CVS banks were to materialize, the regulatory framework for human cells, tissues and cellular and tissue-based products (HCT/Ps) may be a better fit than that for drugs/biologics. HCT/Ps are defined as articles “containing or consisting of human cells or tissues that are intended for implantation, transplantation, infusion, or transfer into a human recipient.”65 The regulatory framework for HCT/Ps is focused on prevention of communicable disease transmission and safe processing and handling. Thus, it includes detailed rules regarding donor screening and methods, facilities, and controls for manufacturing to prevent contamination and cross-contamination.

FDA classifies HCT/Ps into two groups: Section 361 Products and Section 351 Products. (Sections refer to the PHS Act, which addresses prevention of the introduction, transmission, or spread of communicable disease.) Section 361 products are considered less risky than Section 351 products and are less tightly regulated. To be considered a 361 HCT/P, the product must be “minimally manipulated” and must be intended for homologous use (i.e., perform the same use or basic function as in the donor) as determined by labeling and advertising or other indications of the manufacturer's intent. The definition of “minimal manipulation” depends upon whether the HCT/P is a structural tissue, as opposed to cells or nonstructural tissue. For nonstructural tissue, FDA defines “minimal manipulation” as “processing that does not alter the relevant biological characteristics of cells or tissues.”66 In addition, its manufacture must not involve combination with another article, except for water, crystal-loids, or a sterilizing, preserving, or storage agent. Nor can it have a systemic effect or be dependent upon the metabolic activity of living cells for its primary function, or, if it has a systemic effect or is dependent on “the metabolic activity of living cells for its primary function,” it must be intended for autologous use or allogenic use in close relatives (first or second degree blood relatives) or for reproductive use.67

At this time, while FDA has not issued regulatory guidance on CVS/VMT for treatment of BV, it is likely that the agency would, at least initially, consider it a drug/biologic and require an IND application for human subjects research. In our experience, the IRB at Johns Hopkins viewed the issue similarly, and required communication with the FDA prior to considering study applications. Thus, we (LME, KD, FZ, and collaborators) have worked with the FDA to establish a framework for screening potential CVS donors, as well as procedures for handling, storing, and performing quality control checks on CVS. Based on our experience, we describe here some of the issues that may arise for researchers in fulfilling the IND requirements.

CVS delivered by VMT appears to meet each of the criteria for a Section 361 product. However, as regards the last criterion, because of the potential systemic effect on the recipient and because the primary action of CVS would be dependent on the metabolic activity of living cells, it would have to be limited to use in close relatives. This latter criterion would be an obstacle to banking CVS, but FDA could amend the requirement to allow for broader use with adequate regulation of CVS banks.

The regulatory scheme for Section 361 products includes: 1) registration of facilities and submission of a list of all products to FDA; 2) donor screening and testing; 3) current good tissue practices; 4) labeling; 5) adverse-event reporting; and 6) inspection and enforcement.68 Establishments that manufacture an HCT/P must register and submit a list of every HCT/P that is manufactured in the establishment. This provides FDA with a list of facilities that it may then inspect to ensure compliance with all regulations. All cell or tissue donors must be screened for risk factors of relevant communicable diseases. In addition to donor screening, the specimen to be donated must also be tested for specific diseases.69

Good tissue practice refers to the recovery, processing, storage, labeling, packaging and distribution of the product. The focus is on ensuring not only that the cells or tissues do not contain communicable disease agents but also that they are not contaminated in the manufacturing process.70 Manufacturers must also track each HCT/P so that in case of an adverse event, the root cause may be investigated.71 An HCT/P that meets the criteria for regulation solely under section 361 of the PHS Act is not subject to premarket clearance or approval. HCT/Ps that do not meet the criteria for regulation solely as a 361 HCT/P are subject to an additional layer of regulation under section 351 of the PHS and under Sec. 505B of the federal FDCA governing biologics.72

Submitting an IND

At this time, while FDA has not issued regulatory guidance on CVS/VMT for treatment of BV, it is likely that the agency would, at least initially, consider it a drug/biologic and require an IND application for human subjects research. In our experience, the IRB at Johns Hopkins viewed the issue similarly, and required communication with the FDA prior to considering study applications. Thus, we (LME, KD, FZ, and collaborators) have worked with the FDA to establish a framework for screening potential CVS donors,Reference DeLong73 as well as procedures for handling, storing, and performing quality control checks on CVS. Based on our experience, we describe here some of the issues that may arise for researchers in fulfilling the IND requirements.

In addition to the clinical trial design aspects discussed below, an IND application must include information about the Chemistry, Manufacturing, and Controls (CMC) of the drug or biologic. For CVS, this could include key physicochemical properties, such as pH, lactic acid content, and the amount of lactobacilli bacteria present (colony forming units, or CFU) before and after freezing. Additionally, an IND generally includes a summary of the pharmacological, toxicological, and biological disposition of a drug in animals in addition to the extent known in humans. However, the use of preclinical animal models for studying vaginal microbiota is severely limited by the fact that the human vagina is uniquely dominated and acidified by lactobacillus species, and the role of lactic acid in maintaining human vaginal health is well-established.Reference Haya, Garcia and López-Manzanara74 Researchers have demonstrated that it is possible to temporarily colonize the mouse vagina with exogenous lactobacilli, but it requires sustained estradiol treatment, the colonization only lasts a few days, and the bacterial concentrations are as much as 1,000 times lower than in human CVS. Thus, the bacteria do not effectively acidify the vagina.Reference Muench, Kuch, Wu, Pascual, Ruiz, Giordano, Barberis, Zarate, Santos and Nader-Macias75 Similarly, our primate cousins do not have vaginas dominated and acidified by lactobacilli.Reference Yildirim, Yeoman and Jange76 It has been suggested that the normal rhesus macaque genital microbiota shows similarities to that of humans with BV.Reference Spear, Gilbert and Sikaroodi77 Thus, it is not feasible in animal models to study vaginal microbial dynamics, VMT, or factors that facilitate beneficial bacterial colonization in the human vagina. This is just one example of how typical IND requirements do not apply to VMT with CVS.

Another key element of an IND is the clinical protocol. Our team at Johns Hopkins (LME, KD, FZ, and collaborators) has designed a clinical study to determine whether vaginal microbiota can be engrafted from one woman to another in a controlled clinical setting, and whether the process is safe and well-tolerated.Reference Ensign and Weld78 We discuss a few of the factors we considered in designing the protocol below.

Selection of VMT Donors

A key difference between FMT and VMT is the disease target for treatment. If we consider the primary use for FMT, treatment of recurrent CDI, the patients receiving treatment are generally older (two out of every three healthcare-associated CDIs occur in patients 65 and over79) and can die from complications of the disease. In contrast, BV is a non-lethal condition that affects reproductive age women, so the risk-to-benefit ratio is less tolerant of risk to the recipient. Thus, careful screening of the donor participants for VMT is of paramount importance to avoid exposure to infectious agents. Our donor screening approach80 combines the FDA guidance for screening donors for HCT/Ps81 with testing for additional STIs, fungi, the TORCH infections (toxoplasmosis, rubella, cytomegalovirus, etc.) associated with congenital anomalies,Reference Stegmann and Carey82 and general measures of immunocompetence. Screening questionnaires include the standard set of questions asked prior to blood donations, sexual and reproductive history, and behaviors that have been correlated with alterations in vaginal microbiota. Travel exclusions include travel by the participant or a sexual partner to regions or countries where Ebola or Zika outbreaks occurred in the past 12 months.

Similar to the model developed by the stool bank OpenBiome,Reference Costello, Conlon and Vuaran83 donors that pass the initial screening will provide multiple CVS samples that will be frozen until confirmatory testing. Each CVS sample from the donor will further be screened for various swab-based pathogen tests and characterized to ensure acidic pH and dominance by one of the common lactobacillus species. Each CVS sample will be tested for the presence of sperm, and if found, that sample will be excluded. Although the CVS collection procedure poses no inherent risk to women who are pregnant or breastfeeding, as a result of the demonstrated alterations in vaginal microbiota that occur in response to hormone changes during pregnancy, we have precluded those women as donors. Concomitant use of antibiotics for any reason, as well as use of other medications that may affect the vaginal microbiota, may be grounds for exclusion at the discretion of the study physician.

Selection of VMT Recipients

Similar to testing FMT in individuals with recurrent CDI that is unresponsive to standard antibiotics, we propose testing VMT initially in women who have recurrent symptomatic BV. Although there are many theories as to why BV recurs that make effective treatment very challenging, women with recurrent BV are in the most need of alternative therapeutic approaches.84 Currently, there is no universally accepted or clinical definition of recurrent BV.Reference Wilson85 In the case of FMT, the clinical recommendations are to use FMT for CDI after a third recurrence.Reference Surawicz, Brandt and Binion86 For our first pending clinical investigation, we have defined recurrent BV as having had at least three prior lifetime diagnoses and having received treatment at least once in the past five years. However, it is worth considering that such a narrow definition may be limiting in reaching everyone that may benefit from VMT. Women may not always be aware of their BV, as the presence of symptoms can be highly subjective. Of the four Amsel's criteria for clinical diagnosis, only two (discharge and odor) are observable by an individual, and a woman may consider this to be “normal.” In contrast, the other two criteria of pH >4.5 and the presence of “clue” cells can typically only be confirmed in the clinic or laboratory. Thus, not all women with clinically diagnosable BV seek treatment. Some women may cease seeking treatment that does not work long term. Such factors should be considered for future development and clinical application of VMT.

Recipients should also be pre-menopausal, as the hormonal changes associated with menopause cause a shift away from Lactobacillus dominance in the vagina that is unlikely to be altered without concomitant hormone replacement therapy.Reference Brotman, Shardell and Gajer87 Further, vaginal micro-biota and pathogens are known to have an impact on pregnancy and postnatal outcomes. Thus, additional key inclusion criteria for recipients are use of hormonal and/or barrier contraception for heterosexual intercourse during the study, and not currently pregnant, breastfeeding, or planning to become pregnant. Recipient participants should receive condoms and counseling for use and should be screened for the same range of infections as donors, ideally on two separate occasions prior to VMT and at the time of VMT, to define the recipient's pre-VMT infection status. Certain infections, such as HIV and any other condition that may compromise the immune system, yeast, chlamydia, gonorrhea, etc., should be exclusions for VMT. In contrast, certain infections like herpes simplex virus (HSV) and HPV need not be exclusions, but should be clearly defined prior to VMT to document baseline status. The intermittent nature of viral sheddingReference Brotman, Shardell, Gajer, Corey, Wald and Patel88 motivates repeated testing of the recipient prior to VMT.

Test Groups

Importantly, for enrollment into a clinical trial, the recipients should be diagnosed as currently having symptomatic BV, and be given standard of care antibiotics, such as vaginal metronidazole gel daily for five days. This can reduce the burden of BV-associated bacteria prior to VMT, and is analogous to antibiotic use with FMT.89 VMT should occur after an antibiotic “washout period” of a minimum of 24 hours. The placebo group should receive standard of care followed by a placebo treatment of a benign vehicle, such as normal saline. Recipients should also track sexual activity, product use (douches, lubricants, etc.), and other behaviors that may affect the success of bacterial engraftment, as it has been demonstrated that vaginal intercourse decreases likelihood of engraftmentReference Ngugi, Hemmerling and Bukusi90 and sexual activity is associated with microbiota community fluctuations.91

Donor-Recipient “Matching”

With the multitude of factors that could affect treatment success, it may be more informative to test the engraftment of a donor species in multiple recipients rather than a single recipient. Further, the stringency of the screening criteria and the associated costs of testing favor the approach of using fewer donors. However, using one universal donor would be potentially limiting in determining whether a particular Lactobacillus sp. is more successful. Thus, we suggest a small group of donors that could provide multiple samples to a larger group of recipients. The concept of “universal donors” also has precedent in FMT.Reference Woodworth, Neish and Miller92 Further, to reduce the compounded risk of infection and other adverse events to the recipient from receiving multiple doses of CVS, we envision that the first study include a single CVS dose at a standardized volume and dilution. Of course, as clinical information becomes available and safety data established for VMT, these clinical study design parameters should be adjusted accordingly.

Endpoints

The FDA guidance for developing BV treatments suggests assessing clinical cure at seven to 14 days and follow-up at 21-30 days.93 However, as described previously, the “cure” rate at four weeks for antibiotics is typically quite high, while recurrence occurs at a high frequency in the months thereafter. Thus, the need for innovation is in developing therapies that lead to long-lasting resolution of symptoms, which is a goal of “resetting” the microbiota with VMT. Thus, it is important to follow the dynamics of the vaginal microbiota for at least six months following treatment, though obtaining clinical cure within the first four weeks may still be an objective. However, for the first exploratory studies where antibiotics are used prior to VMT, the more pertinent primary objective may be to determine whether engraftment of the donor Lactobacillus occurs in the recipient. In this case, vaginal probiotic study designs may be informative. Secondary objectives may include assessment of local adverse events, characterization of vaginal microbiota dynamics in each group, and the frequency of BV in each group at one to six months after treatment.

Ethical Considerations

At one level, a research ethics review for VMT clinical trials would involve similar issues as is seen in other studies, such as ensuring adequate informed consent for STI screening and availability of counseling if a donor or recipient tests positive for HIV or other STIs. However, there are unique issues to consider. The fact that BV prevalence varies by race/ethnicity and region raises questions regarding what is captured through “race” and “ethnicity” categorizations. The FDA recommends that ethnicity and race be self-reported by (1) Hispanic/Latino or not Hispanic/Latino and (2) One or more of the following: American Indian or Alaska Native, Asian, black or African American, Native Hawaiian or other Pacific Islander, and white.94 However, increasing evidence shows that social determinants of health, race, and ethnicity are intertwined. While race is often assumed to be rooted in biology (e.g. genetics) and ethnicity in cultural ancestry, the reality of institutional racism results in health disparities that disadvantage people of color and ethnic minorities. Heintzman and MarinoReference Heintzman and Marino95 point out that zip code may better predict health outcomes than one's genetic code, and that our ability to understand how race and ethnicity impact biology and health outcomes would be better achieved through linkages of race/ethnicity data to large data sets, rather than analyzing self-reported race/ethnicity alone. Thus, researchers should be thoughtful about the demographic data they collect in order to address issues of race/ethnicity responsibly.

Researchers should also be sensitive to unintended messaging when making study design decisions or analyzing data according to race/ethnicity of donors or recipients. The issue of racial disparity in kidney transplantation may shed light on this issue. African Americans experience end-stage renal disease (ESRD) at a higher rate than others but until recently were less likely than whites to receive a kidney transplant.96 The higher ESRD rate was caused in part by health care access disparities and other systemic racial biases that adversely affect African Americans. As a result, African Americans have exhibited less trust in health care providers and researchers, and have been less likely to designate themselves as organ donors. This exacerbated the kidney transplant disparity since there were fewer kidneys with a compatible tissue match available to African Americans on the kidney transplant wait list. Changes in how tissue matching now occurs and outreach efforts to boost African American organ donation and allocation algorithms have closed this particular disparity gap.97 But, to conclude that African Americans were less likely to receive a kidney transplant because too few signed up as organ donors ignores the history of systemic racism that fed this vicious cycle.

Thus, we recommend addressing issues of racial disparity transparently and mindfully when enrolling VMT donors and recipients. When race/ethnicity may be a factor in enrollment, screening, analysis or dissemination of findings, researchers should explain to donors and recipients that the vaginal microbiome differs by race, ethnicity, and region, that there are some known and other unknown reasons for this, and that VMT research aims to explore such questions. The potential for stigmatizing women of a particular race should be carefully thought through, as Havasupai diabetes researchers learned.Reference Pacheco, Daley and Brown98 For example, if findings support higher BV prevalence in black women, the reasons for this should be reported in full context (e.g., that this could be related to higher baseline stress levels among black women and other factors grounded in social determinants of health).Reference Alcendor99 Another example might be if a higher BV prevalence was associated with certain sexual practices or poor health outcomes such as low birthweight in their offspring, such findings could contribute to group stigma and thus to group harm.

In addition to the issues of racial/ethnic disparity and group stigma, microbiome research raises similar ethical questions to those posed by genetic research, e.g., predisposition to disease, privacy, confidentiality, informational risks, incidental findings, and individual stigma.Reference Hoffmann, Fortenberry and Ravel100 For example, disclosing findings from screening procedures may reveal previously unknown information, such as pregnancy or HIV infection. Risks also include inadvertent disclosure of this information to a subject's partner or other family member, or access to the information by unauthorized personnel. Some of these concerns led to the passage by Congress of the Genetic Information Nondiscrimination Act (GINA) in order to protect individuals from possible discrimination by employers and insurers. Depending on the microbiome sequencing approach, human genetic information may or may not be obtained from microbiome samples/donations. Moreover, GINA may not be protective of some of the more insidious types of risks associated with microbiome based research, such as revealing information about personal and private sexual practices. Whether GINA protects individuals based on discrimination from disclosure of microbiome-based information has yet to be determined. Stigma of the type described above, i.e., associated with predisposition to BV and related adverse health and reproductive health outcomes, may not be a basis for discrimination by employers or insurers, but may affect an individual's inclusion in social groups or intimate relationships. There is much less our laws or regulations can do about this type of discrimination. Thus, it behooves microbiome researchers to spend time translating their findings to the public in full context to minimize the risk of stigma-related harms.101

Lastly, funding and regulatory agencies should acknowledge that the burden of BV and urgency of developing safe and effective treatments should be defined by those affected, namely women who have BV. For example, regulators and those funding research may perceive that less severe BV symptoms (e.g., malodour and itching) do not warrant the same priority and urgency in VMT research as other symptoms and may de-prioritize studies assessing these outcomes or de-emphasize the benefits associated with potential treatments of these symptoms. BV researchers and funders should legitimize the unique perspectives that women with BV bring to these issues by eliciting their values and priorities and factoring these into decisions about research funding, design, and implementation.

Conclusion

Excitement is growing around the clinical potential of microbiota transplantation, and VMT is on the cusp of entering the clinic. While microbiota transplantation itself has unique regulatory issues as a result of not fitting into the typical regulatory pathways, VMT specifically also has unique ethical issues related to the sex, race, and socioeconomic status of women comprising the target recipient population and donors. Here, we discussed the medical, regulatory, and ethical issues related to VMT, as well as design considerations for future clinical studies. We anticipate that the discussions herein will help accelerate the successful development of VMT.

Footnotes

Dr. Ensign reports a patent “CVS transplantation for treatment of bacterial vaginosis” issued. The other authors have no conflicts to disclose.

References

Gajer, P., Brotman, R.M., and Bai, G., et al., “Temporal Dynamics of the Human Vaginal Microbiota,” Science Translational Medicine 4, no. 132 (2012): 132ra52; Ravel, J., Gajer, P., and Abdo, Z., et al., “Vaginal Microbiome of Reproductive-Age Women,” Proceedings of the National Academies of Science U.S.A. 108, supp. 1 (2011): 46804687.CrossRefGoogle Scholar
Bilardi, J., Walker, S., and McNair, R., et al., “Women's Management of Recurrent Bacterial Vaginosis and Experiences of Clinical Care: A Qualitative Study,” PLoS One 11, no. 3 (2016): e0151794.CrossRefGoogle Scholar
Amsel, R., Totten, P.A., and Spiegel, C.A., et al., “Nonspecific Vaginitis. Diagnostic Criteria and Microbial and Epidemio-logic Associations,” American Journal of Medicine 74, no. 1 (1983): 1422.CrossRefGoogle Scholar
McKinnon, L.R., Achilles, S.L., and Bradshaw, C.S., et al., “The Evolving Facets of Bacterial Vaginosis: Implications for HIV Transmission,” AIDS Research and Human Retroviruses 35, no. 3 (2019): 219228.CrossRefGoogle Scholar
Martin, D.H. and Marrazzo, J.M., “The Vaginal Microbiome: Current Understanding and Future Directions,” Journal of Infectious Diseases 214, Supp. 1 (2016): S3641.CrossRefGoogle Scholar
Muzny, C.A. and Schwebke, J.R., “Pathogenesis of Bacterial Vaginosis: Discussion of Current Hypotheses,” Journal of Infectious Diseases 214, Supp. 1 (2016): S15.CrossRefGoogle Scholar
Murphy, K. and Mitchell, C.M., “The Interplay of Host Immunity, Environment and the Risk of Bacterial Vaginosis and Associated Reproductive Health Outcomes,” Journal of Infectious Diseases 214, Supp. 1 (2016): S2935.CrossRefGoogle Scholar
Bradshaw, C.S. and Sobel, J.D., “Current Treatment of Bacterial Vaginosis-Limitations and Need for Innovation,” Journal of Infectious Diseases 214, Supp. 1 (2016): S1420.CrossRefGoogle Scholar
Martin and Marrazzo, supra note 5; Muzny and Schwebke, supra note 6.Google Scholar
Murphy and Mitchell, supra note 7.Google Scholar
Nugent, R.P., Krohn, M.A., and Hillier, S.L., “Reliability of Diagnosing Bacterial Vaginosis Is Improved by a Standardized Method of Gram Stain Interpretation,” Journal of Clinical Microbiology 29, no. 2 (1991): 297301; Bautista, C.T., Wurapa, E., and Sateren, W.B., et al., “Bacterial Vaginosis: A Synthesis of the Literature on Etiology, Prevalence, Risk Factors, and Relationship with Chlamydia and Gonorrhea Infections,” Military Medical Research 3 (2016): art. no. 4. doi: 10.1186/s40779-016-0074-5; Kenyon, C., Colebunders, R., and Crucitti, T., “The Global Epidemiology of Bacterial Vaginosis: A Systematic Review,” American Journal of Obstetrics and Gynecology 209, no. 6 (2013): 505523.CrossRefGoogle Scholar
Koumans, E.H., Sternber, M., and McQuillan, G., et al., “The Prevalence of Bacterial Vaginosis in the United States, 2001-2004; Associations with Symptoms, Sexual Behaviors, and Reproductive Health,” Sexually Transmitted Diseases 34, no. 11 (2007): 864–69.CrossRefGoogle Scholar
Bonham, V.L., Green, E.D., and Perez-Stable, E.J., “Examining How Race, Ethnicity, and Ancestry Data Are Used in Biomedical Research,” Journal of the American Medical Association 320, no. 15 (2018): 15331534.CrossRefGoogle Scholar
Murphy and Mitchell, supra note 7.Google Scholar
Ravel, Gajer, and Abdo, supra note 1.Google Scholar
McKinnon, Achilles, and Bradshaw, et al., supra note 4.Google Scholar
Gajer, Brotman, and Bai, et al., supra note 1; Ravel, J., Brotman, R.M., and Gajer, P., et al., “Daily Temporal Dynamics of Vaginal Microbiota before, during and after Episodes of Bacterial Vaginosis,” Microbiome 1, no. 1 (2013): 29, doi: 10.1186/2049-2618-1-29.CrossRefGoogle Scholar
Ravel, Gajer, and Abdo, et al., supra note 1; Anahtar, M.N., Gootenberg, D.B., Mitchell, C.M., and Kwon, D.S., “Cervicovaginal Microbiota and Reproductive Health: The Virtue of Simplicity,” Cell Host Microbe 23, no. 2 (2018): 159168; Chen, C., Song, X., and Wei, W., et al., “The Microbiota Continuum along the Female Reproductive Tract and its Relation to Uterine-Related Diseases,” Nature Communications 8, no. 1 (2017): art. no. 875; Smith, S.B. and Ravel, J., “The Vaginal Microbiota, Host Defence and Reproductive Physiology,” Journal of Physiology 595, no. 2 (2017): 451463.CrossRefGoogle Scholar
Amsel, supra note 3; Nugent supra note 11.Google Scholar
Bilardi, J.E., Walker, S., and Temple-Smith, M., et al., “The Burden of Bacterial Vaginosis: Women's Experience of the Physical, Emotional, Sexual and Social Impact of Living with Recurrent Bacterial Vaginosis,” PLoS One 8, no. 9 (2013): e74378.CrossRefGoogle Scholar
Allsworth, J.E., Lewis, V.A., and Peipert, J.F., “Viral Sexually Transmitted Infections and Bacterial Vaginosis: 20012004 National Health and Nutrition Examination Survey Data,” Sexually Transmitted Diseases 35, no. 9 (2008): 791796; Brotman, R.M., Klebanoff, M.A., and Nansel, T.R., et al., “Bacterial Vaginosis Assessed by Gram Stain and Diminished Colonization Resistance to Incident Gonococcal, Chlamydial, and Trichomonal Genital Infection,” Journal of Infectious Diseases 202, no. 12 (2010): 19071915.Google Scholar
Mastromarino, P., Vitali, B., and Mosca, L., “Bacterial Vaginosis: a Review on Clinical Trials with Probiotics,” New Microbiologica 36, no. 3 (2013): 229238.Google Scholar
Chen, Song, and Wei, et al., supra note 19.Google Scholar
Reid, G., and Bocking, A., “The Potential for Probiotics to Prevent Bacterial Vaginosis and Preterm Labor,” American Journal of Obstetrics and Gynecology 189, no. 4 (2003): 12021208; Taylor, B.D., Darville, T., and Haggerty, C.L., “Does Bacterial Vaginosis Cause Pelvic Inflammatory Disease?” Sexually Transmitted Diseases 40, no. 2 (2013): 117122.CrossRefGoogle Scholar
Thomas-White, K., Forster, S.C., and Kumar, N., et al., “Culturing of Female Bladder Bacteria Reveals an Interconnected Urogenital Microbiota,” Nature Communications 9, no. 1 (2018): art. no. 1557.CrossRefGoogle Scholar
Stapleton, A.E., “The Vaginal Microbiota and Urinary Tract Infection,” Microbiology Spectrum 4, no. 6 (2016), doi: 10.1128/microbiolspec.UTI-0025-2016; Sumati, A.H. and Saritha, N.K., “Association of Urinary Tract Infection in Women with Bacterial Vaginosis,” Journal of Global Infectious Diseases 1, no. 2 (2009): 151152.CrossRefGoogle Scholar
Kyrgiou, M., Mitra, A., and Moscicki, A.B., “Does the Vaginal Microbiota Play a Role in the Development of Cervical Cancer?” Translational Research 179 (2017): 168182; Nené, N.R., Reisel, D., and Leimbach, A., et al., “Association Between the Cervicovaginal Microbiome, BRCA1 Mutation Status, and Risk of Ovarian Cancer: A Case-Control Study,” Lancet Oncology 20, no. 8 (2019): 11711182; Xu, W. et al., “Mini-Review: Perspective of the Microbiome in the Pathogenesis of Urothelial Carcinoma,” American Journal of Clinical and Experimental Urology 2, no. 1 (2014): 5761.CrossRefGoogle Scholar
Bradshaw and Sobel, supra note 8.Google Scholar
Larsson, P.G. and Forsum, U., “Bacterial Vaginosis — a Disturbed Bacterial Flora and Treatment Enigma,” APMIS 113, no. 5 (2005): 305316; Bradshaw, C.S., Morton, A.N., and Hocking, J., et al., “High Recurrence Rates of Bacterial Vaginosis over the Course of 12 Months after Oral Metronidazole Therapy and Factors Associated with Recurrence,” Journal of Infectious Diseases 193, no. 11 (2006): 14781486; Sobel, J.D., Schmitt, C., and Meriwether, C., Long-Term Follow-up of Patients with Bacterial Vaginosis Treated with Oral Metronidazole and Topical Clindamycin,” Journal of Infectious Diseases 167, no. 3 (1993): 783784.CrossRefGoogle Scholar
Boskey, E.R., Moench, T.R., Hees, P.S., and Cone, R.A., “A Self-Sampling Method to Obtain Large Volumes of Undiluted Cervicovaginal Secretions,” Sexually Transmitted Diseases 30, no. 2 (2003): 107109.CrossRefGoogle Scholar
Gardner, H.L. and Dukes, C.D., “Haemophilus Vaginalis Vaginitis: A Newly Defined Specific Infection Previously Classified Non-Specific Vaginitis,” American Journal of Obstetrics and Gynecology 69, no. 5 (1955): 962976.CrossRefGoogle Scholar
Marrazzo, J.M., Koutsky, L.A., and Eschenbach, D.A., et al., “Characterization of Vaginal Flora and Bacterial Vaginosis in Women Who Have Sex with Women,” Journal of Infectious Diseases 185, no. 9 (2002): 13071313.CrossRefGoogle Scholar
Marrazzo, J.M., Thomas, K.K., Agnew, K., and Ringwood, K., “Prevalence and Risks for Bacterial Vaginosis in Women Who Have Sex with Women,” Sexually Transmitted Diseases 37, no. 5 (2010): 335339.Google Scholar
Marrazzo, J.M., Antonio, M., Agnew, K., and Hillier, S.L., “Distribution of Genital Lactobacillus Strains Shared by Female Sex Partners,” Journal of Infectious Diseases 199, no. 5 (2009): 680683.CrossRefGoogle Scholar
Vodstrcil, L.A., Walker, S.M., and Hocking, J.S., et al., “Incident Bacterial Vaginosis (BV) in Women Who Have Sex with Women Is Associated with Behaviors that Suggest Sexual Transmission of BV,” Clinical Infectious Diseases 60, no. 7 (2015): 10421053.CrossRefGoogle Scholar
Mueller, N.T. et al., “Bacterial Baptism: Scientific, Regulatory Issues Raised by Vaginal Seeding of C-Section-Born Babies,” Journal of Law, Medicine & Ethics 47, no. 4 (2019): 568578.CrossRefGoogle Scholar
Huh, S.Y., Rifas-Shiman, S.L., and Zera, C.A., et al., “Delivery by Caesarean Section and Risk of Obesity in Preschool Age Children: A Prospective Cohort Study,” Archives of Disease in Childhood 97, no. 7 (2012): 610616; Pistiner, M., Gold, D.R., and Abdulkerim, H., et al., “Birth by Cesarean Section, Allergic Rhinitis, and Allergic Sensitization among Children with a Parental History of Atopy,” Journal of Allergy and Clinical Immunology 122, no. 2 (2008): 274279; Sevelsted, A., Stokholm, J., Bønnelykke, K., and Bisgaard, H., “Cesarean Section and Chronic Immune Disorders,” Pediatrics 135, no. 1 (2015): e9298; Thavagnanam, S., Fleming, J., and Bromley, A., et al., “A Meta-Analysis of the Association between Caesarean Section and Childhood Asthma,” Clinical and Experimental Allergy 38, no. 4 (2008): 629633. See also Mueller, N. et al., “Bacterial Baptism: Scientific, Medical and Regulatory Issues Raised by Vaginal Seeding of C-section-born babies,” Journal of Law, Medicine & Ethics 47, no. 4 (2019): 568578.CrossRefGoogle Scholar
Olszak, T., An, D., and Zeissig, S., et al., “Microbial Exposure during Early Life Has Persistent Effects on Natural Killer T Cell Function,” Science 336, no. 6080 (2012): 489493.CrossRefGoogle Scholar
Dominguez-Bello, M.G., De Jesus-Laboy, K.M., and Shen, N., et al., “Partial Restoration of the Microbiota of Cesarean-Born Infants Via Vaginal Microbial Transfer,” Nature Medicine 22, no. 3 (2016): 250253. See also Mueller, supra note 40.CrossRefGoogle Scholar
N. Mueller et al., supra note 40.Google Scholar
Lloyd-Price, J., Abu-Ali, G., and Huttenhower, C., “The Healthy Human Microbiome,” Genome Medicine 8, no. 1 (2016): art. no. 51; Qin, J., Li, R., and Raes, J., et al., “A Human Gut Microbial Gene Catalogue Established by Metagenomic Sequencing,” Nature 464, no. 7285 (2010): 5965.CrossRefGoogle Scholar
Theriot, C.M. and Young, V.B., “Interactions between the Gastrointestinal Microbiome and Clostridium difficile,” Annual Review of Microbiology 69 (2015): 445461.CrossRefGoogle Scholar
Oakley, B.B., Fiedler, T.L., Marrazzo, J.M., and Fredricks, D.N., “Diversity of Human Vaginal Bacterial Communities and Associations With Clinically Defined Bacterial Vaginosis,” Applied and Environmental Microbiology 74, no. 15 (2008): 48984909.CrossRefGoogle Scholar
Staley, C., Kelly, C.R., and Brandt, L.J., et al., “Complete Micro-biota Engraftment Is Not Essential for Recovery from Recurrent Clostridium difficile Infection Following Fecal Microbiota Transplantation,” mBio 7, no. 6 (2016): e0196516, DOI: 10.1128/mBio.01965-16.CrossRefGoogle Scholar
Smillie, C.S., Sauk, J., and Gevers, D., et al., “Strain Tracking Reveals the Determinants of Bacterial Engraftment in the Human Gut Following Fecal Microbiota Transplantation,” Cell Host Microbe 23, no. 2 (2018): 229–40 e5.CrossRefGoogle Scholar
Mayer, B.T., Srinavasan, S., and Fiedler, T.L., et al., “Rapid and Profound Shifts in the Vaginal Microbiota Following Antibiotic Treatment for Bacterial Vaginosis,” Journal of Infectious Diseases 212, no. 5 (2015): 793802; Petrova, M.I., Reid, G., Vaneechoutte, M., and Lebeer, S., “Lactobacillus iners: Friend or Foe?” Trends in Microbiology 25, no. 3 (2017): 182191.CrossRefGoogle Scholar
Gajer, Brotman, and Bai et al., supra note 1.Google Scholar
Eiseman, B., Silen, W., Bascom, G.S., and Kouvar, A.J., “Fecal Enema as an Adjunct in the Treatment of Pseudomembranous Enterocolitis,” Surgery 44, no. 5 (1958): 854859.Google Scholar
van Nood, E., Vreize, A., amd Niewdown, M., et al., “Duodenal Infusion of Donor Feces for Recurrent Clostridium difficile,” New England Journal of Medicine 368, no. 5 (2013): 407415.CrossRefGoogle Scholar
21 U.S. Code §§ 331(k) and 334.Google Scholar
21 U.S. Code § 379a.Google Scholar
United States v. Regenerative Sciences LLC, 741 F.3d 1314 (D.C. Cir. 2014). See also N. Mueller et al., supra note 40.Google Scholar
United States v. Kaplan, 836 F.3d 1199 (9th Cir. 2016). See also N. Mueller et al., supra note 40.Google Scholar
See N. Mueller et al., supra note 40, citing United States v. Geborde, 278 F.3d 926 (9th Cir. 2002) and United States v. Kaplan, 836 F.3d 1199 (9th Cir. 2016).Google Scholar
Reid, G., “Is Bacterial Vaginosis a Disease?” Applied Microbiology and Biotechnology 102, no. 2 (2018): 553558.CrossRefGoogle Scholar
Hickey, R.J., Zhou, X., and Settles, M.L., et al., “Vaginal Micro-biota of Adolescent Girls prior to the Onset of Menarche Resemble Those of Reproductive-Age Women,” MBio 6, no. 2 (2015): e0009715, doi: 10.1128/mBio.00097-15.CrossRefGoogle Scholar
Code of Federal Regulations Sections for Cosmetics Labeling (CFR Title 21, Part 701). 2017, available at <https://www.fda.gov/cosmetics/cosmetics-labeling-regulations/code-federal-regulations-sections-cosmetics-labeling-cfr-title-21-part-701> (last visited October 3, 2019).+(last+visited+October+3,+2019).>Google Scholar
Khoruts, A., Hoffman, D., and Palumbo, F., “The Impact of Regulatory Policies on the Future of Fecal Microbiota Transplantation,” Journal of Law, Medicine & Ethics 47, no. 4 (2019): 482504.CrossRefGoogle Scholar
Sachs, R.E. and Edelstein, C.A., “Ensuring the Safe and Effective FDA Regulation of Fecal Microbiota Transplantation,” Journal of Law and the Biosciences 2, no. 2 (2015): 396415.CrossRefGoogle Scholar
21 C.F.R. 1271.3. 2018.Google Scholar
21 C.F.R. 1271.3 (f)(2). 2018.Google Scholar
21 C.F.R. 1271.10. 2018.Google Scholar
21 C.F.R. 1271.85. 2018.Google Scholar
21 C.F.R. 1271.150. 2018.Google Scholar
21 C.F.R. 1271.290. 2018.Google Scholar
21 U.S. Code § 355c. 2018.Google Scholar
DeLong, K., et al., “Conceptual Design of a Universal Donor Screening Approach for Vaginal Microbiota Transplant,” Frontiers in Cellular and Infection Microbiology (2019), available at <https://www.frontiersin.org/articles/10.3389/fcimb.2019.00306/full> (last visited December 6, 2019).CrossRefGoogle Scholar
Haya, J., Garcia, A., and López-Manzanara, C. L, et al., “Importance of Lactic Acid in Maintaining Vaginal Health: A Review of Vaginitis and Vaginosis Etiopathogenic Bases and a Proposal for a New Treatment,” Open Journal of Obstetrics and Gynecology 4 (2014): 787799.Google Scholar
Muench, D.F., Kuch, D.J., and Wu, H., et al., “Hydrogen Peroxide-Producing Lactobacilli Inhibit Gonococci in Vitro but not during Experimental Genital Tract Infection,” Journal of Infectious Diseases 199, no. 9 (2009): 13691378; Pascual, L., Ruiz, F., Giordano, W., and Barberis, I.L., “Vaginal Colonization and Activity of the Probiotic Bacterium Lactobacillus fermentum L23 in a Murine Model of Vaginal Tract Infection,” Journal of Medical Microbiology 59, no. 3 (2010): 360364; Zarate, G., Santos, V., and Nader-Macias, M.E., “Protective Effect of Vaginal Lactobacillus paracasei CRL 1289 against Urogenital Infection Produced by Staphylococcus aureus in a mouse Animal Model,” Infectious Diseases in Obstetrics and Gynecology (2009): art. no. 48358.CrossRefGoogle Scholar
Yildirim, S., Yeoman, C.J., and Jange, S.C., et al., “Primate Vaginal Microbiomes Exhibit Species Specificity without Universal Lactobacillus Dominance,” The ISME Journal 8 (2014): 24312444.CrossRefGoogle Scholar
Spear, G.T., Gilbert, D., and Sikaroodi, M., et al., “Identification of Rhesus Macaque Genital Microbiota by 16S Pyrosequencing Shows Similarities to Human Bacterial Vaginosis: Implications for Use as an Animal Model for HIV Vaginal Infection,” AIDS Research and Human Retroviruses 26, no. 2 (2010): 193200.CrossRefGoogle Scholar
Ensign, L.M. and Weld, E.D., “Safety and Efficacy of Vaginal Microbiota Transplant (VMT) in Women with Bacterial Vaginosis (BV),” available at <https://clinicaltrials.gov/ct2/show/NCT03769688> (last visited October 3, 2019).+(last+visited+October+3,+2019).>Google Scholar
CDC, “Nearly half a million Americans suffered from Clostridium difficile infections in a single year,” news release, February 25, 2015, available at <https://www.cdc.gov/media/releases/2015/p0225-clostridium-difficile.html> (last visited October 3, 2019).+(last+visited+October+3,+2019).>Google Scholar
DeLong et al., supra note 73.Google Scholar
21 CFR 1271.150. 2018.Google Scholar
Stegmann, B.J. and Carey, J.C., “TORCH Infections. Toxoplasmosis, Other (syphilis, varicella-zoster, parvovirus B19), Rubella, Cytomegalovirus (CMV), and Herpes infections,” Current Women's Health Reports 2, no. 4 (2002): 253258.Google Scholar
Costello, S.P., Conlon, M.A., and Vuaran, M.S., S.P., et al., “Faecal Microbiota Transplant for Recurrent Clostridium difficile Infection Using Long-Term Frozen Stool is Effective: Clinical Efficacy and Bacterial Viability Data,” Alimentary Pharmacology and Therapeutics 42, no. 8 (2015): 10111018.CrossRefGoogle Scholar
Bradshaw and Sobel, supra note 8.Google Scholar
Wilson, J., “Managing Recurrent Bacterial Vaginosis,” Sexually Transmitted Infections 80, no. 1 (2004): 811.CrossRefGoogle Scholar
Surawicz, C.M., Brandt, L.J., and Binion, D.G., et al., “Guidelines for Diagnosis, Treatment, and Prevention of Clostridium difficile Infections,” American Journal of Gastroenterology 108, no. 4 (2013): 478498, at 499.CrossRefGoogle Scholar
Brotman, R.M., Shardell, M.D., and Gajer, P., et al., “Association between the Vaginal Microbiota, Menopause Status, and Signs of Vulvovaginal Atrophy,” Menopause-the Journal of the North American Menopause Society 21, no. 5 (2014): 450458.CrossRefGoogle Scholar
Brotman, R.M., Shardell, M.D., and Gajer, P., et al., “Interplay between the Temporal Dynamics of the Vaginal Microbiota and Human Papillomavirus Detection,” Journal of Infectious Diseases 210, no. 11 (2014): 17231733; Corey, L., Wald, A., and Patel, R., et al., “Once-daily Valacyclovir to Reduce the Risk of Transmission of Genital Herpes,” New England Journal of Medicine 350, no. 1 (2004): 1120.CrossRefGoogle Scholar
Khoruts, Hoffmann, and Palumbo, supra note 63.Google Scholar
Ngugi, B.M., Hemmerling, A., and Bukusi, E.A., et al., “Effects of Bacterial Vaginosis-Associated Bacteria and Sexual Intercourse on Vaginal Colonization with the Probiotic Lactobacillus crispatus CTV-05,” Sexually Transmitted Diseases 38, no. 11 (2011): 10201027.CrossRefGoogle Scholar
Gajer, Brotman, and Bai, et al., supra note 1.Google Scholar
Woodworth, M.H., Neish, E.M., and Miller, N.S., et al., “Laboratory Testing of Donors and Stool Samples for Fecal Microbiota Transplantation for Recurrent Clostridium difficile Infection,” Journal of Clinical Microbiology 55, no. 4 (2017): 10021010.CrossRefGoogle Scholar
U.S. Food and Drug Administration, Bacterial Vaginosis: Developing Drugs for Treatment, Guidance for Industry, August 2019, available at <https://www.fda.gov/media/129530/download> (last visited October 3, 2019).+(last+visited+October+3,+2019).>Google Scholar
U.S. Food and Drug Administration, Guidance for Industry and Food and Drug Administration Staff, Collection of Race and Ethnicity Data in Clinical Trials, October 26, 2016, available at <https://www.fda.gov/media/75453/download> (last visited October 3, 2019).+(last+visited+October+3,+2019).>Google Scholar
Heintzman, J. and Marino, M., “Race and Ethnicity Data in Research,” JAMA 321, no. 12 (2019): 12171218.CrossRefGoogle Scholar
UNOS, Odds for receiving a kidney transplant now equal for black, white and Hispanic candidates, July 12, 2017, available at <https://unos.org/news/odds-equal-of-kidney-transplant-for-minorities/> (last visited October 3, 2019).+(last+visited+October+3,+2019).>Google Scholar
Pacheco, C.M., Daley, S.M., and Brown, T., et al., “Moving Forward: Breaking the Cycle of Mistrust Between American Indians and Researchers,” American Journal of Public Health 103, no. 12 (2013): 21522159.CrossRefGoogle Scholar
Alcendor, D.J., “Evaluation of Health Disparity in Bacterial Vaginosis and the Implications for HIV-1 Acquisition in African American Women,” American Journal of Reproductive Immunology 76, no. 2 (2016): 99107.CrossRefGoogle Scholar
Hoffmann, D.E., Fortenberry, J.D., and Ravel, J., “Are Changes to the Common Rule Necessary to Address Evolving Areas of Research? A Case Study Focusing on the Human Microbiome Project,” Journal of Law, Medicine & Ethics 41, no. 2 (2013): 454469.CrossRefGoogle Scholar