Mammary candidiasis: A medical condition without scientific evidence?

RESEARCH ARTICLE Mammary candidiasis: A medical condition without scientific evidence? Esther Jiménez1¤, Rebeca Arroyo1¤, Nivia Cárdenas1¤, Marı́a Marı́n1, Pilar Serrano2, Leonides Fernández1, Juan M. Rodrı́guez1* 1 Dpt. Nutrition, Food Science and Food Technology, Complutense University of Madrid, Madrid, Spain, 2 Unidadde Endocrinologı́a y Nutrición, Hospital Virgen del Rocı́o, Seville, Spain ¤ Current address: Probisearch, Tres Cantos, Madrid, Spain * a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: Jiménez E, Arroyo R, Cárdenas N, Marı́n M, Serrano P, Fernández L, et al. (2017) Mammary candidiasis: A medical condition without scientific evidence? PLoS ONE 12(7): e0181071. https://doi. org/10.1371/journal.pone.0181071 Editor: Hauke Smidt, Wageningen University, NETHERLANDS Received: December 4, 2016 Accepted: June 26, 2017 Published: July 13, 2017 Copyright: © 2017 Jiménez et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: All relevant data are within the paper. Funding: This work was supported by project AGL2016-75476-R from the Ministerio de Economı́a y Competitividad (Spain). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Competing interests: The authors have declared that no competing interests exist. Abstract Many physicians, midwives and lactation consultants still believe that yeasts (particularly Candida spp.) play an important role as an agent of nipple and breast pain despite the absolute absence of scientific proofs to establish such association. In this context, the objective of this study was to investigate the microorganisms involved in sore nipples and/or painful “shooting” breastfeeding by using a variety of microscopy techniques, as well as culturedependent and–independent identification methods. Initially, 60 women (30 diagnosed as suffering “mammary candidiasis” and 30 with no painful breastfeeding) were recruited to elucidate the role of their pumps on the milk microbial profiles. After realizing the bias introduced by using such devices, manual expression was selected as the collection method for the microbiological analysis of milk samples provided by 529 women with symptoms compatible with “mammary candidiasis”. Nipple swabs and nipple biopsy samples were also collected from the participating women. Results showed that the role played by yeasts in breast and nipple pain is, if any, marginal. In contrast, our results strongly support that coagulasenegative staphylococci and streptococci (mainly from the mitis and salivarius groups) are the agents responsible for such cases. As a consequence, and following the recommendations of the US Library of Medicine for the nomenclature of infectious diseases, the term “mammary candidiasis” or “nipple thrush” should be avoided when referring to such condition and replaced by “subacute mastitis”. Introduction Lactation is probably the only bodily function for which modern medicine has almost no training, protocol or scientifically-acquired knowledge. When women suffer painful breastfeeding, they usually have to face the dilemma of continuing despite the pain or giving it up, preventing mothers and infants from getting the well-recognized health benefits associated to breastfeeding [1–3]. In practice, it is very unusual that they are offered the option of clinical tests (including milk analysis and antibiogram) in order to know the pain etiopathogenesis or to guide the therapeutic approach. PLOS ONE | https://doi.org/10.1371/journal.pone.0181071 July 13, 2017 1 / 19 Are yeasts involved in painful breastfeeding? This situation has contributed to the spread of non-scientific beliefs to explain the origin of painful breastfeeding and to the maintenance of traditional, and often useless, empirical treatments. One of such beliefs is that yeasts (mainly Candida albicans) play an important role in nipple and breast pain. In the absence of fever or flu-like symptoms, the onset of sore burning, painful nipples or radiating or “shooting” pain into the axilla in breastfeeding women has traditionally been diagnosed and treated as “ductal or mammary candidiasis” by many physicians, midwives and lactation consultants [4–9]. Such diagnosis is made in virtually all cases by visual assessment of the breast, without supporting laboratory findings and ignoring that the evidence of a potential association Candida-painful breastfeeding is largely anecdotal [10,11]. Recently, studies applying milk microbial analysis (including some examining for the presence of yeasts) have shown that coagulase-negative staphylococci (CNS), streptococci (mitis and salivarius groups) and corynebacteria may be actually the agents responsible for such symptoms [12–15]. However, studies directed to specifically and systematically investigate the presence or absence of Candida cells and/or DNA in a large collection of milk samples from women with these symptoms are very scarce. In this context, the objective of this work was to elucidate the actual etiology of 529 cases of sore nipples and/or painful breastfeeding, initially diagnosed as “ductal or mammary candidiasis”, by using a great variety of microscopy techniques, as well as culture-dependent and–independent identification methods applied to milk, nipple swabs and nipple biopsy samples. Materials and methods Participating women and collection of the samples Globally, the number of women and the type and number of the samples that were analyzed in this study are shown in Fig 1. Initially, 60 women were recruited in order to elucidate the contribution of milk pumps on the milk microbial load and profile. Among them, 30 women displayed breast/nipple symptoms traditionally associated to “mammary candidiasis” and 30 women had no breastfeeding problems. These women collected one sample obtained by manual expression following the protocol described by Arroyo et al. [16], and a second one by using their own manual milk pump. The internal surfaces of the pumps were also sampled (Fig 1) using a sterile swab, in order to ascertain their role in bacterial milk load. Sample collection was supervised by midwives, gynecologists, pediatricians or nurses. After realizing the strong effect of pumps on the milk microbial pattern, manual expression was selected as the only collection method for further microbiological analyses. Thus, 529 women with symptoms compatible to those related to “mammary candidiasis” were subsequently recruited from July 2011 to July 2015. All of them reported painful breastfeeding with radiating or “shooting” pain into the axilla or the back and 393of these 529 women (74%) also reported sore, burning, or painful nipples. Women with symptoms o (...truncated)