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Menstruation in Adolescents: What Do We Know? and What Do We Do with the Information?
Mini-Review Menstruation in Adolescents: What Do We Know? and What Do We Do with the Information? Paula J. Adams Hillard MD * Department of Obstetrics and Gynecology, Stanford University School of Medicine, Stanford, CA
a b s t r a c t The menstrual cycle has been recognized as a vital sign that gives information about the overall health of an adolescent or young adult female. Significant deviations from monthly cycles can signal disease or dysfunction. This review highlights the evidence based parameters for normal puberty, menarche, cyclicity, and amount of bleeding. The review addresses sources of information available online, noting inaccuracies that appear in web sites, even and especially those targeting adolescents. The review includes a call to action to provide accurate information about the menstrual cycle as a VITAL SIGN. Key Words: adolescent menstruation, amenorrhea, menarche, puberty
Introduction
The menstrual cycle is a vital sign. That is, just like pulse, respiration, blood pressure, and temperature, a menstrual history gives information about a woman's overall health. Girls, adolescents, and adult women need to attend to the regularity of their menstrual cycles, and if the cycles are not regular and approximately monthly, something may be out of balance. It may be a hormone imbalance (hyper-androgenism, most commonly polycystic ovary syndrome (PCOS), or thyroid dysfunction), or over-exercise, or an eating disorder, or an uncommon condition such as primary ovarian insufficiency. In about the year 2000, 2 colleagues of mine, Dr Larry Nelson from the NIH and Dr Justina Trott from the University of New Mexico met me at a women's health conference in Chantilly, Virginia. Over lunch, the three of us talked about how each of us views the menstrual cycle. Dr Nelson, a well respected NICHD researcher, had learned from listening to women who were ultimately diagnosed with primary ovarian insufficiency (POI, a condition previously termed premature ovarian failure1) that over half of the women ultimately diagnosed with POI had visited a clinician 3 or more times before lab work was performed to enable a diagnosis. These women had experienced false reassurances and a delay in the ultimate diagnosis of their condition. In one-quarter of these women, it took longer than 5 years before the diagnosis was made.2 Dr Trott and her colleagues with the American College of Women's Health Physicians had developed an online educational toolda concept map of the menstrual cycledto facilitate the development of an interdisciplinary and womancentered women's curriculum (Fig. 1).3 They described the concept map as highlighting relationships between The author, Paula J. Adams Hillard, MD, has been a consultant and member of the Scientific Advisory Panel for Merck and Bayer Healthcare. * Address correspondence to: Paula J. Adams Hillard, MD, Department of Obstetrics and Gynecology, Stanford University School of Medicine, Stanford, CA 94305-5101; Phone: (650) 725-3755; fax: (650) 723-7737
concepts of menstruation as a knowledge framework that builds capacity and allows the learner to adapt knowledge to multiple settings and across disciplines. I was intrigued by this idea of a concept map, which has more recently been termed “mind-mapping,” and I include here the mind-map that I developed using mind-mapping software (of which many free open source and paid commercial versions are available) in preparation for this talk (Fig. 2). At that chance luncheon meeting and discussion, Dr Nelson, Dr Trott, and I agreed that the menstrual cycle did not get the respect that it deserves. We could all relate to the idea that a complex series of hormonal, psychological, anatomic, and physiologic factors needed to be in balance for regular monthly menses to occur. The absence of such regularity should prompt an assessment of factors that might be adversely impacting the cycledthat is, the menstrual cycle should be assessed as a “vital sign”; cycle irregularity outside of given norms should prompt further assessment to determine what may be “out of balance”djust as an abnormal pulse, blood pressure, respiratory rate, or temperature may signal a pathologic process. This concept has gained traction in ob-gyn and adolescent medicine/pediatrics, with the publication of a joint American College of Obstetricians and Gynecologists (ACOG) and American Academy of Pediatrics (AAP) publication from the ACOG Committee on Adolescent Health Care.4,5 I am proud to trace the origins of this concept to the luncheon conversation with my colleagues in women's health. In recent years, the concept of pain as a fifth vital sign has become a focus of patient assessment. This concept has been sanctioned and given credence by the Joint Commission on Accreditation of Healthcare Organization's institution of pain management standards for hospitals. A number of other signs have been proposed as a 6th vital sign, including urinary continence, emotional distress, shortness of breath, gait speed, and end-tidal CO2.6 But among gynecologists and pediatricians, ACOG and the AAP have implanted the concept that “the menstrual cycle is a vital sign.” I have made this
1083-3188/$ - see front matter Ó 2014 North American Society for Pediatric and Adolescent Gynecology. Published by Elsevier Inc. http://dx.doi.org/10.1016/j.jpag.2013.12.001
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Fig. 1. Menstrual Cycle Concept Map. Reprinted from Hoffman et al, Concept mapping: A tool to bridge the disciplinary divide, Am J Obstet Gynecol 2002; 187(3 Suppl), pages S41-3, Copyright (2002) with permission from Elsevier.
concept a part of my campaign for adolescent girls' wellness, talking about it at every opportunity. I thank the program committee of the North American Society for Pediatric and Adolescent Gynecology (NASPAG) for allowing me to stand on my soapbox to talk about not only what we know about normal menstrual function in adolescents, but also about how we can transmit what we know to our colleagues in other disciplines, to our patients and their parents, to coaches, and other who need to know. Without an understanding for what is normal, girls with abnormal bleedingdtoo heavy, too frequent, lasting too long, or too infrequent, or who have associated menstrual paindare inappropriately reassured and denied appropriate evaluation and management. I stand on my soapbox because I want to change the world and the future for women and girls, to move us beyond our current knowledge and practices, to get ideas from my colleagues and listeners, and to encourage us to work together to change the future for women and girls. The research and advocacy must move knowledge and practices forward. Toward this goal, I want to speak authentically about women's experiences. I speak as I know them personally: as a girl, now woman, who is aspiring to be a crone; as a physician; as a feminist; as a mother; and as a wife. I speak from my soapbox as I hear of women's and girls' experiences from my patients, trying to actively listen. I speak as an educator who focuses on teaching and mentoring trainees through a Stanford University School of Medicine program called Educators for CARE, which stands for Compassion, Advocacy, Responsibility, and Empathy. And I speak as an advocate for the underserved population of young girls and adolescents.
What's Normal?
In my own clinical practice of pediatric and adolescent gynecology, menstrual problems are a large component of the problems that I see. (See another mind map in Fig. 3.) I have several messages about menstrual cycles when I speak with primary clinicians and parents, but one of the messages is that prospectively charting menstrual bleeding can create a visual picture that can be worth a thousand words. I commonly see patients who have been reassured by their primary clinicians that girls often have irregular periods during the first few years after menarche. While this is true, a menstrual calendar like the one pictured in Fig. 4 is clearly outside of the range of normal. A menstrual calendar, whether an old-fashioned paper calendar (Fig. 4) or a menstrual history documented in one of many “apps” available for smartphones, is a wonderful educational tool that primary care clinicians can encourage their patients to complete. The reverse side of the printed card can contain information about normal menstrual cycles (Fig. 5) Most of us learned about normal menstrual cyclicity through textbooks, which are increasingly available online as e-textbooks, but textbooks are typically out of date by the time they are published and we must be sure that we are basing our practices on the best evidencedas collated in evidence-based reviews such as the Cochrane Database of Systematic Reviews. Our professional societies, including ACOG and AAP, publish Committee Opinions and Technical Bulletins, including the ones that summarize the statistically based evidence for normal menstrual cycles.4,5 Typical gynecology textbooks indicate
P.J.A. Hillard / J Pediatr Adolesc Gynecol 27 (2014) 309e319 Fig. 2. Mind Map developed by the author in preparation for the NASPAG Annual Clinical and Research Meeting Elsevier lectureship plenary session on Menstruation as a Vital Sign: Giving the menstrual cycle the attention it deserves, San Diego, CA, April 18, 2013.
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Vaginitis
Frequent Bleeding
Acute Symptoms
Heavy M enstrual Bleeding
STIs UTIs
Amenorrhea
M enstrual Problems
Dysmenorrhea
Other
PCOS
Vulvar lesions
M enstrual Suppression PJAH Adolescent Clinical Practice Ovarian cysts Dysmenorrhea M yofascial Endometriosis
Acute Pain
Adnexal torsion PID
Chronic Pain
Vulvar
Contraception/Hormonal therapy
Fig. 3. PJAH Adolescent Clinical Practice–Menstrual problems figure prominently among the clinical issues in the author's pediatric and adolescent gynecology practice. PJAH5P.J. Adams Hillard.
that the average age of menarche is 12.8, that precocious puberty is defined by any pubertal development prior to the age of 8, that primary amenorrhea is defined as no menstrual periods by age 16, that early cycles in the first 1-2 years after menarches are anovulatory and irregular, that typical cycles last 2-7 days, and that the average blood loss per cycle is 30 ml, ranging from 20-60 ml. While some of this information is backed by evidence, other aspects of this “conventional wisdom” are not. Depending on the source, online resources commonly used by medical students or by clinicians outside of the specialties of pediatrics and obstetrics and gynecology, including Wikipedia, may or may not provide accurate evidence-based information. It must be noted that all of the guidelines and references to menstrual cycles refers to bleeding without the influence of hormonal therapy. Thus a brief review of the evidence is warranted.
Fig. 4. “Irregular bleeding” documented on a menstrual calendar.Ă
Pubertal Onset
Classically, textbooks have described precocious puberty as the onset of signs of pubertal development prior to the age of 8 years. With the publication of the large, prospective study through the Pediatric Research in the Office Setting network, this dictum was called into question.7 In this study, pediatric practitioners in office practices around the country received standardized training in the assessment of pubertal maturation and the level of sexual maturation of over 18,000 girls ages 3-12. Ninety percent of the girls examined were white and 9.6% African American. At age 7, 27.2% of African American girls and 6.7% of white girls had evidence of breast and/or pubic hair development. At the age of 8, the percentages were 48.3% and 14.7%.7 These data were met with skepticism, but a subsequent multisite study confirmed that at age 7, 10.4% of white, 23.4% of black
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Fig. 5. Menstrual CalendardReverse side.Ă
non-Hispanic, and 14.9% of Hispanic girls had attained breast stage 2 as a marker of pubertal development.8 A review panel concluded that there has indeed been a decline in the age of onset of the onset of puberty in girls since 1940.9 This has been linked to increasing rates of obesity.10 Even with some consensus, the call for reexamination of the age limit for defining when puberty is precocious has been controversial.11 As for delayed puberty, lack of breast development by about age 13 represents 2.5 standard deviations from the mean, and thus should prompt evaluation.12
Table 1 Common Causes of Primary Amenorrhea Category
Approximate Frequency (%)
Breast development Mullerian agenesis Androgen insensitivity Vaginal septum Imperforate hymen Constitutional delay No breast development: high FSH 46 XX 46 XY Abnormal No breast development: low FSH Constitutional delay Prolactinomas Kallman syndrome Other CNS Stress, weight loss, anorexia PCOS Congenital adrenal hyperplasia Other
30 10 9 2 1 8 40 15 5 20 30 10 5 2 3 3 3 3 1
Reprinted from Fertility and Sterility, Vol 90 / Practice Committee of American Society for Reproductive Medicine. Current Evaluation of Amenorrhea, S219-25. Copyright 2008 with permission from American Society for Reproductive Medicine.
Menarche
Although there is increasing evidence noting a decline in the age of onset of puberty, there is less agreement as to whether there have been significant declines in the age of menarche.9 There is evidence that the age of menarche in the U.S. has declined from the early 1800s until the 1950s.13 Since this time, the age of menarche may have plateaued, or perhaps declined only slightly, with menarche typically occurring between the ages of 12 and 13.4,14-19,20 Racial and ethnic differences in the age of menarche have been noted in recent studies, with black girls having earlier onset of puberty and menarche than white girls, with Hispanic or Mexican American girls being intermediate between black and white girls.9 Earlier studies, including the classic Marshall and Tanner report, did not include ethnically or racially diverse populations. There is international variation in age of menarche as well, with likely influence of socioeconomic conditions, nutrition, and access to healthcare.4 Menarche typically occurs within 2-3 years after the onset of breast development (thelarche); within this time-frame, the earlier the onset of puberty, the longer the interval to menarche.21 Menarche typically occurs at Tanner stage IV breast development, and menarche is rare prior to the achievement of breast stage III development.22 Age 9 represents 2.5 SD below the mean for age of menarche.23 Primary Amenorrhea
Classically, primary amenorrhea has been defined as no menses by age 16; recent studies have called this dictum into question. By age 15, 95%-98% of adolescents will have had their first menstrual period.15,16,19,23,24 This statistically derived
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Table 2 Menstrual Terminology and Parameters for Adolescent Years Clinical Dimension Frequency (days)
Regularity
Duration of flow (days)
Volume of blood loss (ml)
Description Frequent Normal Infrequent Absent Regular Irregular Prolonged Normal Shortened Heavy Normal Light
Normal Limits 5th-95th Percentile 21-45 days23,26,32,33,43,44 O90 days32,33
2-7 days23,26,43,44 O80 ml associated with anemia37,38 30 ml
definition for primary amenorrhea should lead to an evaluation of girls who have not had the onset of menses by age 15. Failure to evaluate these girls can delay the diagnosis of a number of conditions with the potential for significant adolescent or adult morbidity such as eating disorders or polycystic ovary syndrome, as well as other conditions with implications for future reproductive potential such as primary ovarian insufficiency. See Table 1 for a list of possible causes of primary amenorrhea from the American Society for Reproductive Medicine. Menstrual Bleeding
The terms used to describe abnormal menstrual bleeding have long been confusing, with imprecise definitions and inconsistency in the use of terms such as menorrhagia, metrorrhagia, menometrorrhagia, hypermenorrhea, hypomenorrhea, dysfunctional uterine bleeding, and others. An international meeting was held to make the case for describing menstrual bleeding in terms of cycle regularity, frequency, duration of flow, and volume.25 See Table 2, which list these terms, along with evidence-based norms for adolescents. Menstrual Cyclicity
A longitudinal, multicenter study sponsored by the World Health Organization provides information about Table 3 Causes of Menstrual Irregularity Pregnancy Endocrine causes Poorly controlled diabetes mellitus Polycystic ovary syndrome Cushing's disease Thyroid dysfunction Premature ovarian failure Late-onset congenital adrenal hyperplasia Acquired conditions Stress-related hypothalamic dysfunction Medications Exercise-induced amenorrhea Eating disorders (both anorexia and bulimia) Tumors Ovarian tumors Adrenal tumors Prolactinomas Reprinted from Obstet Gynecol 2006, 108:1323-8. ACOG Committee on Adolescent Health Care: ACOG Committee Opinion No, 349, November 2006: Menstruation in girls and adolescents: using the menstrual cycle as a vital sign. ACOG Committee Opinion Number 349, November 2006 (Reaffirmed 2009), Copyright 2006 with permission from Wolters Kluwer Health.
menstrual cyclicity in adolescents.26 Menstrual cycles are more variable in adolescents than in adults. In particular, the interval from the first to the second menstrual period can be longer than subsequent cycles; in the WHO international multicenter study, the first cycle was longer than 40 days in 38% of girls.26 However, the median length of even the first cycle was 34 days.26 Many, if not most early cycles are anovulatory, with the frequency of ovulation related to the gynecologic age (time since menarche) as well as chronologic age at menarche.27-31 Girls who are younger at the time of menarche achieve regular ovulatory cycles in a shorter period of time that those who are older at the time of menarche.29 In spite of the facts that many menstrual cycles in adolescents are anovulatory and that cycles in adolescents are irregular, it is not true that “anything goes” with regard to cycle length. Bleeding that occurs while an individual is taking hormonal therapy has a different pathophysiologic mechanism compared to bleeding not under such influence and thus this review refers only to bleeding on young women who are not taking any hormonal therapy such as birth control. Two very large studies inform our knowledge of menstrual cyclicity during adolescence; Treloar followed 2702 women over 27 years time, reporting on 275,047 cycles, and Vollman reported data from 656 women with 31,645 cycles.32,33 These studies and others cited above indicate that cycle length in adolescents is usually between 21 and 45 days, in spite of anovulatory cycles.4 By the third gynecologic year, most cycles are 21-34 days long, as is normal in adults.26,31 Ninety days represents the 95% for cycle length, even in the first gynecologic year,32 and thus should prompt evaluation. Cycles should show increasing regularity with time; if this is not the case, pathology (such as PCOS, eating disorders, thyroid disease, or even rare conditions such as primary ovarian insufficiency) should be considered. These conditions may have significant impact on future bone health, cardiovascular risks, and fertility. See Table 3 for causes of menstrual irregularity in adolescents. The most common condition that can cause secondary amenorrhea (besides pregnancy) is PCOS, particularly among girls with signs of hyperandrogenism including moderate to severe acne and excess hair growth. Making the diagnosis of PCOS allows for appropriate management of irregular bleeding, prevention of heavy or prolonged menstrual bleeding, and potentially minimizes the metabolic sequelae that may accompany the condition by a focus on lifestyle interventions such as weight loss and exercise. More research is needed into the topic of adolescent anovulation and the typical progression from anovulatory cycles to normal, regularly ovulatory cycles vs abnormal adolescent anovulation with abnormal menstrual cycles that are associated with hyperandrogenism and that remain abnormal in cyclicity. Other causes of secondary amenorrhea are listed in Table 4, some of which are common, and others rare, particularly in adolescents. Diagnoses such as eating disorders and the female athlete triad have a strong link to bone health and low bone density may be a risk to subsequent health.
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Table 4 (continued)
I. Anatomic defects (outflow tract) € llerian agenesis (Mayer-Rokitansky-Kuster-Hauser syndrome) A. Mu B. Complete androgen resistance (testicular feminization) C. Intrauterine synechiae (Asherman syndrome) D. Imperforate hymen E. Transverse vaginal septum F. Cervical agenesisdisolated G. Cervical stenosisdiatrogenic H. Vaginal agenesisdisolated I. Endometrial hypoplasia or aplasiadcongenital II. Primary hypogonadism A. Gonadal dysgenesis 1. Abnormal Karyotype a. Turner syndrome 45,X b. Mosaicism 2. Normal karyotype a. Pure gonadal dysgenesis i. 46,XX ii. 46,XY (Swyer syndrome) B. Gonadal agenesis C. Enzymatic deficiency 1. 17a-Hydroxylase deficiency 2. 17,20-Lyase deficiency 3. Aromatase deficiency D. Premature ovarian failure 1. Idiopathic 2. Injury a. Chemotherapy b. Radiation c. Mumps oophoritis 3. Resistant ovary a. Idiopathic III. Hypothalamic causes A. Dysfunctional 1. Stress 2. Exercise 3. Nutrition-related a. Weight loss, diet, malnutrition b. Eating disorders (anorexia nervosa, bulimia) 4. Pseudocyesis B. Other disorders 1.Isolated gonadotropin deficiency a. Kalimann syndrome b. Idiopathic hypogonadotropic hypogonadism 2. Infection a. Tuberculosis b. Syphilis c. Encephalitis/meningitis d. Sarcoidosis 3. Chronic debilitating disease 4. Tumors a. Craniopharyngioma b. Germinoma c. Hamartoma d. Langerhans cell histiocytosis e. Teratoma f. Endodermal sinus tumor g. Metastatic carcinoma IV. Pituitary causes A. Tumors 1. Prolactinomas 2. Other hormone-secreting pituitary tumor (ACTH, thyrotropinstimulating hormone, growth hormone, gonadotropin b. Mutations of FSH receptor c. Mutations of LH receptor d. Fragile X syndrome 4. Autoimmune disease 5. Galactosemia V. Other endocrine gland disorders A Adrenal disease 1. Adult-onset adrenal hyperplasia 2. Cushing syndrome B. Thyroid disease 1. Hypothyroidism 2. Hyperthyroidism (continued)
C. Ovarian tumors 1. Granulosa-theca cell tumors 2. Brenner tumors 3. Cystic teratomas 4. Mucinous/serous cystadenomas 5. Krukenberg tumors 3. Nonfunctional tumors (craniopharyngioma) 4. Metastatic carcinoma B. Space-occupying lesions 1. Empty sella 2. Arterial aneurysm C. Necrosis 1. Sheehan syndrome 2. Panhypopituitarism D. Inflammatory/infiltrative 1. Sarcoidosis 2. Hemochromatosis 3. Lymphocytic hypophysitis E. Gonadotropin mutations (FSH) VI. Multifactorial causes A Polycystic ovary syndrome Reprinted from Fertility and Sterility, Vol 90 / Author(s), Current Evaluation of Amenorrhea, S219. Copyright (2008), with permission from American Society for Reproductive Medicine.
Abnormal Menstrual Flow
Menstrual flow has been described using a number of terms that do not have a standard definition: menorrhagia, metrorrhagia, menometrorrhagia, polymenorrhea, hypermenorrhea, hypomenorrhea, oligomenorrhea, dysfunctional uterine bleeding, and abnormal uterine bleeding. These terms have varying definitions and uses, so there has been a move to standardize the terminology, describing cycle regularity as irregular, regular, or absent; frequency of menstruation as frequent, normal, or infrequent; duration of menstrual flow as prolonged, normal, or shortened; and the volume of menstrual flow as heavy, normal, or light.34,35 Absent menstrual flowdamenorrheadsometimes defined as no bleeding for 90 days, is associated with a number of medical conditions such as drug therapy with antipsychotics, depot medroxyprogesterone, GnRH therapy, hyperprolactinemia, ovarian failure with abnormal karyotype, primary ovarian insufficiency, polycystic ovary syndrome, eating disorders, the female athlete tried, and “stress.” Some of these conditions are associated with hypoestrogenism and thus have a relationship to bone health. Heavy Menstrual Bleeding
Excessively heavy bleeding has been defined in the past as blood loss great than 80 ml/period, although it has been suggested that this correlates poorly with patient perceptions, difficulties containing blood flow, impact on daily life, other menstrual symptoms, or other factors such as impact of flow on daily activities.36 The rate of pad/tampon change (requiring a change more than every 1-2 hours) has been shown to correlate with measured blood loss and bleeding O 80 ml/period has been associated with the development of anemia.37,38 The classic study by Claessens, published in 1981, looked at a series of girls presenting to an emergency room with complaints of acute menorrhagia.39 Overall, about one-fifth
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Table 5 Menstrual Conditions That May Require Evaluation Menstrual periods that: Have not started within 3 years of thelarche Have not started by 13 years of age with no signs of pubertal development Have not started by 14 years of age with signs of hirsutism Have not started by 14 years of age with a history or examination suggestive of excessive exercise or eating disorder Have not started by 14 years of age with concerns about genital outflow tract obstruction or anomaly Have not started by 15 years of age Are regular, occurring monthly, and then become markedly irregular Occur more frequently than every 21 days or less frequently than every 45 days Occur 90 days apart even for one cycle Last more than 7 days Require frequent pad or tampon changes (soaking more than one every 1-2 hours) Reprinted from Obstet Gynecol 2006, 108 (5):1323-8. ACOG Committee on Adolescent Health Care, American Academy of Pediatrics Committee on Adolescence, Menstruation in Girls and Adolescents: Using the Menstrual Cycle as a Vital Sign. ACOG Committee Opinion Number 349, November 2006 (Reaffirmed 2009), Copyright (2006) with permission from Wolters Kluwer Health.
of those who presented with heavy bleeding were found to have a primary coagulopathy, with about one-fourth of those whose initial hemoglobin was !10 g/100ml, about one-third of those requiring transfusion, and nearly half of those who presented at menarche having a bleeding disorder, such as von Willebrand disease or idiopathic thrombocytopenic purpura. The incidence of von Willebrand disease in the US is approximately 1%-2%; the statistics rise to 13%-20% of those with heavy menstrual bleeding, and perhaps as many as 50% of teens who present to an Emergency Department with excessive menstrual bleeding have a bleeding disorder.40-42 Thus testing for a bleeding disorder in adolescents with heavy menstrual bleeding is appropriate, particularly those whose cycles fall within the 21-45 day parameters for normal cycles. Prolonged Menstrual Bleeding
Menstrual flow in adolescents, as in older women, typically lasts from 2 to 7 days.23,26,43,44 Unlike other menstrual parameters discussed above, the normal duration of menstrual flow cited in textbooks is typically accurately stated, likely because it does not differ from that seen in adult women. What's Normal: Summary
The parameters for normal menstrual cycles in adolescents have been characterized in terms of onset, frequency, regularity, duration, and amount of flow, as cited above. Table 5, from the ACOG Committee Opinion on adolescent menstruation, lists menstrual conditions that may require evaluation, based on the statistical evidence. It is definitely not true that “anything goes” in terms of menstrual cyclicity, duration, amount of flow, or onset. Failure to evaluate teens who meet the criteria cited in the Committee Opinion can be a significant disservice to young women, leading to unnecessary discomfort, embarrassment, poorer quality of life, adverse self esteem, and current or future health risks such as anemia and low bone mineral density, as well as potential
metabolic and cardiovascular risks.14,45-47 Adolescents deserve our attention to their menstrual cycles as a vital sign. Just as with other vital signs like pulse and respiration, values outside of statistically derived normal parameters may signal disease or derangements in normal health. Today's Girls and the Menstrual Cycle
When most of us were approaching the age of menarche, we typically learned about “periods” from our moms, supplemented by a special “health class” on puberty in the 5th grade, in which the class was segregated by sex, and we were given a talk by a nurse, health educator, or science teacher in which we heard about growing up, including for the girls, primarily menstruation. In my own case, I supplemented these sources by reading my mother's nursing textbooks, as well as the World Book Encyclopedia. I can also recall rather furtive but frequent phone calls to a best friend, in which we talked about puberty and growth. Conversations with older girls on the playground also supplemented the official curriculum. My young pre-adolescent patients today also typically get information from their momsdmost of whom tell me that they vow to do a better job of sexuality education for their daughters than they themselves had experienced. The fifth grade segregated health classes also still exist. Girls and boys still talk about sex on the playground and with friends on the phone, but nowadays the phone may be their own cellphone, rather than a “land line” shared by the family. Girls also learn about menstruation and their changing bodies through more educational books, such as the American Girl series book titled, “The Care & Keeping of YoudThe Body Book for Girls,” of which over 3 million copies have been sold. Many YouTube videos videotaped and uploaded to the internet by 11 and 12-year-old girls explain the “first period” to their near peers. I was unsure about what information a teen might find today, so I made an effort to learn what girls might discover if they used a Google search to get information. I wondered what search terms a girl would use. The results were somewhat different when I googled “period,” a term that I supposed might come to mind, compared with “menstruation.” Googling “period” brought me to a Wikipedia page in which I found 6 categories of definitions and I ultimately found “menstruation” in the science and mathematics category. I supposed that a girl might then follow the hyperlink to “menstruation” on Wikipedia. The exciting (but scary) thing about Wikipedia is that anyone can edit an entry. When I found erroneous information about adolescent menstrual periods on the “menstruation” page, I simply logged in as an editor and provided the evidence-based information that I've cited above! How gratifyingdto be able to correct misinformation with keystrokes. So if a young girl were to find her way to Wikipedia, and be able to wade through the considerable verbiage, she would find accurate information. I'm not sure how often this has happened or will happen, although I'm sure that Wikipedia could provide that information. And it's not an impossibility that a 5th or 6th grader would read the entry; after all, I
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regularly read the encyclopedia at that age. However, there are multiple other web sites where a girl might find herself that would not provide accurate information, or worse, where she might find age-inappropriate information like pornography. I recently had a parent who described to me how his 7year-old daughter had discussed “sex” with a friend on the playground, and who had subsequently googled the word. The parent was more than a little distressed to find multiple pornography sites on the family computers before they were able to install the appropriate parental controls. These parental controls might or might not block web sites that are intended for pre-teens and teens to get health-related information. In searching for menstrual information on the internet, I found 19 web sites targeted for adolescents which varied in the accuracy of the information they provided. I assumed that 1 question a girl might want to know would be “by what age should menstrual periods start?” Of these 19 sites, 5 provided no answer, and only 4 gave the correct answer of 15 years. Notably, youngwomenshealth.org, the excellent web site from Boston Children's Hospital, and a
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governmental web site, womenshealth.gov, gave consistently accurate information. Other web sites in which periods are addressed and girls' questions are answered in an age-appropriate manner included web sites from companies that make menstrual hygiene/catamenial products. These sites were generally informative, but did not provide accurate information about normal menstrual parametersdproviding an opportunity for us to help educate the health educators who design and edit these web sites. In addition to internet web sites, multiple menstrual “apps” now exist for smart phones and tablets that enable girls and women to track their cycles. I downloaded over 30 free web sites (more apps were available for a price). I was sincerely disappointed to learn that not one of them provided notification of menstrual cycles that were outside of the statistically derived normal parameters for either adolescents or for adult women. From my basic high school programming experience (albeit in FORTRAN, over 40 years ago), I would not imagine that such an app would be that difficult to write. I'm disappointed that this
Fig. 6. Mind Map: Who Needs to Know What We Know about the Menstrual Cycle. POI 5 Primary Ovarian Insufficiency, ED 5 Eating Disorders, DD 5 Developmental Disabilities.Ă
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hasn't yet been added as a feature to the multiple menstrual apps that currently compete for advertisers and customers. Which brings me back to my CALL TO ACTION: that we as clinicians and educators would speak to girls themselves, to their parents, to those with medical conditions that may impact or be impacted by the menstrual cycle, to our colleagues in other disciplines, to health educators, to coaches, to catamenial product manufactures, and to those in the pharmaceutical industry who have the opportunity to influence decisions that can have a profound influence on girls' lives. See Fig. 6. The Menstrual Cycle from an International Perspective
Menstruation is beginning to be recognized as an international issue related to the education of girls in developing countries. Nicholas Kristof, columnist for the New York Times, who in 2009 published the book “Half the Sky: Turning Oppression into Opportunity for Women Worldwide” with his journalist wife Sheryl WuDunn, has raised the concern that one of the reasons that girls in Africa and Asia miss school is that they have difficulty managing their menstrual periods.48 They initially suggested that lack of menstrual hygiene products led to increased absenteeism and that this in turn contributed to academic difficulties that ultimately resulted in withdrawal from school. Nonprofit organizations have developed programs to help girls manage their menses. “Days for Girls International” has developed feminine hygiene kits that are sewn by women in micro enterprise projects and distributed to “empower girls and women worldwide with more dignity, health and safety through quality sustainable menstrual management.”49 A TED talk on “how I started a sanitary napkin revolution” has received over a half million views, and features a charismatic speaker advocating for local business using a simple machine he designed, inspired by his wife's challenges in paying for menstrual supplies, to make inexpensive menstrual napkins in India.50 The “Because I am a Girl” campaign supports girls' education, including a project to help girls stay in school through menstrual hygiene education.51 One pilot study in Ghana looked at school attendance in 3 groups: a group of girls who received menstrual pads plus education, another that received only puberty education, and a control group.52 After 3 months, pads plus education improved attendance by 9%; at 5 months, puberty education also improved attendance. Another study from Nepal showed no significant impact of providing girls with menstrual cups on keeping girls in school, but other factors such as cultural beliefs, taboos, menstrual cramps, limitations of underwear and water for hygiene, and bullying were felt to be confounding factors.53 The Museum of Menstruation and Women's Health has solicited input from women about the slang words and expressions that they use to describe their periods; many of these phrases reflect negatives about menstruation, suggesting the limitations and burdens that women experience with regard to difficulty managing their menses and menstrual-associated symptoms.54
What do we do with the evidence-based information about menstruation?
Moving forward, it's clear that the information about statistically-derived norms for menstruation needs to be distributeddto our colleagues, as has been noted; through professional organizations beyond NASPAG, ACOG, and AAP to the American Association for Family Physicians, the Society for Menstrual Cycle Research, through professional organizations for nurse practitioners, physicians' assistants, internists and other primary clinicians; using apps, pointof-care references, electronic media linked to search engines, using social media; and working with organizations that bring together girls and women, non-governmental organizations internationally, nonprofit organizations in the US, pharma, and international aid organizations. The message is that the menstrual cycle is a VITAL SIGN. We need to join together in talking about what is normal with regard to adolescents' menstruation cycles, and what is not. Menstruation Matters; Period! We'd like to grant the menstrual cycle the respect that it deserves as a marker for physiologic wellness. References 1. Nelson LM: Clinical practice. Primary ovarian insufficiency. N Engl J Med 2009; 360:606 2. Alzubaidi NH, Chapin HL, Vanderhoof VH, et al: Meeting the needs of young women with secondary amenorrhea and spontaneous premature ovarian failure. Obstet Gynecol 2002; 99(5 Pt 1):720 3. Hoffman E, Trott J, Neely KP: Concept mapping: a tool to bridge the disciplinary divide. Am J Obstet Gynecol 2002; 187(3 Suppl):S41 4. ACOG Committee on Adolescent Health Care: ACOG Committee Opinion No. 349, November 2006: Menstruation in girls and adolescents: using the menstrual cycle as a vital sign. Obstet Gynecol 2006; 108:1323 5. American Academy of Pediatrics Committee on Adolescence, American College of Obstetricians and Gynecologists Committee on Adolescent Health Care, Diaz A, Laufer MR, Breech LL: Menstruation in girls and adolescents: using the menstrual cycle as a vital sign. Pediatrics 2006; 118:2245 6. Wikipedia contributors. Vital signs. Wikipedia, The Free Encyclopedia. Available: http://en.wikipedia.org/w/index.php?title5Vital_signs&oldid555 0559029. Accessed April 20, 2013 7. Herman-Giddens ME, Slora EJ, Wasserman RC, et al: Secondary sexual characteristics and menses in young girls seen in office practice: a study from the Pediatric Research in Office Settings network. Pediatrics 1997; 99:505 8. Biro FM, Galvez MP, Greenspan LC, et al: Pubertal assessment method and baseline characteristics in a mixed longitudinal study of girls. Pediatrics 2010; 126:e583 9. Euling SY, Herman-Giddens ME, Lee PA, et al: Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics 2008;(121 Suppl 3):S172 10. Biro FM, Greenspan LC, Galvez MP: Puberty in girls of the 21st century. J Pediatr Adolesc Gynecol 2012; 25:289 11. Kaplowitz PB, Oberfield SE: Reexamination of the age limit for defining when puberty is precocious in girls in the United States: implications for evaluation and treatment. Drug and Therapeutics and Executive Committees of the Lawson Wilkins Pediatric Endocrine Society. Pediatrics 1999; 104(4 Pt 1):936 12. Largo RH, Prader A: Pubertal development in Swiss girls. Helv Paediatr Acta 1983; 38:229 13. Wyshak G, Frisch RE: Evidence for a secular trend in age of menarche. N Engl J Med 1982; 306:1033 14. Adams Hillard PJ: Menstruation in Adolescents: What's Normal, What's Not. In: Gordon CM, Welt C, Rebar RW, et al, editors. The Menstrual Cycle and Adolescent Health, vol. 1135. New York, NY, Academy of Sciences, 2008, pp 29e35 15. Freedman DS, Khan LK, Serdula MK, et al: Relation of age at menarche to race, time period, and anthropometric dimensions: the Bogalusa Heart Study. Pediatrics 2002; 110:e43 16. Macmahon B: Age at Menarche: United States, 1973. Rockville, MD: National Center for Health Statistics; 1974. DHEW publication [HRA] 74e1615 17. Demerath EW, Towne B, Chumlea WC, et al: Recent decline in age at menarche: the Fels Longitudinal Study. Am J Hum Biol 2004; 16:453
P.J.A. Hillard / J Pediatr Adolesc Gynecol 27 (2014) 309e319 18. Anderson SE, Must A: Interpreting the continued decline in the average age at menarche: results from two nationally representative surveys of U.S. girls studied 10 years apart. J Pediatr 2005; 147:753 19. McDowell MA, Brody DJ, Hughes JP: Has age at menarche changed? Results from the National Health and Nutrition Examination Survey (NHANES) 1999-2004. J Adolesc Health 2007; 40:227 20. Herman-Giddens ME: The decline in the age of menarche in the United States: should we be concerned? J Adolesc Health 2007; 40:201 21. Marti-Henneberg C, Vizmanos B: The duration of puberty in girls is related to the timing of its onset. J Pediatr 1997; 131:618 22. Marshall WA, Tanner JM: Variations in pattern of pubertal changes in girls. Arch Dis Child 1969; 44(235):291 23. Zacharias L, Rand WM, Wurtman RJ: A prospective study of sexual development and growth in American girls: the statistics of menarchie. Obstet Gynecol Surv 1976; 31:325 24. Chumlea WC, Schubert CM, Roche AF, et al: Age at menarche and racial comparisons in US girls. Pediatrics 2003; 111:110 25. Fraser IS, Critchley HO, Munro MG, et al: Can we achieve international agreement on terminologies and definitions used to describe abnormalities of menstrual bleeding? Hum Reprod 2007; 22:635 26. World Health Organization multicenter study on menstrual and ovulatory patterns in adolescent girls. II. Longitudinal study of menstrual patterns in the early postmenarcheal period, duration of bleeding episodes and menstrual cycles. World Health Organization Task Force on Adolescent Reproductive Health. J Adolesc Health Care 1986; 7:236 27. Venturoli S, Porcu E, Fabbri R, et al: Postmenarchal evolution of endocrine pattern and ovarian aspects in adolescents with menstrual irregularities. Fertil Steril 1987; 48:78 28. Venturoli S, Porcu E, Fabbri R, et al: Longitudinal evaluation of the different gonadotropic pulsatile patterns in anovulatory cycles of young girls. J Clin Endocrinol Metab 1992; 74:836 29. Apter D, Vihko R: Early menarche, a risk factor for breast cancer, indicates early onset of ovulatory cycles. J Clin Endocrinol Metab 1983; 57:82 30. Apter D: Development of the hypothalamic-pituitary-ovarian axis. Ann NY Acad Sci 1997; 816:9 31. Vihko R, Apter D: Endocrine characteristics of adolescent menstrual cycles: impact of early menarche. J Steroid Biochem 1984; 20:231 32. Treloar AE, Boynton RE, Behn BG, et al: Variation of the human menstrual cycle through reproductive life. Int J Fertil 1967; 12:77 33. Vollman RF: The menstrual cycle. In: Friedman E, editor. Major Problems in Obstetrics and Gynecology, vol. 7. Philadelphia, Saunders, 1977 34. Fraser IS, Critchley HO, Munro MG, et al: Abnormal uterine bleeding: getting our terminology straight. Curr Opin Obstet Gynecol 2007; 19:591 35. Fraser IS, Critchley HO, Munro MG, et al: Writing Group for this Menstrual Agreement Process: A process designed to lead to international agreement on terminologies and definitions used to describe abnormalities of menstrual bleeding. Fertil Steril 2007; 87:466
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36. Warner PE, Critchley HO, Lumsden MA, et al: Menorrhagia II: is the 80-mL blood loss criterion useful in management of complaint of menorrhagia? Am J Obstet Gynecol 2004; 190:1224 37. Hallberg L, Hogdahl AM, Nilsson L, et al: Menstrual blood lossea population study. Variation at different ages and attempts to define normality. Acta Obstet Gynecol Scand 1966; 45:320 38. Warner PE, Critchley HO, Lumsden MA, et al: I: measured blood loss, clinical features, and outcome in women with heavy periods: a survey with follow-up data. Am J Obstet Gynecol 2004; 190:1216 39. Claessens E, Cowell CA: Acute adolescent menorrhagia. Am J Obstet Gynecol 1981; 139:277 40. James AH, Manco-Johnson MJ, Yawn BP, et al: Von Willebrand disease: key points from the 2008 National Heart, Lung, and Blood Institute guidelines. Obstet Gynecol 2009; 114:674 41. James AH, Kouides PA, Abdul-Kadir R, et al: Von Willebrand disease and other bleeding disorders in women: consensus on diagnosis and management from an international expert panel. Am J Obstet Gynecol 2009; 201:12.e11 42. Philipp CS, Faiz A, Dowling N, et al: Age and the prevalence of bleeding disorders in women with menorrhagia. Obstet Gynecol 2005; 105:61 43. Widholm O, Kantero RL: A statistical analysis of the menstrual patterns of 8,000 Finnish girls and their mothers. Acta Obstet Gynecol Scand Suppl 1971; 14(Suppl 14):1 44. Flug D, Largo RH, Prader A: A longitudinal study of menstrual patterns in Swiss girls: a longitudinal study. Ann Hum Biol 1984; 11:495 45. Popat VB, Prodanov T, Calis KA, et al: The menstrual cycle: a biological marker of general health in adolescents. Ann N Y Acad Sci 2008; 1135:43 46. Blank SK, Helm KD, McCartney CR, et al: Polycystic ovary syndrome in adolescence. Ann N Y Acad Sci 2008; 1135:76 47. Tfayli H, Arslanian S: Menstrual health and the metabolic syndrome in adolescents. Ann N Y Acad Sci 2008; 1135:85 48. Kristof N: Pssst. Does Menstruation Keep Girls Out of School? The New York Times. September 4, 2009 49. Every Girl. Everywhere. Period. Available: http://www.daysforgirls.org. Accessed July 21, 2013 50. Muruganantham A: How I started a sanitary napkin revoluation. TED Talks [video clip]. 2012; http://www.ted.com/speakers/arunachalam_muruganantham.html. Accessed July 21, 2013 51. Plan International: Because I am a Girl. Available: http://plan-international.org/ girls/index.php?lang5en. Accessed July 21, 2013 52. Montgomery P, Ryus CR, Dolan CS, et al: Sanitary pad interventions for girls' education in Ghana: a pilot study. PloS One 2012; 7:e48274 53. Oster E, Thornton R: Menstruation, sanitary products, and school attendance: evidence from a randomized evaluation. Am Econ J: Appl Econ 2011; 3:91 54. Finley H: Museum of Menstruation and Women's Health. Available: http:// www.mum.org. Accessed July 21, 2013
a b s t r a c t The menstrual cycle has been recognized as a vital sign that gives information about the overall health of an adolescent or young adult female. Significant deviations from monthly cycles can signal disease or dysfunction. This review highlights the evidence based parameters for normal puberty, menarche, cyclicity, and amount of bleeding. The review addresses sources of information available online, noting inaccuracies that appear in web sites, even and especially those targeting adolescents. The review includes a call to action to provide accurate information about the menstrual cycle as a VITAL SIGN. Key Words: adolescent menstruation, amenorrhea, menarche, puberty
Introduction
The menstrual cycle is a vital sign. That is, just like pulse, respiration, blood pressure, and temperature, a menstrual history gives information about a woman's overall health. Girls, adolescents, and adult women need to attend to the regularity of their menstrual cycles, and if the cycles are not regular and approximately monthly, something may be out of balance. It may be a hormone imbalance (hyper-androgenism, most commonly polycystic ovary syndrome (PCOS), or thyroid dysfunction), or over-exercise, or an eating disorder, or an uncommon condition such as primary ovarian insufficiency. In about the year 2000, 2 colleagues of mine, Dr Larry Nelson from the NIH and Dr Justina Trott from the University of New Mexico met me at a women's health conference in Chantilly, Virginia. Over lunch, the three of us talked about how each of us views the menstrual cycle. Dr Nelson, a well respected NICHD researcher, had learned from listening to women who were ultimately diagnosed with primary ovarian insufficiency (POI, a condition previously termed premature ovarian failure1) that over half of the women ultimately diagnosed with POI had visited a clinician 3 or more times before lab work was performed to enable a diagnosis. These women had experienced false reassurances and a delay in the ultimate diagnosis of their condition. In one-quarter of these women, it took longer than 5 years before the diagnosis was made.2 Dr Trott and her colleagues with the American College of Women's Health Physicians had developed an online educational toolda concept map of the menstrual cycledto facilitate the development of an interdisciplinary and womancentered women's curriculum (Fig. 1).3 They described the concept map as highlighting relationships between The author, Paula J. Adams Hillard, MD, has been a consultant and member of the Scientific Advisory Panel for Merck and Bayer Healthcare. * Address correspondence to: Paula J. Adams Hillard, MD, Department of Obstetrics and Gynecology, Stanford University School of Medicine, Stanford, CA 94305-5101; Phone: (650) 725-3755; fax: (650) 723-7737
concepts of menstruation as a knowledge framework that builds capacity and allows the learner to adapt knowledge to multiple settings and across disciplines. I was intrigued by this idea of a concept map, which has more recently been termed “mind-mapping,” and I include here the mind-map that I developed using mind-mapping software (of which many free open source and paid commercial versions are available) in preparation for this talk (Fig. 2). At that chance luncheon meeting and discussion, Dr Nelson, Dr Trott, and I agreed that the menstrual cycle did not get the respect that it deserves. We could all relate to the idea that a complex series of hormonal, psychological, anatomic, and physiologic factors needed to be in balance for regular monthly menses to occur. The absence of such regularity should prompt an assessment of factors that might be adversely impacting the cycledthat is, the menstrual cycle should be assessed as a “vital sign”; cycle irregularity outside of given norms should prompt further assessment to determine what may be “out of balance”djust as an abnormal pulse, blood pressure, respiratory rate, or temperature may signal a pathologic process. This concept has gained traction in ob-gyn and adolescent medicine/pediatrics, with the publication of a joint American College of Obstetricians and Gynecologists (ACOG) and American Academy of Pediatrics (AAP) publication from the ACOG Committee on Adolescent Health Care.4,5 I am proud to trace the origins of this concept to the luncheon conversation with my colleagues in women's health. In recent years, the concept of pain as a fifth vital sign has become a focus of patient assessment. This concept has been sanctioned and given credence by the Joint Commission on Accreditation of Healthcare Organization's institution of pain management standards for hospitals. A number of other signs have been proposed as a 6th vital sign, including urinary continence, emotional distress, shortness of breath, gait speed, and end-tidal CO2.6 But among gynecologists and pediatricians, ACOG and the AAP have implanted the concept that “the menstrual cycle is a vital sign.” I have made this
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Fig. 1. Menstrual Cycle Concept Map. Reprinted from Hoffman et al, Concept mapping: A tool to bridge the disciplinary divide, Am J Obstet Gynecol 2002; 187(3 Suppl), pages S41-3, Copyright (2002) with permission from Elsevier.
concept a part of my campaign for adolescent girls' wellness, talking about it at every opportunity. I thank the program committee of the North American Society for Pediatric and Adolescent Gynecology (NASPAG) for allowing me to stand on my soapbox to talk about not only what we know about normal menstrual function in adolescents, but also about how we can transmit what we know to our colleagues in other disciplines, to our patients and their parents, to coaches, and other who need to know. Without an understanding for what is normal, girls with abnormal bleedingdtoo heavy, too frequent, lasting too long, or too infrequent, or who have associated menstrual paindare inappropriately reassured and denied appropriate evaluation and management. I stand on my soapbox because I want to change the world and the future for women and girls, to move us beyond our current knowledge and practices, to get ideas from my colleagues and listeners, and to encourage us to work together to change the future for women and girls. The research and advocacy must move knowledge and practices forward. Toward this goal, I want to speak authentically about women's experiences. I speak as I know them personally: as a girl, now woman, who is aspiring to be a crone; as a physician; as a feminist; as a mother; and as a wife. I speak from my soapbox as I hear of women's and girls' experiences from my patients, trying to actively listen. I speak as an educator who focuses on teaching and mentoring trainees through a Stanford University School of Medicine program called Educators for CARE, which stands for Compassion, Advocacy, Responsibility, and Empathy. And I speak as an advocate for the underserved population of young girls and adolescents.
What's Normal?
In my own clinical practice of pediatric and adolescent gynecology, menstrual problems are a large component of the problems that I see. (See another mind map in Fig. 3.) I have several messages about menstrual cycles when I speak with primary clinicians and parents, but one of the messages is that prospectively charting menstrual bleeding can create a visual picture that can be worth a thousand words. I commonly see patients who have been reassured by their primary clinicians that girls often have irregular periods during the first few years after menarche. While this is true, a menstrual calendar like the one pictured in Fig. 4 is clearly outside of the range of normal. A menstrual calendar, whether an old-fashioned paper calendar (Fig. 4) or a menstrual history documented in one of many “apps” available for smartphones, is a wonderful educational tool that primary care clinicians can encourage their patients to complete. The reverse side of the printed card can contain information about normal menstrual cycles (Fig. 5) Most of us learned about normal menstrual cyclicity through textbooks, which are increasingly available online as e-textbooks, but textbooks are typically out of date by the time they are published and we must be sure that we are basing our practices on the best evidencedas collated in evidence-based reviews such as the Cochrane Database of Systematic Reviews. Our professional societies, including ACOG and AAP, publish Committee Opinions and Technical Bulletins, including the ones that summarize the statistically based evidence for normal menstrual cycles.4,5 Typical gynecology textbooks indicate
P.J.A. Hillard / J Pediatr Adolesc Gynecol 27 (2014) 309e319 Fig. 2. Mind Map developed by the author in preparation for the NASPAG Annual Clinical and Research Meeting Elsevier lectureship plenary session on Menstruation as a Vital Sign: Giving the menstrual cycle the attention it deserves, San Diego, CA, April 18, 2013.
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Vaginitis
Frequent Bleeding
Acute Symptoms
Heavy M enstrual Bleeding
STIs UTIs
Amenorrhea
M enstrual Problems
Dysmenorrhea
Other
PCOS
Vulvar lesions
M enstrual Suppression PJAH Adolescent Clinical Practice Ovarian cysts Dysmenorrhea M yofascial Endometriosis
Acute Pain
Adnexal torsion PID
Chronic Pain
Vulvar
Contraception/Hormonal therapy
Fig. 3. PJAH Adolescent Clinical Practice–Menstrual problems figure prominently among the clinical issues in the author's pediatric and adolescent gynecology practice. PJAH5P.J. Adams Hillard.
that the average age of menarche is 12.8, that precocious puberty is defined by any pubertal development prior to the age of 8, that primary amenorrhea is defined as no menstrual periods by age 16, that early cycles in the first 1-2 years after menarches are anovulatory and irregular, that typical cycles last 2-7 days, and that the average blood loss per cycle is 30 ml, ranging from 20-60 ml. While some of this information is backed by evidence, other aspects of this “conventional wisdom” are not. Depending on the source, online resources commonly used by medical students or by clinicians outside of the specialties of pediatrics and obstetrics and gynecology, including Wikipedia, may or may not provide accurate evidence-based information. It must be noted that all of the guidelines and references to menstrual cycles refers to bleeding without the influence of hormonal therapy. Thus a brief review of the evidence is warranted.
Fig. 4. “Irregular bleeding” documented on a menstrual calendar.Ă
Pubertal Onset
Classically, textbooks have described precocious puberty as the onset of signs of pubertal development prior to the age of 8 years. With the publication of the large, prospective study through the Pediatric Research in the Office Setting network, this dictum was called into question.7 In this study, pediatric practitioners in office practices around the country received standardized training in the assessment of pubertal maturation and the level of sexual maturation of over 18,000 girls ages 3-12. Ninety percent of the girls examined were white and 9.6% African American. At age 7, 27.2% of African American girls and 6.7% of white girls had evidence of breast and/or pubic hair development. At the age of 8, the percentages were 48.3% and 14.7%.7 These data were met with skepticism, but a subsequent multisite study confirmed that at age 7, 10.4% of white, 23.4% of black
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Fig. 5. Menstrual CalendardReverse side.Ă
non-Hispanic, and 14.9% of Hispanic girls had attained breast stage 2 as a marker of pubertal development.8 A review panel concluded that there has indeed been a decline in the age of onset of the onset of puberty in girls since 1940.9 This has been linked to increasing rates of obesity.10 Even with some consensus, the call for reexamination of the age limit for defining when puberty is precocious has been controversial.11 As for delayed puberty, lack of breast development by about age 13 represents 2.5 standard deviations from the mean, and thus should prompt evaluation.12
Table 1 Common Causes of Primary Amenorrhea Category
Approximate Frequency (%)
Breast development Mullerian agenesis Androgen insensitivity Vaginal septum Imperforate hymen Constitutional delay No breast development: high FSH 46 XX 46 XY Abnormal No breast development: low FSH Constitutional delay Prolactinomas Kallman syndrome Other CNS Stress, weight loss, anorexia PCOS Congenital adrenal hyperplasia Other
30 10 9 2 1 8 40 15 5 20 30 10 5 2 3 3 3 3 1
Reprinted from Fertility and Sterility, Vol 90 / Practice Committee of American Society for Reproductive Medicine. Current Evaluation of Amenorrhea, S219-25. Copyright 2008 with permission from American Society for Reproductive Medicine.
Menarche
Although there is increasing evidence noting a decline in the age of onset of puberty, there is less agreement as to whether there have been significant declines in the age of menarche.9 There is evidence that the age of menarche in the U.S. has declined from the early 1800s until the 1950s.13 Since this time, the age of menarche may have plateaued, or perhaps declined only slightly, with menarche typically occurring between the ages of 12 and 13.4,14-19,20 Racial and ethnic differences in the age of menarche have been noted in recent studies, with black girls having earlier onset of puberty and menarche than white girls, with Hispanic or Mexican American girls being intermediate between black and white girls.9 Earlier studies, including the classic Marshall and Tanner report, did not include ethnically or racially diverse populations. There is international variation in age of menarche as well, with likely influence of socioeconomic conditions, nutrition, and access to healthcare.4 Menarche typically occurs within 2-3 years after the onset of breast development (thelarche); within this time-frame, the earlier the onset of puberty, the longer the interval to menarche.21 Menarche typically occurs at Tanner stage IV breast development, and menarche is rare prior to the achievement of breast stage III development.22 Age 9 represents 2.5 SD below the mean for age of menarche.23 Primary Amenorrhea
Classically, primary amenorrhea has been defined as no menses by age 16; recent studies have called this dictum into question. By age 15, 95%-98% of adolescents will have had their first menstrual period.15,16,19,23,24 This statistically derived
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Table 2 Menstrual Terminology and Parameters for Adolescent Years Clinical Dimension Frequency (days)
Regularity
Duration of flow (days)
Volume of blood loss (ml)
Description Frequent Normal Infrequent Absent Regular Irregular Prolonged Normal Shortened Heavy Normal Light
Normal Limits 5th-95th Percentile 21-45 days23,26,32,33,43,44 O90 days32,33
2-7 days23,26,43,44 O80 ml associated with anemia37,38 30 ml
definition for primary amenorrhea should lead to an evaluation of girls who have not had the onset of menses by age 15. Failure to evaluate these girls can delay the diagnosis of a number of conditions with the potential for significant adolescent or adult morbidity such as eating disorders or polycystic ovary syndrome, as well as other conditions with implications for future reproductive potential such as primary ovarian insufficiency. See Table 1 for a list of possible causes of primary amenorrhea from the American Society for Reproductive Medicine. Menstrual Bleeding
The terms used to describe abnormal menstrual bleeding have long been confusing, with imprecise definitions and inconsistency in the use of terms such as menorrhagia, metrorrhagia, menometrorrhagia, hypermenorrhea, hypomenorrhea, dysfunctional uterine bleeding, and others. An international meeting was held to make the case for describing menstrual bleeding in terms of cycle regularity, frequency, duration of flow, and volume.25 See Table 2, which list these terms, along with evidence-based norms for adolescents. Menstrual Cyclicity
A longitudinal, multicenter study sponsored by the World Health Organization provides information about Table 3 Causes of Menstrual Irregularity Pregnancy Endocrine causes Poorly controlled diabetes mellitus Polycystic ovary syndrome Cushing's disease Thyroid dysfunction Premature ovarian failure Late-onset congenital adrenal hyperplasia Acquired conditions Stress-related hypothalamic dysfunction Medications Exercise-induced amenorrhea Eating disorders (both anorexia and bulimia) Tumors Ovarian tumors Adrenal tumors Prolactinomas Reprinted from Obstet Gynecol 2006, 108:1323-8. ACOG Committee on Adolescent Health Care: ACOG Committee Opinion No, 349, November 2006: Menstruation in girls and adolescents: using the menstrual cycle as a vital sign. ACOG Committee Opinion Number 349, November 2006 (Reaffirmed 2009), Copyright 2006 with permission from Wolters Kluwer Health.
menstrual cyclicity in adolescents.26 Menstrual cycles are more variable in adolescents than in adults. In particular, the interval from the first to the second menstrual period can be longer than subsequent cycles; in the WHO international multicenter study, the first cycle was longer than 40 days in 38% of girls.26 However, the median length of even the first cycle was 34 days.26 Many, if not most early cycles are anovulatory, with the frequency of ovulation related to the gynecologic age (time since menarche) as well as chronologic age at menarche.27-31 Girls who are younger at the time of menarche achieve regular ovulatory cycles in a shorter period of time that those who are older at the time of menarche.29 In spite of the facts that many menstrual cycles in adolescents are anovulatory and that cycles in adolescents are irregular, it is not true that “anything goes” with regard to cycle length. Bleeding that occurs while an individual is taking hormonal therapy has a different pathophysiologic mechanism compared to bleeding not under such influence and thus this review refers only to bleeding on young women who are not taking any hormonal therapy such as birth control. Two very large studies inform our knowledge of menstrual cyclicity during adolescence; Treloar followed 2702 women over 27 years time, reporting on 275,047 cycles, and Vollman reported data from 656 women with 31,645 cycles.32,33 These studies and others cited above indicate that cycle length in adolescents is usually between 21 and 45 days, in spite of anovulatory cycles.4 By the third gynecologic year, most cycles are 21-34 days long, as is normal in adults.26,31 Ninety days represents the 95% for cycle length, even in the first gynecologic year,32 and thus should prompt evaluation. Cycles should show increasing regularity with time; if this is not the case, pathology (such as PCOS, eating disorders, thyroid disease, or even rare conditions such as primary ovarian insufficiency) should be considered. These conditions may have significant impact on future bone health, cardiovascular risks, and fertility. See Table 3 for causes of menstrual irregularity in adolescents. The most common condition that can cause secondary amenorrhea (besides pregnancy) is PCOS, particularly among girls with signs of hyperandrogenism including moderate to severe acne and excess hair growth. Making the diagnosis of PCOS allows for appropriate management of irregular bleeding, prevention of heavy or prolonged menstrual bleeding, and potentially minimizes the metabolic sequelae that may accompany the condition by a focus on lifestyle interventions such as weight loss and exercise. More research is needed into the topic of adolescent anovulation and the typical progression from anovulatory cycles to normal, regularly ovulatory cycles vs abnormal adolescent anovulation with abnormal menstrual cycles that are associated with hyperandrogenism and that remain abnormal in cyclicity. Other causes of secondary amenorrhea are listed in Table 4, some of which are common, and others rare, particularly in adolescents. Diagnoses such as eating disorders and the female athlete triad have a strong link to bone health and low bone density may be a risk to subsequent health.
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Table 4 (continued)
I. Anatomic defects (outflow tract) € llerian agenesis (Mayer-Rokitansky-Kuster-Hauser syndrome) A. Mu B. Complete androgen resistance (testicular feminization) C. Intrauterine synechiae (Asherman syndrome) D. Imperforate hymen E. Transverse vaginal septum F. Cervical agenesisdisolated G. Cervical stenosisdiatrogenic H. Vaginal agenesisdisolated I. Endometrial hypoplasia or aplasiadcongenital II. Primary hypogonadism A. Gonadal dysgenesis 1. Abnormal Karyotype a. Turner syndrome 45,X b. Mosaicism 2. Normal karyotype a. Pure gonadal dysgenesis i. 46,XX ii. 46,XY (Swyer syndrome) B. Gonadal agenesis C. Enzymatic deficiency 1. 17a-Hydroxylase deficiency 2. 17,20-Lyase deficiency 3. Aromatase deficiency D. Premature ovarian failure 1. Idiopathic 2. Injury a. Chemotherapy b. Radiation c. Mumps oophoritis 3. Resistant ovary a. Idiopathic III. Hypothalamic causes A. Dysfunctional 1. Stress 2. Exercise 3. Nutrition-related a. Weight loss, diet, malnutrition b. Eating disorders (anorexia nervosa, bulimia) 4. Pseudocyesis B. Other disorders 1.Isolated gonadotropin deficiency a. Kalimann syndrome b. Idiopathic hypogonadotropic hypogonadism 2. Infection a. Tuberculosis b. Syphilis c. Encephalitis/meningitis d. Sarcoidosis 3. Chronic debilitating disease 4. Tumors a. Craniopharyngioma b. Germinoma c. Hamartoma d. Langerhans cell histiocytosis e. Teratoma f. Endodermal sinus tumor g. Metastatic carcinoma IV. Pituitary causes A. Tumors 1. Prolactinomas 2. Other hormone-secreting pituitary tumor (ACTH, thyrotropinstimulating hormone, growth hormone, gonadotropin b. Mutations of FSH receptor c. Mutations of LH receptor d. Fragile X syndrome 4. Autoimmune disease 5. Galactosemia V. Other endocrine gland disorders A Adrenal disease 1. Adult-onset adrenal hyperplasia 2. Cushing syndrome B. Thyroid disease 1. Hypothyroidism 2. Hyperthyroidism (continued)
C. Ovarian tumors 1. Granulosa-theca cell tumors 2. Brenner tumors 3. Cystic teratomas 4. Mucinous/serous cystadenomas 5. Krukenberg tumors 3. Nonfunctional tumors (craniopharyngioma) 4. Metastatic carcinoma B. Space-occupying lesions 1. Empty sella 2. Arterial aneurysm C. Necrosis 1. Sheehan syndrome 2. Panhypopituitarism D. Inflammatory/infiltrative 1. Sarcoidosis 2. Hemochromatosis 3. Lymphocytic hypophysitis E. Gonadotropin mutations (FSH) VI. Multifactorial causes A Polycystic ovary syndrome Reprinted from Fertility and Sterility, Vol 90 / Author(s), Current Evaluation of Amenorrhea, S219. Copyright (2008), with permission from American Society for Reproductive Medicine.
Abnormal Menstrual Flow
Menstrual flow has been described using a number of terms that do not have a standard definition: menorrhagia, metrorrhagia, menometrorrhagia, polymenorrhea, hypermenorrhea, hypomenorrhea, oligomenorrhea, dysfunctional uterine bleeding, and abnormal uterine bleeding. These terms have varying definitions and uses, so there has been a move to standardize the terminology, describing cycle regularity as irregular, regular, or absent; frequency of menstruation as frequent, normal, or infrequent; duration of menstrual flow as prolonged, normal, or shortened; and the volume of menstrual flow as heavy, normal, or light.34,35 Absent menstrual flowdamenorrheadsometimes defined as no bleeding for 90 days, is associated with a number of medical conditions such as drug therapy with antipsychotics, depot medroxyprogesterone, GnRH therapy, hyperprolactinemia, ovarian failure with abnormal karyotype, primary ovarian insufficiency, polycystic ovary syndrome, eating disorders, the female athlete tried, and “stress.” Some of these conditions are associated with hypoestrogenism and thus have a relationship to bone health. Heavy Menstrual Bleeding
Excessively heavy bleeding has been defined in the past as blood loss great than 80 ml/period, although it has been suggested that this correlates poorly with patient perceptions, difficulties containing blood flow, impact on daily life, other menstrual symptoms, or other factors such as impact of flow on daily activities.36 The rate of pad/tampon change (requiring a change more than every 1-2 hours) has been shown to correlate with measured blood loss and bleeding O 80 ml/period has been associated with the development of anemia.37,38 The classic study by Claessens, published in 1981, looked at a series of girls presenting to an emergency room with complaints of acute menorrhagia.39 Overall, about one-fifth
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Table 5 Menstrual Conditions That May Require Evaluation Menstrual periods that: Have not started within 3 years of thelarche Have not started by 13 years of age with no signs of pubertal development Have not started by 14 years of age with signs of hirsutism Have not started by 14 years of age with a history or examination suggestive of excessive exercise or eating disorder Have not started by 14 years of age with concerns about genital outflow tract obstruction or anomaly Have not started by 15 years of age Are regular, occurring monthly, and then become markedly irregular Occur more frequently than every 21 days or less frequently than every 45 days Occur 90 days apart even for one cycle Last more than 7 days Require frequent pad or tampon changes (soaking more than one every 1-2 hours) Reprinted from Obstet Gynecol 2006, 108 (5):1323-8. ACOG Committee on Adolescent Health Care, American Academy of Pediatrics Committee on Adolescence, Menstruation in Girls and Adolescents: Using the Menstrual Cycle as a Vital Sign. ACOG Committee Opinion Number 349, November 2006 (Reaffirmed 2009), Copyright (2006) with permission from Wolters Kluwer Health.
of those who presented with heavy bleeding were found to have a primary coagulopathy, with about one-fourth of those whose initial hemoglobin was !10 g/100ml, about one-third of those requiring transfusion, and nearly half of those who presented at menarche having a bleeding disorder, such as von Willebrand disease or idiopathic thrombocytopenic purpura. The incidence of von Willebrand disease in the US is approximately 1%-2%; the statistics rise to 13%-20% of those with heavy menstrual bleeding, and perhaps as many as 50% of teens who present to an Emergency Department with excessive menstrual bleeding have a bleeding disorder.40-42 Thus testing for a bleeding disorder in adolescents with heavy menstrual bleeding is appropriate, particularly those whose cycles fall within the 21-45 day parameters for normal cycles. Prolonged Menstrual Bleeding
Menstrual flow in adolescents, as in older women, typically lasts from 2 to 7 days.23,26,43,44 Unlike other menstrual parameters discussed above, the normal duration of menstrual flow cited in textbooks is typically accurately stated, likely because it does not differ from that seen in adult women. What's Normal: Summary
The parameters for normal menstrual cycles in adolescents have been characterized in terms of onset, frequency, regularity, duration, and amount of flow, as cited above. Table 5, from the ACOG Committee Opinion on adolescent menstruation, lists menstrual conditions that may require evaluation, based on the statistical evidence. It is definitely not true that “anything goes” in terms of menstrual cyclicity, duration, amount of flow, or onset. Failure to evaluate teens who meet the criteria cited in the Committee Opinion can be a significant disservice to young women, leading to unnecessary discomfort, embarrassment, poorer quality of life, adverse self esteem, and current or future health risks such as anemia and low bone mineral density, as well as potential
metabolic and cardiovascular risks.14,45-47 Adolescents deserve our attention to their menstrual cycles as a vital sign. Just as with other vital signs like pulse and respiration, values outside of statistically derived normal parameters may signal disease or derangements in normal health. Today's Girls and the Menstrual Cycle
When most of us were approaching the age of menarche, we typically learned about “periods” from our moms, supplemented by a special “health class” on puberty in the 5th grade, in which the class was segregated by sex, and we were given a talk by a nurse, health educator, or science teacher in which we heard about growing up, including for the girls, primarily menstruation. In my own case, I supplemented these sources by reading my mother's nursing textbooks, as well as the World Book Encyclopedia. I can also recall rather furtive but frequent phone calls to a best friend, in which we talked about puberty and growth. Conversations with older girls on the playground also supplemented the official curriculum. My young pre-adolescent patients today also typically get information from their momsdmost of whom tell me that they vow to do a better job of sexuality education for their daughters than they themselves had experienced. The fifth grade segregated health classes also still exist. Girls and boys still talk about sex on the playground and with friends on the phone, but nowadays the phone may be their own cellphone, rather than a “land line” shared by the family. Girls also learn about menstruation and their changing bodies through more educational books, such as the American Girl series book titled, “The Care & Keeping of YoudThe Body Book for Girls,” of which over 3 million copies have been sold. Many YouTube videos videotaped and uploaded to the internet by 11 and 12-year-old girls explain the “first period” to their near peers. I was unsure about what information a teen might find today, so I made an effort to learn what girls might discover if they used a Google search to get information. I wondered what search terms a girl would use. The results were somewhat different when I googled “period,” a term that I supposed might come to mind, compared with “menstruation.” Googling “period” brought me to a Wikipedia page in which I found 6 categories of definitions and I ultimately found “menstruation” in the science and mathematics category. I supposed that a girl might then follow the hyperlink to “menstruation” on Wikipedia. The exciting (but scary) thing about Wikipedia is that anyone can edit an entry. When I found erroneous information about adolescent menstrual periods on the “menstruation” page, I simply logged in as an editor and provided the evidence-based information that I've cited above! How gratifyingdto be able to correct misinformation with keystrokes. So if a young girl were to find her way to Wikipedia, and be able to wade through the considerable verbiage, she would find accurate information. I'm not sure how often this has happened or will happen, although I'm sure that Wikipedia could provide that information. And it's not an impossibility that a 5th or 6th grader would read the entry; after all, I
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regularly read the encyclopedia at that age. However, there are multiple other web sites where a girl might find herself that would not provide accurate information, or worse, where she might find age-inappropriate information like pornography. I recently had a parent who described to me how his 7year-old daughter had discussed “sex” with a friend on the playground, and who had subsequently googled the word. The parent was more than a little distressed to find multiple pornography sites on the family computers before they were able to install the appropriate parental controls. These parental controls might or might not block web sites that are intended for pre-teens and teens to get health-related information. In searching for menstrual information on the internet, I found 19 web sites targeted for adolescents which varied in the accuracy of the information they provided. I assumed that 1 question a girl might want to know would be “by what age should menstrual periods start?” Of these 19 sites, 5 provided no answer, and only 4 gave the correct answer of 15 years. Notably, youngwomenshealth.org, the excellent web site from Boston Children's Hospital, and a
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governmental web site, womenshealth.gov, gave consistently accurate information. Other web sites in which periods are addressed and girls' questions are answered in an age-appropriate manner included web sites from companies that make menstrual hygiene/catamenial products. These sites were generally informative, but did not provide accurate information about normal menstrual parametersdproviding an opportunity for us to help educate the health educators who design and edit these web sites. In addition to internet web sites, multiple menstrual “apps” now exist for smart phones and tablets that enable girls and women to track their cycles. I downloaded over 30 free web sites (more apps were available for a price). I was sincerely disappointed to learn that not one of them provided notification of menstrual cycles that were outside of the statistically derived normal parameters for either adolescents or for adult women. From my basic high school programming experience (albeit in FORTRAN, over 40 years ago), I would not imagine that such an app would be that difficult to write. I'm disappointed that this
Fig. 6. Mind Map: Who Needs to Know What We Know about the Menstrual Cycle. POI 5 Primary Ovarian Insufficiency, ED 5 Eating Disorders, DD 5 Developmental Disabilities.Ă
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hasn't yet been added as a feature to the multiple menstrual apps that currently compete for advertisers and customers. Which brings me back to my CALL TO ACTION: that we as clinicians and educators would speak to girls themselves, to their parents, to those with medical conditions that may impact or be impacted by the menstrual cycle, to our colleagues in other disciplines, to health educators, to coaches, to catamenial product manufactures, and to those in the pharmaceutical industry who have the opportunity to influence decisions that can have a profound influence on girls' lives. See Fig. 6. The Menstrual Cycle from an International Perspective
Menstruation is beginning to be recognized as an international issue related to the education of girls in developing countries. Nicholas Kristof, columnist for the New York Times, who in 2009 published the book “Half the Sky: Turning Oppression into Opportunity for Women Worldwide” with his journalist wife Sheryl WuDunn, has raised the concern that one of the reasons that girls in Africa and Asia miss school is that they have difficulty managing their menstrual periods.48 They initially suggested that lack of menstrual hygiene products led to increased absenteeism and that this in turn contributed to academic difficulties that ultimately resulted in withdrawal from school. Nonprofit organizations have developed programs to help girls manage their menses. “Days for Girls International” has developed feminine hygiene kits that are sewn by women in micro enterprise projects and distributed to “empower girls and women worldwide with more dignity, health and safety through quality sustainable menstrual management.”49 A TED talk on “how I started a sanitary napkin revolution” has received over a half million views, and features a charismatic speaker advocating for local business using a simple machine he designed, inspired by his wife's challenges in paying for menstrual supplies, to make inexpensive menstrual napkins in India.50 The “Because I am a Girl” campaign supports girls' education, including a project to help girls stay in school through menstrual hygiene education.51 One pilot study in Ghana looked at school attendance in 3 groups: a group of girls who received menstrual pads plus education, another that received only puberty education, and a control group.52 After 3 months, pads plus education improved attendance by 9%; at 5 months, puberty education also improved attendance. Another study from Nepal showed no significant impact of providing girls with menstrual cups on keeping girls in school, but other factors such as cultural beliefs, taboos, menstrual cramps, limitations of underwear and water for hygiene, and bullying were felt to be confounding factors.53 The Museum of Menstruation and Women's Health has solicited input from women about the slang words and expressions that they use to describe their periods; many of these phrases reflect negatives about menstruation, suggesting the limitations and burdens that women experience with regard to difficulty managing their menses and menstrual-associated symptoms.54
What do we do with the evidence-based information about menstruation?
Moving forward, it's clear that the information about statistically-derived norms for menstruation needs to be distributeddto our colleagues, as has been noted; through professional organizations beyond NASPAG, ACOG, and AAP to the American Association for Family Physicians, the Society for Menstrual Cycle Research, through professional organizations for nurse practitioners, physicians' assistants, internists and other primary clinicians; using apps, pointof-care references, electronic media linked to search engines, using social media; and working with organizations that bring together girls and women, non-governmental organizations internationally, nonprofit organizations in the US, pharma, and international aid organizations. The message is that the menstrual cycle is a VITAL SIGN. We need to join together in talking about what is normal with regard to adolescents' menstruation cycles, and what is not. Menstruation Matters; Period! We'd like to grant the menstrual cycle the respect that it deserves as a marker for physiologic wellness. References 1. Nelson LM: Clinical practice. Primary ovarian insufficiency. N Engl J Med 2009; 360:606 2. Alzubaidi NH, Chapin HL, Vanderhoof VH, et al: Meeting the needs of young women with secondary amenorrhea and spontaneous premature ovarian failure. Obstet Gynecol 2002; 99(5 Pt 1):720 3. Hoffman E, Trott J, Neely KP: Concept mapping: a tool to bridge the disciplinary divide. Am J Obstet Gynecol 2002; 187(3 Suppl):S41 4. ACOG Committee on Adolescent Health Care: ACOG Committee Opinion No. 349, November 2006: Menstruation in girls and adolescents: using the menstrual cycle as a vital sign. Obstet Gynecol 2006; 108:1323 5. American Academy of Pediatrics Committee on Adolescence, American College of Obstetricians and Gynecologists Committee on Adolescent Health Care, Diaz A, Laufer MR, Breech LL: Menstruation in girls and adolescents: using the menstrual cycle as a vital sign. Pediatrics 2006; 118:2245 6. Wikipedia contributors. Vital signs. Wikipedia, The Free Encyclopedia. Available: http://en.wikipedia.org/w/index.php?title5Vital_signs&oldid555 0559029. Accessed April 20, 2013 7. Herman-Giddens ME, Slora EJ, Wasserman RC, et al: Secondary sexual characteristics and menses in young girls seen in office practice: a study from the Pediatric Research in Office Settings network. Pediatrics 1997; 99:505 8. Biro FM, Galvez MP, Greenspan LC, et al: Pubertal assessment method and baseline characteristics in a mixed longitudinal study of girls. Pediatrics 2010; 126:e583 9. Euling SY, Herman-Giddens ME, Lee PA, et al: Examination of US puberty-timing data from 1940 to 1994 for secular trends: panel findings. Pediatrics 2008;(121 Suppl 3):S172 10. Biro FM, Greenspan LC, Galvez MP: Puberty in girls of the 21st century. J Pediatr Adolesc Gynecol 2012; 25:289 11. Kaplowitz PB, Oberfield SE: Reexamination of the age limit for defining when puberty is precocious in girls in the United States: implications for evaluation and treatment. Drug and Therapeutics and Executive Committees of the Lawson Wilkins Pediatric Endocrine Society. Pediatrics 1999; 104(4 Pt 1):936 12. Largo RH, Prader A: Pubertal development in Swiss girls. Helv Paediatr Acta 1983; 38:229 13. Wyshak G, Frisch RE: Evidence for a secular trend in age of menarche. N Engl J Med 1982; 306:1033 14. Adams Hillard PJ: Menstruation in Adolescents: What's Normal, What's Not. In: Gordon CM, Welt C, Rebar RW, et al, editors. The Menstrual Cycle and Adolescent Health, vol. 1135. New York, NY, Academy of Sciences, 2008, pp 29e35 15. Freedman DS, Khan LK, Serdula MK, et al: Relation of age at menarche to race, time period, and anthropometric dimensions: the Bogalusa Heart Study. Pediatrics 2002; 110:e43 16. Macmahon B: Age at Menarche: United States, 1973. Rockville, MD: National Center for Health Statistics; 1974. DHEW publication [HRA] 74e1615 17. Demerath EW, Towne B, Chumlea WC, et al: Recent decline in age at menarche: the Fels Longitudinal Study. Am J Hum Biol 2004; 16:453
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36. Warner PE, Critchley HO, Lumsden MA, et al: Menorrhagia II: is the 80-mL blood loss criterion useful in management of complaint of menorrhagia? Am J Obstet Gynecol 2004; 190:1224 37. Hallberg L, Hogdahl AM, Nilsson L, et al: Menstrual blood lossea population study. Variation at different ages and attempts to define normality. Acta Obstet Gynecol Scand 1966; 45:320 38. Warner PE, Critchley HO, Lumsden MA, et al: I: measured blood loss, clinical features, and outcome in women with heavy periods: a survey with follow-up data. Am J Obstet Gynecol 2004; 190:1216 39. Claessens E, Cowell CA: Acute adolescent menorrhagia. Am J Obstet Gynecol 1981; 139:277 40. James AH, Manco-Johnson MJ, Yawn BP, et al: Von Willebrand disease: key points from the 2008 National Heart, Lung, and Blood Institute guidelines. Obstet Gynecol 2009; 114:674 41. James AH, Kouides PA, Abdul-Kadir R, et al: Von Willebrand disease and other bleeding disorders in women: consensus on diagnosis and management from an international expert panel. Am J Obstet Gynecol 2009; 201:12.e11 42. Philipp CS, Faiz A, Dowling N, et al: Age and the prevalence of bleeding disorders in women with menorrhagia. Obstet Gynecol 2005; 105:61 43. Widholm O, Kantero RL: A statistical analysis of the menstrual patterns of 8,000 Finnish girls and their mothers. Acta Obstet Gynecol Scand Suppl 1971; 14(Suppl 14):1 44. Flug D, Largo RH, Prader A: A longitudinal study of menstrual patterns in Swiss girls: a longitudinal study. Ann Hum Biol 1984; 11:495 45. Popat VB, Prodanov T, Calis KA, et al: The menstrual cycle: a biological marker of general health in adolescents. Ann N Y Acad Sci 2008; 1135:43 46. Blank SK, Helm KD, McCartney CR, et al: Polycystic ovary syndrome in adolescence. Ann N Y Acad Sci 2008; 1135:76 47. Tfayli H, Arslanian S: Menstrual health and the metabolic syndrome in adolescents. Ann N Y Acad Sci 2008; 1135:85 48. Kristof N: Pssst. Does Menstruation Keep Girls Out of School? The New York Times. September 4, 2009 49. Every Girl. Everywhere. Period. Available: http://www.daysforgirls.org. Accessed July 21, 2013 50. Muruganantham A: How I started a sanitary napkin revoluation. TED Talks [video clip]. 2012; http://www.ted.com/speakers/arunachalam_muruganantham.html. Accessed July 21, 2013 51. Plan International: Because I am a Girl. Available: http://plan-international.org/ girls/index.php?lang5en. Accessed July 21, 2013 52. Montgomery P, Ryus CR, Dolan CS, et al: Sanitary pad interventions for girls' education in Ghana: a pilot study. PloS One 2012; 7:e48274 53. Oster E, Thornton R: Menstruation, sanitary products, and school attendance: evidence from a randomized evaluation. Am Econ J: Appl Econ 2011; 3:91 54. Finley H: Museum of Menstruation and Women's Health. Available: http:// www.mum.org. Accessed July 21, 2013