Quick Search
  Home Journal Information Current Issue Past Issues Services Contact Us  
Vaginal microbiocoenosis and cytology of prepubertal and adolescent girls: their role in health and disease 
Vaginal microbiocoenosis and cytology of prepubertal and adolescent girls: their role in health and disease
  Lyubov A Matytsina, Donald E Greydanus, Yuriy A Gurkin
 [Abstract] [Full Text] [PDF]   Pageviews: 16893 Times

Vaginal microbiocoenosis and cytology of

prepubertal and adolescent girls: their role in

health and disease

Lyubov A Matytsina, Donald E Greydanus, Yuriy A Gurkin

Plymouth, UK

Author Affiliations: Obstetrics, Gynecology, Perinatology and Pediatric & Adolescent Gynecology, Donetsk Medical University, Ukraine, Peninsula Medical School, Plymouth, UK (Matytsina LA); Pediatrics & Human Development, Michigan State University College of Human Medicine, Michigan State University/Kalamazoo Center for Medical Studies, 1000 Oakland Drive, Kalamazoo, Michigan, USA (Greydanus DE); Pediatric Gynecology, St-Peterburgh Pediatric Academy, St-Peterburgh, Russia (Gurkin YA)

Corresponding Author: Lyubov A Matytsina, Obstetrics, Gynecology, Perinatology and Pediatric & Adolescent Gynaecology, Donetsk Medical University, Ukraine, Peninsula Medical School, Plymouth, UK (Tel: 44  1872 274501; Fax: 44 1872 274501; Email: lubore@mail.ru; lyubov.matytsina@yahoo.com)


Background: Clinicians and investigators often do not appreciate the importance of vaginal microbiocoenosis and vaginal cytology in the health of prepubertal and adolescent girls.

Data sources: Based on recent publications in human medicine and our own experience with vaginal cytology and microbiology in children and adolescent girls, we review the principles of vaginal microbiocoenosis and cytology and their roles in disease prevention in prepubertal and adolescent girls.

Results: The main role of vaginal microbiocoenosis and cytology in diagnosing as well as developing vulvovaginitis is demonstrated. Clinicians can identify states of vaginal health and disease by important well-known diagnostic tools, including vaginal cytology. Lactobacilli are infrequently observed in the prepubertal girls, but become more abundant in adolescent girls. Three basic types of vaginal smears are presented in addition to a classification of inflammatory urogenital diseases. Management of common types of vulvovaginitis is also considered.

Conclusions: This essential shift in vaginal bioco-enosis is important to prevent the growth of potentially pathogenic flora in the vagina. The detection of vaginal microbiocoenosis problems and recognition of changing cytology in vaginal development can provide helpful clues to identifying and preventing vaginal diseases in this pediatric population.

Key words: cytology; lactobacilli; vaginal microbiocoenosis; vulvovaginitis             

World J Pediatr 2010;6(1):32-37


Vaginal inflammatory and infectious diseases are the most common gynecological diseases found in prepubertal and adolescent girls. Microbiocoenosis (biocoenosis) refers to a group of interacting organisms that live in a specific habitat such as the vagina and form an ecological community. Cytological evaluation of vaginal cells is an important diagnostic method used in identifying vaginal disorders (Fig.).[1-3] Such an analysis reveals vaginal epithelial status, presence or absence of inflammatory changes, and etiological factor(s) causing vaginal symptomatology.[4-9] An examination of cervical cytology has proven useful in cervical cancer screening for adolescent and adult females.[10,11]

This article focuses on vaginal microbiocoenosis and cytology. The vaginal microbiological picture can be divided into two groups: 1) normal or non-pathogenic agents (normal flora or microbiocoenosis);[7] and 2) potentially dangerous or conditionally pathogenic microorganisms. A decrease of immunological health of an individual can lead to some organisms becoming pathogenic.[1,12-15]

Role of lactobacilli

Vaginal microorganisms are divided into aerobes, facultative anaerobes and obligate (strict) anaerobes. The vaginal lactobacilli flora consists of 11 strains of lactobacilli (gram-positive bacilli); the dominant strain in quantity (42.9%) is Döderlein's bacillus (Lactobacillus acidophilus). The role of this lactobacilli flora is to prevent the presence of potentially pathogenic flora by producing an acidic environment that has a pernicious effect on these other flora.

In the prepubertal girls, the vaginal environment is alkaline or neutral in which the vaginal vestibule and mucosa are pink, tender, and devoid of overt vaginal secretion or fluid. Vaginal cytology reveals few epithelial cells and leukocytes; cytology or culture reveals cocci along with nitrobacteria and corynebacteria. Lactobacilli are absent or in low numbers due to low ovary endocrine function. As sex hormone secretion begins in the peripubertal period and increases as puberty progresses, the vagina becomes inhabited by increasing amounts of lactobacilli. The vaginal milieu becomes acidic and physiologic leukorrhea occurs.[1,4]

Other vaginal flora

A variety of flora can be found in the vagina at different ages and in different stages of health, growth, or disease.[7,15,16] An important group is the cocci bacteria. The biological feature of cocci lies in the fact that young cocci are intensively colored by Gram staining, and when the cocci become older they turn to be gram-negative. Some of the cocci cultures belong to normal microbiological growth in skin, and mucus membranes of the respiratory tract, the gastrointestinal tract, and the genitals. However, some of the cocci flora in the vagina can become pathogenic flora. The staphylococci in the vagina include Staphylococci aureus, epidermidis, and micrococcus (saprophytic). The streptococci include Hemolytic (green) streptococci, Enterococci (Fecal streptococci), and Streptococcus pneumoniae. Environmental niches of Peptostreptococci (anaerobic cocci) are the oral cavity, intestine, and genitals.

Bacillus flora is also conditionally pathogenic and can grow in the vagina. Diphtheroids are gram-positive bacilli that belong to the Corynebacteria group. Some Diphtheroids represent normal flora in the respiratory tract and mucus membranes of the skin and genitals. Enterobacteria are gram-positive bacilli that include Intestinal bacilli, Proteus, Enterobacteria (blue pus bacilli), and Klebsiella. They make up a considerable part of normal flora of the intestine and take part in providing its normal gastrointestinal functioning; however, they can become pathogenic flora when found in the vagina.

Gardnerella vaginalis and other Gardnerella species are small gram-positive bacilli (sometimes found in the form of coccobacilli) that are facultative anaerobes.[7,15,17] Gardnerellas are seen in healthy women (their frequency fluctuates from 47% to 68%) and girls aged from 2 months to 15 years without any clinical manifestations. Thus, Gardnerella vaginalis are considered as co-inhabitants of the vagina, though some experts feel that Gardnerella species can be pathogenic in some cases.[7,15-17]

Leptothrix are gram-variable bacilli that can have the form of coccobacilli; they are facultative anaerobes growing in the vagina and do not grow on ordinary culture media. These bacteria are found in nature in streams of slowing running water polluted by various industries such as paper or milk factories. Acinetobacter are aerobic, thick, short, gram-positive bacilli that have the form of diplococci; in gram stains, they appear similar to gonococcal and meningococcal bacteria. Acinetobacter can be seen in the skin, mucus membranes, respiratory tract, and the urogenital tract in humans. Patients with immunodeficiency can develop sepsis in association with other microbes.[1]

Vaginal cytology and microbiology

There are three basic vaginal smear types in pre-pubertal and adolescent girls: first type (normal state of vaginal biocoenosis), second type (reflection of non-specific vulvovaginitis), and third type (reflection of specific vulvovaginitis) (Table 1).[18] This classification is recommended for clinicians caring for prepubertal and adolescent girls, providing a helpful picture of the clinical-laboratory status of the vagina and its disorders in this pediatric population.

First type

In the first type classification of the vaginal smear (normocoenosis), there is a normal state of vaginal health. The quantity of leukocytes is rather negligible, and presented mainly by granulocytes; phagocytosis is not marked. Also, the flora is lean, containing mainly of a small quantity of gram-positive cocci (diplococci).

Second type

The smear called the second type represents an intermediate picture in which there is a transition state from normocenosis to a non-specific vaginitis picture. There is a low content of leukocytes (mainly granulocytes) and epithelial cells, and Döderlein's bacillus occur with girls of adolescent age. This type has considerable quantity of pathogenic and potentially pathogenic microbiologic flora with absence or minimal clinical characteristics of vaginal genital inflammation. The quantity of degeneratively changed cells is small.

Third type

The third type of vaginal smear reflects marked, specific vulvovaginitis. The quantity of leukocytes is more than 15, mainly neutrophils and macrophages; phagocytosis and mucous reaction are marked. The quantity of degenerative and reactively changed cells is considerable. The quantity of shed epithelium up to age of 9 years is often 9-12, and 10 to 20 for older adolescents. Döderlein's bacillus as a rule are absent. The flora is mixed and represented in considerable quantity. Further evaluation reveals a specific etiology such as Trichomonas vaginalis, Neisseria gonorrhoeae, Chlamydia trachomatis, Candida albicans, anaerobic bacteria reflective of bacterial vaginosis, or others (Table 1).[5,19-22]

Vaginal inflammation

Diagnostic methods used to identify vaginal pathology in prepubertal and adolescent girls are clinical evaluation and specific laboratory tests, including saline as well as potassium hydroxide preparations and microbiology; a major tool in the diagnosis is vaginal cytology (Fig.).[6,7] Vaginal inflammation is noted by exudative, degenerative, reparative, and defensive changes of cell composition (Table 2).

A classification of inflammatory urogenital disorders noted in prepubertal and adolescent girls is shown in Table 3. The specific diagnosis is based on a detailed history, genital examination, recto-abdominal examination, vaginoscopy, and laboratory evaluation of vaginal contents, including microscopic and microbiological testing looking for bacterial, viral, parasitic, and helminthic causes. In the medical history, the clinicians should pay attention to the begining of the disorder, its course, and any possible connection to other disorders the patient may also have.[12] The most common disorder in children is non-specific vulvovaginitis. The bacteria that can lead to vulvovaginitis include Staphylococci, Streptococci, Enterococci, Proteus, Klebsiella, and others.[5,7,12]

Management of vulvovaginitis

Management of vulvovaginitis is dependent on the specific etiology and underlying factors.[8,9,12,23-29] Not all infections are caused by only one microbe (despite Koch's postulate: "one microbe¡ªone disease"), and there can be some blurring of clinical features from one cause to another. Foreign bodies as a cause of vulvovaginitis are usually discovered because of foul smell and/or dark bloody discharge from the vagina. Some foreign bodies such as wads of toilet tissues are quite difficult to discover because they cannot be detected by rectal examination or ultrasound.

Methods of transmission of specific urogenital infections do change as puberty occurs. In the sexually active adolescent girl, sexually transmitted infections may occur.[6,13] This is not the case in a prepubertal child, unless sexual abuse has occurred. Improper hygiene becomes more of a causative factor in children. Table 4 outlines treatment of vulvovaginitis of various causes.[8,9,13,14,30-48]


This article reviews the principles of vaginal microbiocoenosis in prepubertal and adolescent girls. Clinicians can identify states of vaginal health and disease by using important diagnostic tools including vaginal cytology. Lactobacilli are infrequent in the prepubertal girls, but become more abundant in the adolescent girls. This important shift in vaginal biocoenosis is important to prevent the growth of potentially pathogenic flora. Three basic types of vaginal smears are presented in addition to a classification of inflammatory urogenital diseases. Management of common types of vulvovaginitis is also considered.

Funding: None.

Ethical approval: Not needed.

Competing interest: No benefits in any form have been received or will be received from any commercial party related directly or indirectly to the subject of this article.

Contributors: All authors contributed to the intellectual content and approved the final version.


1   Gurkin Y. "New" sexual transmitted diseases in girls. Guide for doctors. St.-Peterburgh: Medical Press, 1999: 5-64.

2   Schmidt F, Grulich-Henn J, Heinrich UE, Bettendorf M. Mucosal cytology in the determination of the pubertal status in girls. Horm Res 2002;58:223-228.

3   Bowen R. Classification of vaginal epithelial cells, 1998. http://www.vivo.colostate.edu/hbooks/pathphys/reprod/vc/cells.html (accessed March 2, 2009).

4   Kokolina V. Vulvavaginitis. In: Kokolina V, eds. Paediatric gynaecology: guide for doctors. §®oscow: Medical Informational Agency, 2003: 78-112.

5   Kuznetsova Y, Zeltonozenko L. Role of bacterioscopic investigation in diagnostic inflammatory diseases of genitals in girl and adolescent girl. In: Chayka V, Matytsina L, eds. Actual problem of rehabilitation of reproductive health. Donetsk: Lebed, 2004: 115-117.

6   Chaika V, Matytsina L, Onipko A. Prophylactic, diagnostic and treatment urogenital infection in girls and adolescents. In: Chayka V, Matytsina L, eds. Diagnostic and correction of disorders of reproductive system in children and adolescents. Donetsk: Lebed, 2000: 106-116.

7   Hammerschlag MR, Alpert S, Rosner I, Thurston P, Semine D, McComb D, et al. Microbiology of the vagina in children: normal and potentially pathogenic organisms. Pediatrics 1978;62:57-62.

8   Pierce AM, Hart CA. Vulvovaginitis: causes and management. Arch Dis Child 1992;67:509.

9   Piippo S, Lenko H, Vuento R. Vulgar symptoms in pediatric and adolescent patients. Acta Paediatr 2000;89:431.

10 Greydanus DE, Omar H, Patel DR. What's new: cervical cancer screening in adolescents. Pediatr Rev 2009;30:23-25.

11 Smith RA, Cokkinides V, Brawley OW. Cancer screening in the United States, 2008: a review of current American Cancer Society guidelines and cancer screening issues. CA Cancer J Clin 2008;58:161-179.

12 Johnson J. The Gynecology System and the Child. In: Greydanus D, Feinberg A, Patel D, Homnick D, eds. The Pediatric Diagnostic Examination. NY: McGraw-Hill Medical Publishers, 2008: 685-699.

13 Johnson J. Sexually transmitted diseases in the adolescent. In: Greydanus D, Patel D, Pratt H, eds. Essential Adolescent Medicine. New York: McGraw-Hill Medical Publishers, 2006: 511-542.

14 Holland-Hall C. Sexually transmitted diseases, syndrome and symptoms. Prim Care: Clin Office Pract 2006;33:433-454.

15 Gardner JJ. Comparison of the vaginal flora in sexually abused and nonabused girls. J Pediatr 1992;120:872-877.

16 Gerstner GJ, Gr¨¹nberger W, Boschitsch E, Rotter M. Vaginal organisms in prepubertal children with and without vulvovaginitis. A vaginoscopic study. Arch Gynecol 1982;231:247-252.

17 Bartley D, Morgan L, Rimsza M. Gardnerella vaginalis in prepubertal girls. Am J Dis Child 1987;141:1014.

18 Matytsina LA, Kuznetsova YI. Vaginal biocoenosis in prepubertal and adolescent girls. In: Chayka V, Matytsina L, eds. Actual problem of rehabilitation of reproductive health. Donetsk: Lebed, 2004: 116.

19 Siegel R, Schubert C, Myers P, Shapiro R. The prevalence of sexually transmitted diseases in children and adolescents evaluated for sexual abuse in Cincinnati: rationale for limited STD testing in prepubertal girls. Pediatrics 1995;96:1090-1094.

20 Ingram DL, Everett VD, Flick LA, Russell TA, White-Sims ST. Vaginal gonococcal cultures in sexual abuse evaluations: evaluation of selective criteria for preteenaged girls. Pediatrics 1997;99:E8.

21 Goodyear-Smith F. What is the evidence for non-sexual transmission of gonorrhoea in children after the neonatal period? A systematic review. J Forensic Leg Med 2007;14:489-502.

22 Palusci VJ, McHugh MT. Abuse in the child and adolescent. In: DE Greydanus, DR Patel, HD Pratt, eds. Behavioral Pediatrics, 2nd ed. NY: iUniverse Publishers, 2006: 769-811.

23 Paek SC, Merritt DF, Mallory SB. Pruritus vulvae in prepubertal children. J Am Acad Dermatol 2001;44:795-802.

24 Paradise JE, Willis ED. Probability of vaginal foreign body in girls with genital complaints. Am J Dis Child 1985; 139:472-476.

25 Loening-Bauecke V. Lichen sclerosus et atrophicus in children. Am J Dis Child 1991;145:1058-1061.

26 Greydanus DE, Omar HA. Sexuality issues and gynecologic care of adolescents with developmental disabilities. Pediatr Clin North Am 2008;55:1315-1335, viii.

27 Hillard PJA. Vaginal signs and symptoms: vaginal discharge. In: Adams PJA, eds. The 5-Minute Obstetrics and Gynecology Consult. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins, 2008: 48-49.

28 Merritt D. Evaluating and managing acute genital trauma in premenarchal girls. J Pediatr Adolesc Gynecol 1999; 12: 237-238.

29 Imai A, Horibe S, Tamaya T. Genital bleeding in premenarcheal children. Int J Gynaecol Obstet 1995;49:41-45.

30 Greydanus D, Bhave S, Patel D. Reproductive tract infections and sexually transmitted diseases. In: Bhave S, Nair M, Parthasarathy A, Menon P, Greydanus D, eds. Bhave's Textbook of Adolescent Medicine. New Delhi, India: JayPee Brothers Medical Publishers, 2006: 199-210.

31 Greydanus D, Patel D. Sexually Transmitted Diseases in Adolescents. In: Burg F, Ingelfinger J, Polin R, Gershon A, eds. Current Pediatric Therapy. Philadelphia: Elsevier, 2006: 326-329.

32 Centers for Disease Control and Prevention. Sexually Transmitted Diseases Treatment Guidelines, 2006. MMWR 2006;55(RR11):1-94.

33 Brown MR, Cartwright PC, Snow BW. Common office problems in pediatric urology and gynecology. Pediatr Clin North Am 1997;44:1091-1115.

34 ACOG Committee on Practice Bulletins¡ªGynecology.ACOG Practice Bulletin. Clinical management guidelines for obstetrician-gynecologists, Number 72, May 2006: Vaginitis. Obstet Gynecol 2006;107:1195-1206.

35 Craighill MC. Pediatric and adolescent gynecology for the primary care pediatrician. Pediatr Clin North Am 1998;45: 1659-1688.

36 Joishy M, Ashtekar CS, Jain A, Gonsalves R. Do we need to treat vulvovaginitis in prepubertal girls? BMJ 2005;330:186-188.

37 Koumantakis EE, Hassan EA, Deligeoroglou EK, Creatsas GK. Vulvovaginitis during childhood and adolescence. J Pediatr Adolesc Gynecol 1997;10:39-43.

38 Lacy J. Vaginitis: prepubertal valvovaginitis. In: Adams PJA, eds. The 5-Minute Obstetrics and Gynecology Consult. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins, 2008: 206-207.

39 Farrington PF. Pediatric vulvo-vaginitis. Clin Obstet Gynecol 1997;40:135-140.

40 Pokorny S. Pediatric & adolescent gynecology. Compr Ther 1997;23:337-345.

41 Sobel JD. Vulvovaginal candidosis. Lancet 2007;369: 1961-1971.

42 Sobel JD. Vaginitis: vulvovaginal candidiasis. In: Adams PJA, eds. The 5-Minute Obstetrics and Gynecology Consult. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins, 2008: 208-209,

43 Quint EH, Oakes MB. Vulvar lichen scherosus. In: Adams PJA, eds. The 5-Minute Obstetrics and Gynecology Consult. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins, 2008: 220-221.

44 Kass-Wolff JH, Wilson EE. Pediatric gynecology: assessment strategies and common problems. Semin Reprod Med 2003;21:329-338.

45 Merkley K. Vulvovaginitis and vaginal discharge in the pediatric patient. J Emerg Nurs 2005;31:400-402.

46 Sugar NF, Graham EA. Common gynecologic problems in prepubertal girls. Pediatr Rev 2006;27:213-223.

47 Perelman SE. Management quandary. Premenarchal vaginal bleeding. J Pediatr Adolesc Gynecol 2001;14:135-136.

48 Wall JW, Strickland JL. Bleeding, abnormal uterine: prepubertal. In: Adams PJA, eds. The 5-Minute Obstetrics and Gynecology Consult. Philadelphia: Wolters Kluwer/Lippincott Williams & Wilkins, 2008: 16-17.

Received November 12, 2008 Accepted after revision March 4, 2009


  [Articles Comment]

  title Author The End Revert Time Revert / Count

  Comment Title: 


World Journal of Pediatric Surgery

roger vivier bags 美女 美女

Home  |  Journal Information  |  Current Issue  |  Past Issues  |  Journal Information  |  Contact Us
Children's Hospital, Zhejiang University School of Medicine, China
Copyright 2007  www.wjpch.com  All Rights Reserved Designed by eb