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An integrative review of current research on the role of the female urinary microbiota in overactive bladder symptoms.

The medical world has long upheld the notion that the female bladder is sterile. Recent studies provide evidence that this might not be the case. Bacterial DNA has been detected in the urine of women who have lower urinary tract symptoms (LUTS) and those who do not, suggesting an intrinsic microbiome of the female urinary tract (Brubaker & Wolfe, 2015; Hilt et al., 2014; Wolfe et al., 2012). The National Institutes of Health (NIH) Human Microbiome Project (2015) defines microbiome as the collection of microorganisms living in the human body, including eukaryotes, archaea, bacteria, and viruses. These discoveries could lead to new insights into little-understood women's health issues, including recurrent urinary tract infections (UTIs), and LUTS, including overactive bladder (OAB) (Brubaker & Wolfe, 2015). Traditional urine cultures do not detect all bacteria present in the urine, resulting in many negative culture UTIs going undiagnosed and untreated. New findings of bacteria present on traditionally negative urine cultures challenge the current practice of urine culturing and diagnosis, and present a need for new definitions, expanded culturing, and treatment options. This new information presents a paradigm shift in the scientific understanding of the female bladder.

Background and Significance

Within the category of LUTS, OAB and incontinence diagnoses are evaluated the most frequently and are reportedly the most problematic. In a worldwide population study, prevalence of LUTS was expected to increase from 45.2% in 2008 to 45.8% by the year 2018 (Irwin, Kopp, Agatep, Milsom, & Abrams, 2011). Worldwide population prevalence of OAB was 10.7% and UI at 8.2% in 2008, and rates were projected to increase to 20.1% and 21.6%, respectively, by 2018 (Irwin et al., 2011). More than half of the female population in the United States report symptoms of urinary incontinence (Markland, Richter, Fwu, Eggers, & Kusek., 2011). OAB is currently defined by the International Continence Society (ICS) as urinary urgency, frequency, and nocturia, with or without urinary incontinence (UI) (Abrams et al., 2009). The National Association for Continence (NAFC) (2015) reports that more than 17% of women over the age of 18 years report signs of OAB. These numbers, although varying throughout the literature, are thought to be dramatically underreported (Irwin et al., 2011; Milsom et al., 2001). Women with OAB report a negative impact on their quality of life, including decreased sleep, work productivity, and physical/sexual activity, as well as increased incidences of depression and anxiety symptoms (Coyne et al., 2011). Researchers report that OAB symptoms range across age, race, and ethnicity, with prevalence increasing with age (Coyne et al., 2011).

Causes of OAB are multi-factorial, and in many cases, unknown. In light of new findings, researchers (Hilt et al., 2014) suggest the possibility that OAB symptoms are influenced by the urinary tract microbiota. This may suggest a need to reconsider symptom management and diagnosis. If symptoms were identified and diagnosed early, and behavior modification implemented at an early age, there may be a delay in progression of symptoms, as well as a decrease in negative health outcomes (Coyne et al., 2011). This integrative review explores current evidence on the microbiota of the female urinary tract as it relates to OAB, and provides direction for researchers and urologic healthcare providers to understand how and what other scientists are doing to measure these emerging concepts.

Search Methods

A comprehensive literature search was conducted using a multistep process to identify articles by first searching the records of six online databases (CINAHL, EMBASE, PubMed, BIOSIS, Web of Science, and Scopus) from 2008 to 2016. In 2008, the NIH launched the Human Microbiome Project; therefore, only literature after this point focuses on the relationship of microbiome on health. The search was carried out with the combination of keywords: "(microbiome OR microbiota) AND (urinary urgency OR overactive bladder) AND (female OR woman)." Second, manual searches of references in identified articles, as well as articles having cited identified articles, were also considered. Only articles published in English were included in this review, and inorganic causes of urgency, including cystitis, infection, and neurological causes, were excluded. A total of 177 articles were identified (see Figure 1). After duplicates were removed, and exclusion criteria were met, six quantitative articles remained. Of the six remaining articles, data were abstracted on study year, sample size, design, instruments, results/ conclusions, and level of evidence (see Table 1). The Johns Hopkins Nursing Evidence-Based Practice Appendix E: Research Evidence Appraisal Tool (Frank, 2014) was used to analytically evaluate the articles for level and quality of the evidence. Each article was assigned a level of evidence (I to III) and quality of evidence (A-C) score. Level I indicates a randomized control trial (RCT), Level II indicates a quasi-experimental study, and Level III indicates a non-experimental study, such as qualitative, descriptive, or case study. Quality ranges from A, indicating high quality, to C, indicating low quality or major flaws (Johns Hopkins Hospital/Johns Hopkins University, 2016).

Results

Sample characteristics, symptoms presentation and measurement, urine collection method, urine culturing method, and culture results were summarized across the studies. Urine collection method, culture method, and bacteria identified are presented in Table 2.

Sample Characteristics

The largest sample sizes were 247 women (Sorrentino et al., 2015) and 182 women (Pearce et al., 2015). Siddiqui and colleagues (2014) presented a case study with one woman. The remaining studies ranged from 65 to 118 women (Hilt et al., 2014; Lee et al., 2010; Pearce et al., 2014). The majority of studies evaluated participants aged 50 to 60 years, except for Hilt et al. (2014), where age was not specified, and Sorrentino et al. (2015), where the mean age was 47.7 years.

Symptom Presentation And Urinary Symptom Measurements

Many studies included in this review evaluated women who presented with OAB symptoms. However, Sorrentino et al. (2015) used a test group of women presenting to a uro-gynecology practice who were not specifically presenting with OAB symptoms alone and a control group of women presenting to a gynecology practice. Pearce et al. (2014, 2015) evaluated women with urge urinary incontinence (UUI), a common symptom of OAB but not necessarily representative of all OAB.

Urinary symptoms were analyzed using several validated tools across the studies. Lee et al. (2010) and Sorrentino et al. (2015) used the International Consultation on Incontinence Questionnaire for Female Lower Urinary Tract Symptoms (ICIQ-FLUTS) (Abrams, Avery, Gardener, Donovan, & Board, 2006; Jackson et al., 1996). Lee et al. (2010) also used the Perception of Bladder Condition questionnaire (PPBC), as cited by Coyne, Matza, Kopp, and Abrams (2006), and a three-day bladder diary to assess symptoms. Hilt et al. (2014) and Pearce et al. (2014) used the Pelvic Floor Distress Inventory (PFDI) (Barber, Kuchibhatla, Pieper, & Bump, 2001) to assess symptoms, and Pearce et al. (2014) used the Overactive Bladder questionnaire (OAB-q) (Coyne et al., 2002). Siddiqui et al. (2014) did not assess symptoms and tools to measure urinary symptoms were not mentioned in Pearce et al. (2015).

The ICIQ-FLUTS is a 12-item scale used to evaluate a broad range of LUTS, including filling, voiding, and incontinence symptoms. The PPBC is a single-item tool to assess perception of bladder condition in patients with OAB. The PFDI measures the effect of pelvic floor disorders on quality of life. OAB-q specifically looks at OAB symptoms and the effect of OAB on quality of life. All of the tools used have been previously validated on similar populations with pelvic floor disorders. The ICIQ-FLUTS (Jackson et al., 1996) has a Cronbach's alpha of 0.78, the PFDI (Barber et al., 2001) has a Cronbach's alpha of 0.82 to 0.89, and the OAB-q (Coyne et al., 2002) has Cronbach's alpha values ranging from 0.86 to 0.94. The Cronbach's alpha demonstrates that all of the tools have high internal consistency and reliability. As a single-item measure, the PPBC had significant correlations between bladder diaries (p < 0.001) and the OAB-q (p < 0.001 (Coyne et al., 2006).

Urine Sample Collection And Analysis

Most commonly, transurethral catheterization (TUC) was used to obtain urinary samples. However, Sorrentino et al. (2015) used midstream clean-catch methods, and Lee et al. (2010) used urethral and vaginal swabs. Siddiqui et al. (2014) did not specify the urine collection method. Standard culture techniques were used in four of the six studies (Hilt et al., 2014; Lee et al., 2010; Siddiqui et al., 2014; Sorrentino et al., 2015). In addition, Hilt et al. (2014) reported the expanded quantitative culture (EQUC) and 16SrRNA sequencing (DNA sequence found in all bacteria and is commonly used in bacterial taxonomy), and Siddiqui et al. (2014) reported the results of a urine dipstick, urinalysis, and 16SrRNA sequencing. Pearce et al. (2014) evaluated the EQUC and 16SrRNA results, and Pearce et al. (2015) described the results of 16SrRNA sequencing and DNA sequencing.

Urine Culture Results

False negatives for routine cultures were noted in Hilt et al. (2014) and Pearce et al. (2014), with about 6% showing positive growth on routine culture, and 60% to 80% growth on EQUC. Similar routine culture findings were found in Sorrentino et al. (2015), with 6% showing significant bacteriuria supporting prior results. Pearce et al. (2015) found 51.1% were 16SrRNA sequence positive similar to EQUC results, suggesting accuracy across these methods. Lee et al. (2010) had high routine culture results of 42%, which may be due to collection methods. Hilt et al. (2014) found a significant correlation between results of EQUC and 16SrRNA sequencing.

Table 2 lists the bacteria and dominant urotypes isolated across the studies. However, differences in frequency and dominance of bacteria might be due to differences in collection and culturing methods, symptoms of sample, and purpose of the study. Two studies (Pearce et al., 2014, 2015) identified one dominant bacteria --a "urotype." Lactobacillus were identified in Hilt et al. (2014) and Pearce et al. (2014, 2015). Pearce et al. (2014) found different strands of Lactobacillus in the UUI group (Gasseri) and control group (Crispatus). Ureaplasma were identified in Lee et al. (2010) and Siddiqui et al. (2014) as linked to OAB symptoms. Hilt et al. (2014) and Pearce et al. (2014) identified Aerococcus in OAB/ UUI groups and not in the control groups. Findings ranged from symptom relief with treatment (Lee et al., 2010) to a suggestive protective role of the microbiome in post-procedure UTIs (Pearce et al., 2015).

Limitations

The level of evidence across these studies was low. The primary study design of the articles reviewed was descriptive (Hilt et al., 2014; Lee et al., 2010; Pearce et al., 2014; Sorrentino et al., 2015), utilizing varying culture mechanisms and symptom scales. Sample sizes varied; however, the majority of studies reported small sample sizes. There was also a high level of homogeneity across studies, resulting in a lack of analysis based on race, geographic, and other demographic data. The purpose of four of the six articles was to evaluate the female urinary microbiome either by culture method (Hilt et al., 2014; Pearce et al., 2014) or in relation to OAB and other urinary symptoms (Pearce et al., 2015; Sorrentino et al., 2015). Lee et al. (2010) focused on mycoplasma infections in particular and the efficacy of azithromycin antibiotic therapy on overactive bladder symptoms. Siddiqui et al. (2014) did not specify a study purpose. This is an emerging area; thus, these findings across this cadre of studies were not unexpected.

The age range (50 to 60 years) of women may also present some limitations in transferability. The majority of women were postmenopausal, which may represent a different urinary microbiome due to hormonal changes than younger premenopausal women. Additionally, the variances in collection and analysis methods also limit this review. The different symptom measurement tools do not all measure the same OAB symptoms or quality of life. Some looked at overarching LUTS and pelvic floor disorders and not specifically OAB symptoms. Variances in symptom construct and bacteria identified by various culture methods make results difficult to compare across studies.

Implications for Nursing And Patient Care

The integrative review supports the role of the female urinary microbiome on OAB symptom presentation and potential protection. The studies reviewed represent emerging literature on the presence of bacteria in the urinary tract and impact on OAB symptoms. Findings from this integrative review suggest that bacteria in the female urinary tract could contribute to OAB symptomology and challenge the traditional understanding of OAB management. These findings support the need to better understand the urinary microbiome and to disregard the old notion of urine as sterile. Based on this information, practice changes are needed to identify bacterial causes of OAB symptoms, individualize treatment, and suggest prevention strategies. Standard culturing practice needs to be re-evaluated in light of the research findings discussed. Results from these studies also provide direction for further research in terms of how previous researchers have collected and measured bacteria in urine.

The findings of Hilt et al. (2014) and Pearce et al. (2014) support a significant false negative rate using standard urine culturing practices. This challenges current culturing practice and our understanding of "culture negative" because many bacterial infections go undetected, leading to chronic UTI symptoms similar to OAB. Lee et al. (2010) found women with OAB reported symptom relief after treatment with azithromycin for positive cultures; however, there was a potential placebo effect as the five women that remained culture positive after antibiotic therapy also reported relief of symptoms.

Hilt et al. (2014) reports a significant correlation between results of EQUC and 16SrRNA sequencing were supported by rates of detection in other studies (Lee et al., 2010; Pearce et al., 2014, 2015). Therefore either method would be an appropriate substitute for the traditional culture when results of traditional culture are "negative" and yet symptoms remain.

The identification of a dominant bacteria, or urotype, is a new concept and could represent overgrowth indicative of urinary symptom presentation or protection (Pearce et al., 2014, 2015). Some dominant bacteria were associated with OAB symptom presentation, including Aerococcus and Streptococcus (Hilt et al., 2014; Pearce et al., 2014), and Ureaplasma (Lee et al., 2010; Siddiqui et al., 2014). This supports a potential microbial cause of OAB symptomatology. The presence of Lactobacillus in women without OAB symptoms (Hilt et al., 2014; Pearce et al., 2014, 2015) suggests a protective role in preventing OAB and UUI symptoms. Based on these findings, there may be a role for probiotics in supporting healthy urinary microbiome and preventing symptoms. Results of Pearce et al. (2014) with Lactobacillus gasseri associated with the UUI group and Lactobacillus crispatus with the control group require further research as to the effects of certain bacteria at the species level. More research is needed to determine causation to make recommendations for screening, diagnosing, and managing women who present with OAB symptoms.

Recommendations for Future Research

This is an emerging field, and research is limited regarding the effects of bacteriuria on OAB symptoms; thus, more research is needed to support knowledge development. Research with larger sample sizes, younger populations, and more diverse women is needed to truly understand the impact of the bladder microbiome on symptom presentation. Identifying which bacteria are markers for symptoms and whether a protective function of the microbiome exists is needed. Changes with age and hormones in women and how this affects the microbiome of the bladder would also need to be addressed. It is also important to assess the effect of dietary consumption of known bladder irritants (e.g., caffeine, tobacco, carbonation, alcohol) on the urinary microbiome; findings from such studies could lead to clinical interventions.

Conclusion

As the population continues to age and OAB symptoms become more prevalent, management and treatment interventions starting at a young age will be increasingly important. Understanding pathophysiology of this condition will aid in diagnosis and treatment. Findings from this review support a urinary microbiome, and suggest protective and pathologic roles of certain bacteria in symptom presentation. Further research into the management of specific bacteria on symptom relief will need to be conducted.

doi:10.7257/1053-816X.2017.37.2.94

References

Abrams, P., Artibani, W., Cardozo, L., Dmochowski, R., van Kerrebroeck, P., & Sand, P. (2009). Reviewing the ICS 2002 terminology report: The ongoing debate. Neurology and Urodynamics, 28(4), 287. doi:10.10 02/nau.20737

Abrams, P., Avery, K., Gardener, N., Donovan, J., & Board, I. A. (2006). The International Consultation on Incontinence Modular Questionnaire: www.iciq.net. The Journal of Urology, 175(3), 1063-1066.

Barber, M.D., Kuchibhatla, M.N., Pieper, C. F., & Bump, R.C. (2001). Psychometric evaluation of 2 comprehensive condition-specific quality of life instruments for women with pelvic floor disorders. American Journal of Obstetrics and Gynecology, 185(6), 1388-1395.

Brubaker, L., & Wolfe, A.J. (2015). The new world of the urinary microbiota in women. American Journal of Obstetrics and Gynecology, 213(5), 644-649.

Coyne, K.S., Matza, L.S., Kopp, Z., & Abrams, P. (2006). The validation of the patient perception of bladder condition (PPBC): A single-item global measure for patients with overactive bladder. European Urology, 49(6), 1079-1086.

Coyne, K., Revicki, D., Hunt, T., Corey, R., Stewart, W., Bentkover, J., ... Abrams, P. (2002). Psychometric validation of an overactive bladder symptom and health-related quality of life questionnaire: The OAB-q. Quality of Life Research, 11(6), 563-574.

Coyne, K.S., Sexton, C.C., Vats, V., Thompson, C., Kopp, Z.S., & Milsom, I. (2011). National community prevalence of overactive bladder in the United States stratified by sex and age. Urology, 77(5), 1081-1087.

Frank, B. (2014). Book review--Johns Hopkins nursing evidence-based practice: Models and guidelines (2nd edition). Nurse Education Today, 34(1), e1. doi:10.1016/j.nedt. 2012.07.001

Hilt, E.E., McKinley, K., Pearce, M.M., Rosenfeld, A.B., Zilliox, M.J., Mueller, E.R., Brubaker, L., ... Schreckenberger, P.C. (2014). Urine is not sterile: Use of enhanced urine culture techniques to detect resident bacterial flora in the adult female bladder. Journal of Clinical Microbiology, 52(3), 871-876.

Irwin, D.E., Kopp, Z.S., Agatep, B., Milsom, I., & Abrams, P. (2011). Worldwide prevalence estimates of lower urinary tract symptoms, overactive bladder, urinary incontinence and bladder outlet obstruction. BJU International, 108(7), 1132-1138.

Jackson, S., Donovan, J., Brookes, S., Eckford, S., Swithinbank, L., & Abrams, P. (1996). The Bristol female lower urinary tract symptoms questionnaire: Development and psychometric testing. BJU International, 77(6), 805-812.

Johns Hopkins Hospital/Johns Hopkins University. (2016). Johns Hopkins Nursing Evidence-Based Practice Model - Appendix C: Evidence level and quality guide. Retrieved from http://www.hopkinsmedicine.org/ evidence-based-practice/jhn_ebp.html

Lee, Y.S., Kim, J.Y., Kim, J.C., Park, W.H., Choo, M.S., & Lee, K.S. (2010). Prevalence and treatment efficacy of genitourinary mycoplasmas in women with overactive bladder symptoms. Korean Journal of Urology, 51(9), 625-630.

Markland, A.D., Richter, H.E., Fwu, C.W., Eggers, P., & Kusek, J.W. (2011). Prevalence and trends of urinary incontinence in adults in the United States, 2001-2008. The Journal of Urology, 186(2), 589-593.

Milsom, I., Abrams, P., Cardazo, L., Roberts, R.G., Thuroff, J., & Wein, A.J. (2001). How widespread are symptoms of overactive bladder and how are they managed? BJU International, 88(7), 760-766.

National Association for Continence (NAFC). (2015) Overactive bladder. Retrieved from http://www.nafc.org/ overactive-bladder

National Institutes of Health (NIH) Human Microbiome Project (HMP). (2015). The human microbiome. Retrieved from http://hmpdacc. org/overview/about.php

Pearce, M.M., Hilt, E.E., Rosenfeld, A.B., Zilliox, M.J., Thomas-White, K., Fok, C., ... Wolfe, A.J. (2014). The female urinary microbiome: A comparison of women with and without urgency urinary incontinence. MBio, 5(4), e01283-14. doi:10.1128/mBio. 01283-14

Pearce, M.M., Zilliox, M.J., Rosenfeld, A.B., Thomas-White, K.J., Richter, H.E., Nager, C.W., ... Moalli, P. (2015). The female urinary microbiome in urgency urinary incontinence. American Journal of Obstetrics and Gynecology, 213(3), 347e1. doi:10.1016/j.ajog.2015.07.009

Siddiqui, H., Lagesen, K., Nederbragt, A.J., Eri, L.M., Jeansson, S.L., & Jakobsen, K.S. (2014). Pathogens in urine from a female patient with overactive bladder syndrome detected by culture-independent high throughput sequencing: A case report. The Open Microbiology Journal, 8, 148-153.

Sorrentino, F., Cartwright, R., Digesu, G.A., Tolton, L., Franklin, L., Singh, A., ... Khullar, V. (2015). Associations between individual lower urinary tract symptoms and bacteriuria in random urine samples in women. Neurourology and Urodynamics, 34(5), 429-433.

Wolfe, A.J., Toh, E., Shibata, N., Rong, R., Kenton, K., Fitzgerald, M., ... Brubaker, L. (2012). Evidence of uncultivated bacteria in the adult female bladder. Journal of Clinical Microbiology, 50(4), 1376-1383.

Kimberly J. Angelini, WHNP-BC, is a PhD Student, Boston College, Boston, MA, and a Board Certified Women's Health Nurse Practitioner, Dowd Medical Gynecology, Reading, MA.

Caption: Figure 1. PRISMA Chart of Literature Search
Table 1.
Literature Table

Article        Level of      Sample/ Symptoms
              Evidence *

Lee et          III-C      n = 84 Mean age
  al., 2010                  = 51 years OAB

Hilt et         III-C      n = 65 Mean age
  al., 2014                  = Not specified
                             OAB control
                             (routine GYN
                             surgery)
Pearce et       III-B      n = 118 Mean age
  al., 2014                  = 63 years for
                             UUI and 49 years
                             for control UUI
                             control (no UUI)
Siddiqui et     III-C      n = 1 Mean age
  al., 2014                  = 61 years OAB
Pearce et       III-B      n = 182 Mean age
  al., 2015                  = 55.8 years for
                             sequence positive
                             and 61.3 years
                             for sequence
                             negative UUI
Sorrentino      III-B      n = 247 Mean age
  et al.,                    = 47.2 years
  2015                       Uro-Gyn and GYN
                             practice

Article            Design/ Purpose             Tool

Lee et        Multicenter longitudinal     PPBC ICIQ
  al., 2010     descriptive study.           -FLUTS
                Identify incidence of        3-day
                mycoplasma infections        diary
                and evaluate antibiotic
                efficacy in women with
                OAB.
Hilt et       Cross-sectional              PFDI
  al., 2014     descriptive study.
                Determine whether the
                urinary microbiome
                comprises of live
                bacteria missed on
                routine culture.
Pearce et     Cross-sectional              PFDI OAB-q
  al., 2014     descriptive study.
                Characterize female
                urinary microbiome
                with EQUC and 16SrRNA
                sequencing.
Siddiqui et   Case study. Not specified.   NA
  al., 2014
Pearce et     Secondary Analysis of        Not specified
  al., 2015     ABC trial. Characterize
                female urinary
                microbiota by 16SrRNA
                sequence. Assess
                relationship of
                bacteriuria to treatment
                response and post
                treatment UTI risk.
Sorrentino    Cross-sectional              ICIQ-FLUTS
  et al.,       descriptive study.
  2015          Evaluate presence of
                bacteriuria in women
                without acute UTI
                symptoms. Association
                of bacteriuria with
                urinary symptoms.

Article            Culture Results

Lee et        42.5% positive cultures.
  al., 2010

Hilt et       6.2% positive standard
  al., 2014     culture. 80% showed
                growth on EQUC.
                Correlation between
                bacteria found on EQUC
                and 16SrRNA sequencing.
Pearce et     5.9% positive standard
  al., 2014     culture. 60% showed
                growth on EQUC.
                Majority of samples
                dominated by one
                genus (urotype).
Siddiqui et   Baseline routine culture
  al., 2014     positive for
                Streptococcus. After
                treatment, routine
                culture negative but
                16SrRNA had
                Streptococcus in 2
                times higher sequence.
Pearce et     51.1% sequence positive.
  al., 2015     Sequence negative were
                at greater risk for
                post treatment UTI;
                suggests protective
                role of microbiome.
Sorrentino    6.5% had significant
  et al.,       bacertiuria (6 GYN and
  2015          10 urogyn). After
                adjusting for age,
                parity, symptomatic
                prolapse, menopause,
                and surgical history
                --urinary urgency,
                bladder pain, nocturia,
                and nocturnal enuresis
                remained significantly
                associated with
                bacteriuria (p < 0.05).

Notes: OAB = overactive bladder, GYN = gynecologic,
UUI = urge urinary incontinence, Uro-Gyn = urogynecologic,
EQUC = expanded quantitative urinary culture, PPBC
= Patient Perception of Bladder Condition questionnaire,
ICIQ-FLUTS = International Consultation on Incontinence
Questionnaire for Female Lower Urinary Tract Symptoms,
PFDI = Pelvic Floor Distress Inventory, OAB-q = Overactive
Bladder Questionnaire.

* The Johns Hopkins Nursing Evidence-Based Practice
Appendix E: Research Evidence Appraisal Tool (Frank,
2014) ratings for Level of Evidence (I-III) and quality
of evidence (A-C) score. Level I indicates a randomized
control trial (RCT), Level II indicates a
quasi-experimental study, and Level III indicates a
non-experimental study, such as qualitative, descriptive,
or case study. Quality ranges from A, indicating high
quality, to C, indicating low quality or major flaws
(Johns Hopkins Hospital/Johns Hopkins University,
2016).

Table 2.
Bacteria Identified and Collection

Article        Lactobacillus   Gardnerella   Ureaplasma   Mycoplasma
                                                           hominis

Lee et al.,                                      X            X
  2010
Hilt et al.,         X              x
  2014
Pearce et            X              X            x
  al., 2014
Siddiqui et          x                           X
  al., 2014
Pearce et            X              X
  al., 2015
Sorrentino
  et al.,
  2015

Article         Chlamydia    Corynebacterium   Streptococcus
               trachomatis

Lee et al.,         X
  2010
Hilt et al.,                        X                X
  2014
Pearce et                           x                x
  al., 2014
Siddiqui et                                          X
  al., 2014
Pearce et                           x                x
  al., 2015
Sorrentino
  et al.,
  2015

Article        Actinomyces   Staphylococcus   Aerococcus   Sneathia

Lee et al.,
  2010
Hilt et al.,        X              X              X
  2014
Pearce et           x              X              x           X
  al., 2014
Siddiqui et
  al., 2014
Pearce et                          x              X           x
  al., 2015
Sorrentino
  et al.,
  2015

Article        Enterobacterace   Atopobium   Prevotella   Bacteroides
                                                          urealyticus

Lee et al.,
  2010
Hilt et al.,          x                          x
  2014
Pearce et             X              x           x
  al., 2014
Siddiqui et                          X           X
  al., 2014
Pearce et             X              x           X             X
  al., 2015
Sorrentino
  et al.,
  2015

Article        GBS   E. Coli   Coliform   Other   Urine Sample

Lee et al.,                                       Urethral and
  2010                                              cervical
                                                    swab TUC
Hilt et al.,            x                   x     TUC
  2014
Pearce et       X                           x     Not specified
  al., 2014
Siddiqui et                       X         x     TUC
  al., 2014
Pearce et                                   X     Clean catch
  al., 2015                                         mid-stream
Sorrentino              X                   X
  et al.,
  2015

Article                Test

Lee et al.,    Mycoplasma IST2
  2010           kit and PCR

Hilt et al.,   Standard culture,
  2014           EQUC, 16SrRNA
                 sequencing
Pearce et      EQUC, 16SrRNA
  al., 2014      sequencing
Siddiqui et    Dipstick,
  al., 2014      routine
                 culture, UA,
                 16SrRNA sequencing
Pearce et      16SrRNA sequencing
  al., 2015
Sorrentino     Routine culture
  et al.,
  2015

Notes: TUC = transurethral catheterization, PCR
= polymerase chain reaction, EQUC = expanded
quantitative urine culture, UA = urinalysis;
X = dominant finding/"urotype," x = found in
lesser amounts.
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Date:Mar 1, 2017
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