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Consumption of cranberry as adjuvant therapy for urinary tract infections in susceptible populations: A systematic review and meta-analysis with trial sequential analysis

  • Jia-yue Xia,
  • Chao Yang,
  • Deng-feng Xu,
  • Hui Xia,
  • Li-gang Yang,
  • Gui-ju Sun

PLOS

10

  • Published: September ii, 2021
  • https://doi.org/10.1371/periodical.pone.0256992

Abstruse

The efficacy of cranberry (Vaccinium spp.) as adjuvant therapy in preventing urinary tract infections (UTIs) remains controversial. This study aims to update and decide cranberry effects equally adjuvant therapy on the recurrence rate of UTIs in susceptible groups. Co-ordinate to PRISMA guidelines, we conducted a literature search in Spider web of Science, PubMed, Embase, Scopus, and the Cochrane Library from their inception dates to June 2021. Nosotros included manufactures with information on the incidence of UTIs in susceptible populations using cranberry-containing products. We then conducted a trial sequential assay to control the run a risk of type I and blazon II errors. This meta-assay included 23 trials with 3979 participants. We found that cranberry-based products intake can significantly reduce the incidence of UTIs in susceptible populations (risk ratio (RR) = 0.70; 95% conviction interval(CI): 0.59 ~ 0.83; P<0.01). We identified a relative chance reduction of 32%, 45% and 51% in women with recurrent UTIs (RR = 0.68; 95% CI: 0.56 ~ 0.81), children (RR = 0.55; 95% CI: 0.31 ~ 0.97) and patients using indwelling catheters (RR = 0.49; 95% CI: 0.33 ~ 0.73). Meanwhile, a relative adventure reduction of 35% in people who use cranberry juice compared with those who use cranberry capsule or tablet was observed in the subgroup analysis (RR = 0.65; 95% CI: 0.54 ~ 0.77). The TSA issue for the furnishings of cranberry intake and the decreased chance of UTIs in susceptible groups indicated that the effects were conclusive. In decision, our meta-assay demonstrates that cranberry supplementation significantly reduced the risk of developing UTIs in susceptible populations. Cranberry can exist considered equally adjuvant therapy for preventing UTIs in susceptible populations. Still, given the limitations of the included studies in this meta-analysis, the decision should exist interpreted with caution.

Citation: Xia J-y, Yang C, Xu D-f, Xia H, Yang L-m, Sun Chiliad-j (2021) Consumption of cranberry as adjuvant therapy for urinary tract infections in susceptible populations: A systematic review and meta-analysis with trial sequential assay. PLoS I sixteen(9): e0256992. https://doi.org/10.1371/periodical.pone.0256992

Editor: Frank T. Spradley, University of Mississippi Medical Center, UNITED STATES

Received: June 20, 2021; Accepted: Baronial 19, 2021; Published: September 2, 2021

Copyright: © 2021 Xia et al. This is an open up access article distributed under the terms of the Artistic Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All relevant data are inside the manuscript and its Supporting data files.

Funding: The author(south) received no specific funding for this piece of work.

Competing interests: The authors take declared that no competing interests be.

Introduction

Urinary tract infections (UTIs) are amid the near prevalent bacterial infections in the community, outpatient and inpatient facilities, affecting about 150 million people annually [i]. Generally, UTIs can exist categorized into complicated and uncomplicated, or as upper (pyelonephritis) and lower (confined to the bladder). According to U.S. Centers for Illness Command and Prevention, UTIs crusade about 13,000 deaths each year [2]. Bacteriuria is a typical characteristic of UTI, with a high prevalence among young people and an historic period-related increase in both men and women [1]. Until the historic period of threescore years and older, the prevalence of bacteriuria is significantly higher in women than in men [three]. Adult women, in particular, are susceptible to UTIs, with well-nigh 20% to xxx% of women with an infection experiencing recurrence [4]. Other populations with a loftier risk of UTIs include pregnant women, children, elderly patients, participants with indwelling catheters, and patients with neuropathic bladder [five, 6].

Cranberries (Vaccinium macrocarpon), originated in New Zealand, are rich in complex phytochemical compositions, such as A-type proanthocyanidins (PACS), anthocyanins, benzoic acid and ursolic acid [7]. Escherichia coli, a primary pathogen involved in UTIs, is reported to be prevented from adhering to uroepithelial cells past PACs contained in cranberries in the urinary tract [8, 9]. According to several recent consensus and guidelines on UTI management, the efficacy of cranberry supplementation as an adjuvant therapy has not nevertheless reached a definitive decision on preventing and treating UTIs, and the quality of evidence was low. Therefore, it is necessary to assess the effects of cranberry intake on the incidence of UTIs in susceptible groups.

In 2012, Jepson et al. [6] conducted a systematic review of cranberry intake as adjuvant therapy for preventing and treating UTIs, and it was concluded that cranberry products failed to significantly reduce the occurrence of UTIs when compared with placebo or control groups. Additionally, a meta-analysis included 28 clinical studies in 2017 demonstrated that cranberry intake is associated with preventing UTIs, and that supplementing cranberry-based products provides a beneficial effect on reducing the incidence of UTIs [x]. However, few previous studies evaluated the effects of cranberry and UTIs in susceptible populations. Additionally, the efficacy of cranberry intake in preventing UTIs in susceptible individuals is yet not conclusive.

Some new relevant trials with inconsistent conclusions on using cranberry to preclude and treat UTIs take recently been published. The trial sequential analysis (TSA) method was practical to control the inflation of type I error rates. We, therefore, conducted an updated systematic review and meta-analysis with TSA to evaluate the furnishings of cranberry intake every bit adjuvant therapy for preventing and treating UTIs in susceptible populations.

Materials and methods

Ideals statement

In that location was no need for ethical blessing since all included studies in this systematic review of meta-assay were officially published in a peer-reviewed periodical.

Literature search strategy

Post-obit Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines, a systematic review and meta-assay were conducted [xi]. Relevant literature was identified through searching systematically in June 2021 in the post-obit five electronic databases: Web of Scientific discipline, PubMed, Embase, Scopus and Cochrane Library. Search terms included cranberry, Vaccinium macrocarpon, Vaccinium microcarpum, Vaccinium oxycoccus, Vaccinium erythrocarpum AND Urinary Tract Infection(s), UTI, bacteriuria, pyelonephritis, cystitis, pyuria, dysuria, Escherichia coli, and coli, without linguistic communication restrictions. Additionally, the reference lists of the eligible articles were further manually retrieved by the reviewers to recognize potentially relevant studies. Information extraction was performed past two reviewers independently (J. Y. 10. and C. Y.). Whatsoever disagreements were resolved past give-and-take or, if needed, by consultation with a third review author (10. H.). The details of the search strategy are shown in S1 Tabular array.

Inclusion and exclusion criteria

Two review authors (J. Y. X. and C. Y.) independently extracted the study data of the eligible articles from the literature search. Original studies were included if they met the following inclusion criteria:(1) written report pattern was limited simply to randomized controlled trial; (2) For the intervention used, we only include trials which compared cranberry-containing products to a placebo or non-placebo control group; (3) outcomes which can be calculated or reported as the number of participants experiencing a UTI; (4) The study susceptible populations included participants with recurrent UTIs, elderly men and women, pregnant women, children, participants with indwelling catheter, and participants with neuropathic bladder. The following exclusion criteria were used: (ane) the trials whose intervention independent cranberry in combination with some other bioactive compound; (two) studies that conspicuously did not adhere to the aforementioned inclusion criteria; (3) creature studies, case reports, reviews, conference papers, editorials, and studies with insufficient information. Any discrepancy upon inclusion or exclusion of the study was resolved past word amid the authors (J. Y. X., C. Y. and X. H.).

Data extraction and methodological assessment

The cumulative incidence of participants with recurrent urinary tract infection(southward) was used for pooled chance ratio estimates. Two authors (J. Y. X. and C. Y.) extracted detailed information of study methodology, characteristics of participants, intervention details, and outcomes reported. Nosotros causeless the incidence of UTI as the prespecified main outcome, which was expressed as either incidence or cumulative incidence rate. Trials which compared cranberry-based products to a placebo or non-treatment control were included. Quality assessment of included studies was performed based on the Cochrane Risk of Bias tool [12], and the tool covers seven domains (random sequence generation, allocation concealment, blinding of participants and personnel, blinding of outcome assessment, incomplete event data, selective outcome reporting and other bias) and each item was scored every bit "loftier risk," "low take a chance," or "unclear" for all selected studies.

Data synthesis and assay

Meta-analyses were performed past using Stata SE (15.0) and R (v four.0.3). Statistical significance was divers as P < 0.05 (2-sided). Data were calculated equally risk ratios with 95% conviction interval (95% CI). Heterogeneity inside studies was assessed past ways of the I2 metrics and chi-foursquare statistics, either Iii >50% or p value of χ2 test <0.10 was considered every bit statistically significant heterogeneity. Nosotros applied a stock-still-effect model by Mantel-Haenszel to estimate the summary risk if the heterogeneity was low to moderate (I2 < fifty%). Otherwise, the random-effects model by DerSimonian and Laird method was used [xiii]. We conducted subgroup analyses by prespecified covariates, including study design, study analysis, run a risk of random sequence generation, treatment in control grouping, population blazon, age, grade of cranberry-containing products, and dose frequency used. A Galbraith plot was constructed to identify potential outlier studies. Funnel plot and egger'due south regression were fatigued to graphically evaluate publication bias, and a 'trim and fill' analysis was used to further observe the stability of results if in that location is any asymmetry in funnel plot [xiv].

Trial Sequential Analysis (TSA)

In order to control the risk of type I and blazon 2 errors, a trial sequential analysis method was conducted on the incidence of UTIs. We performed TSA software (version 0.nine.five.10 beta) to accommodate CIs due to sparse data and repeat testing on the cumulative meta-analysis. If the cumulative Z-curve crosses the TSA monitoring purlieus, or enters the Required Information Size line, the result can be concluded that a firm conclusion tin can be reached and no further studies are needed [xv]. TSA was performed at the level of an overall 5% chance of a type I fault and with 80% power.

Results

Search results and trial characteristics

A catamenia diagram for included trials is shown in Fig 1. A total of 3431 manufactures were identified initially with the search strategy from five electronic databases, of which 3217 were removed afterwards reviewing title and abstracts, including 1916 duplications. And then, 214 full-text trials were retrieved for further information; of those, 186 studied were excluded for the following reasons: 140 for review articles, 31 for not available full articles, 15 for non-randomized controlled trials. Finally, eight trials were excluded for not being expressed as incidence charge per unit and three of the 20 included studies were each divided into ii trials. The written report by Caljouw et al. was divided since it included participants at high and low UTI hazard [17]. Stothers used two ways of orally administering cranberry-based products, that is cranberry tablets and cranberry juice [xvi]. Fly et al. administered 2 doses of PACs, including a loftier dose (240 mg PACs per day) and a low dose (80 mg PACs per day) [xviii]. Therefore, twenty-3 trials with sufficient information were eligible for inclusion into the final meta-assay.

In this systematic review, we identified twenty-eight trials that were eligible for qualitative synthesis. At that place were 24 parallel-group and 4 crossover group (S2 Table). All of these crossover trials had no washout periods. Nineteen trials were conducted co-ordinate to the intention-to-care for principle, and 9 trials used per-protocol assay. Twelve trials did not provide their randomization information, and suffered from a loftier rate of participants lost to follow-upwardly (0%-48%). In addition, 9 trials had high reporting bias (S3 Tabular array).

There were 4699 subjects included in the qualitative analysis (S4 Table). Of the 28 trials, 16 were performed in North America (United States and Canada), 5 were conducted in Europe (Britain, Republic of finland, and Italia), 2 were performed in the Kingdom of the Netherlands, and 5 separate studies from Japan, Taiwan (China), Republic of india, Czech republic and Turkey. The vast majority of studies followed subjects from Hospital clinic. According to the characteristics of included study subjects, the written report population were farther categorized into 6 unlike subgroups: women with recurrent UTIs, neuropathic bladder, children, significant patients, elderly patients and patients with indwelling catheters.

Characteristics of interventions of the included trials are summarized in S5 Table. Cranberry-containing products differed remarkably in cranberry course, manufacturer, daily dosage, PAC content, and dosing frequency. Fifteen trials administered cranberry juice, whereas i trial used both cranberry juice and cranberry tablets, and twelve trials used cranberry capsules. Xi trials used cranberry-based products from the manufacturer Ocean Spray. Daily cranberry amount ranged from 0.four to 194.4g and the actual cranberry amount was not reported in the eleven trials. Twenty-three trials used a formula placebo, whereas 5 trials did not used a placebo.

Differences were about notable in the definitions of UTI (S6 Table). Clinical symptoms to define UTI were required in virtually trials, and the baseline bacteriuria were not excluded in eighteen trials; In addition, the thresholds of bacteriuria ranged from ≥103 to ≥105 CFU/mL. The presence of UTI symptoms was non required in 11 trials. Because at that place were no reliable biological detection methods to examine the compliance of subjects, most studies utilize indirect methods for purpose. These included periodic interviews, self-reported questionnaires and recording the number of remaining pills. In most trials, the occurrence of UTI was expressed as incidence or cumulative incidence. At that place were 4 trials for which we were unable to calculate and obtain cumulative incidence, and four trials did not provide specific number of events. Finally, eight trials were excluded, and a total of 20-three trials were further analyzed in quantitative synthesis.

Quantitative information synthesis

Data on UTI cumulative incidence included 3979 participants across the 23 trials [sixteen–35], with 1978 in the cranberry intervention groups and 2001 in the placebo or command groups. There was moderate heterogeneity across trials (RR = 0.70; 95% CI: 0.59 ~ 0.83; Iii = 48%) (Fig two). The Galbraith plot showed that the trials past Ferrara et al. [25], Caljouw et al. [17] and Barbosa-Cesnik et al. [26] were potential sources of heterogeneity (Fig 3). Influential plot further demonstrated that these three trials [17, 25, 26] had pregnant bear upon on the pooled summary estimate (Fig iv), justifying its exclusion from the primary analysis. Later exclusion of these three trials, heterogeneity decreased from 48% to 6% (RR = 0.62; 95% CI: 0.54 ~ 0.79; I2 = 6%; P = 0.39) (Fig 5). The results suggested that the trials by Ferrara et al. [25], Caljouw et al. [17] and Barbosa-Cesnik et al. [26] may contribute to the source of heterogeneity.

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Fig 3. Galbraith plot.

At that place are three statistical outliers, A, B and C, which represent the trials by Ferrara et al., Barbosa-Cesnik et al., and Caljouw et al. (b) Low UTI risk, respectively. And in that location is a statistical extreme point, D, which stand for the trial by Caljouw et al. (a) High UTI run a risk.

https://doi.org/10.1371/journal.pone.0256992.g003

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Fig five. Woods plot: Summary effect of cranberry in prevention of urinary tract infection later on excluding three possible sources of heterogeneity, expressed every bit take chances ratio (RR).

W(fixed) indicates weights in fixed-effect Mantel-Haenszel model.

https://doi.org/10.1371/journal.pone.0256992.g005

Cranberry ingestion effects

According to all included twenty-three studies, the estimated weighted risk ratio significantly reduced in the risk of recurrent UTIs with cranberry intervention compared to placebo or command (RR = 0.70, 95% CI:0.59 ~ 0.83; P<0.01). There was a moderate caste of heterogeneity (I2 = 48%). TSA resulted in a required data size of 3,823, which was reached, and the cumulative Z-curve crossed the boundaries (Fig 6). Therefore, it was possible to reach a conclusion with no need for farther additional trials. The application of the TSA of cranberry-containing products ingestion on the incidence of UTIs in susceptible populations was strengthening the conclusions achieved.

Subgroup and sensitivity analyses

A subgroup assay was conducted to assess the influence of population type, mean patient age, course of cranberry-containing products, and dose frequency on the effectiveness of cranberries in the prevention of UTIs. The effects of cranberry intake on UTIs in subgroup based on characteristics of subjects and interventions are summarized in Fig 7. Although the previous evidence indicated that cranberries may reduce UTIs overall [20, 32], the subgroup analysis showed that compared with placebo or control, cranberries did not significantly decrease recurrent UTIs in some of the subgroups, including patients with neuropathic bladder (RR = 0.80; 95% CI:0.57 ~ 1.14), pregnant patients (RR = 0.79; 95% CI:0.37 ~ i.67) and elderly patients (RR = 0.89; 95% CI:0.75 ~ i.05).

Additionally, a sensitivity analysis was performed to approximate the influence of each individual written report on pooled RRs. we did not discover a relatively change, which indicated that the summary pooled guess was stable to study characteristics, treatment in control group and definitions of UTIs (S7 Table). On the whole, the sensitivity analysis revealed that the findings of our meta-analysis were robust.

Publication bias

In this meta-analysis, A funnel plot was used to evaluate the publication bias qualitatively, and Egger'southward regression were used to judge the publication bias quantitatively. Visual scanning of funnel plot suggested no asymmetry with Egger's regression test (t = -ane.34, p-value = 0.1956) (Fig 8). Results did not indicate show of publication bias.

Give-and-take

Our meta-assay results revealed a xxx% reduction in the risk of developing UTI in susceptible populations who consumed cranberry-containing products than those who did non (RR = 0.70; 95% CI: 0.59 ~ 0.83; I2 = 48%). We conducted a subgroup analysis to decide the source of heterogeneity. Moreover, we performed meta-regression to explore the potential sources of heterogeneity; however, no statistically significant sources of heterogeneity were identified. The influential and Galbraith plots indicated that three studies were the main sources of heterogeneity [17, 25, 26], and they may explicate some unknown heterogeneity.

Barbosa-Cesnik et al. [26] concluded that cranberry juice has no protective result against UTIs in women compared to those using a placebo(RR = 1.43; 95% CI: 0.87 ~ two.33). Two potential reasons may business relationship for this written report's departure. Start, different previous studies, Barbosa-Cesnik et al. [26] divers UTI using the everyman bacteriuria threshold, which is not less than grand colony-forming units [CFU]/mL. According to Kontiokari et al. [20], who used a college bacteriuria threshold (100,000 CFU/mL), cranberry juice provided positive effects on lowering the recurrence of UTIs. Second, we found that the morbidity of UTIs in the control group in the trial by Barbosa-Cesnik et al. [26] was significantly lower than that in the trial by Kontiokari et al. [xx]. Barbosa-Cesnik et al. [26] argued that placebo containing ascorbic acid, might exist benign to forbid UTI. For the trial past Ferrara et al. [25], they concluded that iii handling arms are among children anile 3–14 years, and children recruited in this study did not run into the original inclusion criteria. In addition, compared to the trial by Salo et al. [28], the intervention amount of cranberry is relatively at a high dose, resulting in a meaning divergence between the incidence rate of cranberry intervention and control or placebo groups. In the study by Caljouw et al. [17], they evaluated the effectiveness of cranberry capsules amongst vulnerable elderly. The results indicated that for residents with a high risk of UTI at baseline, taking cranberry capsules twice daily tin can significantly lower the incidence rate of clinically defined UTI. A possible reason in our assay for the heterogeneity is that this study used two dissimilar criteria for defining UTI, which was distinctly different from that in others studies. When we extracted amass data from this study, some errors will be unavoidable. All the same, it remains unknown whether the population studied in the trial by Ferrara et al. [25], Barbosa-Cesnik et al. [26] and Caljouw et al. [17] were markedly dissimilar in other aspects from other trials in our meta-analysis.

Our meta-assay results exhibit some similarities with previous studies. According to Wang et al. [36] and Jepson et al. [6], consuming cranberry-containing products provided benign effects on preventing UTIs. However, Jepson et al. [6] suggested that the benefit of cranberry-containing products might exist limited in some subgroups, mostly for women with recurrent UTI, and might exist absent in most population groups. We ended that supplementing cranberry may be benign in preventing and treating UTIs in susceptible populations, particularly for women with recurrent UTIs (RR = 0.68; 95% CI: 0.56 ~ 0.81), children (RR = 0.55; 95% CI: 0.31 ~ 0.97) and patients using indwelling catheters (RR = 0.49; 95% CI: 0.33 ~ 0.73).

Our sensitivity analysis revealed that our findings remained stable across report designs, placebo controls, and definitions, and that the consequence estimate did non modify significantly when the iii studies were excluded (RR = 0.62; 95% CI: 0.54 ~ 0.79; Itwo = 6%). We conducted a subgroup analysis to explore potential sources of heterogeneity, and discovered no meaning sources of heterogeneity between subgroups of age, different individuals, cranberry forms, and dose frequency.

Cranberry in juice form was observed to exist more than effective than cranberry capsule or tablets in the subgroup analysis. The antibacterial activity of cranberry juice may be due to the intake of large corporeality of liquid. This result in our analysis might be because people who consuming cranberry juice were improve hydrated than those using cranberry capsules or tablets. Additionally, since the precise mechanism of the protective effect of cranberries against UTIs is notwithstanding not fully elucidated, the better preventive effect of cranberry juice, to some extent, might be due to the additive or synergistic upshot of other yet unknown substances in the juice. However, a large volume of cranberry juice with loftier sugar content may cause severe gastrointestinal symptoms or other adverse effects, as observed past Fly et al. [18], who had to alter their treatment regimens to allow less frequent dosing to maintain compliance and avoid early withdrawal. Notwithstanding, although these agin effects are a concern, until the exact mechanism behind the protective furnishings of cranberries against UTIs is conspicuously comprehended, employ of cranberry in juice grade might be more than favorable than cranberry in capsules or tablets.

The nowadays systematic review and meta-analysis with TSA indicate that cranberry intake can foreclose UTIs in susceptible populations. Still, although European Association of Urology recommends regular consumption of cranberries as a nutritive method to effectively prevent UTIs, the data from relevant studies are inconclusive considering few available studies lasted longer than a twelvemonth. Equally a outcome, there is bereft evidence to back up the efficacy of cranberry products in clinical use. Future studies should continue to exist performed for a longer menstruation.

The treatment upshot of cranberry products may depend on their PAC concentration. Currently, the virtually recognized mechanism by which cranberry can prevent UTIs ordinarily involves its interference with bacterial adhesion in the urinary tract [37]. Cranberry consumption can cause an antiadhesion response in urine. If bacteria are unable to adhere to cells, they cannot grow and cause infection [37].

This meta-analysis possessed several strengths. Our study examined the efficacy of cranberry-containing products in susceptible populations and used trial sequential analysis to determine whether the evidence for cranberry consumption preventing UTIs in susceptible populations is sufficient. Additionally, it was performed and reported based on current guidelines [38, 39], and comprised an evaluation of results employing numerous sensitivity analyses, besides equally investigation of the adventure of bias using an updated assessment tool. In addition, there were potential limitations to our review.: first, insufficient data in several included studies caused certain limitations. We attempted to contact the authors three times but were unable to obtain whatever pertinent information. Second, 1 study used a mixture of juice concentrate including cranberry juice and lingonberry juice [twenty]. Lingonberry (Vaccinium visit-idaea) and Cranberry would most likely contain similar phytochemical composition, and then the observed benign effects may not be entirely attributed to cranberry alone. Tertiary, there was lack of in-consistency amidst the doses of PACs used in the included studies. The daily recommended intake of PACs, to subtract the number of recurrent UTIs, is not lower than 36 mg, and inconsistent dosages between unlike studies may cause different outcomes.

Conclusion

In summary, bear witness from our updated meta-analysis indicated that cranberry supplementation significantly reduced the incidence of occurring UTIs in susceptible populations. Furthermore, cranberry may exist considered every bit a promising adjuvant therapy for preventing UTIs in susceptible individuals. Withal, due to some limits of the included trials in this review, the conclusion therefore should be interpreted with caution. Further high-quality studies with appropriate large sample size are required to verify our results.

Supporting information

Acknowledgments

We sincerely thank all support from all authors.

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