Oral Microbiological Evidence among Palliative Patients: An Integrated Systematic Review

Data sources

Search strategy was devised by the research team comprising of a dentist (JSD), a palliative nurse (MRV), a medical doctor (DR), and a health-care researcher (ZR). Five electronic databases were used: ScienceDirect, PubMed, Google Scholar, Ovid, and EBSCOhost. Manual search was also conducted through key journals and reference list. We limited our search to articles published from January 2000 to December 2017. The search terms were “oral condition” OR “oral disease” OR “dental disease” OR “mouth disease” OR “mouth condition” OR mucositis OR stomatitis OR candidiasis OR cheilitis OR xerostomia OR “periodontal disease” OR halitosis OR thrush OR “angular cheilitis” OR “denture stomatitis” OR gingivitis OR periodontitis OR “mouth ulcer” OR “aphthous ulcer” AND palliative OR terminally-ill OR “terminally ill” OR “advanced disease” OR “advanced illness” OR dying OR end-of-life OR hospice OR cancer AND treatment OR intervention OR therapy OR management OR “oral care” OR “mouth care” OR “dental management” AND “end-of-life care.”

Study selection

Inclusion criteria specified that studies must be: (1) in full text, (2) in English language – to ensure no bias in translation, (3) research articles only – to ensure the articles retrieved had gone through peer-reviewed process, (4) published between year 2000 and 2017 – to ensure up-to-date research studies of the topic, (5) focused on palliative patients, and (6) analysis on microbiological evidence of oral conditions.

Figure 1 illustrates the PRISMA flow chart of study selection process. The initial combined search identified 25,311 articles from 5 databases and 19 articles from other sources (manual searching and through references). The titles of the articles were reviewed, and duplicates were removed which resulted in 25,263 being excluded as they did not focus on oral conditions among palliative patients. The abstracts of the remaining 67 articles were read to ensure the relevance of the articles to our study. This resulted in 28 articles being excluded. Two reviewers (ZR and DR) then independently read the remaining 39 articles and coded them for inclusion or exclusion. Following the independent review, the two reviewers met to discuss preliminary findings and to reach a consensus on the studies to be included, and thirty studies were excluded. Thus, for the purpose of analysis, there were a total of nine articles.

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Figure 1

Process of study selection

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Data extraction

In the data extraction process, the study details are extracted in Table 1. This was done by two reviewers (ZR and DR). All reviewers discussed each article to reach consensus regarding the study details. The following information was extracted from each included study: author (s), year published, title, purpose, setting, origin of specimens, techniques, and microflora.

Assessment of study quality

The quality of the identified studies was assessed using Joanna Briggs Institute critical appraisal tool (a checklist for analytical cross-sectional studies) which consisted of eight questions focusing on the clarity of inclusion criteria, study subjects, setting, validity and reliability of the exposure and outcome measures, issues on confounding factors, and appropriateness of statistical analysis used.[9] Each question has a choice of “yes,” “no,” “unclear,” or “not applicable” as an answer. Then, an overall appraisal was made whether to include or exclude each study, or to seek further information, with comments. Only the articles that were agreed by all involved researchers were included in this systematic review to inform the findings.

Data analysis

Extracted data from all included studies were analyzed using the Whittemore and Knafl principles of integrative review with four stages: data reduction, data display, data comparison, and conclusion drawing and verification.[10] At data reduction stage, all nine primary sources included in the integrative review were divided into a predetermined conceptual classification aligned with the aim of this review which is microbiological presence in the oral cavity of palliative patients and its identification techniques. Each primary source was reduced to a single page (available on request from authors). This helped us to systematically compare primary sources on specific issues, variables, and sample characteristics. It also allowed us to organize data into a manageable framework.

At Stage 2 – data display, the single-page data from the nine included studies are then extracted and displayed in Table 1. This helped us to visualize the patterns and relationships between and within primary data sources.

At Stage 3 – data comparison, we used constant comparison as a method of an iterative process of examining data to identify themes that had similar patterns and relations.

Finally, at Stage 4 – conclusion and verification, we verified patterns using primary data and identified any similarities, differences, and any spurious findings. These were dealt with in order to ensure that valuable information was not lost. Five meetings were held in order to identify and reach a consensus on the final themes.

Characteristics of study

Overall, nine articles were found eligible and included in this review. The included study settings involved patients of advanced cancer conditions or palliative patients from five European, three Asian, and one American country. The total number of each study participants ranged from 54 to 390. The microbiological evidence of oral conditions among palliative patients of the nine eligible studies is summarized in Table 1.

Common oral microorganisms present in palliative patients

Of nine studies, seven specifically reported Candida presence in the oral cavity of palliative patients.[3111213141516] Two studies reported the presence of yeast carriage.[1718] C. albicans was the predominant species with at least 50% of the total mycological infection reported in seven of nine studies [Table 1]. Other species of Candida reported were Candida glabrata, Candida dubliniensis, Candida tropicalis, Candida parapsilosis, and Candida krusei.

Predisposing factors for oral microbial pathology among palliative patient

Two studies reported dentures, xerostomia, and oral hygiene as predisposing factors for oral microbial pathology among palliative patients.[1117] Another study reported antibiotic and corticosteroid usage as predisposing factors for Candida species infections.[15] Another prospective study considered clinical findings and laboratory findings to develop appropriate treatment strategies.[18]

Association between oral symptoms and oral microbial flora

Only three studies reported a significant association between the presence of oral symptoms and the oral microbial flora, Jayachandran et al. found a significant association between dry mouth symptom and presence of Candida species.[3] Davies reported that oral yeast carriage and denture wearing were significantly associated (P < 0.006). Similarly, there was an association between oral yeast carriage and low salivary flow rate (P < 0.009).[11] Finally, a significant association was reported between prior treatment with triazole and isolation of fluconazole-resistant C. albicans (P < 0.005), but this relationship was not observed in C. glabrata isolates (P = 0.4).[13] The other six studies reported only the mean and percentage of various Candida species.

Techniques used for identification of microbiological presence

Of the nine studies, eight studies used oral swabs to identify the microbiological presence except one,[13] where a germ tube test was used for presumptive identification of C. albicans. In five studies, Sabouraud dextrose agar and/or CHROMagar were used for isolation of microbes,[311121517] one study used Trypticase agar slants,[13] another study used HiCrome Candida differential agar,[14] and two studies did not specify the type of agar used.[1618]

Two studies adapted antifungal susceptibility test that used minimum inhibition concentration of various antifungal agents such as azoles, nystatin, and amphotericin against different isolates of Candida species.[1216]

Another two studies performed Clinical and Laboratory Standards Institute-guided microbroth dilution method to detect antifungal susceptibility.[314] Another study used the National Committee for Clinical Laboratory Standards guidelines to identify antifungal susceptibility.[13]

Financial support and sponsorship

This study was financially supported by Universiti Brunei Darussalam, Grant information: UBD/OAVCRI/CRGWG (014)/171001.

Conflicts of interest

There are no conflicts of interest.