Changes in bacterial number at different sites of oral cavity during perioperative oral care management in gastrointestinal cancer patients: preliminary study

Abstract Objective The objective of this study was to clarify differences in bacterial accumulation between gastrointestinal cancer patients who underwent severely invasive surgery and those who underwent minimally invasive surgery. Material and Methods We performed a preliminary investigation of gastrointestinal cancer patients who were treated at the Department of Surgery, Takarazuka Municipal Hospital, from 2015 to 2017 (n=71; 42 laparoscopic surgery, 29 open surgery) to determine changes in bacterial numbers at different sites of the oral cavity (tongue dorsum, gingiva of upper anterior teeth, palatoglossal arch), as well as mouth dryness and tongue coating indices. Specifically, patients received professional tooth cleaning (PTC), scaling, tongue cleaning, and self-care instruction regarding tooth brushing from a dental hygienist a day before the operation. Professional oral health care was also performed by a dental hygienist two and seven days after surgery. Oral bacteria numbers were determined using a bacterial counter with a dielectrophoretic impedance measurement method. Results The number of bacteria at all three examined sites were significantly higher in the open surgery group when compared to the laparoscopic surgery group on the second postoperative day. Relevantly, bacterial count in samples from the gingiva of the upper anterior teeth remained greater seven days after the operation in patients who underwent open surgery. Furthermore, the dry mouth index level was higher in the open surgery group when compared to the laparoscopic surgery group on postoperative days 2 and 7. Conclusions Even with regular oral health care, bacterial numbers remained high in the upper incisor tooth gingiva in gastrointestinal cancer patients who received open surgery. Additional procedures are likely needed to effectively reduce the number of bacteria in the gingival area associated with the upper anterior teeth.


Introduction
Performing dental treatments, such as periodontal and dental caries treatments, extraction of nonpreservable teeth and replacement of missing teeth, are required before starting cancer treatment to reduce postoperative complications. In addition, perioperative professional oral health care is recognized to be important for cancer patients 18, 26 .
Colorectal cancer is a predominant type of cancer and the third leading cause of cancer-associated death worldwide 1 , while gastric cancer is also one of the most common types of malignancies throughout the world 2 .
Surgical resection is the primary procedure to treat patients with gastrointestinal cancer, with laparoscopic surgery being widely adopted for gastrointestinal cancers, such as gastric and colorectal cancer 10,20 .
There are reports that perioperative oral care may   as well as scaling and professional tooth cleaning (PTC) by a dental hygienist at the Oral Surgery Department a day before the operation. Two days after the operation the patients received oral health care and self-care instruction in the inpatient ward by a dental hygienist, then seven days after the operation oral health care such as PTC was given again. In addition, a 0.025%

Evaluation of dry mouth
Changes in dry mouth, also known as xerostomia, and subjective symptoms (i.e., severely dry, moderately dry, slightly dry, moderately wet, fully wet) were evaluated based on interviews performed on preoperative day 1, and on postoperative days 2 and 7. In addition, dry mouth was also classified as normal, light (increased saliva viscosity), moderate (small bubbles observed in saliva), and severe (dry tongue surface without saliva), using a previously reported method 14 .

Tongue coating index
Tongue coating index (TCI) values were determined on preoperative day 1, and postoperative days 2 and 7.
To determine both the extension and thickness of the tongue coating, we used a detailed index previously proposed 29 . With this method, the tongue dorsum is divided into 9 sections, including 1 middle and 2 lateral areas for each of the posterior, middle, and anterior thirds of the tongue. The presence of tongue coating was classified as none (Score 0), light-thin (Score 1, pink color underneath coating visible), and heavythick coating (Score 2, no pink color observed) for each section. We obtained a personal tongue coating index by adding the scores for all 9 sections (total score 0-18).

Clinical examinations
We examined clinical markers such as body temperature (BT), white blood cell (WBC) count, and C-reactive protein (CRP) level to evaluate inflammatory response 1 day before, and 1, 3, and 7 days after the surgery. Increased WBC count is commonly related to inflammatory response, while CRP is a major plasma protein which presents dramatically elevated levels during acute-phase inflammation. In addition, albumin (ALB) level is considered a reliable marker of nutritional status in patients following surgery 24 . We also noted the occurrence of complications after surgery, such as surgical site infection (SSI), anastomotic leakage, and aspiration pneumonia.

Statistical analysis
We used the Wilcoxon signed-rank test to compare paired data as a non-parametric analysis alternative to a paired t-test, statistically significant p-values were considered p<0.05. We also used Mann-Whitney's U test and Fisher's exact test for statistical analysis.

Clinical factors of the gastrointestinal cancer patients
The clinical factors of the gastrointestinal cancer patients are summarized in Table 1

Inflammatory response and ALB level in laparoscopic surgery and open surgery groups
The results of WBC count, CRP level, BT, and ALB are summarized in Table 2. There was a significant difference in mean WBC count between the groups at 1 day after surgery (p=0.026, Mann-Whitney's U test) ( Figure 1A). Mean CRP in the laparoscopic surgery group was lower than that in the open surgery group at all moments after surgery. In addition, on postoperative days 1 and 3, the level of CRP was significantly lower in the laparoscopic surgery group (p<0.001 and p=0.020, respectively, Mann-Whitney's    Figure   4C). In addition, patients with stage III/IV tumors showed increased bacterial count in the gingiva of the upper anterior teeth when compared to those with stage I/II tumors on postoperative day 7, however, the difference was not significant ( Figure 4B).

Comparison of dry mouth between patient groups
We investigated changes in subjective symptoms    This observation suggests that the stability of the oral microbiome may play a key role in better outcome for cancer patients.
There are reports that the variability of the oral mucosal microbiome is enhanced by denture use and that increased numbers of disease-related bacterial species (i.e., Streptococcus mutans) were found on mucosal surfaces after wearing a partial denture 30 . Another study also reported that dental plaque presented a more diversified microbiome when compared to denture plaque and mucosal plaque obtained from denture wearers, while mucosal plaque obtained from partial denture wearers showed a more significantly diversified microbiome when compared to that from full denture wearers 19 . Furthermore, that study also found that mucosal plaque obtained from dentate individuals possessed a significantly more diversified microbiome when compared to that from edentate individuals. Collectively, these findings indicate that remaining natural teeth as well as denture use may have predominant influences on the diversity of the oral mucosal flora in denture wearers.
Furthermore, reports claim that aging is significantly associated with changes in the composition of the oral microbiome in both gingiva and saliva in periodontally healthy individuals who do not use a denture 21 . Thus, aging as well as denture use, may have important roles in the microbiome diversity in the oral cavity.
Combining the mechanical cleaning of the tongue surface, with use of mouth wash and mouth moisturizing gel can effectively reduce bacterial count on the tongue 16