Oral health and incidence of nosocomial infection and mortality in patients undergoing elective cardiac surgery

Objective: To analyze the relationship between oral disease and the risk of developing hospital pneumonia, mediastinitis, endocarditis, surgical site infection and hospital death in patients undergoing elective cardiac surgery. Assess which risk factors would be related to the risk of nosocomial infection and death after cardiac surgery. Methodology: It was an analytical, observational, prospective study, carried out from January to December 2018. The study included 46 patients candidates for elective cardiac surgery and evaluated as to the type of heart disease, type of surgery, associated comorbidities, age, NYHA classification, BMI, ICU stay days, oral health assessment by a dental surgeon, occurrence of infection and hospital death. The analysis was done through analysis of absolute and relative frequencies, estimation of odds ratios, chi-square test and Mann-Whitney test. Results: Of the 46 patients analyzed, 11 (23.9%) of them had hospital infections and 4 (8.7%) died, there was no statistically significant difference in the variables studied with the occurrence of infection or death. The heterogeneity of the findings in the oral evaluation that ranged from edentulous patients with partial or total dentures, partial edentulous with or without prosthesis and varying degrees of oral disease that ranged from gingivitis, periodontitis to abscesses. The prostheses had varying degrees of conservation and hygiene. This great variability of findings may have implied no statistical significance in the variables. Conclusion: There was no statistical difference in the occurrence of hospital pneumonia, mediastinitis, endocarditis, surgical site infection and hospital death according to the patients' oral health condition.


Introduction
Cardiovascular diseases (CVD) are among the main causes of death in women and men in Brazil. In 2016, these diseases were the cause of death for more than 360 thousand people in the country, with a predominance of males, whites and over 65 years of age (Datasus, 2019). Cardiac surgeries are in line with the treatment of these diseases, and in 2012, more than 102 million cardiac surgeries were performed (Dordetto, Pinto  Rosa, 2016).
Patients undergoing cardiac surgery, in turn, have a higher risk of systemic infection due to multiple factors (Sabatier, Peredo  Valles, 2009). Hospital infections, including postoperative ones, are preventable, most of the time, and have an important impact on hospital costs, increased length of hospital stay and morbidity and mortality (Gelijins et al., 2014).
Oral health affects health in general and this can be evidenced through the relationship of some systemic diseases (such as cardiovascular diseases) and some oral diseases, especially periodontal diseases (Belinga et al., 2018). We know that the inflammatory reactions generated by these diseases are not restricted to the place of origin, as microorganisms and inflammatory mediators, such as interleukin-1 (IL-1) and tumor necrosis factor alpha (TNF-alpha) can disseminate via the bloodstream, inducing systemic inflammatory reagents and the formation of serum antibodies against periodontal bacteria (Paula e Silva et al., 2010;Bansal, Khatri  Taneja, 2013).
Given the above, several studies show the relationship between the presence of periodontitis and several systemic diseases, such as atherosclerosis, cardiovascular diseases, respiratory diseases and diabetes mellitus (Paula e Silva et al., 2010).
Bacterial toxins and the long term continuous exposure to the oral bacteremia can even induce an immune response and a systemic inflammatory response that might contribute to coronary atherosclerosis and, in combination with additional risk factors, lead to coronary heart disease and /or myocardial infarction (Blanck  Halaszynski, 2015).
However, the intraoral health condition of patients is not a preoperative concern in most hospitals (Blanck  Halaszynski, 2015) for several reasons, such as: lack of knowledge of the patient about this association, lack of knowledge of surgeons of the real importance of eradicating a possible source of infection and lack of financial resources to provide adequate preoperative care (Yasny  White, 2009).
Thus, it is necessary to search for new pre-operative interventions that might reduce the chance of appearance of postoperative infections and therefore generate increased survival, reduction of costs and improvement rates of preventable infections. Therefore, this study aims to evaluate the association between the presence of oral disease with the occurrence of nosocomial infection and death after elective cardiac surgery.
In addition, it was evaluated whether other variables such as comorbidities, type of surgery, length of stay in the intensive care unit (ICU) and NYHA classification (functional classification of the New York Heart Association), correlated with the risk of hospital infection and death after cardiac surgery.

Study Type
An analytical, observational, cohort, prospective, blind study, carried out from January to December 2018 (Pereira et al, 2018). The study was carried out with 46 patients who were candidates for cardiac surgery, operated by one of the three cardiac surgeons of the same hospital team. All were informed about the nature of the research and signed the free and informed consent form in accordance with resolution 466/2012 of the National Health Council of the Ministry of Health. Data were collected from patients hospitalized at Santa Casa and at Hospital Vicentino of Ponta Grossa/PR, Brazil. This project was approved by the Research Ethics Committee of the State University of Ponta Grossa, under protocol number 2,991,272.

Inclusion and Exclusion Criteria
The inclusion criteria were patients who were candidates for elective cardiac surgery, who had signed the free and informed consent form and over 18 years of age.
The exclusion criteria were emergency or emergency surgeries in which there was no possibility of performing an oral health assessment.
Sampling was carried out for convenience and depended on the availability of the dental surgeon to carry out the assessment of patients' oral conditions.
g) Time of ICU stay. Research, Society andDevelopment, v. 10, n. 5, e14910514658, 2021 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v10i5.14658 4 h) Presence of healthcare-related infections (HAI), which are pneumonia, endocarditis, mediastinitis and surgical site infection, diagnosed according to the criteria of National Health Surveillance Agency (ANVISA) (2017). These criteria were evaluated during hospitalization and by outpatient return 30 days after heart surgery. i) Occurrence of hospital death in the first 30 days after cardiac surgery. j) Oral health assessment, analyzed using an instrument to assess inflammatory / infectious conditions of the mouthevaluation of the maxilla and mandible, evaluation of the periodontal condition (gingivitis, periodontitis, periodontal risk and presence of suppuration), possible endodontic involvement, need for extraction, assessment of the cleanliness of the prosthesis, condition of the prosthesis and denture stomatitis . The clinical examination of oral health was performed by a single dental surgeon from the interdisciplinary team. All the studied variables and criteria are described in Table 1, all of which are qualitative, except number of teeth with possible endodontic involvement or with indicated extraction. It was also decided to make an assessment of quality of life related to oral health, to understand the limitations and suffering of individuals with oral disorders. The study used the instrument called Oral Health Impact Profile or OHIP (Slade, 1997).

Variable Unit
Upper Jaw 1-Toothless without prosthesis 2-Toothless with total prosthesis 3-Partial edentulous without prosthesis 4-Partial edentulous with removable partial denture 5-Partial edentulous with fixed prosthesis / implants 6-Oral function maintained by the presence of most teeth / fixed prostheses / implants 7-Oral function maintained by the presence of all teeth (except third molar) Lower Jaw 1-Toothless without prosthesis 2-Toothless with total prosthesis 3-Partial edentulous without prosthesis 4-Partial edentulous with removable partial denture 5-Partial edentulous with fixed prosthesis / implants 6-Oral function maintained by the presence of most teeth / fixed prostheses / implants 7-Oral function maintained by the presence of all teeth (except third molar)

Statistical Analysis
Initially, we proceeded the analysis of the descriptive data to estimate frequency of all qualitative variables. Then, we verified the frequencies related to the occurrence of infection and the occurrence of death with an odds ratio (OR) estimate with a 95% confidence interval (CI) and the chi-square test.
Finally, we verified the adherence of the quantitative variables to the normal distribution by the Shapiro-Wilk test and all did not have a normal distribution, therefore, to verify their differences between the groups with and without infection and with death and without death, we performed the Mann-Whitney U test. The tests were considered significant when p <0.05 and the analyzes were performed using SPSS 21.0 (IBM, 2012).

Results
The age of the patients analyzed ranged from 35 to 86 years, with an average of 65 years. Of the 46 patients analyzed, 11 (23.9%) of them had hospital infections and 4 (8.7%) died (Table 1). Regarding the heart diseases that motivated the surgery, coronary artery disease (CAD) was the most common and, consequently, the majority of patients underwent coronary artery bypass graft surgery. In reference to comorbidities, the most common was diabetes mellitus (DM) present in 34.8% of cases. Mood disorders such as anxiety and depression were also common ( Table 2).  As for the ICU time after cardiac surgery, the average was 4.5 days, with a maximum of 26 days (1 patient) and a minimum of 2 days (6 patients).
Regarding the Oral Evaluation, the questionnaire on quality of life (OHIP-14) obtained an average of 6.6 points, which demonstrated that the quality of life of the oral health of the patients analyzed was not bad. The other results are described in Table 4. Average of 6.6 points --Notes: The variables gingivitis, periodontitis, periodontal risk, suppurated teeth and teeth with possible endodontic involvement or indication of tooth extraction were evaluated only among the 28 patients with teeth. Source: Authors.
As for heart disease and surgery, there was no statistical difference in relation to the occurrence of hospital infection or death. The same occurred when comparing variables with morbidities, NYHA and BMI (Table 5). Regarding the oral evaluation, the variables of number of teeth, time of use of upper denture, time of use of lower denture and presence of oral lesions due to the use of prosthesis, comparing them with the presence of hospital infection and death, there was no significant difference (Table 6).  (Table 7).  Research, Society andDevelopment, v. 10, n. 5, e14910514658, 2021 (CC BY 4.0) | ISSN 2525-3409 | DOI: http://dx.doi.org/10.33448/rsd-v10i5.14658 When comparing the variables of quality of life, age of patients and number of days in the ICU with the presence or absence of infection or death, there was no statistically significant difference (Table 8).

Discussion
This study evaluated 46 patients with the objective of evaluating the impact of oral health on the occurrence of infections and death in the postoperative period of cardiac surgery and did not find a significant result for the studied variables or for other clinical variables included in the research. It is worth mentioning the heterogeneity of the findings in the oral evaluation that ranged from edentulous patients with partial or total dentures, partial edentulous with or without prosthesis and varying degrees of oral disease that ranged from gingivitis, periodontitis to abscesses. The prostheses had varying degrees of conservation and hygiene. This great variability of findings may have implied no statistical significance for the variables. A sample significantly larger than this could find relationships between oral disease and infections or death. Nevertheless, the study has value for which can be a material with important and useful data for future meta-analysis, as the collection and evaluation of data was thorough and followed a strict scientific standard.
With regard to ISC rates, a 4-year retrospective study carried out at a University Hospital in Minas Gerais, Brazil, found a rate of 18.6% (Braz, Evangelista, Evangelista, Garbaccio  Oliveira, 2018), another retrospective study carried out in several French institutions (Cossin et al., 2018) found an ISC rate of 1.9% to 2.5% in 4 years. This demonstrates that the ISC rates can vary widely from region to region and that the one found in this study is within the expected value.
Regarding the NYHA classification, a prospective study conducted in Florianópolis -Santa Catarina, Brazil, (Cani et al., 2015) with patients undergoing cardiac surgery found that 35.4% of the 48 patients analyzed, had no limitation in routine activities, which suggests that in our study, patients were more severe and symptomatic, in which only 17.4% of patients had no limitation in routine activities.
The average number of ICU days found in the study (4.5 days) is similar to the study carried out by Laizo and collaborators, who found that of the 85 patients who underwent cardiac surgery, the length of stay in the ICU was 1 to 21 days, with average of 4.16 days.
In the study of oral assessment in the preoperative period of cardiac surgery by Bergan, Tura  Lamas (2014), 36.6% of the patients were edentulous, a rate that is similar to that found in the present study, which was 39.1%.
Of the 28 patients who were not edentulous, 78% were diagnosed with gingivitis and 20 patients (71.4%) were diagnosed with periodontitis and 1 patient (3.5%) with severe periodontitis. A study published in 2013 found a prevalence of 15.3% for moderate periodontal disease and 5.8% for severe condition (Vettore, Marques  Peres, 2013), which differs greatly from the prevalence of our study.
Regarding the use of the OHIP-14 questionnaire, it is observed that despite the poor oral condition found in the study, with a high rate of edentulous and high prevalence of periodontitis, the patients' self-perceived oral health was not bad. This can be explained by the low health literacy of our Brazilian population, associated with less ability to understand how to prevent diseases and promote health (Quemelo, Milani, Bento, Vieira  Zaia, 2017). It is clear that even with the precariousness of the dentition found, the patients' perception of themselves can be considered impaired. The poor oral health that we found also reflects a poor public health policy, in which dental condition is not a priority in the country's health actions.
Given the studies that relate periodontitis to cardiovascular diseases and postoperative infections, this study had an important limitation because the number of patients who presented this type of oral disease was small (20 patients). This could justify the result found, where there was no significant association with any oral disease and especially periodontitis and gingivitis with the analyzed outcomes.
In addition, almost half of the patients analyzed were edentulous, but unfortunately, the cause of this condition is not known. This can be associated with the socioeconomic condition of the population studied. The high rates of dental mutilation and edentulism, according to the literature, have dental caries and periodontal disease as the main determining factors (Batista, 2010). The socioeconomic condition of our country, associated with periodontal causes, the presence of plaques and cavities contribute to the high rates of edentulism in Brazil.
In the study conducted in the city of Rio de Janeiro, Brazil, the presence of plaques on the tongue and poor hygiene of the total upper prostheses in the preoperative period of cardiac surgeries significantly increased the chance of postoperative pneumonia ( Bergan, Tura  Lamas , 2014), which demonstrates that despite the absence of teeth, care with oral hygiene and preoperative evaluation is essential, despite the result found in our study. This study used indexes for oral evaluation such as DMFT (index of full teeth), OHI-S (simplified oral hygiene index) and CPITN (Community periodontal index of treatment needs) and all patients were evaluated only by a single dental surgeon. .A systematic review published in 2017 (Cotti et al.) Assessed whether there was a consensus on perioperative dental screening and management of patients undergoing cardiothoracic, vascular and other invasive cardiovascular procedures. Cotti et al. (2017) observed that there is still no consensus on the need for dental care before invasive cardiovascular procedures.
This work has limitations, due to the small number of individuals evaluated due to the small amount of time for data collection. In addition, the oral assessment of all patients was performed by a single dentist, which may have been a limiting factor because some points were assessed subjectively. On the other hand, the evaluation carried out by a single person suggests a standardization of care and evaluations.
In addition, the evaluation of the oral condition was performed only with a clinical examination. The periapical radiography of all patients would assist in a more objective assessment of the cases. Unfortunately, due to the patients' financial condition and the preoperative in-hospital evaluation, it was not possible to perform the complementary examination.
It is important to emphasize that the preoperative measures indicated by Anvisa (Brasil, 2017) were all performed in all patients: 2% chlorhexidine bath before surgery, 0.12% chlorhexidine gargle before orotracheal intubation and prophylactic cefazoline before surgical incision.
It is observed that most of the studies analyzed associate cardiovascular diseases and the occurrence of respiratory diseases (in surgical postoperative periods or not) exclusively with periodontal diseases, which makes us question whether other oral diseases are relevant for future studies and whether other sources of postoperative infection are related to the disease.
New studies are suggested with a greater number of individuals evaluated so that the relationship between oral health and postoperative outcomes is analyzed, or further studies only with the selection of patients with teeth and evaluation of periodontal diseases to associate the proposed outcomes or exclusively with the occurrence of hospital pneumonia in the postoperative period of cardiac surgery.
A study with the exclusive evaluation of periodontal disease and the relationship between periodontitis and the incidence of pneumonia in the postoperative period can provide more relevant data for future planning for the prevention of postoperative infection.
In addition, despite the results found, public health actions aimed at improving oral health could improve the quality of life of patients, decrease the risk of cardiovascular diseases and, thus, reduce the morbidity and mortality resulting from these diseases.

Conclusion
Oral condition was not a determinant of hospital infection and death after elective cardiac surgery.
There was no statistical difference between patients with oral disease and the occurrence of nosocomial pneumonia, mediastinitis, endocarditis and surgical site infection. In addition, there was also no difference in relation to other variables such as age, body mass index, presence of comorbidities, NYHA classification, days of ICU stay and type of cardiac surgery with the occurrence of hospital infection and hospital death.