ORIGINAL ARTICLE

Oral evaluation and procedures performed by dentists in patientsadmitted to the intensive care unit of a cancer center

Ana Paula Silva & Pedro Caruso & Graziella Chagas Jaguar &

Paulo Andre G. Carvalho & Fabio Abreu Alves

Received: 1 August 2013 /Accepted: 31 March 2014# Springer-Verlag Berlin Heidelberg 2014

AbstractBackground Most of the oral problems affecting patients inthe ICU (intensive care unit) are conditions resulting fromtheir general health status/immunosuppression, medications,and trauma due to tracheal intubation. Furthermore, microor-ganisms present in the oral cavity and oropharynx may betransported into the lungs resulting in pneumonia.Purpose The objectives of this study were to evaluate the oralproblems in patients in the ICU of a cancer center and describethe procedures performed by the dentists in such patients.Methods The sample consisted of 116 patients and 329 pro-cedures performed in the period between May 2007 and July2011 at A.C. Camargo Cancer Center.Results Oral mucositis was the main problem (20.3 %), espe-cially in immunosuppressed patients (p<0.001). Other mostprevalent problems were candidiasis (16.6 %), bacterial bio-film (14.9 %), and xerostomia (7.18 %). The main proceduresperformed were clinical evaluation and medication prescrip-tion corresponding to 35.10 and 27.81 %, respectively.Conclusions In conclusion, most of the patients presented oralproblems related to side effects of oncological treatment. Thedentist’s participation in the ICU is important for the preven-tion, diagnosis, and treatment of oral problems.

Keywords Intensivecareunits . Immunosuppressedpatients .

Oral diseases . Oral hygiene . Oral health

Introduction

Patients admitted to the intensive care unit (ICU) usuallypresent critical systemic conditions and may be immunosup-pressed due to underlying diseases or drugs. Furthermore,sepsis is a common cause of ICU admission and a frequentcomplication in hospitalized patients. Moreover, it can berelated to contamination of the mouth, and consequently, animportant issue raised at multidisciplinary team discussions.Strategies for decreasing such contamination are related to thepurpose of reducing biofilm and consist of local hygienetechniques and use of antiseptics [1–3].

Some drugs used in the ICU affect the quality and quantityof saliva secretion. In addition, decreased salivary flow leadsto alteration of the oral microbiota, favoring the emergence oforal changes such as fungal and bacterial infections. In the oralcavity, traumatic lesions as a result of traumatic intubation canalso be observed [4–6].

Despite collateral effects of antineoplastic therapy (chemo-therapy and radiotherapy in the head and neck), oncologicalpatients are frequently affected by oral mucositis. This condi-tion can be exacerbated by dryness of mucosal membranescaused by drugs and by keeping the mouth open in intubatedpatients. Further, the loss of integrity of the epithelium mayincrease the probability of systemic infections caused bymicroorganisms present in the oral cavity [7–10].

Health-care-associated pneumonia and ventilator-associated pneumonia (VAP) can be related to oropharynxmicroorganisms. The intubation and decrease of the level ofconsciousness may lead to the aspiration of these microorgan-isms into the lungs [7, 10, 11]. In general, the dentist is theprofessional trained to identify oral problems presented by

A. P. Silva :G. C. Jaguar : P. A. G. Carvalho : F. A. AlvesStomatology Department, A.C. Camargo Cancer Center, Sao Paulo,Brazil

P. CarusoIntensive Care Unit, A.C. Camargo Cancer Center, Sao Paulo, Brazil

P. CarusoPulmonologist Department, University of Sao Paulo, Sao Paulo,Brazil

F. A. Alves (*)Stomatology Department, AC Camargo Hospital, Prof. AntonioPrudente, 211, Liberdade, Sao Paulo 01509-010, Brazile-mail: falves@accamargo.org.br

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patients in the ICU, and in conjunction with a multidisciplin-ary team, should develop strategies to prevent and treat pos-sible complications. The objectives of this study were toevaluate the oral problems presented by oncologic ICU pa-tients and to characterize the procedures performed by thedentists in this group of patients.

Methods

This is a retrospective, observational, and descriptive study,which analyzed oral problems and dental procedures in pa-tients in the ICU at A.C. Camargo Cancer Center betweenMay 2007 and July 2011. The patients’ data were obtainedfrom careful examination of medical charts.

ICU and Stomatology Department

The ICU of our oncological center comprises 31 beds andadmits approximately 2,200 patients per year. In general, 70%of them are admitted due to postoperative monitoring and30 % to medical complications. The Stomatology Departmentteam consists of 5 dentists (2 stomatology specialists, 2 oralmaxillofacial surgeons, and 1 maxillofacial prosthodontist)and 8 resident students.

A resident and a specialist in stomatology diagnose the oralproblems and perform all the procedures. The nurse teamroutinely performs the patients’ oral hygiene. Teeth and oralmucosa are cleaned with toothbrushes and gauze soaked inchlorhexidine digluconate 0.12 %, three times a day.

Conscious patients who are able to self-care perform con-ventional brushing with toothbrush and toothpaste, andmouthwash with chlorhexidine digluconate 0.12 %, threetimes a day.

Subjects

Inclusion criteria. All patients admitted to the adult ICU(16-year-old patients or older) at A.C. Camargo CancerCenter who were evaluated and treated by theStomatology Department.Exclusion criteria. Patients who were not seen by theStomatology Department.

Data collection

When a patient shows oral problems, the ICU staff sends anelectronic message to the Stomatology Department for assess-ment. Through this registry, it was possible to identify all thepatients evaluated by the Stomatology team.

Demographic data, underlying diseases, treatments towhich the patients were submitted (transplantation,

chemotherapy, radiotherapy), cause of ICU admission, trache-al intubation, length of ICU stay, oral problems, immunologicstatus (leukocytes and platelets cell counts), and proceduresperformed by the Stomatology Department were collectedfrom patients’ medical charts.

Statistical analysis

The statistical software programs comprised R software ver-sion 2.15 (www.r-project.org.br) and Microsoft Excel 2010version. Numeric variables were described by measures ofcentral tendency and variability. Categorical variables wererepresented by distribution of frequencies. The chi-square testwas used to verify the association between mucositis and theimmunologic status of the patients (with significance set forp<0.05).

Results

The study population consisted of 59 (50.9 %) male and 57(49.1 %) female patients, adding to a total of 116. The pa-tients’mean agewas 57 years old, ranging from17 to 83 years.The main disease was lymphoma (12.9 %), followed byleukemia (11.2 %), melanoma (8.6 %), head and neck cancer(8.6 %), and breast cancer (7.8 %). The most common criteriafor admission to the ICU was respiratory insufficiency (31patients, 26.7 %), followed by sepsis (27, 23.3 %), and post-operative monitoring (19, 16.4 %).

Two patients were affected by health-care-associated pneu-monia, although this is not a criterion for ICU admission atthis center. Therefore, such patients were admitted for respi-ratory insufficiency and sepsis (Table 1).

Oral problems

A total of 167 oral problemswas observed in these patients, andthe most prevalent ones were mucositis and candidiasis. How-ever, some patients presented more than one type (Table 2).

Of the 34 patients with mucositis, 8 had undergone bonemarrow transplant and the other 26 patients were in chemo-therapy for oncological treatment. There was a statisticalsignificance between the number of patients affected by mu-cositis and the immunological status. Most patients wereleukopenic and thrombocytopenic (p<0.001; Table 3). More-over, the infectious diseases (candidiasis, herpes, anddentoalveolar abscess) were grouped, totalizing 35 lesions.No statistical significance was observed between the immu-nological status and oral infections (leukopenic, p>0.228;thrombocytopenic, p>0.7873).

Oral trauma derived from tracheal intubation consisted ofulcers (12 patients), avulsion of upper incisors (2), prosthesisfracture (3), and dental fracture (1).

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Procedures performed by the Stomatology Department

A total of 329 procedures was performed by the dentists of theStomatology Department in the 116 patients. Clinical evalua-tion and medication prescription were the most frequent ones(Table 4). Such prescriptions consisted of vitamin E (34patients, 10.3 %), artificial saliva (16, 4.8 %), antifungals(14, 4.24 %), chlorhexidine (14, 4.24 %), sodium bicarbonatewater (7, 2.12%), antivirals (4, 1.21%), lip protector (2, 0.60%),and antibiotic (1, 0.30 %).

Discussion

In the last years, the dentist participation in the evaluation ofICU patients has been evidenced and acknowledged amongthe multidisciplinary team professionals who are responsiblefor critically ill patients. At A.C. Camargo Cancer Center, thestomatologists are summoned to evaluate the ICU patientswhen they present oral problems. This is a pioneer study thatanalyses the participation of dentists in the cancer center ICU.

Mucositis (20.35 %) and candidiasis (16.16 %) were themost frequent oral problems observed in the present study, andboth lesions are related to side effects of oncological treat-ments. The incidence of oral mucositis varies from 5 to 100%,depending on the type of tumor and treatment (radiotherapydoses and fields, and types of chemotherapy) [9, 12, 13]. Theintensity and incidence of the mucositis-related chemotherapymay be dependent on the chemotherapy regimen and thepatient’s immunological status. Some hematopoietic stem celltransplantation (HSCT) conditioning regimens (5-fluorouraciland high doses of methotrexate) present higher risk of

Table 1 Underlying diseases and admission criteria of 116 patients in theICU

Variables Category N (%)

Gender Male 59 (50.9)

Female 57 (49.1)

Age (years) Mean 57

Length of ICU stay (days) Mean 14

Underlying diseases Lymphoma 15 (12.9)

Leukemia 13 (11.2)

Melanoma 10 (8.6)

Head and neck carcinoma 10 (8.6)

Breast carcinoma 9 (7.8)

Intestine carcinoma 7 (6.0)

Lung carcinoma 6 (5.2)

Multiple myeloma 5 (4.3)

Stomach carcinoma 5 (4.3)

Carcinoma unknown primary site 4 (3.4)

Ovary carcinoma 4 (3.4)

Prostate carcinoma 4 (3.4)

Central nervous system carcinoma 3 (2.6)

Kidney carcinoma 3 (2.6)

Uterus carcinoma 3 (2.6)

Osteoradionecrosis 3 (2.6)

Maxillofacial hemangioma 2 (1.7)

Pancreatic carcinoma 2 (1.7)

Othersa 8 (7.2)

ICU admission criteria Respiratory insufficiency 31 (26.7)

Sepsis 27 (23.3)

Postoperative monitoring 19 (16.4)

Coma 10 (8.6)

Monitoring chemotherapy 9 (7.8)

Arrhythmia 3 (2.6)

Seizure 3 (2.6)

Cardiopulmonary arrest 2 (1.7)

Anaphylactic shock 1 (0.9)

Hypovolemic shock orhemorrhagic

1 (0.9)

Focal neurological deficit 1 (0.9)

Mass effect intracranial 1 (0.9)

Hemorrhage 1 (0.9)

Agitation delirium 1 (0.9)

Hepatic impairment 1 (0.9)

Othersb 5 (4.3)

a One case each of the following: thymic carcinoma, liver carcinoma, skincarcinoma, peritoneal carcinoma, osteosarcoma, lung sarcoma, Budd-Chiari syndrome, and Kaposi sarcomabOne case each of the following: Stevens-Johnson syndrome, intracranialhemorrhage, congestive heart failure, anemia, and acute intoxication bychemotherapy

Table 2 Oral problems presented by ICU patients

Oral problems N (%)

Mucositis 34 (20.35)

Candidiasis 27 (16.16)

Bacterial biofilm 25 (14.97)

Oral trauma occurred for tracheal intubation 18 (10.77)

Xerostomia 12 (7.18)

Herpes 11 (6.58)

Damaged teeth 10 (5.98)

Hemorrhage 10 (5.98)

Depapillated tongue 7 (4.19)

Facial swelling after oral surgery 5 (2.99)

Dry lips 3 (1.79)

Temporomandibular joint dysfunction 2 (1.19)

Dentoalveolar abscess 1 (0.60)

Drooling 1 (0.60)

Trismus 1 (0.60)

Total 167 (100)

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mucositis [14, 15]. The incidence of oral mucositis is close to100 % in patients with oral cancer or oropharynx cancertreated with chemotherapy associated to radiotherapy [9,14]. A total of 34 patients of our sample presented mucositis.Eighteen of them were related to HSCT conditioning regimenand 2 to radiotherapy/chemotherapy in head and neck cancer,while 14 were due to chemotherapy.

Immunosuppression and alterations in the oral cavity suchas imbalance in the oral microbiota, changes in the salivaryflow, and mucositis are not only predisposing factors to oralcandidiasis, but also frequent conditions in cancer patients.Lalla et al. [16] have performed a systematic review on oralcandidiasis in oncological patients. The Candida prevalencewas 7.5 % before the antineoplastic therapy, 39.1 % during,and 32.6 % after the treatment. Moreover, according toMañaset al. [17], the prevalence of oropharyngeal candidiasis was26 % in patients with head and neck cancer who underwentradiotherapy alone or associated with chemotherapy. No in-formation about oral candidiasis in ICU patients was obtainedin the studies above. In the present study, oral candidiasisaffected 27 out of 116 patients (16.6 %). Pseudomembranouscandidiasis occurred in 23 of such patients, while angular

cheilitis in 4. Out of the 23 patients who presentedpseudomembranous candidiasis, 13 were on chemotherapy,while 8 were on immunosuppressive therapy with corticoids,and 2 were in the ICU due to sepsis—but not undergoingoncological treatment. Out of the 4 patients who presentedangular cheilitis, 2 were on chemotherapy and the other 2 onimmunosuppressive therapy.

Nurses are usually responsible for oral hygiene in ICUpatients [1, 18–20]. Similarly, in our cancer center, oral hy-giene is performed by the nursing staff, who cleans the pa-tients’ teeth and oral mucosal with gauze soaked with chlor-hexidine digluconate 0.12 %, three times a day. Interestingly,the difficulty to perform the cleaning of the mouth by nurseswas documented by Rello et al. [21]. The authors evaluatedoral care practices in ICU through questionnaires answered bynurses and found that 77% of them received adequate trainingin providing oral care. Most of them (93%) also expressed thedesire to learn more about oral care. Cleaning the oral cavitywas considered difficult by 68 % and both unpleasant anddifficult by 32%. In addition, 37% of the nurses felt that therewas a worsening of oral health over time in intubated patients.In the present study, oral biofilm was observed in 25 out of the116 evaluated patients. Furthermore, 2 patients were affectedby health-care-associated pneumonia—they had been admit-ted at ICU due to sepsis and acute respiratory insufficiency. Itis noteworthy that oral microbiota is the most important factorrelated to health-care-associated pneumonia [1, 10, 22, 23].

Oral trauma in soft tissue occurred in 12 of the 116 evalu-ated patients, while trauma in dental tissues affected another6—2 presented avulsion (upper central incisor), 3 had pros-thesis fracture, and another 1 had dental fracture. Similarly,Givol et al. [24] and Vogel et al. [25] also observed that centralincisor teeth were the most commonly affected during trachealintubation, as these teeth are normally used as a support for thelaryngoscope, and the patients have previous periodontal dis-ease, especially if they are more than 50 years of age [25]. Inthis study, the mean age of the patients affected by dentaltrauma was 52.7. On the other hand, Newland’s study [26]showed that the most prevalent dental trauma occurred in ICUpatients was enamel fractures (32.1 %).

Sasportas et al. [27] reported that more than 400 medica-tions can cause changes in the salivary flow, inducinghypossalivation or xerostomia. As the elderly frequently suf-fer from chronic diseases and use many medications, they arethe most affected by this condition. In addition, xerostomia isthe most common complaint of head and neck cancer survi-vors who have been treated with radiotherapy (RT). Its prev-alence is 93 % during RT and 74–85 % after RT.

Dennesen et al. [28] have evaluated stimulated salivaryflow and the status of oral mucosa in ICU patients. Theycompared patients whowere in need ofmechanical ventilationfor ≥48 h (24 patients) and patients who had undergoneelective coronary artery bypass graft surgery (20 patients

Table 3 Association between immune status and the presence of muco-sitis in ICU patients evaluated by the stomatologist

Category Cell counts Mucositis p value

Yes (%) No (%)

Leukocytes <1,000 16 (57) 12 (43) 0.001≥1,000 18 (20) 70 (80)

Platelets <50,000 21 (44) 27 (56) 0.004≥50,000 13 (19) 55 (81)

Table 4 The total of 329 procedures performed by the StomatologyDepartment in ICU patients

Procedures N (%)

Clinical evaluation 116 (35.10)

Medication prescriptions 92 (27.87)

Oral hygiene instruction 47 (14.20)

Laser therapy 35 (10.60)

Oral cavity hygiene 14 (4.24)

Exfoliative cytology 13 (3.90)

Position change of the tube in order to avoid trauma 3 (0.90)

Device to keep the mouth open (avoid trauma on the tongue) 2 (0.60)

Teeth extraction 2 (0.60)

Suture removal 2 (0.60)

Oral secretion aspiration 1 (0.30)

Biopsy 1 (0.30)

Suture 1 (0.30)

Total 329 (100)

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who were extubated in less than 24 h.). All patients werefollowed up for 3 weeks. The stimulated salivary flow ratein surgery patients decreased significantly postoperatively andgradually returned to normal within 14 days. Conversely, theintubated patients experienced an almost absent stimulatedsalivary flow during the length of ICU stay. Furthermore, theinadequate saliva flow may contribute to Gram-negative bac-teria colonization of the oropharyngeal mucosa. Althoughxerostomia evaluation has not been a goal of the present study,12 patients (7.18 %) presented this complaint, out of which, 2patients had undergone radiotherapy 1 year before, while theothers were using various medications (antidepressants, anti-hypertensive, sedatives, muscle relaxants, antihistamines, an-algesics, opioids, non-steroidal anti-inflammatory drugs, anti-spasmodic, and bronchodilators). Artificial saliva and lipmoisturizer were prescribed to control this complication.

A total of 329 procedures were performed in the 116patients. The observational procedures (clinical evaluation)corresponded to 35.10 %, while the others were clinical inter-ventions. The most frequent interventions were medicationprescriptions (27.87 %), followed by oral hygiene instructions(14.20 %), and laser therapy (10.60 %).

Limitations

The retrospective character of this study is its main limitation,as there is the possibility of the Stomatology Department notbeing advised when patients present an oral problem. How-ever, in our institution, the oral diagnosis is a responsibility ofthe Stomatology Department, and we assure that the vastmajority of the patients who present oral problems are evalu-ated by a stomatologist.

Conclusions

In summary, the oral problems observed in oncological ICUpatients were related to cancer treatment side effects, patientimmunosuppression, and tracheal intubation procedures. Thestomatologists play an important role in the prevention andtreatment of such problems. Furthermore, patients in longperiods of ICU stay ought to be followed up by a dentist inorder to improve oral health care and control symptoms suchas xerostomia.

Acknowledgement The authors would like to thank CAPES(Coordenação de Aperfeiçoamento de Pessoal de Nível Superior) forthe financial support.

Conflict of interest None of the authors have a financial relationshipwith the organization that sponsored the research. All authors have fullcontrol of all primary data and agree to allow the journal to review theirdata if requested.

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