The Journals of Gerontology Series A: Biological Sciences and Medical Sciences 58:M52-M55 (2003)
© 2003 The Gerontological Society of America
Pathogenic Colonization of Oral Flora in Frail Elderly Patients Fed by Nasogastric Tube or Percutaneous Enterogastric Tube
Arthur Leibovitz1,
Galina Plotnikov1,
Beni Habot1,
Mel Rosenberg2 and
Rephael Segal1
1 Shmuel Harofe Hospital (affiliated with the Sackler Faculty of Medicine), Geriatric Medical Center, Beer-Yaakov, Israel.
2 Department of Oral Microbiology, Tel-Aviv University, Israel.
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Abstract
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Background. Aspiration of infected oropharyngeal content is the main cause of aspiration pneumonia. This complication, mainly related to gram-negative bacteria, threatens percutaneous enterogastric tube as well as nasogastric tube (NGT) fed patients. The objective of this study was to examine the oral microbiota of tuboenterally fed patients and compare it with that of orally fed counterparts.
Methods. Patients were recruited for this study from six nursing and skilled nursing facilities with an overall number of 845 beds. Enrolled were 215 patients: Group 1 consisted of 78 patients on NGT feeding, Group 2 consisted of 57 patients on percutaneous enterogastric tube feeding, and Group 3 consisted of 80 patients fed orally who were from the same facilities. Cultures were performed by sampling the oropharynx of each subject in order to identify gram-negative bacteria and Staphylococcus aureus.
Results. A high prevalence of potentially pathogenic isolations was found in tuboenterally fed patients: 81% in Group 1 and 51% in Group 2, as compared with only 17.5% in Group 3 (p <.0001). Pseudomonas aeruginosa was cultured from 31% of the subjects in Group 1 and 10% of Group 2, but in none of Group 3 (p <.001). Klebsiella and Proteus were isolated mainly from the NGT fed patients (p <.003). No correlation was found between the time duration on tube feeding or the presence of residual dentition and pathogenic microbiota.
Conclusion. This study shows that tuboenteral feeding in elderly patients is associated with pathogenic colonization of the oropharynx. These findings are related to the risk of aspiration pneumonia and are compelling for the reevaluation of current oral cleansing procedures.
ENTERAL feeding, either by percutaneous enterogastric tube (PEG) or by nasogastric tube (NGT), is becoming increasingly common for providing nutrition and hydration to frail elderly patients with severe oropharyngeal dysphagia (1). This procedure is fraught with ethical and medical concerns regarding the extent of life-maintaining procedures and their complications in frail patients (2–4). Whereas the ethical concerns are a subject of debate for the whole society, it is our duty as physicians to explore the medical problems associated with these procedures.
Aspiration pneumonia, with its high morbidity and mortality, is a major threat for enterally fed patients. Its main cause is the aspiration of infected oropharyngeal content (5,6). Aspiration of saliva is not a rare phenomenon, but it is the presence of pathogenic organisms, especially gram-negative bacteria (GNB), that increases the risk for pneumonia (6,7). Physiologically, oropharyngeal colonization by pathogenic organisms is prevented by the mechanical clearance provided by chewing and swallowing (8). However, in tuboenterally fed patients, the oropharynx is devoid of this protective effect, rendering it prone to colonization by pathogenic organisms. Such a process could be crucial with regard to aspiration pneumonia. Colonization of dental plaque by respiratory pathogens has been previously reported in medical intensive care patients (9). However, data on the impact of prolonged enteral feeding on oral microbiota are scanty, because frail elderly patients are seldom included in such epidemiological studies (10,11). Therefore, we initiated this study with the purpose of examining the pathogenic oral flora found in tuboenterally fed patients, whether fed by PEG or by NGT, and comparing it with that found in a similar group of orally fed subjects.
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Methods
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This cross-sectional comparative survey was conducted in six nursing and skilled nursing facilities with a total number of 845 beds. Skilled nursing facilities are those that are licensed for providing care for nursing patients that also have an active disease that requires close medical supervision (e.g., such patients might require NGT feeding or suffer from severe bed sores, advanced cancer, or hemodynamic instability). Eligible for the study were all patients on tuboenteral nutrition, either by NGT or by PEG. Excluded were patients with advanced cancer and those with a history of irradiation to the neck. The control group consisted of matched orally fed patients with no swallowing disturbances who resided in the same facilities. Excluded from both groups were patients who had received any antibiotic treatment up to 2 weeks prior to the study. Informed consent was obtained from the patients or from their proxies.
Cultures were performed by sampling the oropharynx with swabs; these samples were taken from the base of the tongue dorsum by rubbing the buccal mucosa with a sterile cotton swab, which was then placed in transport medium. The samples were taken during the morning hours, before breakfast and before the daily oral cleansing procedure. Routine oral hygiene for the tuboenteral patients was performed by cleaning the oral cavity before meals three times a day with lemon-glycerine wadding sticks impregnated with a solution of glycerine-citric acid, lemon flavoring, and sodium benzoate 0.1% (12).
Cultures were inoculated within 1 hour of collection on blood, MacConkey's, and chocolate agar plates, and they were aerobically incubated at 35°C. Staphylococcus aureus was identified by manual methods, using tryptic soy blood agar (TSA, Hy-Labs Laboratories, Israel), and then Gram stained. It was further identified by coagulase and catalase tests and then by subculturing on chromium and manitol agar (Hy-Labs). Gram-negative bacterial identification was performed by specific biochemical tests (Kligler iron agar, UMI [urea motility indol], MIO [ornitine decarboxylase], Lysin, MRVP [methyl red Voges-Proskauer], and Oxydase). In a few inconclusive cases, the BBL Crystal Enteric/Nonfermenter ID System was used (Becton Dickinson, Cockeysville, MD). Only moderate or heavy growth was considered to be a positive result. Culture of fungal organisms was not performed.
Statistical processing was performed by using the SPSS software (SPSS, Chicago, IL). A chi-square or Fisher's exact test was used for comparative studies, and a Pearson test was used for correlations.
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Results
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Three groups of patients participated in the study. Group 1 consisted of 78 patients on NGT feeding, with an average duration of 17 ± 26 months and a range of 1–168 months. Group 2 consisted of 57 patients on PEG feeding, with an average duration of 20 ± 15 months and a range of 2–60 months. Group 3 consisted of 80 orally fed patients from the same departments, who were included as controls.
Table 1 presents the demographic and the medical characteristics of each group. All patients were confined to wheelchairs. Noted should be the significantly higher prevalence of stroke and dementia among the patients on tube feeding. These are indeed the two leading causes for oropharyngeal dysphagia and subsequent tuboenteral feeding. No significant differences were found among the study groups regarding all other clinical parameters.
Pathogenic bacterial isolations obtained from each group are presented in Table 2. Noteworthy is the high prevalence of pathogenic isolations in Groups 1 and 2, at 81% and 51%, respectively, as compared with 17.5% in the control group (p <.0001). Pseudomonas aeruginosa was highly prevalent, mainly in the NGT fed patients (31%; p <.001). Pseudomonas was also cultured from 10% of the PEG fed patients, but it was not found in any of the orally fed patients (p <.001). Klebsiella and Proteus were also isolated, primarily from the NGT fed patients (p <.003).
Not surprisingly, the NGT fed patients had a higher prevalence of each pathogenic GNB as compared with those on PEG feeding (Table 2; t-test number 1 vs t-test number 2). Isolation of other GNB such as Enterobacter, Escherichia coli, and mixed cultures was low and showed no significant differences among the groups. Interestingly, S. aureus isolations, half of them methycillin resistant, were similar in all study groups. In the majority of the cases, colonization was of a single species of pathogen, whereas two or three species were found in 6.8% of the samples only.
No correlation was found between the length of stay in the facility or the duration on tube feeding (either NGT or PEG) and bacterial isolations (Pearson's correlation and t test). The presence of residual dentition was not significantly different among the study groups (Table 1). No correlation was found between the presence of residual dentition and pathogenic microbiota.
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Discussion
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The main finding in this study is the significantly higher rate of pathogenic isolations from the oropharynx of tuboenterally fed patients. GNB have been isolated from 81% of the NGT fed patients and from 51% of the PEG fed patients, as opposed to only 17.5% of the orally fed group (p <.0001). The prevalence of Pseudomonas in the oral flora was extremely high and was found only in those fed by NGT or PEG. Some of the highly pathogenic bacteria such as P. aeruginosa and Klebsiella, uncommon in the oral flora of normal persons (13), have been cultured exclusively in tube-fed patients. Interestingly, S. aureus was equally prevalent in all study groups. Early studies reported on the propensity of GNB to colonize the elderly patient's oropharynx (14,15). However, at that time, the number of tuboenterally fed patients was small, and these patients were not studied as a distinct group (15). To our knowledge, the present study is the first to make a comparative examination of NGT, PEG and orally fed elderly patients with respect to oral flora.
Our results are consistent with the view that it is the mechanical clearance associated with proper chewing and swallowing that provides the main defense against oral pathogenic contamination.
The higher incidence of GNB colonization in the NGT-fed patients as compared with those fed by PEG may have several explanations. The presence of an abiotic surface such as the tube itself may constitute a site of biofilm formation, bolstering the growth of bacteria such as Pseudomonas (16). Moreover, an association has been reported between the short-term use of NGTs and sinusitis (17). Prolonged use could have a higher impact on the pathological colonization of the sinuses, leading to chronic sinusitis that may be a source of pathogenic bacteria.
Tuboenteral feeding, in spite of existing reservations, is the only present solution for providing hydration and nutrition and reducing aspiration in patients with severe oropharyngeal dysphagia (2,18). Nevertheless, aspiration pneumonia is the main complication of tuboenterally fed patients. Apart from high morbidity and mortality, this process constitutes a high expenditure for the health system, with a cost recently estimated for PEG alone at $800,000,000 a year (19).
Conclusions
The relationship between oropharyngeal pathogenic colonization in prolonged tuboenterally fed patients and the risk of aspiration pneumonia should be investigated further. One factor to be studied is the flow and composition of the saliva. Detailed dental status of prolonged tuboenterally fed patients should also be evaluated. The lack of a thorough dental examination in our patients was a limitation of our study. Recent reports suggest that dental and oral factors are significant in the control of aspiration pneumonia in the elderly population (20). The role of oral care in preventing pneumonia in nursing home patients was also recently emphasized (21). A successful attempt at oropharyngeal decontamination with a resulting decrease in pneumonia was reported in patients on mechanical ventilation (22).
Our results suggest the need for a reexamination of the existing oral cleansing procedures in prolonged tube-fed patients and a search for new methods of decontamination.
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Acknowledgments
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Address correspondence to Arthur Leibovitz, MD, Shmuel Harofe Hospital, Geriatric Medical Center, P.O. Box 2, Beer-Yaakov, Israel.
Received May 21, 2002
Accepted July 18, 2002
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References
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|---|
- Guenter P, Jones S, Swed MR, Ericson M. Delivery systems and administration of enteral nutrition. In: Rombeau I, Rolandelli R, ed. Enteral and Tube Feeding. 3rd ed. New York: W.B. Saunders; 1997:240–253.
- Gillick M. Rethinking the role of tube feeding in patients with advanced dementia. N Engl J Med. 2000;342:206-207.[Free Full Text]
- Mitchell S, Kiely D, Lipsitz L. Does artificial enteral nutrition prolong the survival of institutionalized elders with chewing and swallowing problems?. J Gerontol Med Sci. 1998;53A:M207-M213.
- Ouslander JG, Thimckuk AJ, Krynski MD. Decisions about enteral tube feeding among the elderly. J Am Geriatr Soc. 1993;41:70-77.[Medline]
- Langmore SE, Terpenning MS, Schork A, et al. Predictors of aspiration pneumonia: how important is dysphagia?. Dysphagia (U.S.). 1998;13:69-81.[Medline]
- Yamaya M, Yanai M, Ohmi T, Arai H, Sasaki H. Interventions to prevent pneumonia among older adults. J Am Geriatr Soc. 2001;49:85-90.[Medline]
- Marik EP. Aspiration pneumonitis and aspiration pneumonia. N Engl J Med. 2001;344:665-671.[Free Full Text]
- Palmer LB, Albulak K, Fields S, Filkin AM, Simon S, Smaldone GC. Oral clearance and pathogenic oropharyngeal colonization in the elderly. Am J Respir Crit Care Med. 2001;164:464-468.[Abstract/Free Full Text]
- Scannapieco FA, Stewart EM, Mylotte JM. Colonization of dental plaque by respiratory pathogens in medical intensive care patients. Crit Care Med. 1992;20:740-745.[Medline]
- Pajukoski H, Meurman JH, Odont D, Snellman-Grohn S, Sulkava R. Oral heath in hospitalized and non-hospitalized community dwelling elderly patients. Oral Surg Oral Med Oral Pathol. 1999;88:437-443.
- Ettinger RC. Aging: a global issue. J Dent Res. 1995;74:724-726.[Free Full Text]
- Warner LA. Lemon-glycerine swabs should be used for routine oral care. Crit Care Nurse. 1986;6:82-83.[Medline]
- Thomas S, Rajagopalan R, Idikula J, Brahmadathan N. Alterations in oropharyngeal flora in patients with a nasogastric tube: a cohort study. Crit Care Med. 1992;20:1677-1680.[Medline]
- Valenti WM, Trudell RG, Bentley DW. Factors predisposing to oropharyngeal colonization with gram-negative bacilli in the aged. N Engl J Med. 1978;298:1108-1111.[Abstract]
- Irwin RS, Whitaker S, Pratter MR, Millard CE, Tarpey JT, Corwin RW. The transiency of oropharyngeal colonization with gram-negative bacilli in residents of a skilled nursing facility. Chest. 1982;81:31-35.[Abstract/Free Full Text]
- Hogt AH, Dankert JA, de Vries JA, et al. Pseudomonas aeruginosa biofilm as a diffusion barrier to piperacillin. Antimicrob Agents Chemother. 1992;36:2054-2056.[Abstract/Free Full Text]
- George DL, Falk FS, Umberto Meduri G, et al. Nosocomial sinusitis in patients in the medical intensive care unit: a prospective epidemiological study. Clin Infect Dis. 1998;27:463-470.[Medline]
- Finucane TE, Christmas C. More caution about tube feeding. J Am Geriatr Soc. 2000;48:1167-1168.[Medline]
- Siddique R, Neslusan CA, Crown WH, Crystal-Peters J, Sloan S, Farup C. A national inpatient cost estimate of percutaneous endoscopic gastrostomy (PEG)—associated aspiration pneumonia. Am J Manag Care. 2000;6:490-496.[Medline]
- Terpenning MS, Taylor GW, Lopatin DE, Kerr CK, Domingues BL, Loesche WJ. Aspiration pneumonia: dental and oral risk factors in an older veteran population. J Am Geriatr Soc. 2001;49:557-563.[Medline]
- Yoneyama T, Yoshida M, Obrui T, et al. Oral care reduces pneumonia in older patients in nursing homes. J Am Geriatr Soc. 2002;50:430-433.[Medline]
- Pugin J, Auckenthaler R, Lew DP, Suter PM. Oropharyngeal decontamination decreases incidence of ventilator-associated pneumonia. JAMA. 1991;265:2704-2710.[Abstract]
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