Postmortem Bacteriology and Pneumonia in a Mentally Retarded Population ANTHONY P. POLEDNAK, PH.D.
PNEUMONIA AND other respiratory diseases continue to be the major cause of death in institutionalized mentally retarded persons. 13,16 ' 18 ' 19 Autopsy data on specific types of pneumonia in these populations have apparently not been reported, and antemortem or postmortem microbiologic data are also lacking. Together, these data could be of great value in identifying diseases and probable causal agents, upon which therapeutic and prevention programs could concentrate. The present retrospective study describes the frequencies of specific types of pneumonia and postmortem bacteriologic findings in an autopsy population of institutionalized mentally retarded persons. Received November 11, 1975; received revised manuscript February 16, 1976; accepted for publication February 16, 1976. Address reprint requests to Dr. Polednak at his present address: Center for Human Radiobiology, Argonne National Laboratory, Argonne, Illinois 60439.
Birth Defects Institute, State Department of Health, Albany, New York
Materials and Methods The Ontario Hospital School at Orillia is the oldest and largest institution for the mentally retarded in Ontario, Canada. Records of deaths of patients were available for 1958 to 1973. The total population varied between about 2,900 and 2,100 per year. The total population at risk for the entire period could not be accurately estimated; the population was rather stable, however, with relatively few new admissions each year, as reported for other similar institutions. 17 A trend toward aging of the population, as reported elsewhere, 17 was also evident; by 1970, an at-risk population less than 5 years of age was virtually nonexistent. From the centralized record system of the institution, records were located for 676 of the total of 707 deaths that occurred from 1958 to 1973. These records included case histories and all medical information available, including death certificates and autopsy reports. Autopsy reports were available for 237 of the 246 performed. Pneumonias and other respiratory diseases reported at autopsy were coded according to the International Classification of Diseases, Eighth Revision (World Health Organization, 1965).22 The sex composition, average age at death, and intellectual status (level of retardation) of the autopsy series were very similar to those of the entire group of 676 decedents. Most autopsies were performed in the morgue of the institution. Of the 237 autopsies, at least one bacteriologic culture report was avilable for 113 (47.7%). These included 56 nose and throat, 26 bronchus or lung, and 71 heart blood cultures. Cultures were examined by standard technics (Gram's method and coagulase test); cultures for anaerobic bacteria were not done.
190
Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
Polednak, Anthony P.: Postmortem bacteriology and pneumonia in a mentally retarded population. Am J Clin Pathol 67: 190-195, 1977. Postmortem pathologic and bacteriologic reports were analyzed for 237 deaths occurring at a large institution for the mentally retarded from 1958 to 1973. Bronchopneumonia, aspiration pneumonia, and lipid pneumonia were frequently reported at autopsy, and in a total of 146 cases (61.6%) at least one type of pneumonia was reported. Postmortem bacteriologic cultures in a smaller group revealed high recovery rates of staphylococci (coagulase-positive), hemolytic streptococci, and gram-negative bacilli in throat and lung cultures. Enteric aerobic gram-negative bacilli were particularly frequent, along with yeast (Candida albicans). The institutionalized retarded appear similar to other hospitalized populations, in that a large proportion of hospitalacquired respiratory infections is related to aerobic gramnegative bacilli. The high frequency of aspiration and its sequelae in this population is unusual, however, and postmortem bacteriologic findings appear consistent with those of antemortem studies of cases of aspiration pneumonia. (Key words: Postmortem bacteriology; Aspiration pneumonia; Gram-negative bacteria; Lipoid pneumonia; Nosocomial respiratory infections.)
191
PNEUMONIA IN THE MENTALLY RETARDED
Vol. 67 • No. 2
Chest x-ray reports were examined for all deaths occurring during a five-year period (1969-73), and reports for 56 autopsied deaths were obtained. Reports of chest x-rays of individuals with pneumonia reported at autopsy obtained less than a year prior to death were analyzed. Reports of the most recent medical examinations, especially the section pertaining to the lungs, were also examined. Results Pneumonia
Male Type of Pneumonia (ICD Code)
Female
Total
No.
%
No.
%
No.
%
22 0 5 0 34 8
18.3 0.0 4.2 0.0 28.3 6.7
16 1 11 1 44 3
13.7 0.9 9.4 0.9 37.6 2.6
38 1 16 1 78 11
16.0 0.4 6.8 0.4 32.9 4.6
17 Other chronic interstitial pneumonia
6
5.0
9
7.7
15
6.3
19.2 Lipid pneumonia
7
5.8
8
6.8
15
6.3
otal with one or more
69
57.5
77
65.8
146
61.6
480-486 Pneumonia * Aspiration 480 Viral 481, 482 Bacterial 484 Acute interstitial 485 Bronchopneumonia 486 Unspecified
Total number of autopsies
120
117
237
Mean age at death (years)
15.6
24.5
20.0
* There is no specific ICD code for aspiration pneumonia.
hemorrhage), and pneumonia (three cases). These are recognized causes of pleural effusion; tuberculous pleural effusion could also be involved, but direct evidence may be difficult to obtain.21 Only one of the 45 autopsy reports describing pleurisy mentioned tuberculosis; this was "arrested" tuberculosis (bilateral, upper lobe) with pleural adhesions in a 65year-old man. Postmortem bacteriology Microorganisms were recovered from cultures from at least one site (nose and throat, bronchus or lung, and heart blood) in 94 (83.2%) of 113 cases, excluding "contaminants" in heart blood cultures. Table 2 shows the frequencies of postmortem recoveries of microorganisms from the three sources. Staphylococci were found frequently in the nose and throat, and somewhat less frequently in bronchus or lung. Noteworthy are the high recovery rates of E. coli and Klebsiella-Aerobacter species, especially in the bronchus or lung. Candida albicans was also relatively frequent in nose and throat, and bronchus or lung, cultures. Positive cultures were relatively less frequent from heart-blood samples; only 40 of 71 cultures (56.3%) were positive, and the pattern of microorganisms recovered was somewhat different from those at the other sites (i.e., coagulase-positive staphylococci were less frequent and coagulase-negative staphylococci more frequent). Of the 26 cases in which cultures from the lung or bronchus were obtained, 17 reportedly had evidence of pneumonia at autopsy. A total of 27 microorganisms was recovered from these 17 cases, or 1.6 organisms
Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
Table 1 shows the frequencies of specific types of pneumonia reported at autopsy. Bronchopneumonia was most frequently reported (32.9%), followed by aspiration pneumonia (16.0%). Other types of pneumonia were relatively infrequent. The occurrence of lipid pneumonia in 15 autopsies (6.3%) is noteworthy, in view of the high frequency of aspiration pneumonia. In a total of 146 cases (61.6%), at least one type of pneumonia was reported. In addition to the 38 cases of aspiration pneumonia, evidence of aspiration was obtained in another 22 autopsies. Of these 22 cases, seven involved pneumonia (five bronchopneumonia, one bacterial, and one lipid), five involved bronchitis or emphysema, and four involved pulmonary collapse (atelectasis, a feature of aspiration pneumonia). It is probable that aspiration often preceded (and was causally related to) these pulmonary conditions; this was indicated by the reporting of "old" or "chronic" aspiration pneumonia along with other pulmonary conditions of apparently more recent development. The pathologic features of aspiration pneumonia included edema, hemorrhage (with hemosiderin-filled macrophages), patchy atelectasis, and some necrosis, as described in previous studies.4'6 Aspiration or aspiration pneumonia was mentioned in autopsy reports of only five of 15 cases with lipid pneumonia. The pathologic features were similar to those for aspiration pneumonia (patchy atelectasis, edema and hemorrhage); fat-filled macrophages (with positive histologic staining for fat) were often reported, along with an inflammatory process and vacuolated cells. Pleurisy was also frequently found at autopsy— i.e., in 45 of 237 cases, or 19.0%. Fibrinous pleurisy is most commonly due to bacterial pneumonia, but pneumonia may also cause effusion.21 Only ten of the 45 autopsy reports describing pleurisy mentioned effusion. Effusion was apparently related to esophageal ulcer, secondary carcinomatous deposits in the lung (from an ovarian tumor in one case, and a fascial fibrosarcoma in another case), myocardial infarction, hemothorax with aspiration (asphyxia and pulmonary
Table 1. Types of Pneumonia Reported at Autopsy
POLEDNAK
192 Table 2. Recovery of Microorganisms from Postmortem Cultures Nose and Throat (N = 56)
Bronchus or Lung (N = 26)
Heart Blood (N = 71)
%
No.
%
No.
%
Staphylococci Coagulase-positive Coagulase-negative
32 3
57.1 5.4
9 1
34.6 3.8
4 10
5.6 14.1
Streptococci Beta-hemolytic Alpha-hemolytic
17 10
30.4 17.9
6 5
23.1 19.2
7 7
9.9 9.9
Escherichia coli
8
14.3
8
30.8
6
8.5
Enterobacterial species
3
5.4
1
3.8
1
1.4
Klebsiella-Aerobacter species
6
10.7
6
23.1
5
7.0
Pseudomonas species
2
3.6
0
0.0
3
4.2
Proteus species
3
5.4
2
7.7
3
4.2
11
19.6
3
11.5
2
2.8
Miscellaneous
2
3.6
3
11.5
5
7.0
Contaminants
0
0.0
0
0.0
9
12.7
No growth
2
3.6
0
0.0
22
31.0
Candida albicans
Ratio of number of organisms to number of cultures
1.7:1
1.7:1
0.7:1
per culture. The microorganisms involved were: coagulase-positive staphylococci in five (29.4%); E. coli in five (29.4%); Klebsiella in four (23.5%); alphahemolytic streptococci in three (17.6%); staphylococci coagulase-negative, Proteus, Achromobacter, other enterobacteria, Haemophilus, and unspecified gramnegative organisms in one case (5.9%) each. Table 3 shows the bacteriologic findings in 21 cases with aspiration (N = 12) or aspiration pneumonia (N = 9) reported at autopsy. Enterobacteria (£. coli, Proteus mirabilis, and Klebsiella) and yeast (Candida albicans) are evident. Hemolytic streptococci {viridans and pyogenes) were also frequently reported. Chest X-ray Reports As mentioned above, chest x-ray reports were available for 56 autopsied deaths (1969-73). Chest x-ray reports were obtained for 21 cases with aspiration pneumonia reported at autopsy, but only 12 of these were recent {i.e., within a year of death). Findings reported were negative for most of these, even those obtained within a few days (N = 3), two weeks (N = 1), and a month (N = 2) of death. In
one case "resolved pneumonitis or cardiac failure" (with Down's syndrome) was found one month before death, and another individual had "interstitial disease of both lungs" found five months before death, but no recommendation for treatment was given. Chest x-ray or medical examination reports made mention of rales in three of the 12 cases. One person who had lipid pneumonia reported at autopsy had had a chest x-ray two weeks before death; crepitant rales in the lower lung regions had been detected, but were not attributed to an infectious process. Of 11 persons with bronchopneumonia reported at autopsy, seven had had chest x-rays taken within a year of death. One report, about a month before death (from bronchopneumonia), indicated a stable infiltration of the left lung, with no recommendation for treatment; in this case bronchopneumonia and aspiration of bile were reported at autopsy. The other six individuals, including one who had bronchopneumonia and aspiration found at autopsy, had been reported as without evidence of disease. This included a person who had had an x-ray taken three days before death with "no sign of pneumonia in either lung" who died from bronchopneumonia (certified as the underlying cause of death and reported at autopsy). It should be noted that tuberculosis did not appear to be frequent in this population. Tuberculin test results were noted on almost all chest x-ray reports, along with diagnostic impressions regarding tuberculosis. Of the 56 autopsied deaths (1969-73) with chest x-ray reports, three early reports (from the 1950's) mentioned positive tuberculin skin tests, and two of these reported tuberculosis (old and arrested, with pleurisy). One other report mentioned a positive tuberculin test in 1970, two years before death, but no diagnosis of tuberculosis was mentioned, and the death was attributed to aspiration pneumonia and intestinal obstruction. Chest x-ray reports for nonautopsied deaths (1969-73) were also examined for evidence of tuberculosis. Of 37 cases in which roentgenograms had been obtained within a year of death, tuberculosis was reported in none, one person had a positive tuberculin test but "no evidence of pulmonary tuberculosis" was reported. Of 47 other non-autopsied deaths with chest x-ray reports on file, two had had minimal, arrested pulmonary tuberculosis reported some years before death. Parenthetically, it was found that only two of the 676 death certificates mentioned tuberculosis (LCD. codes 010-019), and these were for relatively old persons (62 and 65 years old at death). One of these two individuals had an autopsy, and is mentioned above with reference to pleurisy.
Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
No.
A.J.C.I'. • i-ebruury 1977
193
PNEUMONIA IN THE MENTALLY RETARDED
Vol. 67 • No. 2
Discussion
Streptococci Staphylococci E. coli Proteus mirabilis Achromobacter Klebsiella aerobacter Hemophilus Bacterium anitratum Candida albicans Sterile Number of cultures Ratio of number of organisms to number of cultures
Nose, Throat No.
Bronchus, Lung No.
Heart Blood No.
4 3 1 1 0 1 0 0 2 0 6 12/6 = 2:1
2 1 2 1 1 0 1 0 1 0 8 9/8 = 1.1:1
4 1 3 1 0 1 0 2 1 2* 12 13/12 = 1.1:1
* Two of these were in cases with aspiration alone.
reports, and chest x-ray reports. Similarly, Richards and Sylvester19 reported that tuberculosis has been an insignificant cause of death in mental deficiency institutions in England since 1950. Changes in the age structure of institutions for the retarded,17 however, could be involved; the highest mortality rate for tuberculosis is in the first few years of life, and the proportion of institutionalized retarded young children has declined considerably. Since postmortem bacteriologic cultures were not available for all cases, these findings must also be interpreted with caution. The 56.3% positive rate for heart blood cultures agrees closely with the 53% rate in a recent study.11 As in previous studies,10 postmortem swabs from the throat almost always showed bacterial growth (Table 2). Gram-positive organisms (staphylococci and streptococci) predominated. These are common commensals of the upper respiratory tract, but coagulase-positive staphylococci are regarded as potential pathogens, and were frequently recovered from nose and throat cultures. Enteric gram-negative bacilli, however, are rarely found in the oropharyngeal flora of non-hospitalized persons.915 The bronchi and lungs are sterile when healthy, and postmortem invasion of bacteria is unlikely1011; hence, lung cultures may be of particular importance. The recovery of staphylococci in bronchus or lung cultures is not unexpected, in view of their high invasion rate10 and occurrence in debilitated hospitalized patients. Several studies, reviewed by Pierce and Sanford,15 have shown that autopsy cultures of human lungs provide bacterial species similar to those cultured in the pharynx. Tables 2 and 3 show this similarity. Coagulase-positive staphylococci, for
Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
Autopsy reports were examined to evaluate the prevalences of specific types of pneumonia at death. Since autopsies are not representative of all deaths, these data must be interpreted with caution. Bronchopneumonia was found in about a third of all autopsies (Table 1), which is similar to the figure reported from a large Veterans Administration hospital.14 The finding that 60 of 237 autopsies (25.3%) made mention of aspiration suggests that this is a significant potential health problem in this population. These 60 cases included 38 with aspiration pneumonia; in the others, pneumonia was sometimes reported along with aspiration, but the relationship was apparently unclear. Cases of lipid pneumonia also undoubtedly involved aspiration, although it was mentioned in only five of 15 cases. In "exogenous" lipid (lipoid) pneumonia, animal fats are introduced into the lung by aspiration (often of regurgitated food).7 Phagocytosis of the fat by alveolar macrophages occurs, as in the present case where fat-filled macrophages were found histologically. The true incidence of aspiration and its sequelae is difficult to determine, since postmortem examination may reveal only nonspecific results of aspiration.8 In 11 of the 38 cases of aspiration pneumonia, bronchopneumonia was also reported; other cases of bronchopneumonia may have been related to aspiration, which was unrecognized. The rather large number of cases of "other chronic interstitial pneumonia" (Table 1) suggests the possibility of aspiration as a precursor; the cellular infiltration and increase in fibrous tissue in interstitial pulmonary disease suggest the possibility of unrecognized lipoid pneumonia, but this is speculative. Chest x-ray reports on a smaller group with pneumonia found at autopsy suggested that bronchopneumonia and aspiration pneumonia often develop rapidly, with few recognized symptoms. This is in agreement with findings in a large veterans' hospital, in which bronchopneumonia was often associated with aspiration, and was usually insidious, with few symptoms and a rapid course.14 Arms and associates1 did find classic bilateral diffuse infiltration in about 25% of cases of aspiration pneumonia, which suggests that roentgenograms of the chest may be of some value in detection of aspiration pneumonia. Rales were reported to occur in three of 12 cases of aspiration pneumonia, and in the one case of lipid pneumonia. Diffuse rales are reportedly common in patients who have aspiration pneumonitis.6 Tuberculosis did not appear to be frequent in this population, according to death certificates, autopsy
Table 3. Postmortem Cultures in Cases with Aspiration or Aspiration Pneumonia (N = 21)
194
A.J.C.P. . l-ebruary 1977
POLEDNAK
Recent reports20 suggest possible involvement of Candida albicans in pneumonia related to aspiration of pharyngeal contents. The postmortem recovery of Candida in patients with evidence of aspiration (Table 3), as well as in other cases (Table 2), is noteworthy in this regard. The presence of hemolytic streptococci in bronchus or lung cultures is noteworthy. Although streptococcal pneumonia has been rare since the introduction of penicillin, recent outbreaks have been reported to occur in institutionalized populations {i.e., military recruits).3 Systematic records of antibiotic treatment were not available, but chemotherapy or antibiotic treatment prescribed within 48 hours of death does not appear to influence the total postmortem recovery of microorganisms significantly.11 Perhaps the most significant finding in this population is the high frequency of aspiration and aspiration pneumonia, and the postmortem bacteriologic
culture data apparently consistent with this. The high frequency of aspiration and its sequelae is not unexpected in institutionalized populations. In institutionalized elderly patients,14 aspiration pneumonia is a frequent finding at autopsy. States of impaired consciousness, related to epilepsy or cerebral dysfunction, are known risk factors for aspiration.1,2,4,5 The occurrences of epilepsy, cerebral palsy, encephalitis, and various congenital malformations of the digestive tract in retarded populations suggest that they may be at high risk for aspiration. Prolonged bed rest, reducing drainage of tracheobronchial secretions, may be an additional factor. As Richards and Sylvester19 have observed, severely retarded patients with infrequency and inefficiency of throat-clearing, coughing and noseblowing could be at high risk for respiratory disease, including aspiration. Poor personal hygienic habits could also facilitate the spread of infection, but this requires further study. Proper positioning in bed to facilitate drainage of tracheobronchial sections,5 and special feeding procedures1'5 may be useful measures in prevention of aspiration pneumonia in institutionalized retarded populations. Observation, recording and modification of personal hygienic behavior (coughing, nose-blowing, throat-clearing, and washing) could also be considered. Periodic chest x-rays, collection of sputum to be examined for evidence of lipoid pneumonia, and transtracheal aspiration of material for culture for gram-negative microorganisms (including anaerobes) would be useful in early detection of aspiration and its sequelae. Pulmonary function tests would also be useful in studying such sequelae as atelectasis and fibrosis. Acknowledgments. Cooperation and assistance were provided by Mrs. Lillian Mayor, Supervisor of Resident Record Services at the Huronia Regional Centre (formerly the Ontario Hospital School), Orillia, Ontario, Canada. Part of this work was supported by a grant from the University of Waterloo, Waterloo, Ontario.
References 1. Arms RA, Dines DE, Tinstman TC: Aspiration pneumonia. Chest 65:136-139, 1974 2. Bartlett JG, Gorbach SL, Finegold SM: The bacteriology of aspiration pneumonia. Am J Med 56:202-207, 1974 3. Basiliere JL, Bistrong HW, Spence WF: Streptococcal pneumonia: Recent outbreaks in military recruit populations. Am J Med 44:580-589, 1968 4. Cameron JL, Anderson RP, Zuidema GD: Aspiration pneumonia. A clinical and experimental review. J Surg Res 7: 44-53, 1967 5. Cameron JL, Zuidema GD: Aspiration pneumonia. Magnitude and frequency of the problem. JAMA 219:11941196, 1972 6. Dines DE, Titus JL, Sessler AD: Aspiration pneumonia. Mayo Clin Proc 45:347-360, 1970 7. Ebert RV: Lipoid pneumonia, Cecil-Loeb Textbook of Medi-
Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
example, were frequent in both nose (and throat) and bronchus or lung cultures (Table 2). Aerobic gram-negative bacilli are also frequent in cultures from both regions (Table 2). In hospitalized patients the oropharynx is commonly colonized with gram-negative aerobes, which cause many nosocomial respiratory infections.9,15 Pierce and Sanford15 have estimated that about half of all pneumonias acquired within a hospital setting are due to aerobic gram-negative bacilli. The present findings, albeit based on postmortem cultures alone, are not inconsistent with this estimate. The high postmortem recovery rate of certain gramnegative bacilli and other microorganisms in this study could be correlated with the high frequency of aspiration pneumonia in the population (Table 1). E. coli and related organisms (other enterobacteria, such as Aerobacter) are frequent isolates in the upper respiratory tracts of young children, presumably regurgitated from the alimentary tract. E. coli reportedly has a high invasion rate,10 and in the present study was frequently recovered in the bronchus or lung, as well as the nose and throat (Tables 2 and 3). Antemortem cultures from patients with aspiration and aspiration pneumonia1'2,6'12 have shown E. coli and Klebsiella, along with staphylococci. Anaerobic bacteria are also common pathogens in aspiration pneumonia, however, and anaerobic cultures were not available in the present study. On the other hand, aerobic enteric gram-negative bacilli are particularly common in patients with hospitalacquired aspiration pneumonia.12 Thus, the present findings may be indicative (at least in part) of hospitalacquired aspiration pneumonia in this population (Table 3), within the limitations of the validity of postmortem cultures.
Vol. 67 • No. 2
PNEUMONIA IN THE MENTALLY RETARDED
cine. 13th edition. Volume 1. Edited by Beeson PB, McDermott W. Philadelphia, W. B. Saunders, 1971 8. Heroy WW: Unrecognized aspiration. Ann Thorac Surg 8: 580-581, 1969 9. Johanson WG, Pierce AK, Sanford JP: Changing pharyngeal bacterial flora of hospitalized patients: Emergence of gramnegative bacilli. N Engl J Med 281:1137-1140, 1969 10. Kneeland Y, Price CM: Antiboitics and terminal pneumonia. A postmortem microbiological study. Am J Med 29: 967-979, 1960 11. Koneman EW, Davis MA: Postmortem bacteriology. III. Clinical significance of microorganisms recovered at autopsy. Am J Clin Pathol 61:28-40, 1974 12. Lorber B, Swenson RM: Bacteriology of aspiration pneumonia. A prospective study of community and hospital-acquired cases. Ann Intern Med 81:329-331, 1974 13. McCurley R, Mackay DN, Serially BG: The life expectation of the mentally subnormal under community and hospital care. J Ment Defic Res 16:57-66, 1972 14. Mrazek SA: Bronchopneumonia in terminally ill patients. J Am Geriat Soc 17:969-973, 1969
195
15. Pierce AK, Sanford JP: Aerobic gram-negative bacillary pneumonias. Am Rev Resp Dis 110:647-658, 1974 16. Polednak AP: Respiratory disease mortality in an institutionalized mentally retarded population. J Ment Defic Res 20:9-15, 1976 17. Richards BW: Age trends in mental deficiency institutions. J Ment Defic Res 13:171-183, 1969 18. Richards BW: Mental Subnormality. Modern Trends in Research. London, Pitman, 1971 19. Richards BW, Sylvester PE: Mortality trends in mental deficiency institutions. J Ment Defic Res 13:276-292, 1969 20. Rosenbaum RB, Barber JV, Stevens DA: Candida albicans pneumonia. Diagnosis by pulmonary aspiration, recovery without treatment. Am Rev Resp Dis 109:373-378, 1974 21. Stead WW: Diseases of the pleura, Cecil-Loeb Textbook of Medicine, 13th edition. Volume I. Edited by Beeson PB, McDermott W. Philadelphia, W. B. Saunders, 1971 22. World Health Organization: International Classification of Diseases, Eighth Revision. World Health Organization, Geneva, 1967 Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
PNEUMONIA AND other respiratory diseases continue to be the major cause of death in institutionalized mentally retarded persons. 13,16 ' 18 ' 19 Autopsy data on specific types of pneumonia in these populations have apparently not been reported, and antemortem or postmortem microbiologic data are also lacking. Together, these data could be of great value in identifying diseases and probable causal agents, upon which therapeutic and prevention programs could concentrate. The present retrospective study describes the frequencies of specific types of pneumonia and postmortem bacteriologic findings in an autopsy population of institutionalized mentally retarded persons. Received November 11, 1975; received revised manuscript February 16, 1976; accepted for publication February 16, 1976. Address reprint requests to Dr. Polednak at his present address: Center for Human Radiobiology, Argonne National Laboratory, Argonne, Illinois 60439.
Birth Defects Institute, State Department of Health, Albany, New York
Materials and Methods The Ontario Hospital School at Orillia is the oldest and largest institution for the mentally retarded in Ontario, Canada. Records of deaths of patients were available for 1958 to 1973. The total population varied between about 2,900 and 2,100 per year. The total population at risk for the entire period could not be accurately estimated; the population was rather stable, however, with relatively few new admissions each year, as reported for other similar institutions. 17 A trend toward aging of the population, as reported elsewhere, 17 was also evident; by 1970, an at-risk population less than 5 years of age was virtually nonexistent. From the centralized record system of the institution, records were located for 676 of the total of 707 deaths that occurred from 1958 to 1973. These records included case histories and all medical information available, including death certificates and autopsy reports. Autopsy reports were available for 237 of the 246 performed. Pneumonias and other respiratory diseases reported at autopsy were coded according to the International Classification of Diseases, Eighth Revision (World Health Organization, 1965).22 The sex composition, average age at death, and intellectual status (level of retardation) of the autopsy series were very similar to those of the entire group of 676 decedents. Most autopsies were performed in the morgue of the institution. Of the 237 autopsies, at least one bacteriologic culture report was avilable for 113 (47.7%). These included 56 nose and throat, 26 bronchus or lung, and 71 heart blood cultures. Cultures were examined by standard technics (Gram's method and coagulase test); cultures for anaerobic bacteria were not done.
190
Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
Polednak, Anthony P.: Postmortem bacteriology and pneumonia in a mentally retarded population. Am J Clin Pathol 67: 190-195, 1977. Postmortem pathologic and bacteriologic reports were analyzed for 237 deaths occurring at a large institution for the mentally retarded from 1958 to 1973. Bronchopneumonia, aspiration pneumonia, and lipid pneumonia were frequently reported at autopsy, and in a total of 146 cases (61.6%) at least one type of pneumonia was reported. Postmortem bacteriologic cultures in a smaller group revealed high recovery rates of staphylococci (coagulase-positive), hemolytic streptococci, and gram-negative bacilli in throat and lung cultures. Enteric aerobic gram-negative bacilli were particularly frequent, along with yeast (Candida albicans). The institutionalized retarded appear similar to other hospitalized populations, in that a large proportion of hospitalacquired respiratory infections is related to aerobic gramnegative bacilli. The high frequency of aspiration and its sequelae in this population is unusual, however, and postmortem bacteriologic findings appear consistent with those of antemortem studies of cases of aspiration pneumonia. (Key words: Postmortem bacteriology; Aspiration pneumonia; Gram-negative bacteria; Lipoid pneumonia; Nosocomial respiratory infections.)
191
PNEUMONIA IN THE MENTALLY RETARDED
Vol. 67 • No. 2
Chest x-ray reports were examined for all deaths occurring during a five-year period (1969-73), and reports for 56 autopsied deaths were obtained. Reports of chest x-rays of individuals with pneumonia reported at autopsy obtained less than a year prior to death were analyzed. Reports of the most recent medical examinations, especially the section pertaining to the lungs, were also examined. Results Pneumonia
Male Type of Pneumonia (ICD Code)
Female
Total
No.
%
No.
%
No.
%
22 0 5 0 34 8
18.3 0.0 4.2 0.0 28.3 6.7
16 1 11 1 44 3
13.7 0.9 9.4 0.9 37.6 2.6
38 1 16 1 78 11
16.0 0.4 6.8 0.4 32.9 4.6
17 Other chronic interstitial pneumonia
6
5.0
9
7.7
15
6.3
19.2 Lipid pneumonia
7
5.8
8
6.8
15
6.3
otal with one or more
69
57.5
77
65.8
146
61.6
480-486 Pneumonia * Aspiration 480 Viral 481, 482 Bacterial 484 Acute interstitial 485 Bronchopneumonia 486 Unspecified
Total number of autopsies
120
117
237
Mean age at death (years)
15.6
24.5
20.0
* There is no specific ICD code for aspiration pneumonia.
hemorrhage), and pneumonia (three cases). These are recognized causes of pleural effusion; tuberculous pleural effusion could also be involved, but direct evidence may be difficult to obtain.21 Only one of the 45 autopsy reports describing pleurisy mentioned tuberculosis; this was "arrested" tuberculosis (bilateral, upper lobe) with pleural adhesions in a 65year-old man. Postmortem bacteriology Microorganisms were recovered from cultures from at least one site (nose and throat, bronchus or lung, and heart blood) in 94 (83.2%) of 113 cases, excluding "contaminants" in heart blood cultures. Table 2 shows the frequencies of postmortem recoveries of microorganisms from the three sources. Staphylococci were found frequently in the nose and throat, and somewhat less frequently in bronchus or lung. Noteworthy are the high recovery rates of E. coli and Klebsiella-Aerobacter species, especially in the bronchus or lung. Candida albicans was also relatively frequent in nose and throat, and bronchus or lung, cultures. Positive cultures were relatively less frequent from heart-blood samples; only 40 of 71 cultures (56.3%) were positive, and the pattern of microorganisms recovered was somewhat different from those at the other sites (i.e., coagulase-positive staphylococci were less frequent and coagulase-negative staphylococci more frequent). Of the 26 cases in which cultures from the lung or bronchus were obtained, 17 reportedly had evidence of pneumonia at autopsy. A total of 27 microorganisms was recovered from these 17 cases, or 1.6 organisms
Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
Table 1 shows the frequencies of specific types of pneumonia reported at autopsy. Bronchopneumonia was most frequently reported (32.9%), followed by aspiration pneumonia (16.0%). Other types of pneumonia were relatively infrequent. The occurrence of lipid pneumonia in 15 autopsies (6.3%) is noteworthy, in view of the high frequency of aspiration pneumonia. In a total of 146 cases (61.6%), at least one type of pneumonia was reported. In addition to the 38 cases of aspiration pneumonia, evidence of aspiration was obtained in another 22 autopsies. Of these 22 cases, seven involved pneumonia (five bronchopneumonia, one bacterial, and one lipid), five involved bronchitis or emphysema, and four involved pulmonary collapse (atelectasis, a feature of aspiration pneumonia). It is probable that aspiration often preceded (and was causally related to) these pulmonary conditions; this was indicated by the reporting of "old" or "chronic" aspiration pneumonia along with other pulmonary conditions of apparently more recent development. The pathologic features of aspiration pneumonia included edema, hemorrhage (with hemosiderin-filled macrophages), patchy atelectasis, and some necrosis, as described in previous studies.4'6 Aspiration or aspiration pneumonia was mentioned in autopsy reports of only five of 15 cases with lipid pneumonia. The pathologic features were similar to those for aspiration pneumonia (patchy atelectasis, edema and hemorrhage); fat-filled macrophages (with positive histologic staining for fat) were often reported, along with an inflammatory process and vacuolated cells. Pleurisy was also frequently found at autopsy— i.e., in 45 of 237 cases, or 19.0%. Fibrinous pleurisy is most commonly due to bacterial pneumonia, but pneumonia may also cause effusion.21 Only ten of the 45 autopsy reports describing pleurisy mentioned effusion. Effusion was apparently related to esophageal ulcer, secondary carcinomatous deposits in the lung (from an ovarian tumor in one case, and a fascial fibrosarcoma in another case), myocardial infarction, hemothorax with aspiration (asphyxia and pulmonary
Table 1. Types of Pneumonia Reported at Autopsy
POLEDNAK
192 Table 2. Recovery of Microorganisms from Postmortem Cultures Nose and Throat (N = 56)
Bronchus or Lung (N = 26)
Heart Blood (N = 71)
%
No.
%
No.
%
Staphylococci Coagulase-positive Coagulase-negative
32 3
57.1 5.4
9 1
34.6 3.8
4 10
5.6 14.1
Streptococci Beta-hemolytic Alpha-hemolytic
17 10
30.4 17.9
6 5
23.1 19.2
7 7
9.9 9.9
Escherichia coli
8
14.3
8
30.8
6
8.5
Enterobacterial species
3
5.4
1
3.8
1
1.4
Klebsiella-Aerobacter species
6
10.7
6
23.1
5
7.0
Pseudomonas species
2
3.6
0
0.0
3
4.2
Proteus species
3
5.4
2
7.7
3
4.2
11
19.6
3
11.5
2
2.8
Miscellaneous
2
3.6
3
11.5
5
7.0
Contaminants
0
0.0
0
0.0
9
12.7
No growth
2
3.6
0
0.0
22
31.0
Candida albicans
Ratio of number of organisms to number of cultures
1.7:1
1.7:1
0.7:1
per culture. The microorganisms involved were: coagulase-positive staphylococci in five (29.4%); E. coli in five (29.4%); Klebsiella in four (23.5%); alphahemolytic streptococci in three (17.6%); staphylococci coagulase-negative, Proteus, Achromobacter, other enterobacteria, Haemophilus, and unspecified gramnegative organisms in one case (5.9%) each. Table 3 shows the bacteriologic findings in 21 cases with aspiration (N = 12) or aspiration pneumonia (N = 9) reported at autopsy. Enterobacteria (£. coli, Proteus mirabilis, and Klebsiella) and yeast (Candida albicans) are evident. Hemolytic streptococci {viridans and pyogenes) were also frequently reported. Chest X-ray Reports As mentioned above, chest x-ray reports were available for 56 autopsied deaths (1969-73). Chest x-ray reports were obtained for 21 cases with aspiration pneumonia reported at autopsy, but only 12 of these were recent {i.e., within a year of death). Findings reported were negative for most of these, even those obtained within a few days (N = 3), two weeks (N = 1), and a month (N = 2) of death. In
one case "resolved pneumonitis or cardiac failure" (with Down's syndrome) was found one month before death, and another individual had "interstitial disease of both lungs" found five months before death, but no recommendation for treatment was given. Chest x-ray or medical examination reports made mention of rales in three of the 12 cases. One person who had lipid pneumonia reported at autopsy had had a chest x-ray two weeks before death; crepitant rales in the lower lung regions had been detected, but were not attributed to an infectious process. Of 11 persons with bronchopneumonia reported at autopsy, seven had had chest x-rays taken within a year of death. One report, about a month before death (from bronchopneumonia), indicated a stable infiltration of the left lung, with no recommendation for treatment; in this case bronchopneumonia and aspiration of bile were reported at autopsy. The other six individuals, including one who had bronchopneumonia and aspiration found at autopsy, had been reported as without evidence of disease. This included a person who had had an x-ray taken three days before death with "no sign of pneumonia in either lung" who died from bronchopneumonia (certified as the underlying cause of death and reported at autopsy). It should be noted that tuberculosis did not appear to be frequent in this population. Tuberculin test results were noted on almost all chest x-ray reports, along with diagnostic impressions regarding tuberculosis. Of the 56 autopsied deaths (1969-73) with chest x-ray reports, three early reports (from the 1950's) mentioned positive tuberculin skin tests, and two of these reported tuberculosis (old and arrested, with pleurisy). One other report mentioned a positive tuberculin test in 1970, two years before death, but no diagnosis of tuberculosis was mentioned, and the death was attributed to aspiration pneumonia and intestinal obstruction. Chest x-ray reports for nonautopsied deaths (1969-73) were also examined for evidence of tuberculosis. Of 37 cases in which roentgenograms had been obtained within a year of death, tuberculosis was reported in none, one person had a positive tuberculin test but "no evidence of pulmonary tuberculosis" was reported. Of 47 other non-autopsied deaths with chest x-ray reports on file, two had had minimal, arrested pulmonary tuberculosis reported some years before death. Parenthetically, it was found that only two of the 676 death certificates mentioned tuberculosis (LCD. codes 010-019), and these were for relatively old persons (62 and 65 years old at death). One of these two individuals had an autopsy, and is mentioned above with reference to pleurisy.
Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
No.
A.J.C.I'. • i-ebruury 1977
193
PNEUMONIA IN THE MENTALLY RETARDED
Vol. 67 • No. 2
Discussion
Streptococci Staphylococci E. coli Proteus mirabilis Achromobacter Klebsiella aerobacter Hemophilus Bacterium anitratum Candida albicans Sterile Number of cultures Ratio of number of organisms to number of cultures
Nose, Throat No.
Bronchus, Lung No.
Heart Blood No.
4 3 1 1 0 1 0 0 2 0 6 12/6 = 2:1
2 1 2 1 1 0 1 0 1 0 8 9/8 = 1.1:1
4 1 3 1 0 1 0 2 1 2* 12 13/12 = 1.1:1
* Two of these were in cases with aspiration alone.
reports, and chest x-ray reports. Similarly, Richards and Sylvester19 reported that tuberculosis has been an insignificant cause of death in mental deficiency institutions in England since 1950. Changes in the age structure of institutions for the retarded,17 however, could be involved; the highest mortality rate for tuberculosis is in the first few years of life, and the proportion of institutionalized retarded young children has declined considerably. Since postmortem bacteriologic cultures were not available for all cases, these findings must also be interpreted with caution. The 56.3% positive rate for heart blood cultures agrees closely with the 53% rate in a recent study.11 As in previous studies,10 postmortem swabs from the throat almost always showed bacterial growth (Table 2). Gram-positive organisms (staphylococci and streptococci) predominated. These are common commensals of the upper respiratory tract, but coagulase-positive staphylococci are regarded as potential pathogens, and were frequently recovered from nose and throat cultures. Enteric gram-negative bacilli, however, are rarely found in the oropharyngeal flora of non-hospitalized persons.915 The bronchi and lungs are sterile when healthy, and postmortem invasion of bacteria is unlikely1011; hence, lung cultures may be of particular importance. The recovery of staphylococci in bronchus or lung cultures is not unexpected, in view of their high invasion rate10 and occurrence in debilitated hospitalized patients. Several studies, reviewed by Pierce and Sanford,15 have shown that autopsy cultures of human lungs provide bacterial species similar to those cultured in the pharynx. Tables 2 and 3 show this similarity. Coagulase-positive staphylococci, for
Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
Autopsy reports were examined to evaluate the prevalences of specific types of pneumonia at death. Since autopsies are not representative of all deaths, these data must be interpreted with caution. Bronchopneumonia was found in about a third of all autopsies (Table 1), which is similar to the figure reported from a large Veterans Administration hospital.14 The finding that 60 of 237 autopsies (25.3%) made mention of aspiration suggests that this is a significant potential health problem in this population. These 60 cases included 38 with aspiration pneumonia; in the others, pneumonia was sometimes reported along with aspiration, but the relationship was apparently unclear. Cases of lipid pneumonia also undoubtedly involved aspiration, although it was mentioned in only five of 15 cases. In "exogenous" lipid (lipoid) pneumonia, animal fats are introduced into the lung by aspiration (often of regurgitated food).7 Phagocytosis of the fat by alveolar macrophages occurs, as in the present case where fat-filled macrophages were found histologically. The true incidence of aspiration and its sequelae is difficult to determine, since postmortem examination may reveal only nonspecific results of aspiration.8 In 11 of the 38 cases of aspiration pneumonia, bronchopneumonia was also reported; other cases of bronchopneumonia may have been related to aspiration, which was unrecognized. The rather large number of cases of "other chronic interstitial pneumonia" (Table 1) suggests the possibility of aspiration as a precursor; the cellular infiltration and increase in fibrous tissue in interstitial pulmonary disease suggest the possibility of unrecognized lipoid pneumonia, but this is speculative. Chest x-ray reports on a smaller group with pneumonia found at autopsy suggested that bronchopneumonia and aspiration pneumonia often develop rapidly, with few recognized symptoms. This is in agreement with findings in a large veterans' hospital, in which bronchopneumonia was often associated with aspiration, and was usually insidious, with few symptoms and a rapid course.14 Arms and associates1 did find classic bilateral diffuse infiltration in about 25% of cases of aspiration pneumonia, which suggests that roentgenograms of the chest may be of some value in detection of aspiration pneumonia. Rales were reported to occur in three of 12 cases of aspiration pneumonia, and in the one case of lipid pneumonia. Diffuse rales are reportedly common in patients who have aspiration pneumonitis.6 Tuberculosis did not appear to be frequent in this population, according to death certificates, autopsy
Table 3. Postmortem Cultures in Cases with Aspiration or Aspiration Pneumonia (N = 21)
194
A.J.C.P. . l-ebruary 1977
POLEDNAK
Recent reports20 suggest possible involvement of Candida albicans in pneumonia related to aspiration of pharyngeal contents. The postmortem recovery of Candida in patients with evidence of aspiration (Table 3), as well as in other cases (Table 2), is noteworthy in this regard. The presence of hemolytic streptococci in bronchus or lung cultures is noteworthy. Although streptococcal pneumonia has been rare since the introduction of penicillin, recent outbreaks have been reported to occur in institutionalized populations {i.e., military recruits).3 Systematic records of antibiotic treatment were not available, but chemotherapy or antibiotic treatment prescribed within 48 hours of death does not appear to influence the total postmortem recovery of microorganisms significantly.11 Perhaps the most significant finding in this population is the high frequency of aspiration and aspiration pneumonia, and the postmortem bacteriologic
culture data apparently consistent with this. The high frequency of aspiration and its sequelae is not unexpected in institutionalized populations. In institutionalized elderly patients,14 aspiration pneumonia is a frequent finding at autopsy. States of impaired consciousness, related to epilepsy or cerebral dysfunction, are known risk factors for aspiration.1,2,4,5 The occurrences of epilepsy, cerebral palsy, encephalitis, and various congenital malformations of the digestive tract in retarded populations suggest that they may be at high risk for aspiration. Prolonged bed rest, reducing drainage of tracheobronchial secretions, may be an additional factor. As Richards and Sylvester19 have observed, severely retarded patients with infrequency and inefficiency of throat-clearing, coughing and noseblowing could be at high risk for respiratory disease, including aspiration. Poor personal hygienic habits could also facilitate the spread of infection, but this requires further study. Proper positioning in bed to facilitate drainage of tracheobronchial sections,5 and special feeding procedures1'5 may be useful measures in prevention of aspiration pneumonia in institutionalized retarded populations. Observation, recording and modification of personal hygienic behavior (coughing, nose-blowing, throat-clearing, and washing) could also be considered. Periodic chest x-rays, collection of sputum to be examined for evidence of lipoid pneumonia, and transtracheal aspiration of material for culture for gram-negative microorganisms (including anaerobes) would be useful in early detection of aspiration and its sequelae. Pulmonary function tests would also be useful in studying such sequelae as atelectasis and fibrosis. Acknowledgments. Cooperation and assistance were provided by Mrs. Lillian Mayor, Supervisor of Resident Record Services at the Huronia Regional Centre (formerly the Ontario Hospital School), Orillia, Ontario, Canada. Part of this work was supported by a grant from the University of Waterloo, Waterloo, Ontario.
References 1. Arms RA, Dines DE, Tinstman TC: Aspiration pneumonia. Chest 65:136-139, 1974 2. Bartlett JG, Gorbach SL, Finegold SM: The bacteriology of aspiration pneumonia. Am J Med 56:202-207, 1974 3. Basiliere JL, Bistrong HW, Spence WF: Streptococcal pneumonia: Recent outbreaks in military recruit populations. Am J Med 44:580-589, 1968 4. Cameron JL, Anderson RP, Zuidema GD: Aspiration pneumonia. A clinical and experimental review. J Surg Res 7: 44-53, 1967 5. Cameron JL, Zuidema GD: Aspiration pneumonia. Magnitude and frequency of the problem. JAMA 219:11941196, 1972 6. Dines DE, Titus JL, Sessler AD: Aspiration pneumonia. Mayo Clin Proc 45:347-360, 1970 7. Ebert RV: Lipoid pneumonia, Cecil-Loeb Textbook of Medi-
Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
example, were frequent in both nose (and throat) and bronchus or lung cultures (Table 2). Aerobic gram-negative bacilli are also frequent in cultures from both regions (Table 2). In hospitalized patients the oropharynx is commonly colonized with gram-negative aerobes, which cause many nosocomial respiratory infections.9,15 Pierce and Sanford15 have estimated that about half of all pneumonias acquired within a hospital setting are due to aerobic gram-negative bacilli. The present findings, albeit based on postmortem cultures alone, are not inconsistent with this estimate. The high postmortem recovery rate of certain gramnegative bacilli and other microorganisms in this study could be correlated with the high frequency of aspiration pneumonia in the population (Table 1). E. coli and related organisms (other enterobacteria, such as Aerobacter) are frequent isolates in the upper respiratory tracts of young children, presumably regurgitated from the alimentary tract. E. coli reportedly has a high invasion rate,10 and in the present study was frequently recovered in the bronchus or lung, as well as the nose and throat (Tables 2 and 3). Antemortem cultures from patients with aspiration and aspiration pneumonia1'2,6'12 have shown E. coli and Klebsiella, along with staphylococci. Anaerobic bacteria are also common pathogens in aspiration pneumonia, however, and anaerobic cultures were not available in the present study. On the other hand, aerobic enteric gram-negative bacilli are particularly common in patients with hospitalacquired aspiration pneumonia.12 Thus, the present findings may be indicative (at least in part) of hospitalacquired aspiration pneumonia in this population (Table 3), within the limitations of the validity of postmortem cultures.
Vol. 67 • No. 2
PNEUMONIA IN THE MENTALLY RETARDED
cine. 13th edition. Volume 1. Edited by Beeson PB, McDermott W. Philadelphia, W. B. Saunders, 1971 8. Heroy WW: Unrecognized aspiration. Ann Thorac Surg 8: 580-581, 1969 9. Johanson WG, Pierce AK, Sanford JP: Changing pharyngeal bacterial flora of hospitalized patients: Emergence of gramnegative bacilli. N Engl J Med 281:1137-1140, 1969 10. Kneeland Y, Price CM: Antiboitics and terminal pneumonia. A postmortem microbiological study. Am J Med 29: 967-979, 1960 11. Koneman EW, Davis MA: Postmortem bacteriology. III. Clinical significance of microorganisms recovered at autopsy. Am J Clin Pathol 61:28-40, 1974 12. Lorber B, Swenson RM: Bacteriology of aspiration pneumonia. A prospective study of community and hospital-acquired cases. Ann Intern Med 81:329-331, 1974 13. McCurley R, Mackay DN, Serially BG: The life expectation of the mentally subnormal under community and hospital care. J Ment Defic Res 16:57-66, 1972 14. Mrazek SA: Bronchopneumonia in terminally ill patients. J Am Geriat Soc 17:969-973, 1969
195
15. Pierce AK, Sanford JP: Aerobic gram-negative bacillary pneumonias. Am Rev Resp Dis 110:647-658, 1974 16. Polednak AP: Respiratory disease mortality in an institutionalized mentally retarded population. J Ment Defic Res 20:9-15, 1976 17. Richards BW: Age trends in mental deficiency institutions. J Ment Defic Res 13:171-183, 1969 18. Richards BW: Mental Subnormality. Modern Trends in Research. London, Pitman, 1971 19. Richards BW, Sylvester PE: Mortality trends in mental deficiency institutions. J Ment Defic Res 13:276-292, 1969 20. Rosenbaum RB, Barber JV, Stevens DA: Candida albicans pneumonia. Diagnosis by pulmonary aspiration, recovery without treatment. Am Rev Resp Dis 109:373-378, 1974 21. Stead WW: Diseases of the pleura, Cecil-Loeb Textbook of Medicine, 13th edition. Volume I. Edited by Beeson PB, McDermott W. Philadelphia, W. B. Saunders, 1971 22. World Health Organization: International Classification of Diseases, Eighth Revision. World Health Organization, Geneva, 1967 Downloaded from http://ajcp.oxfordjournals.org/ by guest on June 5, 2016
