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The causes of death in pulmonary tuberculosis
Tubercle, Lond., (1963), 44, 230
230
THE CAUSES OF DEATH IN P U L M O N A R Y TUBERCULOSIS By F. A. H. S1MMONDS fi'om Clare Hall Hospital, Sottth Mimms, Barnet, Hefts.
SUMMARY Tile data concerning 87 persons dying in hospital and whose death certificates included the words 'pulmonary tuberculosis' were reviewed. A number of certificates appeared to be inaccurate. 49 patients died of other causes, though 21 of these also had active tuberculosis. There was no evidence of active tuberculous disease in 28 persons. Reasons for inaccuracies are considered: an important factor is tile number of deaths in old persons, ill whom degenerative diseases are a frequent cause of death. The presence of inactive, or even active, tuberculosis of the lungs in a dying person may not be a significant factor in causing death. This consideration assumes increased importance in rccent years with the availability of effective treatment for tuberculosis.
During tile five years 1957-1961 inclusive, a diagnosis of pulmonary tuberculosis appeared in the death certificates of 87 patients who died in this hospital. These patients were certified either as having died from tuberculosis, or as having suffered from tuberculosis of the lungs which was a contributory factor to the death. The official death certificate reports the cause of death under two heads: (I) Disease or condition directly leading to death (i.e. disease or injury etc., which caused death and not the mode ofdying). Antecedent causes--morbid conditions, if any, giving rise to the above cause, stating the underlying condition last. (11) Other significant conditions contributhlg to the death, but not related to the disease or condition causing it. Of the 87 certificates, 50 gave tuberculosis as a primary cause of death under Part I; in the others, tuberculosis was described as a factor contributory to death (Part 11). The total number of patients discharged after treatment for pulmonary tuberculosis, and of deaths, in each of these five years were as follows:
Year
Patients discharged Deaths Deaths/discharge (per cent)
1957 508 14 2.8 1958 516 10 1.9 1959 506 18 3"6 1960 597 20 3-5 1961 545 25 4-6 Hence, although the number of patients discharged from the hospital suffering from pulmonary tuberculosis had increased only slightly, the annual number of patients dying nearly doubled. Certificates are usually completed by a member of the junior medical staff, who has in most cases known the patient for some months at least, though a few patients die within a few days or
C A U S E S OF D E A T H
231
TABLE [.--AGE AND SEX OF 87 PATIENTS IN WHOM PULMONARY TUBERCULOSIS WAS CER'HFIED AS A CAUSE OF DEATH
Certified umter Age (years)
Part !*
25-34 35-44 45 -54 55-64 65-74 75 -fi
Part 11"
M.
F.
Total
M.
F.
Total
2 4 5 10 15 4
2 1 2 2 2 1
4 5 7 12 17 5
2 1 12 10 3
2 I 3 2
1 4 1 13 13 5
40
I0
50
30
7
37
* F o r definition see text.
weeks of admission. On the other hand, the certificate often has to be given before the results of the post mortem or other detailed anatomical and histological findings are known, and this may cause some inaccuracy in certification. (The Registrar can be informed of any change in the certificate which needs to be made if new information is obtained). An increasing proportion of patients dying in tuberculosis hospitals die from non-tuberculous causes; according to Bobrowitz (1960), speaking of New York City hospitals, the latter have risen from seven to 40 per cent in twenty years. The case notes were therefore reviewed for further information, including that becoming available after the certificate had been completed. The review of all the available data revealed some inaccuacies in the certificates. Moreover, it became clear that often there were several causes contributing to death; the decision as to the actual cause was sometimes difficult and it could only be classified after the later data were obtained. Of the 87 patients, 70 were men and 17 were women, the age and sex distribution being shown in Table I. Men between 55 and 75 years of age accounted for over half the total deaths. The recorded deaths may be divided into five groups (1) Death clearly due to tuberculosis of the lungs. (2) Death not actually due to tuberculosis, but tuberculosis the original cause leading to the death. (3) Death due to another cause, but tuberculous disease active. (4) Death due to another cause, and the tuberculosis inactive. (5) No evidence of tuberculosis; disease and death due to other cause. The figures for these groups are in Table I I. Post-mortem examination was made on 17 of 51 who died with active tuberculosis, and on 13 of 36 of the remainder. All those reported as showing no evidence of tuberculosis had post mortem examination; on the other hand, this was seldom done where the clinical course of the disease plainly pointed to tuberculosis as the cause. Death Directly Due to Tuberculosis The first group -died of tuberculosis does not require special consideration here. it is worth mentioning that 18 of these 29 patients had bacilli resistant to at least two of the main drugs and that in those with bacilli sensitive to the drugs (or of unknown sensitivity) special unfavourable features like old age, death within a week of admission or mental disorder were prominent.
232
TUBERCLF TABLE l l . - - T n ~ : ROLE OF TUI~IERCULOSIS IN THE DEATH OF 87 PATIENTS IN WHOM IT WAS CERTIFIED AS -~ CAUSE
Certified trader Part I
Died of p u l m o n a r y tuberculosis Death not tuberculous but tuberculosis contributory Tuberculosis a c t i v e ~ n o t contributory Death not tuberculous--tuberculosis inactive No evidence of tubcrculosis
Part II M.
t':
Total
I
I 4 !0 12 3
2 ! 2 I !
3 5 12 13 4
50
30
7
37
M.
F.
18 4 7
8 ~
10
~
10
I
~
40
2
10
I Total 26 4 9
In this group are included three cases in which tuberculosis was certified in Part I!, i.e. only as contributory to death. These were described as dying fiom bronchopneumonia in one case (actually tuberculous bronchopneumonia)" from bronchopneumonia and transverse myelitis of the cord (actually tuberculosis of the spine with involvement of tile cord, tile abscess being connected with a tuberculous apical empyema and a pulmonary cavity)" and from sudden cardiac arrest and hypopotassaemia (actually intrabronchial haemorrhage from a pulmonary tuberculous focus). All three were confirmed by post-mortem examination. Death hTdirectly Due to Tuberculosis in the second group, where tuberculosis was basically important as a factor in the death, the following were the actual immediate causes:-I--pleural haemorrhage after pleuropneumonectomy for gross tuberculosis and empyema.* I -operation for removal of plomb (prolonged sepsis)" the tuberculous disease for which the plomb was originally inserted was soundly healed. 2..... cor pulmonale due to extensive pulmonary tuberculosis of 10 years duration (1"). The five cases certified under Part II were similar: and on the same principle should have been allocated to Part I. !. bronchopneumonia after pleuropneumonectomy for tuberculosis bilateral pulmonary tuberculosis active.* I pericarditis and generalized staphyioccal infection after pneumonectomy for active tuberculosis; previous thoracoplasty and plombage.* 1 pneumonia and cardiac failure following prolonged sepsis resulting from operation for tuberculosis 15 years before; tuberculosis healed. I 'cirrhosis of liver'; actually congestion of the liver due to cot pulmona]e secondary to active tuberculosis.* I bronchopneumonia, bronchitis and e m p h y s e m a extensive pulmonary tuberculosis, healed, with fibrosis and thoracoplasty nine years earlier (age 40).* This last case raised the difficulty of assessing whether, in a patient dying of cor pulmonale or respiratory failure who has also had tuberculosis, the latter is a factor in death. If the patient was young (under 50) and there was gross fibrosis the death is included in the group above. Where, however, the patient seemed to suffer primarily with typical chronic bronchitis and emphysema, the tuberculous disease appearing insufficient to cause death, the latter has been included as non* Indicates post-mortem examination.
CAUSES OF D E A T H
233
tuberculous. As a result of chemotherapy in patients with extensive disease, the healing of tuberculosis may result in much fibrosis with clean cystic cavity formation, and with emphysema, so that such cases are frequently seen. Five patients in the second group died after severe surgical operations designed to relieve conditions which resulted from the failure of medical treatment applied several years earlier, in some cases prior to chemotherapy, and in others during the period of inadequate treatment of this type.
Death Not Due to Tuberculosis The third group where the tuberculosis was active but death was not due to tuberculosis include tile following causes: Certified under Part 11 (12 cases) Cert![ied under Part I (nine cases) Carcinoma of bronchus five cases (2*). Myocardial failure: cot pulmonale three cases (1"). Carcinoma larynx: mediastinitis.* Acute bronchopneumonia: chronic bronchitis and Primary carcinoma liver.* emphysema. Arteriosclerosis and congestive cardiac Staphylococcal pneumonia*. failure. Repeated spontaneous pneumothorax. Repeated coronary infarction.* Hypertension and arteriosclerosis. Acute pyelonephritis with abcesses: ParkinRenal failure. sonism. Gangrene of leg: infected pulmonary infarct: Chronic nephritis: uraemia. arteriosclerosis. Chronic bronchitis and emphysema: cor pulmonale. These diseases provided sufficient explanation of the deaths which occurred. The concurrent tuberculous disease was incidental to the fatality, being insufficient to cause death: it was in some cases well controlled by chemotherapy and in the others of limited extent and activity. In the fourth group, death due to other causes, tuberculosis inactive, there were: Certified under Part 1 (10 cases) Certified under Part II (13 cases) 6---cor pulmonale, chronic bronchitis and emphy(the causes are not significant for the present sema (ages 80, 73, 72, 68, 63, 50). discussion.) l wbronchopneumonia. 1 staphylococcal bronchopneumonia. 1 -multiple lung abcesses* ! carcinoma of bronchus.* In the fifth group, with no evidence of tuberculosis there were: Certified under Part I Certified under Part II Reticulo-zarcoma with adrenal failure. 3 carcinoma of bronchus. 1 .volvulus and staphylococcal enteritis. All in this group were examined post-mortem. Tile patient dying of volvulus and enteritis also had nephritis and arthritis. Two years before she had had treatment in Clare Hall Hospital for tuberculosis of the left lung with Myco. tuberculosis in the sputum. Complete radiographic and bacteriological clearance was obtained. At post-mortem, no evidence of tuberculous disease was found, except a little localized bronchiectasis in the left lung, the right being free of disease. In one patient with carcinoma the evidence suggesting tuberculosis was a cavity, which proved to be a large emphysematous cyst. In another, there was no evidence of tuberculosis post-mortem, but in life tubercle bacilli had been found on one occasion, obviously an incidental erroneous finding. To summarise the findings in the five groups, of 50 patients certified under Part I as having died from pulmonary tuberculosis, 20 were found to have died of other causes, though nine of these had active tuberculosis at the time of death. On the other hand, in 37 certified under Part II, tuberculosis might well have been recorded as the prime cause in eight, while in 18 no evidence of active tuberculous disease was present at death. Of the total 87, 28 patients (32 ~ ) died without evidence of active tuberculous disease.
234
TUBERCLE
Activity o/" the Tuberculous Disease Tubercle bacilli were found at some time in all but six of the patients. However, the finding of tubercle bacilli even within the twelve months before death is not necessarily evidence that the death was due to pulmonary tuberculosis, even less so if the discovery of the bacilli last occurred several years before. In a few patients chemotherapy had rendered the sputum negative and the disease was under control at death, which was due to another cause. Furthermore, there was doubt about the significance of the finding of tubercle bacilli in one patient who clearly died of carcinoma of the bronchus, tubercle bacilli had been reported only once, and that within the last year. Of the six patients, three had no evidence of pulmonary tuberculosis post-mortem and three showed evidence of well healed disease. Only one was reported under Category l and this man actually died of reticulo-sarcoma. Some attempt at estimating the duration of tuberculous disease was made, judging from the recorded history. Tile greater proportion had tuberculous disease for many years, one-third of those in whom estimates could be made having had tuberculosis for over ten years. In the others, either the duration was unknown, or disease was first discovered at post mortem examination, or there was no post mortem evidence of tuberculosis. Treatment by Chemotherapy had been employed in rather more than half the patients, but only in 14 had the duration ofchemotherapy been 12 months or more. The tubercle bacilli present were resistant to streptomycin and isoniazid in 28 % of the patients; in 51%, the bacilli were sensitive to streptomycin, PAS and isoniazid.
Association With Carcinoma qf the Bronchus There were six patients with carcinoma of the bronchus associated with active or inactive tuberculosis, and three patients with carcinoma of the bronchus but no evidence of pulmonary tuberculosis. Thus, combined carcinoma and tuberculosis occurred in 6 (7.3 %) out of 82 deaths with which tuberculosis was associated.
Discussion Anderson (1959) examined the circumstances of 56 deaths in Leicester, reported as due to pulmonary tuberculosis. Of these, ! 5 (27 %) were found to be due to other causes and not primarily to tuberculosis: three had limited or moderate tuberculosis but other gross disease was obviously the cause of death, five had pulmonary tuberculosis with negative sputum and were doing well in this respect, in three the coroner's post-mortem examination reported tuberculosis as a significant contributory factor but not causative of death, and in four no evidence of tuberculosis was found post mortem. Singh & Smith (1957) investigated 224 deaths in Birmingham ascribed to tuberculosis as the primary cause of death. In this group, most deaths were established as due to tuberculosis, but in 18 per cent death was thought to have been hastened by other diseases--carcinoma and tuberculosis in 12, pneumoconiosis, diabetes, chronic bronchitis, mental disorder being the chief remaining factors. The series presented here has shown that for 87 persons whose death certificates mentioned tuberculosis, there was no evidence of active disease or of a contributory effect from formerly active tuberculosis in 28, and that tuberculosis could not be considered a significant factor in tile death in 49. In the Statistical Review of England and Wales in tile year 1956, the Registrar General (1958) referred to a series of cases from a large teaching hospital where the death certificate was issued to the relatives prior to necropsy being carried out; the certificate was found to be correct in only 258 of the 448 cases (57.6 %). This stimulated a larger enquiry, which has been reported by Heasman (1962). Nine thousand five hundred and one necropsies were performed on persons included in the series. This revealed that the assigned cause of death decided before necropsy may need to be changed as a result of that examination in a considerable proportion of cases: this applied to a wide range of causes of death. The clinical and pathological diagnosis agreed in only 45.3 % of cases
CAUSES OF DEATH
235
though in about half of these the difference of opinion was largely a matter of phraseology. Nor does it follow that a clinical opinion on the cause of death which differs fiom that of the pathologist is necessarily erroneous, in this enquiry tuberculosis was the assigned cause of death in 58 cases before necropsy and after necropsy in 95: necropsy was not performed in 25. Thus the apparently simple matter of the certification of death in patients suffering from tuberculosis is liable to a degree of error. One of the principal reasons for this is that a large proportion of deaths occur in older persons: 65 of the 87 in this series were over 55 years of age, and 40 were over 65. In older patients, the presence of other diseases and disabilities is more common. Degenerative diseases of the vessels, heart o1" kidneys, were an important cause of death in this series. So also were acute pulmonary infections such as bronchopneumonia, ill-tolerated by the aged. Carcinoma o f the bronchus frequently provides a difficult diagnostic problem and may not be distinguished from tuberculosis of the lungs without thoracotomy or post-mortem examination. Confusion also arises in this condition when the growth involves a quiescent tuberculous focus, releasing tubercle bacilli which are found in the sputum. Moreover, both active tuberculosis and carcinoma of tlle bronchus may co-exist; while the latter is most likely to be the cause of death, some cases make it difficult to decide what weight to give to the tuberculous element of the chest disease. In the past, the association of tuberculosis with other disease has had strong significance in deciding the cause of death. Death would be ascribed to the tuberculous disease as the primary cause in many such combinations. Now that tuberculosis can be brought under control by chemotherapy with considerable success, even in older patients and in extensive disease, the fact that a dying patient has tuberculosis does not necessarily mean that this disease is a significant factor in the causation of the death. Still less is this true if the tuberculosis is healed or inactive. True relapse of tuberculous disease is not common in those who have received chemotherapy of the right quality and duration. Logan (1953) in discussing death certificates wrote 'Part I! is for the mention of any other conditions that had something to do with the death, but did not by themselves play the major part or enter into the sequence of events directly leading to death, and reported in Part I'. Hence pulmonary tuberculosis need not be mentioned under Part !I merely because there is evidence of some tuberculosis in the lungs--it should have 'sometiling to do with the death'. Thus healed disease need not be quoted unless it has contributed to the death, as when resulting pulmonary fibrosis has led to cardio-respiratory failure (cot pulmonale). If the tuberculous disease is well controlled by drugs, it is probably not a cause of death. Its incidental finding at post-mortem examination need not necessarily be significant for certification--only if the disease played some part in assisting the main cause. As for certification under Part I, the sire.pier the certificate the better, In most cases it should simply read 'pulmonary tuberculosis' whatever the immediate cause (e.g. haemoptysis) which arose out of the tuberculosis. In many patients who die while suffering from tuberculosis it may be difficult to assign the true cause of death. Both the clinical course of the disease and all relevant findings of any investigations undertaken must be considered before coming to a decision. In a considerable proportion, including particularly the aged, other causes than tuberculosis may play an important part, and may be the true or the principal cause of death. ANDERSON,J. P. (1959). Tubercle, Lond., 40, 99.
REFERENCES
BOBROWtIZ, i. D. (1960). Sea View Hosp, Bull., 18, 13, and in N.Y.J. Med., 60, 1581. HEASMAN, M. A. (1962). Proc. roy. Soc. Med., 55, 733. LOGAN, W. P. D. (1953). Brit, reed. J., i, 1272. REGiSTRAR-GENERAL, 1958, Statistical Review of England attd Wales.for 1956, Part 3, p. 182, H.M.S.O., London. SINGH, M. M., & SMITH. J. M. (1957). Tubercle, Lond., 38, 129.
230
THE CAUSES OF DEATH IN P U L M O N A R Y TUBERCULOSIS By F. A. H. S1MMONDS fi'om Clare Hall Hospital, Sottth Mimms, Barnet, Hefts.
SUMMARY Tile data concerning 87 persons dying in hospital and whose death certificates included the words 'pulmonary tuberculosis' were reviewed. A number of certificates appeared to be inaccurate. 49 patients died of other causes, though 21 of these also had active tuberculosis. There was no evidence of active tuberculous disease in 28 persons. Reasons for inaccuracies are considered: an important factor is tile number of deaths in old persons, ill whom degenerative diseases are a frequent cause of death. The presence of inactive, or even active, tuberculosis of the lungs in a dying person may not be a significant factor in causing death. This consideration assumes increased importance in rccent years with the availability of effective treatment for tuberculosis.
During tile five years 1957-1961 inclusive, a diagnosis of pulmonary tuberculosis appeared in the death certificates of 87 patients who died in this hospital. These patients were certified either as having died from tuberculosis, or as having suffered from tuberculosis of the lungs which was a contributory factor to the death. The official death certificate reports the cause of death under two heads: (I) Disease or condition directly leading to death (i.e. disease or injury etc., which caused death and not the mode ofdying). Antecedent causes--morbid conditions, if any, giving rise to the above cause, stating the underlying condition last. (11) Other significant conditions contributhlg to the death, but not related to the disease or condition causing it. Of the 87 certificates, 50 gave tuberculosis as a primary cause of death under Part I; in the others, tuberculosis was described as a factor contributory to death (Part 11). The total number of patients discharged after treatment for pulmonary tuberculosis, and of deaths, in each of these five years were as follows:
Year
Patients discharged Deaths Deaths/discharge (per cent)
1957 508 14 2.8 1958 516 10 1.9 1959 506 18 3"6 1960 597 20 3-5 1961 545 25 4-6 Hence, although the number of patients discharged from the hospital suffering from pulmonary tuberculosis had increased only slightly, the annual number of patients dying nearly doubled. Certificates are usually completed by a member of the junior medical staff, who has in most cases known the patient for some months at least, though a few patients die within a few days or
C A U S E S OF D E A T H
231
TABLE [.--AGE AND SEX OF 87 PATIENTS IN WHOM PULMONARY TUBERCULOSIS WAS CER'HFIED AS A CAUSE OF DEATH
Certified umter Age (years)
Part !*
25-34 35-44 45 -54 55-64 65-74 75 -fi
Part 11"
M.
F.
Total
M.
F.
Total
2 4 5 10 15 4
2 1 2 2 2 1
4 5 7 12 17 5
2 1 12 10 3
2 I 3 2
1 4 1 13 13 5
40
I0
50
30
7
37
* F o r definition see text.
weeks of admission. On the other hand, the certificate often has to be given before the results of the post mortem or other detailed anatomical and histological findings are known, and this may cause some inaccuracy in certification. (The Registrar can be informed of any change in the certificate which needs to be made if new information is obtained). An increasing proportion of patients dying in tuberculosis hospitals die from non-tuberculous causes; according to Bobrowitz (1960), speaking of New York City hospitals, the latter have risen from seven to 40 per cent in twenty years. The case notes were therefore reviewed for further information, including that becoming available after the certificate had been completed. The review of all the available data revealed some inaccuacies in the certificates. Moreover, it became clear that often there were several causes contributing to death; the decision as to the actual cause was sometimes difficult and it could only be classified after the later data were obtained. Of the 87 patients, 70 were men and 17 were women, the age and sex distribution being shown in Table I. Men between 55 and 75 years of age accounted for over half the total deaths. The recorded deaths may be divided into five groups (1) Death clearly due to tuberculosis of the lungs. (2) Death not actually due to tuberculosis, but tuberculosis the original cause leading to the death. (3) Death due to another cause, but tuberculous disease active. (4) Death due to another cause, and the tuberculosis inactive. (5) No evidence of tuberculosis; disease and death due to other cause. The figures for these groups are in Table I I. Post-mortem examination was made on 17 of 51 who died with active tuberculosis, and on 13 of 36 of the remainder. All those reported as showing no evidence of tuberculosis had post mortem examination; on the other hand, this was seldom done where the clinical course of the disease plainly pointed to tuberculosis as the cause. Death Directly Due to Tuberculosis The first group -died of tuberculosis does not require special consideration here. it is worth mentioning that 18 of these 29 patients had bacilli resistant to at least two of the main drugs and that in those with bacilli sensitive to the drugs (or of unknown sensitivity) special unfavourable features like old age, death within a week of admission or mental disorder were prominent.
232
TUBERCLF TABLE l l . - - T n ~ : ROLE OF TUI~IERCULOSIS IN THE DEATH OF 87 PATIENTS IN WHOM IT WAS CERTIFIED AS -~ CAUSE
Certified trader Part I
Died of p u l m o n a r y tuberculosis Death not tuberculous but tuberculosis contributory Tuberculosis a c t i v e ~ n o t contributory Death not tuberculous--tuberculosis inactive No evidence of tubcrculosis
Part II M.
t':
Total
I
I 4 !0 12 3
2 ! 2 I !
3 5 12 13 4
50
30
7
37
M.
F.
18 4 7
8 ~
10
~
10
I
~
40
2
10
I Total 26 4 9
In this group are included three cases in which tuberculosis was certified in Part I!, i.e. only as contributory to death. These were described as dying fiom bronchopneumonia in one case (actually tuberculous bronchopneumonia)" from bronchopneumonia and transverse myelitis of the cord (actually tuberculosis of the spine with involvement of tile cord, tile abscess being connected with a tuberculous apical empyema and a pulmonary cavity)" and from sudden cardiac arrest and hypopotassaemia (actually intrabronchial haemorrhage from a pulmonary tuberculous focus). All three were confirmed by post-mortem examination. Death hTdirectly Due to Tuberculosis in the second group, where tuberculosis was basically important as a factor in the death, the following were the actual immediate causes:-I--pleural haemorrhage after pleuropneumonectomy for gross tuberculosis and empyema.* I -operation for removal of plomb (prolonged sepsis)" the tuberculous disease for which the plomb was originally inserted was soundly healed. 2..... cor pulmonale due to extensive pulmonary tuberculosis of 10 years duration (1"). The five cases certified under Part II were similar: and on the same principle should have been allocated to Part I. !. bronchopneumonia after pleuropneumonectomy for tuberculosis bilateral pulmonary tuberculosis active.* I pericarditis and generalized staphyioccal infection after pneumonectomy for active tuberculosis; previous thoracoplasty and plombage.* 1 pneumonia and cardiac failure following prolonged sepsis resulting from operation for tuberculosis 15 years before; tuberculosis healed. I 'cirrhosis of liver'; actually congestion of the liver due to cot pulmona]e secondary to active tuberculosis.* I bronchopneumonia, bronchitis and e m p h y s e m a extensive pulmonary tuberculosis, healed, with fibrosis and thoracoplasty nine years earlier (age 40).* This last case raised the difficulty of assessing whether, in a patient dying of cor pulmonale or respiratory failure who has also had tuberculosis, the latter is a factor in death. If the patient was young (under 50) and there was gross fibrosis the death is included in the group above. Where, however, the patient seemed to suffer primarily with typical chronic bronchitis and emphysema, the tuberculous disease appearing insufficient to cause death, the latter has been included as non* Indicates post-mortem examination.
CAUSES OF D E A T H
233
tuberculous. As a result of chemotherapy in patients with extensive disease, the healing of tuberculosis may result in much fibrosis with clean cystic cavity formation, and with emphysema, so that such cases are frequently seen. Five patients in the second group died after severe surgical operations designed to relieve conditions which resulted from the failure of medical treatment applied several years earlier, in some cases prior to chemotherapy, and in others during the period of inadequate treatment of this type.
Death Not Due to Tuberculosis The third group where the tuberculosis was active but death was not due to tuberculosis include tile following causes: Certified under Part 11 (12 cases) Cert![ied under Part I (nine cases) Carcinoma of bronchus five cases (2*). Myocardial failure: cot pulmonale three cases (1"). Carcinoma larynx: mediastinitis.* Acute bronchopneumonia: chronic bronchitis and Primary carcinoma liver.* emphysema. Arteriosclerosis and congestive cardiac Staphylococcal pneumonia*. failure. Repeated spontaneous pneumothorax. Repeated coronary infarction.* Hypertension and arteriosclerosis. Acute pyelonephritis with abcesses: ParkinRenal failure. sonism. Gangrene of leg: infected pulmonary infarct: Chronic nephritis: uraemia. arteriosclerosis. Chronic bronchitis and emphysema: cor pulmonale. These diseases provided sufficient explanation of the deaths which occurred. The concurrent tuberculous disease was incidental to the fatality, being insufficient to cause death: it was in some cases well controlled by chemotherapy and in the others of limited extent and activity. In the fourth group, death due to other causes, tuberculosis inactive, there were: Certified under Part 1 (10 cases) Certified under Part II (13 cases) 6---cor pulmonale, chronic bronchitis and emphy(the causes are not significant for the present sema (ages 80, 73, 72, 68, 63, 50). discussion.) l wbronchopneumonia. 1 staphylococcal bronchopneumonia. 1 -multiple lung abcesses* ! carcinoma of bronchus.* In the fifth group, with no evidence of tuberculosis there were: Certified under Part I Certified under Part II Reticulo-zarcoma with adrenal failure. 3 carcinoma of bronchus. 1 .volvulus and staphylococcal enteritis. All in this group were examined post-mortem. Tile patient dying of volvulus and enteritis also had nephritis and arthritis. Two years before she had had treatment in Clare Hall Hospital for tuberculosis of the left lung with Myco. tuberculosis in the sputum. Complete radiographic and bacteriological clearance was obtained. At post-mortem, no evidence of tuberculous disease was found, except a little localized bronchiectasis in the left lung, the right being free of disease. In one patient with carcinoma the evidence suggesting tuberculosis was a cavity, which proved to be a large emphysematous cyst. In another, there was no evidence of tuberculosis post-mortem, but in life tubercle bacilli had been found on one occasion, obviously an incidental erroneous finding. To summarise the findings in the five groups, of 50 patients certified under Part I as having died from pulmonary tuberculosis, 20 were found to have died of other causes, though nine of these had active tuberculosis at the time of death. On the other hand, in 37 certified under Part II, tuberculosis might well have been recorded as the prime cause in eight, while in 18 no evidence of active tuberculous disease was present at death. Of the total 87, 28 patients (32 ~ ) died without evidence of active tuberculous disease.
234
TUBERCLE
Activity o/" the Tuberculous Disease Tubercle bacilli were found at some time in all but six of the patients. However, the finding of tubercle bacilli even within the twelve months before death is not necessarily evidence that the death was due to pulmonary tuberculosis, even less so if the discovery of the bacilli last occurred several years before. In a few patients chemotherapy had rendered the sputum negative and the disease was under control at death, which was due to another cause. Furthermore, there was doubt about the significance of the finding of tubercle bacilli in one patient who clearly died of carcinoma of the bronchus, tubercle bacilli had been reported only once, and that within the last year. Of the six patients, three had no evidence of pulmonary tuberculosis post-mortem and three showed evidence of well healed disease. Only one was reported under Category l and this man actually died of reticulo-sarcoma. Some attempt at estimating the duration of tuberculous disease was made, judging from the recorded history. Tile greater proportion had tuberculous disease for many years, one-third of those in whom estimates could be made having had tuberculosis for over ten years. In the others, either the duration was unknown, or disease was first discovered at post mortem examination, or there was no post mortem evidence of tuberculosis. Treatment by Chemotherapy had been employed in rather more than half the patients, but only in 14 had the duration ofchemotherapy been 12 months or more. The tubercle bacilli present were resistant to streptomycin and isoniazid in 28 % of the patients; in 51%, the bacilli were sensitive to streptomycin, PAS and isoniazid.
Association With Carcinoma qf the Bronchus There were six patients with carcinoma of the bronchus associated with active or inactive tuberculosis, and three patients with carcinoma of the bronchus but no evidence of pulmonary tuberculosis. Thus, combined carcinoma and tuberculosis occurred in 6 (7.3 %) out of 82 deaths with which tuberculosis was associated.
Discussion Anderson (1959) examined the circumstances of 56 deaths in Leicester, reported as due to pulmonary tuberculosis. Of these, ! 5 (27 %) were found to be due to other causes and not primarily to tuberculosis: three had limited or moderate tuberculosis but other gross disease was obviously the cause of death, five had pulmonary tuberculosis with negative sputum and were doing well in this respect, in three the coroner's post-mortem examination reported tuberculosis as a significant contributory factor but not causative of death, and in four no evidence of tuberculosis was found post mortem. Singh & Smith (1957) investigated 224 deaths in Birmingham ascribed to tuberculosis as the primary cause of death. In this group, most deaths were established as due to tuberculosis, but in 18 per cent death was thought to have been hastened by other diseases--carcinoma and tuberculosis in 12, pneumoconiosis, diabetes, chronic bronchitis, mental disorder being the chief remaining factors. The series presented here has shown that for 87 persons whose death certificates mentioned tuberculosis, there was no evidence of active disease or of a contributory effect from formerly active tuberculosis in 28, and that tuberculosis could not be considered a significant factor in tile death in 49. In the Statistical Review of England and Wales in tile year 1956, the Registrar General (1958) referred to a series of cases from a large teaching hospital where the death certificate was issued to the relatives prior to necropsy being carried out; the certificate was found to be correct in only 258 of the 448 cases (57.6 %). This stimulated a larger enquiry, which has been reported by Heasman (1962). Nine thousand five hundred and one necropsies were performed on persons included in the series. This revealed that the assigned cause of death decided before necropsy may need to be changed as a result of that examination in a considerable proportion of cases: this applied to a wide range of causes of death. The clinical and pathological diagnosis agreed in only 45.3 % of cases
CAUSES OF DEATH
235
though in about half of these the difference of opinion was largely a matter of phraseology. Nor does it follow that a clinical opinion on the cause of death which differs fiom that of the pathologist is necessarily erroneous, in this enquiry tuberculosis was the assigned cause of death in 58 cases before necropsy and after necropsy in 95: necropsy was not performed in 25. Thus the apparently simple matter of the certification of death in patients suffering from tuberculosis is liable to a degree of error. One of the principal reasons for this is that a large proportion of deaths occur in older persons: 65 of the 87 in this series were over 55 years of age, and 40 were over 65. In older patients, the presence of other diseases and disabilities is more common. Degenerative diseases of the vessels, heart o1" kidneys, were an important cause of death in this series. So also were acute pulmonary infections such as bronchopneumonia, ill-tolerated by the aged. Carcinoma o f the bronchus frequently provides a difficult diagnostic problem and may not be distinguished from tuberculosis of the lungs without thoracotomy or post-mortem examination. Confusion also arises in this condition when the growth involves a quiescent tuberculous focus, releasing tubercle bacilli which are found in the sputum. Moreover, both active tuberculosis and carcinoma of tlle bronchus may co-exist; while the latter is most likely to be the cause of death, some cases make it difficult to decide what weight to give to the tuberculous element of the chest disease. In the past, the association of tuberculosis with other disease has had strong significance in deciding the cause of death. Death would be ascribed to the tuberculous disease as the primary cause in many such combinations. Now that tuberculosis can be brought under control by chemotherapy with considerable success, even in older patients and in extensive disease, the fact that a dying patient has tuberculosis does not necessarily mean that this disease is a significant factor in the causation of the death. Still less is this true if the tuberculosis is healed or inactive. True relapse of tuberculous disease is not common in those who have received chemotherapy of the right quality and duration. Logan (1953) in discussing death certificates wrote 'Part I! is for the mention of any other conditions that had something to do with the death, but did not by themselves play the major part or enter into the sequence of events directly leading to death, and reported in Part I'. Hence pulmonary tuberculosis need not be mentioned under Part !I merely because there is evidence of some tuberculosis in the lungs--it should have 'sometiling to do with the death'. Thus healed disease need not be quoted unless it has contributed to the death, as when resulting pulmonary fibrosis has led to cardio-respiratory failure (cot pulmonale). If the tuberculous disease is well controlled by drugs, it is probably not a cause of death. Its incidental finding at post-mortem examination need not necessarily be significant for certification--only if the disease played some part in assisting the main cause. As for certification under Part I, the sire.pier the certificate the better, In most cases it should simply read 'pulmonary tuberculosis' whatever the immediate cause (e.g. haemoptysis) which arose out of the tuberculosis. In many patients who die while suffering from tuberculosis it may be difficult to assign the true cause of death. Both the clinical course of the disease and all relevant findings of any investigations undertaken must be considered before coming to a decision. In a considerable proportion, including particularly the aged, other causes than tuberculosis may play an important part, and may be the true or the principal cause of death. ANDERSON,J. P. (1959). Tubercle, Lond., 40, 99.
REFERENCES
BOBROWtIZ, i. D. (1960). Sea View Hosp, Bull., 18, 13, and in N.Y.J. Med., 60, 1581. HEASMAN, M. A. (1962). Proc. roy. Soc. Med., 55, 733. LOGAN, W. P. D. (1953). Brit, reed. J., i, 1272. REGiSTRAR-GENERAL, 1958, Statistical Review of England attd Wales.for 1956, Part 3, p. 182, H.M.S.O., London. SINGH, M. M., & SMITH. J. M. (1957). Tubercle, Lond., 38, 129.