Title

Author(s)

Subtle presentation of cryptic tuberculosis in the elderly

Tsui, Sui-na;

Citation

Issued Date

URL

Rights

2011

http://hdl.handle.net/10722/144855

Creative Commons: Attribution 3.0 Hong Kong License

Subtle presentation of cryptic tuberculosis in the elderly

By

Dr TSUI Sui Na

This work is submitted to

Faculty of Medicine of The University of Hong Kong
In partial fulfillment of the requirements for
The Postgraduate Diploma in Infectious Diseases, PDipID (HK)

Date: 20 August 2011

Supervisor: Professor KY Yuen

Declaration

I, Tsui Sui Na, declare that this dissertation represents my own work and that it has not
been submitted to this or other institution in application for a degree, diploma or any
other qualifications.
I, Tsui Sui Na also declare that I have read and understand the guideline on What is
plagiarism? published by The University of Hong Kong (available at
http://www.hku.hk/plagiarism/) and that all parts of this work complies with the
guideline.

Candidate: Tsui Sui Na

Signature:
Date:

Acknowledgement
I would like to express my sincere thanks to Professor KY Yuen for his valuable
advices and guidance, and to all staff of the Department of Microbiology for the
fruitful teaching throughout this course.

Abstract
Background Tuberculosis in the elderly in an increasing problem globally due to
increasing longevity. Presentation of tuberculosis in the elderly may be atypical and
subtle resulting in delay in diagnosis and treatment, and spread of the disease. It is
important to identify any special features of tuberculosis in the elderly in order to
facilitate management.
Objective To study the characteristics of the very old-aged patients with tuberculosis,
including their clinical presentation, radiological and laboratory features, adverse drug
reactions, and treatment outcomes.
Method Patients aged 85 and above with culture confirmed tuberculosis admitted to a
chest hospital from January 2008 to December 2009 were studied. Data was retrieved
from the hospital microbiology database. Patients characteristics, presenting
symptoms,

radiological

features,

laboratory

results,

adverse

reactions

to

anti-tuberculous drugs and treatment outcomes were analyzed.

Results 41 patients with culture-confirmed tuberculosis were included in the study.
Their mean age was 89.7 +/- 3.6 years old. 14 (34.1%) of them were nursing home
residents and most of them had co-morbidities. 33 patients had pulmonary
tuberculosis, 7 patients had TB pleuritis and 1 patient had TB lymphadenitis. Around
half of the diagnoses were made by positive culture of acid-fast bacilli (48.8%) while

one-third were diagnosed by positive smear results (31.7%). The most common
symptoms were cough and/or sputum (48.8%) and dyspnoea (51.2%). Around
one-fifth of patients (19.5%) did not have any symptoms. The typical upper zone
involvement on chest X-ray was only seen in 12 patients (29.3%). One-third of
patients (34.1%) had bilateral involvement. Normal white cell count, low lymphocyte
count, high ESR and low serum albumin were common. Treatment was not started in
6 patients (14.6%) as the culture results were only available after the death of the
patients. In the remaining 35 patients with treatment started, 17 expired before
completion of treatment.
Conclusion Presentation of tuberculosis in the elderly is variable. The radiological
features can be atypical but there may be clues from the laboratory tests. Delay in
diagnosis and treatment is common. It is important to keep a high index of suspicion
of tuberculosis in the elderly to avoid delay in diagnosis and treatment and to prevent
spread of infection.

Background
Tuberculosis (TB) is an airborne infectious disease caused by the bacteria
Mycobacterium tuberculosis. It can affect people of any age and involve any site in
the body, with pulmonary TB being the most common. Being infected does not equal
to having the disease. The risk of developing active tuberculosis after being infected
depends on many factors, both genetic and environmental (1). If left untreated, each
person with active TB can infect on average 10 to 15 people a year (2). And one in
every 10 people being infected will develop active TB in his or her lifetime (2).
TB is still a major infectious disease worldwide. According to the World Health
Organization, the incidence rates of TB are falling globally. There were 9.4 million
new tuberculosis cases globally in 2009 (including 1.1 million cases among people
with HIV) and the incidence rate was 137 cases per 100,000 population. The mortality
rates at global level have fallen by 35% between 1990 and 2009, and the number of
deaths is also declining. There were 1.7 million people died from TB in 2009 (equal
to 4700 deaths a day), including 380,000 people with HIV. The vast majority of TB
deaths are in the developing world, with more than half occurring in Asia (2).
The notification rate of tuberculosis in Hong Kong has decreased over the years
from the peak of 697/100,000 population (14,831 cases) in 1952 to 72/100,000
population (5,132 cases) in 2010. The death rate has also largely decreased from

36/100,000 population (1,436 cases) in 1970 to 2.7/100,000 population (187 cases) in

2010. With aging of the population, around 40% of the TB patients are aged 65 or
above. In particular, the notification rate and the death rate are highest in the age
group of 85 and above, which are 382/100,000 population and 51/100,000 population
in 2010 respectively (3). This likely reflects both the high TB burden in the past and
the declining immunity and increasing co-morbidities with age, which result in
reactivation of TB in the elderly (4, 5).
As the life expectancy of the population in Hong Kong has increased, it is
expected to see more and more elderly with TB (5). The very old-aged may be in
dependent state and non-communicable, which results in delay in symptom
recognition and delay in seeking early medical care. When they present, the disease
may already be advanced. On the other hand, their presentation may be atypical and
subtle (6), which results in delay in diagnosis and treatment, and may cause spread of
the infection. Therefore, it is important to be familiar with TB in the elderly so that
early diagnosis and timely treatment could be achieved, in order to reduce morbidity
and mortality and to reduce transmission in the community.
The notification rate and the death rate of TB in Hong Kong have remained
highest in the age group of 85 and above in recent years (3) but there is lack of review
in this group of very old-aged patients.

Subjects and Method

This is a retrospective review of patients aged 85 and above with
culture-confirmed tuberculosis admitted to Haven of Hope Hospital from January
2008 to December 2009. Data was retrieved from the hospital microbiology database.
Patients characteristics, presenting symptoms, radiological features, laboratory results,
adverse reactions to anti-tuberculous drugs and treatment outcomes were analyzed.
Results
Patient characteristics and Co-morbidities (Table 1)
From the year 2008 to 2009, there were a total of 61 patients aged 85 and above
with positive growth of acid-fast bacilli (AFB) on culture from all specimens. 45 AFB
culture grew Mycobacterium tuberculosis while 16 grew Mycobacterium other than
tuberculosis. 4 patients records were unable to be retrieved and the records of the
remaining 41 patients with culture-confirmed tuberculosis were retrieved and
analyzed. Their age ranged from 85 to 99 years old and the mean age was 89.7 +/- 3.6
years old. 24 (58.5%) were male patients and 17 (41.5%) were female patients. 14
(34.1%) of them were nursing home residents and 15 (36.6%) of them were
documented as bed-ridden or in dependent state.
Most of the patients had co-morbidities, including diabetes mellitus,
cardiovascular diseases (including hypertension, ischaemic heart disease, congestive

heart failure and cerebrovascular accident), chronic lung diseases, renal diseases and
malignancy. 10 patients (24.4%) were documented to have dementia. No patient had
hepatitis B or C or HIV.

Table 1. Patient characteristics

Number ( % )
Age (mean +/- SD)

89.7 +/- 3.6 (85 99)

Gender
Male

24 (58.5%)

Female

17 (41.5%)

Nursing home residents

14 (34.1%)

Dependent state

15 (36.6%)

Co-morbidities
Diabetes mellitus

8 (19.5%)

Cardiovascular diseases

26 (63.4%)

Chronic lung diseases

14 (34.1%)

Renal diseases

4 (9.8%)

Malignancy

9 (22%)

Dementia

10 (24.4%)

Diagnostic methods (Table 2)

Thirty-three patients had pulmonary tuberculosis while eight patients had
extra-pulmonary tuberculosis, including seven TB pleuritis and one TB lymphadenitis.
Only one patient had TB contact and only one had history of old TB. Around half of
the diagnoses were made by positive AFB culture (48.8%) while one-third were
diagnosed by positive smear results (31.7%). One was diagnosed by trans-bronchial
biopsy and was confirmed by culture of broncho-alveolar lavage later. Four diagnoses
were obtained histologically from pleural biopsy and later confirmed by positive
9

culture from sputum or pleural fluid. One was by pleural fluid culture. The TB
lymphadenitis was diagnosed by AFB smear from fine needle aspiration of the
cervical lymph node. In one patient, treatment was started empirically in view of
clinical and radiological features and later confirmed by sputum culture.

Table 2. Diagnostic methods

Number ( % )
Pulmonary TB

33 (80.5%)

Extra-pulmonary TB
TB pleuritis

7 (17.1%)

TB lymphadenitis

1 (2.4%)

Diagnostic methods
Sputum AFB smear +

13 (31.7%)

Sputum AFB culture +

17 (41.5%)

Broncho-alveolar lavage culture +

3 (7.3%)

Trans-bronchial biopsy

1 (2.4%)

Pleural biopsy

4 (9.8%)

Pleural fluid culture

1 (2.4%)

Fine needle aspiration cytology

1 (2.4%)

Clinical and radiological features

1 (2.4%)

Symptoms and Initial admission diagnosis (Table 3)

The most common symptoms were cough and/or sputum (48.8%) and dyspnoea
(51.2%). Only one patient complained of chest pain and none presented with
haemoptysis. 39% of patient had fever. Anorexia (22%) and weakness (24.4%) were
also common. The duration of symptoms ranged from a few days to upto 6 months.
However, around one-fifth of patients (19.5%) did not have any respiratory or general
symptoms, and they were admitted for diagnosis not related to TB initially.
10

For the initial admission diagnosis, only 6 patients (14.6%) were diagnosed as
TB. 10 patients (24.4%) were diagnosed as pneumonia which was the most common
diagnosis, followed by acute exacerbation of chronic obstructive pulmonary disease
(COPD) in 7 patients (17.1%) and pleural effusion in 6 patients (14.6%). 4 patients
(9.8%) were referred from chest clinic for investigation of lung shadow or lung
infiltrate. A significant proportion of patients (19.5%) were admitted for diagnosis not
related to the chest, including fall, dehydration, anaemia, congestive heart failure, etc.
12 out of 41 patients (29.3%) had 1-2 admissions in the previous 3 months for
chest-related condition including pneumonia, COPD, sputum retention, fever, etc.
Table 3. Symptoms and Initial admission diagnosis
Number ( % )
Respiratory symptoms
Cough and/or sputum

20 (48.8%)

Dyspnoea

21 (51.2%)

Chest pain

1 (2.4%)

General symptoms
Fever

16 (39%)

Weight loss

4 (9.8%)

Anorexia

9 (22%)

Weakness

10 (24.4%)

No symptoms

8 (19.5%)

Initial admission diagnosis

Tuberculosis

6 (14.6%)

Pneumonia

10 (24.4%)

COPD exacerbation

7 (17.1%)

Pleural effusion

6 (14.6%)

Lung shadow or infiltrate

4 (9.8%)

Others

8 (19.5%)

Admission in previous 3 months

12 (29.3%)
11

Radiological and Laboratory features (Table 4)

The chest X-ray showed the typical upper zone involvement in 12 patients
(29.3%). 8 patients (19.5%) had lower zone involvement and 11 patients (26.8%) had
both upper and lower zone involvement, together they accounted for nearly half of the
cases (46.3%). Pleural effusion was seen on chest X-ray in 7 patients (17.1%).
Mass-like lesions were seen in 2 patients (4.9%) and miliary shadows in another 2
patients (4.9%). One-third of the patients (34.1%) had bilateral involvement which
reflected extensive and advanced disease. One patient who had left pleural effusion as
well as a right upper zone nodule, was diagnosed to have concomitant TB pleuritis
and carcinoma of the lung.
The mean white cell count was 9.4 +/- 5.3 x10*9/L and around 60% of patients
had normal white cell count. The mean lymphocyte count was 0.9 +/- 0.5 x10*9/L and
70% of patients had low lymphocyte count. The mean ESR was 79.0 +/- 40.1mm/hr
and 65% of patients had raised ESR over 50mm/hr. The mean haemoglobin level was
11.0 +/- 2.0g/dL and 34.1% of patients had haemoglobin level less than 10g/dL. The
mean serum albumin level was 30.2 +/- 5.9g/L and it was low in 70% of patients and
70% of patients had reversed albumin / globulin level. One of the patients had
significant reversed albumin/globulin level was diagnosed as having concomitant
multiple myeloma.

12

Table 4. Radiological and Laboratory features

Number ( % )
Radiological findings
Upper zone

12 (29.3%)

Lower zone

8 (19.5%)

Upper and lower zones

11 (26.8%)

Pleural effusion

6 (14.6%)

Mass-like

2 (4.9%)

Miliary shadows

2 (4.9%)

Bilateral

14 (34.1%)
Mean +/- SD

Laboratory findings
Total white cell count (x10*9/L)
Normal (3.5 8.5)
Lymphocyte count (x10*9/L)
Low (below 1.3)
ESR (mm/hr)
High >50mmHg
Haemoglobin (g/dL)
Low <10g/dL
Serum albumin (g/L)
Low (below 35g/dL)
Reversed albumin/globulin ratio (no.)

9.4 +/- 5.3

58.5%
0.9 +/- 0.5
71.1%
79.0 +/- 40.1
65.2%
11.0 +/- 2.0
34.1%
30.2 +/- 5.9
73.2%
29 (70.7%)

Adverse drug reactions and Treatment outcomes (Table 5)

Treatment was not started in 6 patients (14.6%) as the culture results were only
available after the patients expired. In the remaining 35 patients with treatment started,
17 of them (48.6%) completed treatment. Total 25 patients (61.0%) expired including
6 without treatment, 17 before completion of treatment and 2 with treatment
completed. 16 patients still survive during the time of this review and 15 of them have
completed treatment while one with miliary TB is still on treatment.

13

For adverse drug reactions, hepatitis was the most common and was seen in 5
patients (14.3%), followed by gastrointestinal upset with poor feeding in 4 patients
(11.4%). 3 patients (8.6%) had allergic reaction with skin rash. 2 patients had
interstitial nephritis with renal impairment. 1 patient had thrombocytopenia and 1
patient developed drug fever after treatment.

Table 5. Adverse drug reactions and Treatment outcomes

Number ( % )
Treatment outcomes
Treatment not started

6/41 (14.6%)

Completed treatment

17/35 (48.6%)

Expired (total)

25/41 (61.0%)

Expired before treatment completed

17/35 (48.6%)

Adverse drug reactions (number = 35)

Hepatitis

5 (14.3%)

Gastrointestinal upset

4 (11.4%)

Skin rash

3 (8.6%)

Renal impairment

2 (5.7%)

Thrombocytopenia

1 (2.9%)

Drug fever

1 (2.9%)

Table 6 showed the characteristics of the six patients whose culture results were
only available after the patients expired. Their age ranged from 85-95 years old with
2-3 co-morbidities in each patient. They were admitted for different diagnoses and
two of them were admitted for fall initially. The chest X-ray showed variable
involvement with two showing the typical upper zone involvement. The white cell
count was high in 3 patients and normal in 3 patients. The lymphocyte count was low

14

in 4 patients and normal in 2 patients. ESR was only checked in two patients and was
both high. Three had haemoglobin level below 10g/dL. Three had hypoalbuminaemia
while five had reversed albumin/globulin level. There was no single feature that was
consistent in all the six cases and the presentation was variable which made early
diagnosis of TB difficult.

Table 6. Characteristics of 6 patients who expired before diagnosis of TB

Patient

Age

Co-morbidities

Admission

CXR

WCC

Lym

ESR

Hb

Alb

Glo

Upper and

34.8

1.1

109

8.9

36

40

2.7

0.4

N/A

11.9

28

70

7.7

1.7

N/A

12.8

28

37

Upper

9.3

0.4

N/A

10.8

37

35

diagnosis
1

85

88

90

DM

Pneumonia

IHD

lower

Renal impairment

Bilateral

HT

Left pleural

Left pleural

Myeloma

effusion

effusion

CVA

Lung

Upper and

Lung cancer

cancer

lower
Bilateral

92

95

HT

COPD

COPD

exacerbation

HT

Fall

Lower

19.2

2.1

N/A

8.9

20

33

HT

Fall

Upper

10.9

0.6

99

6.7

35

40

IHD

Pneumonia

CHF
6

95

Renal impairment

DM diabetes mellitus

CXR chest x-ray

IHD ischaemic heart disease

WCC white cell count

HT hypertension

Lym lymphocyte count

CVA cerebrovascular accident

Hb haemoglobin level

COPD chronic obstructive pulmonary disease

Alb albumin

CHF congestive heart failure

Glo - globulin

15

Discussion
Tuberculosis (TB) in the elderly is not just a local problem but an increasing
problem worldwide (1), especially in developed countries with increasing longevity (5,
7). Reactivation of TB is considered to be the most important risk factor for
developing active TB in the elderly due to reduced cellular immunity with aging (4).
In developing countries, elderly suffer from poverty, malnutrition and difficult access
to medical care, which are also risk factors for developing TB (4).
This review focused on the oldest age group patients whom had the highest
incidence and mortality of TB. The mean age was 89.7 years old and one-third of
them were nursing home residents. The increased number of elderly in nursing homes
in Hong Kong can be another reason for the increased rate of TB in the elderly (5). A
local study conducted on 587 nursing home residents demonstrated a relatively high
rate of positive tuberculin reaction (43.8%) among the residents (8). The estimated
rates of active TB in the nursing homes in Hong Kong ranged from 1,200/100,000 to
2,600/100,000 population (8). Although reactivation accounts for the majority cases
of TB in the elderly, recent infection due to transmission in nursing homes has been
reported in previous study (9).
Old age has been found to be a risk factor for diagnostic delay (10). And such
delay increases the risk of TB transmission within the community, and may result in

16

outbreaks in nursing homes (11). In this review, 6 out of 41 patients (14.6%) did not
received anti-tuberculous treatment as the diagnosis of TB was only known after they
had expired. And 12 patients (29.3%) had admission in the previous 3 months for
respiratory symptoms but the diagnosis of TB could not be made. This reflected that a
timely diagnosis of TB could not be achieved in a considerable number of patients.
During the period before the diagnosis was made, infection could be spread in the
community or in the nursing homes.
Sputum smear microscopy is a powerful test for diagnosis of TB (12). However,
in the elderly, it is not always possible to obtain sputum for investigation as some
patients may not have sputum production. And elderly patients with cognitive
impairment or in dependent state could not produce good quality sputum. In this
review, only one-third of the diagnoses were made by positive smear results (31.7%)
while around half were made by positive AFB culture (48.8%). For cases that were
diagnosed with positive AFB culture, again there was a period of diagnostic delay
with risk of TB transmission.
Bronchoscopy has been reported to be useful in the diagnosis of TB (13). It is
useful in elderly patients who are suspected to have TB but are unable to produce
sputum or in patients with repeatedly negative AFB smear results (13). For our
patients, four underwent bronchoscopy. Two of them presented with lung shadow on

17

chest x-ray and the initial diagnosis was lung tumour rather than TB. Diagnosis of TB
was obtained from culture of broncho-alveolar lavage or trans-bronchial biopsy.
Many studies have reported that elderly with TB present with atypical symptoms
or radiological features, which make early diagnosis difficult (14, 15, 16).

Some

studies have reported that elderly patients presented more frequently with systemic
symptoms and less frequently with respiratory symptoms (14, 16). For our patients,
the most common symptoms were cough and/or sputum (48.8%) and dyspnoea
(51.2%). However, a significant proportion of patients presented with systemic
symptoms only without respiratory symptoms and 8 patients (19.5%) even had no
related symptoms and were admitted for other diagnosis. It is therefore important to
keep a high index of suspicion even the symptoms may not be typical.
Some studies have reported no differences in radiological features among young
and old patients (17, 18) while others have reported more middle and lower zone
involvement in the elderly (15, 19). In this review, the typical upper zone involvement
was only seen in 12 patients (29.3%) while 8 patients (19.5%) had lower zone
involvement. 11 patients (26.8%) had both upper and lower zone involvement and
one-third of patients (34.1%) had bilateral involvement, which reflected extensive and
advanced disease already when they presented. Therefore, it is important to consider
TB as a differential diagnosis even when the chest x-ray appearance is not typical.

18

Normal white cell count, low lymphocyte count, high ESR, low serum albumin
level and reversed albumin/globulin level were common in patients with TB in this
review. They were present in 60% to 70% of patients. When these abnormal
laboratory results are noted, further or more aggressive investigations may be
warranted to achieve an early diagnosis of TB.
Most of the elderly patients had co-morbidities which may be confused with the
presentation of TB, especially in patients with chronic lung diseases. For the initial
admission diagnosis, a significant number of patients (17.1%) were diagnosed as
having acute exacerbation of chronic obstructive pulmonary disease. Only 6 patients
(14.6%) were diagnosed as TB initially while pneumonia was the most common
initial diagnosis (24.4%). Diagnosis of TB was only known after the culture results
came back which was usually over 1 month after admission.
Elderly patients were more likely to have adverse reactions to anti-tuberculous
drugs (6, 20). The treatment success rate was lower and the mortality rate was higher
(21, 22). Similar to other studies, the most common adverse reaction was
drug-induced hepatotoxicity (14.3%) in this review. Gastrointestinal upset (11.4%)
and skin reactions (8.6%) were also common. Total 25 patients (61.0%) expired at the
time of this review, including 6 without treatment, 17 before completion of treatment
and 2 with treatment completed. Some of the deaths were related to TB while some

19

were not. Due to the advanced age and co-morbidities, the cause of death could be
multi-factorial. But overall the mortality was high.
This review had a number of limitations. First, the number of patients was too
small and so the results might not be generalized or representative. And there was no
comparison with younger patients to compare the differences in presentation and
investigation between young and old patients, the rate of adverse drug reactions and
the mortality. Moreover, only patients with culture-confirmed tuberculosis were
included but there was a significant proportion of tuberculosis that was diagnosed
histologically, for example from trans-bronchial biopsy and pleural biopsy, which may
not have microbiological confirmation. The presentation of these patients might be
more subtle or atypical, which makes diagnosis even more difficult.

20

Conclusion
Tuberculosis in the elderly is an important problem in Hong Kong. With
increasing life expectancy, the rate of tuberculosis in the very old-aged is expected to
remain high. However, presentation of tuberculosis in this age group is often atypical
and subtle, which make early diagnosis difficult with risk of transmission in the
community or in the nursing homes. Early awareness of suspicious symptoms is
important. Radiological involvement may not be typical and is often extensive.
Diagnosis needs to be confirmed microbiologically but clues can be obtained from
laboratory tests that prompt early investigation. Health care workers should be
familiar with tuberculosis in the elderly and keep a high index of suspicious to avoid
delay in diagnosis and treatment and to prevent spread of infection.

21

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