Sustained intra- and interjurisdictional transmission of tuberculosis within a mobile, multi-ethnic social network: lessons for tuberculosis elimination.
Aspler, Anne ; Chong, Huey ; Kunimoto, Dennis 等
The World Health Organization Global Plan to Stop TB: 2006-2015
aims to halve by 2015 the prevalence of TB reported in 1990. (1)
Consistent with this goal, the Canadian Tuberculosis Committee of the
Public Health Agency of Canada set a target Canadian TB incidence rate
of 3.6 per 100,000 persons (one-half the incidence rate in Canada in
1990) for 2015.2 So far, the achievement of this goal has been hampered
by sustained high rates of TB in Aboriginal peoples and the
foreign-born. Strategies aimed at eliminating TB focus on interrupting
transmission and preventing TB in persons already infected. (2)
This study is focused on the Canadian-born and describes in detail
and places into context a complex cluster (chain of transmission) of TB
cases in Alberta. Further, it uses the exercise to inform TB elimination
strategy. A cluster of TB cases is one whose causative isolates of
Mycobacterium tuberculosis share a common DNA fingerprint, suggesting a
transmission link between them. (3) In instances where housing is
unstable and patients may not know the names and locations of contacts,
studies that incorporate DNA fingerprinting of isolates have provided
insight into spatial and temporal patterns of transmission as well as
factors that might contribute to rapid progression of disease. (4-8) In
addition to DNA fingerprint data, contact tracing, mobility and
socio-economic data were used to further describe the chain of
transmission and interpret its implications for TB elimination.
METHODS
This study was performed in Alberta, a province of Western Canada
having a population of 2.94 million in 2001 (Statistics Canada) and
where the majority of First Nations (66%) are living on-reserve (Indian
and Northern Affairs Canada, 2001). In Alberta, initial isolates of M.
tuberculosis are DNA fingerprinted in the Provincial Laboratory for
Public Health using restriction fragment-length polymorphism (RFLP)
supplemented by spoligotyping as necessary. (9,10) Over the 17-year
period 1991-2007, all large clusters defined as those having 15 or more
case-patients--were identified and described according to the age, sex,
population group (Aboriginal [First Nations, Metis, Inuit],
Canadian-born non-Aboriginal and foreign-born) and place of residence
(on-reserve or off-reserve) of their constituent members. One large
cluster was selected for study. To assess the inter-jurisdictional
spread of this cluster strain, it was compared to all isolates from the
Northwest Territories (NWT) in 1993-2001 (n=122) and all isolates from
British Columbia (BC), Saskatchewan and Manitoba in 1995-1997 (n=944).
(11)
Case and contact analysis
Public health and hospital records of cluster cases were reviewed
retrospectively. Cases were described according to age, sex, population
group, date of diagnosis (the start date of treatment), place of
residence at diagnosis (city borough, reserve community), disease site
(pulmonary or extra-pulmonary), sputum smear status (positive or
negative), chest radiograph status (cavitary or non-cavitary), risk
factors for reactivation and outcome. (2) Epidemiologic links, defined
as likely exposure to another case of TB within the cluster within 2
years of diagnosis, were categorized as 'Type 1': clear
epidemiologic links confirmed at the time of diagnosis by traditional
contact tracing or review of case records or 'Type 2': unclear
epidemiologic links, connection based on place of residence at
diagnosis, molecular genotyping and diagnosis date within 2 years of
another case in the cluster. Results are presented in diagrammatic
format to maintain the anonymity of cases and communities.
Contact summary reports for each case were reviewed to identify
potential linkages within the cluster (contact tracing had been
performed by public health nurses in accordance with the recommendations
of the Canadian Tuberculosis Standards).2 Data extracted from contact
tracing included total number of contacts, the nature of their
association to the source case (close, casual, or other) and
geographical location. Contacts were assigned to one of 17 geographical
locations based on residence and Regional Health Authority (RHA)
divisions used in the province up until 2003. Locations of contacts were
tabulated by patient, and average distances of contact locations from
source locations were calculated, based on residence at diagnosis.
Mobility analysis
Three indicators were used to assess the mobility of cases: 1)
documented out-of-province travel or change of address during treatment
for active TB, 2) history of homelessness evidenced by record of
residence in a publicly operated shelter in the 12 months preceding
diagnosis or during treatment for active TB and 3) geographical location
of contacts.
[FIGURE 1 OMITTED]
Community-level analysis
Loci of transmission were assigned according to address and postal
code at diagnosis. The major locus of transmission in Edmonton consisted
of three adjoining census areas; in Calgary one census area. Data were
obtained from the 2001 census on total population, income, employment,
and population mobility for crude comparison of area-based
socio-economic measures between loci of transmission and the province at
large.
Statistical analysis
The statistical significance of differences between area-level
indicators was assessed using chi-squared tests for proportions and
t-tests for quantitative variables with STATA, version 9.2. The study
was approved by the Health Research Ethics Board of the University of
Alberta.
RESULTS
Between 1991 and 2007, there were 1,926 cases of culture-positive
TB in Alberta; 404 (21.0%) in Aboriginal peoples, 262 (13.6%) in
Canadian-born non-Aboriginal peoples and 1,260 (65.4%) in foreign-born
peoples. Initial isolates from 1,880 (97.6%) cases were DNA
fingerprinted and 7 large clusters identified (Table 1). Subsets of
clusters 'C' and 'G' had been reported previously.
(12) Cluster 'D' was chosen as being the most likely to inform
TB elimination strategy. It involved four different population groups
and a drug-susceptible strain; its extent was unrecognized at the time
(routine and catch-up [historical isolates] RFLP typing did not begin
until later). All cluster cases occurred within 2 years of each other.
Between 1993 and 2001, there were multiple (>10) NWT cases with the
same strain. Between 1995 and 1997, there were no BC, Saskatchewan and
Manitoba cases with the same strain. The incidence of TB in Alberta was
6.7 and 3.2 per 100,000 persons in 1991 and 2007, respectively. (13)
Case and contact analysis
Most of the 18 Cluster "D" cases were young (median age
39 years), male (72.2%), and Aboriginal (72.2%) (Table 2). All had
pulmonary or pleuro-pulmonary TB. Three cases had 1 and five cases had 2
independent determinants of infectiousness (sputum smear positivity and
cavitation on chest radiograph).14 Fourteen patients were HIV tested and
negative; non-tested patients had no record of a positive HIV test
result in the provincial HIV database up to the end of 2007. Substance
abuse was very common (88.2% of the adult cases). Intra- and
inter-jurisdictional management was well coordinated and all but one
case (#4 who was diagnosed at death) completed directly observed
treatment (DOT).15 Three loci of transmission were identified: a reserve
community, an Edmonton borough, and a Calgary borough, spanning 26,569
[km.sup.2] (Figure 1). Ten cases had 'Type 1' and 7 cases had
'Type 2' transmission links.
Most contacts (57.0% of 1,080) were attached to a single highly
infectious homeless shelter resident (#8). Many (24.4%) of this
case's contacts were already known to be tuberculin skin test (TST)
positive. Most of the 254 non-assessed case contacts (186 or 73.2%) were
contacts of this case. Of the 71 new TST positive/TST converted contacts
of this patient, 58 (81.7%) were recommended, 30 (42.3%) accepted, and
16 (22.5%) completed treatment of latent tuberculosis infection (LTBI).
Close contacts were more likely than those who were casual or
'other' to have a new positive TST or TST conversion, 51.3%
versus 31.3% versus 20.4%, respectively (Table 3).
Case mobility
On average, the five most infectious cases and all cases changed
addresses 4 times and 2.8 times, respectively, during treatment. Five
patients had a history of shelter living before and 3 during treatment;
shelters were without engineering controls. Three cases (case #s 1, 7,
and 14) originated from an NWT band and had a documented history of
travel to the NWT either prior to diagnosis or during treatment.
Contacts of sputum smear-positive cases were widely distributed,
involving 9 of 17 RHAs.
Area-based socio-economic indicators
Median household income and rates of higher education were lower
and unemployment rates and population mobility higher in the
transmission loci than in the province at large, p<0.0001 (Table 4) .
DISCUSSION
At a time when the overall incidence of TB in Alberta was falling,
sustained transmission was occurring in a difficult-to-reach population.
Cluster cases were from multiple population groups, occurred over an
extended period of time, and with few exceptions were not connected one
with another at the time. Though cluster cases were HIV negative and the
cluster strain drug-susceptible, there was ongoing intra-jurisdictional
transmission between three loci in Alberta and inter-jurisdictional
transmission between Alberta and the Northwest Territories. Upon review
of the experience, central oversight, integrated case management and DOT
were seen as fostering TB elimination. The absence of
'real-time' DNA fingerprinting (see definition of
'real-time' in next paragraph), social network analysis, and
engineering controls in shelters and the presence of poor determinants
of health in loci of transmission were seen as sustaining the outbreak
and hampering TB elimination.
In contrast to outbreaks in isolated or semi-isolated reserve
communities which rely on conventional epidemiology--sometimes to the
point of screening 'community contacts'--complex outbreaks
such as the one reported here rely on molecular epidemiology,
geographical-spatial analysis, and the application of unconventional
contact-tracing paradigms for investigation. (12,16-22) They can be much
more challenging. Clearly, it would have been helpful to have recognized
the extent of the outbreak earlier. In this regard, newer,
polymerase-chain-reaction-based methods of genotyping M. tuberculosis
(for example, "mycobacterial interspersed repetitive-unit-variable
number tandem repeats" [MIRU-VNTR]) offer the promise of
'real-time' (results in 1 to 2 weeks [national], versus 2 to
12 weeks for RFLP [provincial]) intra- and inter-jurisdictional outbreak
detection. (23-26) Such genotyping can also unmask the role that social
networks play in disease transmission and the extent to which failure to
consider unnamed contacts can lead to missed cases. Disease control in
the context of social networks requires identification of groups of
persons who share similar social settings and mores with infected
people. Once these groups are identified, testing and treatment is
offered not only to the infected person and the few named contacts, but
to the entire network. This approach improves rapport with clientele,
helps eliminate stigma, and identifies persons who may have otherwise
been missed. (27,28)
Such strategies might have minimized the effect of case-patient
mobility which was substantial. In general, high degrees of mobility are
seen in young adults and those with unstable or transient living
conditions. (29) With respect to the former, migration of First Nations
off-reserve is known to have a clear age pattern with young adults being
the most mobile. Two of the most infectious First Nations cases were
mobile across jurisdictions. With respect to those with unstable or
transient living conditions, 57% of the contacts were attached to a
single highly infectious shelter resident. Shelter contacts are
difficult to assess (30% of this patient's contacts went
unassessed), subject to re-infection (8 of the cluster cases had a
history of TB or a positive TST) and difficult to treat if infected
(only 22.5% of this patient's newly infected/TST-converted contacts
completed treatment of LTBI). Engineering controls such as ultraviolet
light might have reduced transmission had they been present in the
shelter in question. (30) Mandated compliance with TB screening, as a
condition of admission, and spot sputum screening are strategies that
have been used with success in homeless shelters in the United States.
(31,32)
Our crude comparison of socio-economic indicators at the community
level suggested a link between TB and social determinants of health. TB
cluster size and social disadvantage are known to be associated. (33)
Substance abuse was a common risk factor among case-patients; excessive
alcohol use is known to be disproportionately high in clustered
patients. (23) Substance abuse is the most commonly reported modifiable
behaviour impeding TB elimination efforts in the United States. (34)
Poor socio-economic conditions and substance abuse have been linked;
together they may contribute to delayed diagnosis and more advanced
disease (greater transmission) at presentation.
The major limitation of this study is its retrospective design,
requiring the use of proxies for mobility analysis and aggregate data
for area-based analysis.
In conclusion, as TB rates continue to decline, an increasing
proportion of cases are likely to occur in difficult-to-reach
populations. New technology and better understanding of complex chains
of transmission can expose barriers to TB elimination.
Acknowledgements: The authors thank Karen Sutherland and Norah
Landry for their assistance in preparing the manuscript and the Canadian
Molecular Epidemiology of TB Study Group for the use of their Western
Canada DNA fingerprint database (1995-1997).
Supported by grants from the Aboriginal Health Strategy Project
Fund, Alberta Health and Wellness, and First Nations and Inuit Health,
Health Canada, Alberta Region.
This work was prepared in partial fulfillment of a Master's of
Science degree in Public Health by Anne Aspler.
Received: August 4, 2009
Accepted: February 5, 2010
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Anne Aspler, MSc, [1] Huey Chong, BSc, [1] Dennis Kunimoto, MD,
[1,2] Linda Chui, PhD, [2] Evelina Der, BScN, [3] Jody Boffa, MIH, [1]
Richard Long, MD [1]
Author Affiliations
[1.] Tuberculosis Program Evaluation and Research Unit, University
of Alberta, Edmonton, AB
[2.] Provincial Laboratory for Public Health, Edmonton and Calgary,
AB
[3.] Edmonton Tuberculosis Clinic, Edmonton, AB
Correspondence: Dr. Richard Long, Tuberculosis Program Evaluation
and Research Unit, Room 8325, Aberhart Hospital, 11402 University
Avenue, Edmonton, AB T6G 2J3, Tel: 780-407-1427, Fax: 780-407-1429,
E-mail: richard.long@ualberta.ca
Conflict of Interest: None to declare.
Table 1. Large (>15 Members) Chains of Tuberculosis Transmission
(Clusters) in Alberta by Age, Sex, Population Group and Place of
Residence (On-reserve/Off-reserve) at Diagnosis, 1991-2007
Number of Age of Cluster
Cluster * Cluster Members Members (Years)
<15 15-64 >64
A 15 1 14 0
B 15 0 9 6
C 18 7 11 0
D 18 1 17 0
E 23 0 20 3
F 25 1 12 12
G 43 3 34 6
Male Population Group of Cluter Members
Cluster *
CBA CBO
FN Metis Inuit
A 8 6 2 1 6
B 7 10 4 0 0
C 7 18 0 0 0
D 13 8 4 0 5
E 11 21 0 0 0
F 15 0 0 0 0
G 28 30 6 0 6
Residence
Cluster * On-/Off-reserve
([dagger])
FB
A 0 3/12
B 1 10/5
C 0 18/0
D 1 4/14
E 2 20/3
F 25 0/25
G 1 30/13
Shaded cluster = study cluster
CBA=Canadian-born Aboriginal, CBO=Canadian-born 'Other', FN=First
nation, FB=foreign-born
* Cluster member's M. tuberculosis isolates had 100% identical DNA
fingerprint patterns. The number of IS67 70 bands in each cluster
strain, a measure of the power to discriminate one strain from
another, was 12, 9, 13, 11, 11, 1, 10, respectively. Subsets of
cluster 'C' and 'G' had been reported previously. (12)
([dagger]) Of the 85 persons listed as on-reserve at the time of
diagnosis, 78 were First Nations and 7 were Metis.
Table 2. Demographic, Clinical and Epidemiological Features of
Cluster "D" Members
Case No. * Demographic
Date of Age Sex Population
Diagnosis (yrs) Group
(mo/yr)
1 (09/92) 24 F FN
2 (10/92) 9 F FN
3 (05/93) 32 M FN
4 (08/93) 27 M FN
5 (09/94) 44 M CBO
6 (04/95) 46 M Metis
7 (05/95) 37 M FN
8 (05/96) 45 M CBO
9 (08/96) 48 M CBO
10 (08/96) 46 M Metis
11 (06/97) 38 M FN
12 (12/97) 46 M CBO
13 (06/98) 49 F FN
14 (12/98) 63 M FN
15 (01/99) 31 M Metis
16 (08/02) 42 M CBO
17 (07/04) 29 F FB
18 (02/06) 40 F Metis
Case No. * Clinical
Date of Sputum Cavity Risk
Diagnosis Smear on Factors
(mo/yr) Positive CXR ([dagger])
1 (09/92) Y Y 1,2
2 (10/92) N N
3 (05/93) N N 1
4 (08/93) N N 1
5 (09/94) Y Y 1
6 (04/95) Y Y 1,3
7 (05/95) Y Y 1,2
8 (05/96) Y Y 1,2
9 (08/96) N N 1
10 (08/96) N N 1
11 (06/97) N N 3,4
12 (12/97) N N 1,2
13 (06/98) N N 1
14 (12/98) Y N 1
15 (01/99) N N
16 (08/02) Y N 1,3
17 (07/04) N N
18 (02/06) N Y 1
Case No. * Epidemiologic
Date of Links Between Cases Number of Contacts
([double dagger])
Diagnosis
(mo/yr) Past TST Not
Positive Assessed
Source #'s 2,5,8,11,
1 (09/92) possibly #3,4 18 1
2 (10/92) Household contact of #1 13 1
3 (05/93) Unknown
4 (08/93) Unknown 8 --
5 (09/94) Lived with #1 for two weeks -- 1
6 (04/95) Probable source case of #7,10 11 7
7 (05/95) Roommate of #6 2 --
8 (05/96) Probable source #'s 9,12,13,16 150 186
9 (08/96) Co-worker contact of #8 1 1
10 (08/96) Roommate of #6, contact of #8 -- --
11 (06/97) Contact of #1 10 11
12 (12/97) Contact of #8 33 36
13 (06/98) Contact of #8 -- --
14 (12/98) Unknown 2 2
15 (01/99) Visited Edmonton in near past 2 1
16 (08/02) Contact of #8 4 7
17 (07/04) Customer at #16's workplace -- --
18 (02/06) Unknown -- --
Case No. * Epidemiologic
Date of Number of Contacts
([double dagger])
Diagnosis
(mo/yr) TST New TST
Negative Positive/
Converter
1 (09/92) 18 15
2 (10/92) 90 19
3 (05/93) 1
4 (08/93) 11 8
5 (09/94) 4 --
6 (04/95) 33 7
7 (05/95) -- 1
8 (05/96) 209 71
9 (08/96) 5 5
10 (08/96) -- --
11 (06/97) 9 6
12 (12/97) 15 12
13 (06/98) 1 1
14 (12/98) -- 2
15 (01/99) 5 --
16 (08/02) 9 9
17 (07/04) 1
18 (02/06) 8
M=male, F=female; FN=First Nation, CBO=Canadian-born 'Other',
FB=foreign-born; Y=yes, N=no; CXR=chest x-ray; TST=tuberculin skin test
* Cases are numbered according to their order of occurrence (see
figure). Case #14 had a past history of TB; case # 1, 5, 6, 10, 11,
13, and 18 had a past history of a positive TST.
([dagger])t Risk Factors: 1=Alcohol abuse defined as patient-reported
alcoholism or disclosure of excessive alcohol use, 2=injection drug
use, 3=substance abuse, unspecified or other, 4=severe malnutrition.
([double dagger]) Contacts who were 'not assessed' were those with no
past positive TST and, either a negative TST that was performed at
less than 8 weeks post-contact, or no TST. TST negative contacts are
those who were negative >8 weeks post-final contact with the source
case. A TST converter was defined according to the Canadian
Tuberculosis Standards. (2)
Table 3. Tuberculin Skin Test Results in Contacts of Cluster "D"
Patients by Type of Contact and Place of Residence of Contact
Tuberculin Skin
Test Results
Close
R E C O
Old Positive 18 38 4 3
New Positive 9 22 2 1
Converter 2 4
Negative (>8 wks) ([dagger]) 8 23 4 3
Negative (<8 wks) ([dagge]) 1 11
Unknown 1 25 2
Total 39 123 12 7
Tuberculin Skin Type of Contact
Test Results
Casual
R E C O
Old Positive 7 27 3
New Positive 10 19 1
Converter 3 2
Negative (>8 wks) ([dagger]) 5 70 2
Negative (<8 wks) ([dagger]) 4 15 3
Unknown 12
Total 29 145 1 8
Tuberculin Skin
Test Results
Other *
R E C O
Old Positive 18 108 4 24
New Positive 13 39 7
Converter 11 7 1
Negative (>8 wks) ([dagger]) 93 192 1 18
Negative (<8 wks) ([dagger]) 2 53 6
Unknown 5 109 1 4
Total 142 508 6 60
Tuberculin Skin Total
Test Results
Old Positive 254
New Positive 123
Converter 30
Negative (>8 wks) ([dagger]) 419
Negative (<8 wks) ([dagger]) 95
Unknown 159
Total 1080
R=reserve community, E=Edmonton, C=Calgary, O=other communities
* Other: refers to those whose contact type (close, casual, etc.) was
not specified by the public health department at the time of
reporting.
([dagger]) Refers to >8 weeks or <8 weeks after contact with the
source case was broken.
Table 4. Socio-economic Indicators in Communities Where the Cluster
"D" Strain was Transmitted, Compared to Provincial-level Indicators
Socio-economic Indicators Provincial- Community-level
level
Reserve Community
(n=18) * (n=4) p-value
([dagger])
Total Population 2,941,150 580 --
Income
Incidence of low Data not
income in 2000 (%) 10.50% available --
Median household income ($) $52,524 $4,724 p<0.0001
Employment
Labour force participation 73.4% 50.0% p<0.0001
Unemployment rate 4.0% 28.6% p<0.0001
Education
Less than high school 6.2% 16% p<0.0001
High school graduation 31.5% 46% p=0.0008
Trades school 14.0% 6% p=0.013
[greater than or equal to]
1 year of college
or university 51.0% 32% p<0.0001
Population Mobility
Persons who
moved, 2000-2001 17.6% 11% p=0.052
Socio-economic Indicators Community-level
Edmonton Borough
(n=12) p-valuet
Total Population 12,415 --
Income
Incidence of low
income in 2000 (%) 39.0% p<0.0001
Median household income ($) $21,920 p<0.0001
Employment
Labour force participation 59.2% p<0.0001
Unemployment rate 11.5% p<0.0001
Education
Less than high school 18.8% p<0.0001
High school graduation 36.1% p<0.0001
Trades school 8.9% p<0.0001
[greater than or equal to]
1 year of college
or university 36.3% p<0.0001
Population Mobility
Persons who
moved, 2000-2001 34.4% p<0.0001
Socio-economic Indicators Community-level
Calgary Borough
(n=2) p-value
([dagger])
Total Population 8002 --
Income
Incidence of low
income in 2000 (%) 27.5% p<0.0001
Median household income ($) $40,396 p<0.0001
Employment
Labour force participation 70.8% P=0.019
Unemployment rate 7.6% p<0.0001
Education
Less than high school 43.4% p<0.0001
High school graduation 16.3% p<0.0001
Trades school 16.5% P=0.004
[greater than or equal to]
1 year of college
or university 24.0% p<0.0001
Population Mobility
Persons who
moved, 2000-2001 29.7% p<0.0001
* Number of individuals in chain of transmission.
([dagger]) Chi-squared tests comparing proportion at
community level to proportion at regional level.
