Early detection of tuberculosis through

community-based active case finding

in Cambodia
Eang et al.
Eang et al. BMC Public Health 2012, 12:469
http://www.biomedcentral.com/1471-2458/12/469
RESEARCH ARTI CLE Open Access
Early detection of tuberculosis through
community-based active case finding
in Cambodia
Mao Tan Eang
1
, Peou Satha
1
, Rajendra Prasad Yadav
2
, Fukushi Morishita
3
, Nobuyuki Nishikiori
3*
,
Pieter van-Maaren
2
and Catharina Lambregts-van Weezenbeek
3
Abstract
Background: Since 2005, Cambodias national tuberculosis programme has been conducting active case finding
(ACF) with mobile radiography units, targeting household contacts of TB patients in poor and vulnerable
communities in addition to routine passive case finding (PCF). This paper examines the differences in the
demographic characteristics, smear grades, and treatment outcomes of pulmonary TB cases detected through both
active and passive case finding to determine if ACF could contribute to early case finding, considering associated
project costs for ACF.
Methods: Demographic characteristics, smear grades, and treatment outcomes were compared between actively
(n =405) and passively (n =602) detected patients by reviewing the existing programme records (including TB
registers) of 2009 and 2010. Additional analyses were performed for PCF cases detected after the ACF sessions
(n =91).
Results: The overall cost per case detected through ACF was US$ 108. The ACF approach detected patients from
older populations (median age of 55 years) compared to PCF (median age of 48 years; p <0.001). The percentage
of smear-negative TB cases detected through ACF was significantly higher (71.4%) than that of PCF (40.5%). Among
smear-positive patients, lower smear grades were observed in the ACF group compared to the PCF group
(p =0.002). A fairly low initial defaulter rate (21 patients, 5.2%) was observed in the ACF group. Once treatment was
initiated, high treatment success rates were achieved with 96.4% in ACF and with 95.2% in PCF. After the ACF
session, the smear grade of TB patients detected through routine PCF continued to be low, suggesting increased
awareness and early case detection.
Conclusions: The community-based ACF in Cambodia was found to be a cost-effective activity that is likely to have
additional benefits such as contribution to early case finding and detection of patients from a vulnerable age
group, possibly with an extended benefit for reducing secondary cases in the community. Further investigations are
required to clarify the primary benefits of ACF in early and increased case detection and to assess its secondary
impact on reducing on-going transmission.
* Correspondence: [email protected]
3
World Health Organization, Regional Office for the Western Pacific, Manila,
Philippines
Full list of author information is available at the end of the article
2012 Eang et al.; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative
Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and
reproduction in any medium, provided the original work is properly cited.
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Background
Successful expansion of the internationally recommended
directly observed treatment, short-course (DOTS) strategy
since the mid-1990s has achieved remarkable progress in
TB control in many parts of the world. The strategy,
which promotes direct observation of therapy under
one of its key principles, has contributed substantially
to treatment success across the globe [1]. The World
Health Organization (WHO) reported that 46 million
people were successfully treated between 1995 and 2010,
and the treatment success rate at the global level
increased by 30% during this period [2]. Despite progress
in treatment, however, case detection has stagnated in
recent years [2,3].
The DOTS strategy promotes passive case finding
(PCF), whereby patients with signs and symptoms of TB
present themselves at health facilities for diagnosis and
treatment [4]. While this conventional approach has
been recognized as cost-effective [5], people who have
limited access to TB services often fail to receive timely
diagnosis and life-saving treatment. Delays in seeking
care have been widely observed in various settings, par-
ticularly in TB high-risk and vulnerable populations,
which has posed major challenges for improving case
detection [5,6]. Active case finding (ACF), on the other
hand, systematically looks for cases of TB, rather than
waiting for people to develop symptoms and seek treat-
ment. Although ACF has been implemented for decades
primarily in resource rich settings, there is growing
interest in using this approach for early case detection in
developing countries [4,7].
Cambodia, one of 22 countries with a high burden of
TB, has faced stagnation in case notification and has
strived to increase case detection [2,8]. The country has
adopted many case-finding approaches to promote early
diagnosis, including ACF among contacts of TB cases
at the community level [8]. Since 2005, the National
Centre for Tuberculosis and Leprosy Control (CENAT),
Cambodia, has been conducting outreach ACF sessions
with mobile radiography units to target household con-
tacts of TB patients in poor and vulnerable communities.
Looking back in the history of TB control, ACF has
been discouraged for many years because it is prohibi-
tively expensive in some settings especially when it is
conducted as a population screening and/or where TB
prevalence is low [4]. Despite general recommendations
against community-based ACF [9-11], these activities
have been conducted effectively in Cambodia at a rela-
tively low cost, employing an innovative approach that
promotes retrospective contact investigations combined
with symptom screening by community workers. However,
the cost-effectiveness of the ACF approach and potential
benefits for the patients, particularly comparing ACF with
the conventional PCF approach, have yet to be examined.
This study examined whether ACF contributes to early
detection of TB cases by comparing the smear grades of
actively and passively detected pulmonary TB patients.
The study also examined the potential benefits of ACF
by analysing the demographic differences of patients and
evaluated the cost-effectiveness of the ACF approach.
The results of the study constitute an evidence base for
future policy formulations on ACF in Cambodia.
Methods
Programmatic information
The ACF sessions were organized by CENAT in coord-
ination with peripheral TB control staff and health ser-
vices. Target operational districts (ODs) were selected
based on the TB burden and vulnerability of the com-
munities. About 7-10 days prior to the scheduled ACF
session, local health workers visited community health
volunteers and community leaders, and with them, vis-
ited household contacts of smear-positive patients who
had registered for treatment in the past two years, and
orally advised them to present at prearranged health
centres on the day of the ACF session. If the immediate
neighbours of the index cases had TB symptoms, pro-
ductive cough lasting two weeks or more, they were also
invited for the session. If the suspects were not at home,
they continued to be followed up by community health
volunteers. On the day of the ACF session, CENAT team
together with local health staff set up a screening venue
including mobile X-ray and microscopy stations. All TB
suspects who presented to the ACF session underwent
chest X-ray screening. The films were read by an experi-
enced radiologist and categorized according to prede-
fined criteria that included the categories of normal,
active TB, TB suspected, healed, and others. Those in
the categories of TB suspected, healed, and others
were further evaluated based on the individual risk of
infection including clinical history to see if sputum-
smear microscopy is required. For all in the active
category and those who required further investigations,
three sputum samples were collected and examined by
microscopy with ZiehlNeelsen method on the day of
the visit and on the following day in collaboration with a
local laboratory. A senior physician on the ACF team
diagnosed smear-negative TB based on radiological, clin-
ical, and physical findings that were consistent with TB
but not explained by other illnesses. Local health centres
initiated treatment for both smear-positive and smear-
negative patients.
Beside this distinctive ACF activity, TB cases registered
under the routine programme were diagnosed according
to national guidelines. Most cases were self-referral
patients presenting to the health centres where a sputum
smear microscopy is available. In case TB is still sus-
pected in smear-negative subjects after anti-biotic trial,
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they should be referred to district health hospital for
chest X-ray and subsequent assessment for diagnosis of
smear-negative TB.
Quantitative data
ACF sessions were conducted in 39 health centres across
eight ODs in 2009 and 2010. We reviewed the records
of all pulmonary TB cases detected by both active
and passive case finding in the designated health centres
(including PCF records from the same quarter and
two quarters prior to the ACF sessions). Patients under
15 years and those with unknown sex and age were
excluded from the study. As a result, out of 1109 TB
case records that were reviewed, 405 ACF cases and 693
PCF cases were enrolled in the study (Figure 1). Among
the PCF cases, 91 cases were registered after the
ACF sessions and composed a separate group. Hence,
the dataset consists of three groups: PCF-before, ACF,
and PCF-after.
Primary variables such as smear grade and demo-
graphic characteristics were sourced from existing TB
and laboratory resisters kept at CENAT. Smear grades
were defined and recorded as follows: scanty (19 acid-
fast bacilli [AFB] per 100 fields), 1+ (1099 AFB per 100
fields), 2+ (110 AFB per field), and 3+ (>10 AFB per
field) [12].
As this study used existing programme records and no
personal identifying information was collected, ethical
clearance was not required according to local regulations.
Statistical analysis
The raw data were entered into a Microsoft Excel
(Microsoft, USA) spreadsheet with predefined coding
and error-checking formulas. The statistical analyses
were performed using R 2.14.1 (CRAN: the Comprehen-
sive R Archive Network at http://cran.r-project.org/).
Distribution and frequency of smear grades, demo-
graphic characteristics, and other key variables were cal-
culated and compared between the PCF-before and ACF
groups. Pearson's chi-square test or Fishers exact test
were applied to examine associations. In addition, to
compare age distributions by case finding strategies,
Mann-Whitney test was applied. The PCF-after group
was used later as a secondary comparable group to as-
sess the impact of ACF in the community.
Results
Number needed to screen
Between 2005 and 2010, 33 631 TB suspects who pre-
sented to the ACF sessions were registered for screening
across Cambodia and all were screened by chest radiog-
raphy. Among them, 5844 (17.4%) underwent sputum-
smear microscopy, and 885 (2.6%) were found to be
smear-positive patients. Hence, the number needed to
screen (NNS) to identify one smear-positive case was 38.
Cost of active case finding
Cost information was available only for ACF sessions
conducted in five ODs in 2010. A total of 2561 suspects
were screened by chest radiography, of which 337
(13.2%) underwent a sputum-smear test. These tests
resulted in the detection of 56 smear-positive and 101
smear-negative cases (2.2% and 3.9% of all participants,
respectively). Applying the local standard unit costs of
US$ 1.20 for chest X-ray and US$ 0.70 for sputum-
smear test per slide, the diagnostic cost per case
detected including smear negatives was US$ 24 (ranging
from US$ 16 to US$ 41 among five ODs). Using the
overall project cost of US$ 16 917, including the costs of
logistic support and human resources (with additional
pay for the time involved in the activities but excluding
basic salaries), the calculated overall cost per case
detected was US$ 108.
Demography
A comparison of the cases found by ACF and PCF-
before is summarized in Table 1. Both case-finding
methods detected slightly more female patients than
male patients, which is consistent with overall case noti-
fication in Cambodia [2]. Although ACF yielded a
slightly larger proportion of female patients compared to
PCF, the difference was insignificant.
In terms of age distribution, ACF detected a higher
proportion of older patients compared to PCF. The
Figure 1 Sampling process. <15 =Patient is under 15 years of age.
ACF, active case finding; PCF, passive case finding; SS +ve, sputum-
smear positive; SS -ve, sputum-smear negative.
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difference was statistically significant, with the median
(IQR; inter-quartile range) being 55 (IQR 47-64) years
in the ACF group and 48 (IQR 36-59) years in the
PCF-before group (p<0.001 by Mann-Whitney test).
Figures 2(a) and 2(b) clearly indicate a shift in age distri-
bution by case-finding method, with the highest pro-
portion of cases found in the 4554 year age group for
PCF-before and the 5564 year group for ACF. Patients
aged 55 or older accounted for 32.5% in the PCF-Before
group, while the ACF group had a higher proportion
of 51.3%.
Result of sputum-smear test
The ACF group had higher proportions of smear-
negative patients and smear-positive patients with lower
smear grades than the PCF-before group. In fact, the
percentage of smear-negative TB in the ACF group was
significantly higher than that of the PCF-before group
(71.4% and 40.5%, respectively, as shown in Figure 3(a);
p <0.001). Among the smear-positive patients, lower
smear grades were observed in the ACF group compared
to the PCF-before group, which was statistically signifi-
cant (Figure 3(b); p =0.002). Cases with lower smear
grades (i.e. scanty and 1+) accounted for 56.9% of all
smear-positive cases in the ACF group, compared to
42.7% in the PCF-before group (p <0.010).
Treatment outcome
In the ACF group, no TB suspects dropped out during
the diagnostic pathway after the registration for ACF
sessions. However, 21 patients (5.2%) including five
smear-positive cases were not registered for treatment in
the quarter of the ACF session or the following quarter.
These patients are considered as initial defaulters who
were lost to follow-up before treatment initiation.
Among those registered, all actively detected patients
were categorized as new cases, whereas other types
of patients were also reported in PCF. Both case find-
ing methods achieved a fairly high treatment success
rate with more than 95%, excluding initial defaulters.
The proportion of unfavourable outcomes (default, died,
failure, and transfer-out) was slightly higher in the PCF-
before group although this difference was not statisti-
cally significant. A small number of HIV-positive cases
were reported from both case-finding methods.
Patients detected through PCF after the ACF sessions
(PCF-after)
Of the 91 cases detected through PCF after the ACF ses-
sions, 45 (49.5%) were male and the median age was
49 (IQR 36.5-60) years, revealing similarities with the
PCF-before group in respect of age distribution (Man-
Whitney test results; p <0.001 between ACF and PCF-
after groups, while p =0.541 between PCF-before and
after groups). The smear status, however, was more like
that of the ACF group, with 39 (42.9%) smear-positive
cases (Figure 3[a]). The grade distribution was also simi-
lar to the ACF group, as shown in Figure 3(b). The num-
ber of cases diagnosed as 1+, 2+, and 3+ were 23 (59%),
9 (23.1%), and 7 (17.9%), respectively. Among them, one
was HIV-positive, one was previously treated, and three
died. The treatment success rate was 96.7%.
Table 1 Characteristics of patients by case-finding
method
ACF (%)
(n=405)
PCF-before
(%) (n=602)
P-value
(chi-squared test)
Sex
Male 178 (44.0) 278 (46.2) 0.527
Age group
1524 10 (2.5) 44 (7.3) <0.001
2534 25 (6.2) 100 (16.6)
3544 51 (12.6) 104 (17.3)
4554 111 (27.4) 158 (26.2)
5564 114 (28.1) 108 (17.9)
>65 94 (23.2) 88 (14.6)
Smear status
Negative 289 (71.4) 244 (40.5) <0.001
Positive 116 (28.6) 358 (59.6)
Smear grade of smear-positive cases**
Scanty 10 (8.6) 8 (2.3) 0.003*
1+ 56 (48.3) 143 (40.4)
2+ 30 (25.9) 137 (38.7)
3+ 20 (17.2) 66 (18.6)
Treatment initiation
Initial defaulter 21 (5.2) NA NA
Patient category
New 384 (100) 592 (98.3) 0.006*
Re-treatment 0 (0) 1 (0.2)
Transfer-in 0 (0) 3 (0.5)
Others 0 (0) 6 (1.0)
Treatment outcome
Success (cure and complete) 370 (96.4) 573 (95.2) 0.323*
Default 3 (0.8) 4 (0.7)
Died 3 (0.8) 11 (1.8)
Transfer-out 0 (0.0) 4 (0.7)
Failure 0 (0.0) 0 (0.0)
Unknown/not evaluated 8 (2.1) 10 (1.7)
HIV status
Unknown 145 (35.8) 186 (30.9)
0.120
Known 260 (64.2) 416 (69.1)
- Positive 1 (0.4) 4 (1.0) 0.696*
* Fishers exact test was employed due to small cell counts.
** Smear grades were not available for four cases in the PCF-before group.
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Figure 2 Age distribution of cases by case-finding method.
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Discussion
The community-based ACF approach employed in
Cambodia, which focussed on TB contacts in poor com-
munities with a high burden of TB, was found to be
cost-effective, considering that the overall cost per case
detected was US$ 108 and the NNS was 38. In compari-
son, eight FIDELIS projects (Fund for Innovative DOTS
Expansion through Local Initiatives to Stop TB), sup-
ported by the Canadian International Development
Agency (CIDA), reported a cost per case detected ran-
ging from US$ 60 to US$ 1626 by ACF [13], which
implies that the Cambodian ACF approach is compar-
ably cost-effective. Besides, the NNS of 38 is very similar
to those reported through intensified case finding in
HIV-prevalent and congregate settings [14]. Considering
the low HIV prevalence in this study population, the low
NNS further justifies the cost-effectiveness of the strat-
egy. The results of this study also revealed that the ACF
approach could contribute to the detection of smear-
negative TB cases or smear-positive TB cases with low
smear grades. The approach could also detect more TB
patients from older age groups, which demonstrates
an equalizing role for ACF in TB service provision,
especially as the elderly run the risk of dying without
any attempt to diagnose the underlying source of their
complaints or disease.
The elderly are generally considered vulnerable to TB
as they belong to age cohorts with high TB infection
Figure 3 Distribution of smear grade by case-finding method.
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rates, have relatively low immune status and limited
access to health services [15,16]. A survey conducted in
Cambodia in 2002 demonstrated that TB prevalence was
up to seven times higher in the older age groups than in
the general population. Yet the level of case detection
among them was low [17]. In that sense, detecting TB
among older patients could be seen as an additional
value of ACF in the Cambodian context. Studies con-
ducted in South India and Eastern Nepal showed similar
results [9,18]. Some may argue that ACF in Cambodia
missed out part of the younger population since most
of the sessions were conducted during the day, which
is more convenient for the elderly and not for the eco-
nomically active age group. Yet one of the primary
objectives of ACF is to identify and treat more patients
who have remained undetected in the community with
special attention to health inequity. Given that more
than half of actively detected patients were older than
55 years of age compared to around one third of pas-
sively detected patients being older than 55 years of age,
it is reasonable to conclude that the ACF approach has
successfully complemented routine PCF in Cambodia
by detecting older patients. The finding that all of the
actively detected patients were new cases without any
history of previous treatment further supports its com-
plementary function.
Smear grade, a quantitative measure of TB bacilli in
the sputum samples, has been suggested as a parameter
that can represent the severity and the infectiousness of
the disease [19,20]. The lower smear grades observed
in the ACF group in this study, therefore, suggest that
actively detected patients were at a relatively early stage
of their disease. This was consistent with the findings of
Santha et al. in South India [9]. Another study exploring
the association between smear grade and diagnostic
delay in Japan showed that patients with delayed diagno-
sis had significantly higher smear grades than those with
timely diagnosis [21]. This finding implies that there is a
link between smear positivity and timing of diagnosis,
and further supports our argument that ACF can con-
tribute to early case finding in a developing country set-
ting. Looking at the newly detected cases among
contacts of index smear-positive cases, Liippo et al. con-
cluded that limiting contact investigation to close con-
tacts of patients heavily positive by sputum smear makes
contact tracing more effective [19]. From a different
angle, Lin et al. examined the effect of treatment delay
on secondary TB infection among household contacts
[22]. The study demonstrated a linear positive relation-
ship between the delays in treatment of index cases and
the secondary attack rates among household contacts.
Thus, both existing literature and our findings strongly
suggest that ACF can reduce diagnostic delay and
thereby reduce the risk of further transmission.
As programmatic operational research using routine
programme data, our study has several limitations. It is
important to note that smear grade is both directly and
indirectly influenced by other factors including volume
and quality of sputum specimens, capacity of laboratory
technicians, and possibly characteristics of screened sub-
jects such as HIV and smoking status [23-27]. However,
as smear slides were read by local technicians under
routine conditions within the standard external quality
assurance system, these factors may not have been ser-
ious confounders. Nevertheless, it may be desirable to
obtain additional evidence on ACF by conducting, for
instance, a delay study (comparing the extent of various
delays from onset of symptoms, treatment seeking, final
diagnosis, to treatment initiation between ACF and PCF)
to reconfirm our findings and further quantify its contri-
bution to early case detection.
Another limitation may have been the diagnosis of
smear-negative TB during the outreach sessions. Our
findings, showing a larger proportion of smear-negative
TB detected in ACF than in PCF, might have been partly
due to the different diagnostic methods used in between
ACF and PCF, and over-diagnosis of smear-negative TB
during the ACF sessions. A similarly high proportion of
smear-negative TB was reported in a study conducted in
South India [9]. To overcome this limitation, CENAT
has been implementing a new project employing Xpert
MTB/RIF as more sensitive diagnostic tool.
Our data lack the information on the number of
households visited and individuals interviewed in the
communities which could serve as primary denomina-
tors of NNS. However, our results are still valuable by
using the number of individuals attended in the ACF
sessions as shown in the result.
Finally, this study was unable to perform a compara-
tive analysis between ACF and PCF in terms of cost-
effectiveness since cost calculation of PCF requires an
extensive assessment of the health system costs. A
proper cost-effectiveness analysis should also include the
assessment of disability-adjusted life-years (DALY) lost
under the conditions with or without ACF. Obviously,
these are beyond the scope of this field-based oper-
ational research study.
As one of the negative aspects of ACF, the issue of
initial defaulters has been discussed in several articles
[4,9,18,28]. Refusal to start treatment might be attributed
to a lack of motivation due to the absence or mildness
of symptoms [9]. Although the available evidence is lim-
ited and its definition may vary depending on research-
ers, the initial defaulter rates in ACF reported in other
countries ranged from 26% to 32% [9,28], which was
much higher than our observation of 5.2%. Taking into
account that the TB programme in Cambodia has main-
tained a high treatment success rate and a low defaulter
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rate at national level over the years [2], these program-
matic strengths may be reflected in the low initial
defaulter rate among actively detected cases. This
assumption suggests that ACF is likely to result in more
initial defaulters in places with poor TB programmatic
indicators, and further suggests that, when adopting
ACF, such indicators need consideration in order to
maximize effectiveness of the activities.
In this study, the smear grades of patients diagnosed
through PCF after the ACF sessions were as low as those
of actively detected patients, which might imply that
ACF had a sustained impact on smear positivity among
patients in the community. The one-time ACF sessions
identified and treated many patients with relatively mild
symptoms as well as those with heavy bacterial load.
This may have contributed to the reduction of the over-
all patient pool in the community and thus led to the
lower smear grades among patients in routine PCF. In
addition, taking into account that the previous national
prevalence survey was conducted in 2002, those
reviewed in the study had not been exposed to massive
ACF or TB awareness campaigns for a substantial period
of time. Thus our ACF activities were likely to have
contributed to increased community awareness about
the disease and availability of services. Community
mobilization might have promoted early health seeking
and diagnosis.
Conclusion
Cambodias ACF approach targeting TB contacts in
communities was found to be a cost-effective approach
that is likely to have additional benefits such as contri-
bution to early case detection and detection of patients
from a vulnerable age group, possibly with an extended
benefit for reducing secondary cases in the community.
Further investigations are required to clarify the primary
benefits of ACF in early case detection and to assess its
secondary impact on reducing on-going transmission.
Competing interests
The authors declare that they have no competing interests.
Authors contributions
NN and RPY designed the study, developed the research protocol and
supervised data collection. FM and PS substantially contributed to the
acquisition and interpretation of the data. NN and FM performed statistical
analyses and drafted the first version of the manuscript. MTE, RPY, PVM, and
CL have been involved in revising it critically for important intellectual
content. All authors read and approved the final manuscript.
Acknowledgements
The authors wish to thank The Global Fund to Fight AIDS, Tuberculosis and
Malaria, The United State Agency for International Development, and The
Family Health International for their financial contributions to the ACF
operations as well as for sharing programmatic information. The authors also
wish to extend our thanks to all staff members of CENAT and Mr Naro Chea
for their support in retrieving programmatic data.
The cost of fieldwork was supported by the Government of Japan through
Ministry of Health, Labour and Welfare. RPY, PVM, NN, and CL are staff
members of WHO. The authors alone are responsible for the views expressed
in this publication and they do not necessarily represent the decisions or
policies of WHO.
Author details
1
National Centre for Tuberculosis and Leprosy Control (CENAT), Ministry of
Health, Phnom Penh, Cambodia.
2
World Health Organization, Representative
Office in Cambodia, Phnom Penh, Cambodia.
3
World Health Organization,
Regional Office for the Western Pacific, Manila, Philippines.
Received: 3 March 2012 Accepted: 15 June 2012
Published: 21 June 2012
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doi:10.1186/1471-2458-12-469
Cite this article as: Eang et al.: Early detection of tuberculosis through
community-based active case finding in Cambodia. BMC Public Health
2012 12:469.
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