Baseline CD4 Cell Counts of Newly Diagnosed HIV Cases in China: 2006–2012
Citation: Tang H, Mao Y, Shi CX, Han J, Wang L, et al. (
Baseline CD4 Cell Counts of Newly Diagnosed HIV Cases in China: 2006-2012
Houlin Tang 0
Yurong Mao 0
Cynthia X. Shi 0
Jing Han 0
Liyan Wang 0
Juan Xu 0
Qianqian Qin 0
Roger Detels 0
Zunyou Wu 0
Barbara Ensoli, Istituto Superiore di Sanita`, Italy
0 1 Division of Integration and Evaluation, National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention , Beijing , China , 2 Department of Epidemiology, School of Public Health, Harvard University , Boston , Massachusetts, United States of America, 3 Division of Epidemiology, National Center for AIDS/STD Control and Prevention, Chinese Center for Disease Control and Prevention , Beijing , China , 4 Department of Epidemiology, School of Public Health, University of California at Los Angeles , California , United States of America
Background: Late diagnosis of HIV infection is common. We aim to assess the proportion of newly diagnosed HIV cases receiving timely baseline CD4 count testing and the associated factors in China. Methods: Data were extracted from the Chinese HIV/AIDS Comprehensive Response Information Management System. Adult patients over 15 years old who had been newly diagnosed with HIV infection in China between 2006 and 2012 were identified. The study cohort comprised individuals who had a measured baseline CD4 count. Results: Among 388,496 newly identified HIV cases, the median baseline CD4 count was 294 cells/ml (IQR: 130-454), and over half (N = 130,442, 58.8%) were less than 350 cells/ml. The median baseline CD4 count increased from 221 (IQR: 63-410) in 2006 to 314 (IQR: 159-460) in 2012. A slight majority of patients (N = 221,980, 57.1%) received baseline CD4 count testing within 6 months of diagnosis. The proportion of individuals who received timely baseline CD4 count testing increased significantly from 20.0% in 2006 to 76.9% in 2012. Factors associated with failing to receiving timely CD4 count testing were: being male (OR: 1.17, 95% CI: 1.15-1.19), age 55 years or older (OR:1.03, 95% CI: 1.00-1.06), educational attainment of primary school education or below (OR: 1.30, 95% CI: 1.28-1.32), infection with HIV through injection drug use (OR: 2.07, 95% CI: 2.02-2.12) or sexual contact and injection drug use (OR: 1.87, 95% CI: 1.76-1.99), diagnosis in a hospital (OR: 1.91, 95% CI: 1.88-1.95) or in a detention center (OR: 1.75, 95% CI: 1.70-1.80), and employment as a migrant worker (OR:1.55, 95% CI:1.53-1.58). Conclusion: The proportion of newly identified HIV patients receiving timely baseline CD4 testing has increased significantly in China from 2006-2012. Continued effort is needed for further promotion of early HIV diagnosis and timely baseline CD4 cell count testing.
Funding: The authors report funding from the National Health and Family Planning Commission of the Peoples Republic of China (grant#131-11-0001-0501),
and the US National Institutes of Health (grant# U2RTW06918). The funders had no role in study design, data collection and analysis, decision to publish, or
preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
CD4 cell count is a major indicator of human
immunodeficiency virus (HIV) infection disease progression [1,2]. Patients who
receive a late diagnosis, defined as a baseline CD4 cell count,200
cells/ml, have significantly poorer responses to antiretroviral
therapy (ART) and worse prognoses [3,4,5,6]. The proportion of
patients who present late to diagnosis and treatment remains
unacceptably high [7,8,9,10]. Internationally, the observed
proportion of patients with late diagnoses is stable or worsening .
Although it is recommended that CD4 cell count testing should be
carried out promptly after diagnosis, many patients fail to receive
on-time testing [11,12]. In the United States, an ongoing
outpatient study in eight cities found that 78% of patients had a
measured CD4 count within 3 months of HIV diagnosis . This
proportion was significantly lower in developing countries. Studies
in Thailand, Vietnam, and South Africa reported that only 34%,
49%, and 62.6% of patients, respectively, received CD4 count
assessment with 6 months of HIV diagnosis [13,14,15].
In 2002, China implemented the National Free Antiretroviral
Therapy Program (NFATP) to address the issue of poor access to
HIV/AIDS treatment. Patients who meet the national treatment
criteria of a CD4 count #200 cells/ml (revised to #350cells/ml in
2008) are eligible for ART at no cost to the patient . The
program has contributed to a dramatic reduction in mortality
among patients receiving HIV treatment . In order to expand
NFATP coverage, the government has increased HIV screening
access, leading to a rise in the number of people diagnosed with
HIV . After the diagnosis of HIV infection, timely CD4 cell
count testing is a crucial step in determining whether the patient
meets criteria for ART initiation and engaging the patient in
appropriate care and treatment [19,20]. From 2007, the national
HIV/AIDS program set quantitative targets of core indicators to
monitor progress in key areas of HIV work. From 2007 to 2009,
the proportion of CD4 cell count monitoring for people diagnosed
with HIV and AIDS increased from 45.3% and 10.1% in 2007 to
54.2% and 62.5% in 2009, respectively .
However, past studies have indicated that many patients are lost
or delayed along the continuum of care. A study in Guangxi and
Yunnan found that only 37% of patients who were diagnosed with
HIV from 2005 to 2009 received baseline CD4 testing within 6
months . The proportion increased dramatically from 7% in
2005 to 62% in 2009. A separate study noted that in 2009,
approximately 30% of the ART-initiated patients who received
baseline CD4 testing had CD4 ,50 cells/ml, indicating that many
patients were being diagnosed and treated late [22,23]. Prompt
baseline CD4 testing is a critical step in successful linkage to HIV
By using data extracted from the Chinese HIV/AIDS
Comprehensive Response Information Management System
(CRIMS) , we aimed to identify trends in the proportion of
individuals who received timely baseline CD4 cell count testing
within 6 months of HIV diagnosis in China from 2006 to 2012.
We also sought to determine changes in median baseline CD4 cell
counts over time and factors associated with failing to receive CD4
cell count testing.
Data were collected from CRIMS, a web-based real-time
database system managed by the National Centre for AIDS/STD
Control and Prevention (NCAIDS), Chinese Center for Disease
Control and Prevention (CDC). CRIMS was developed in 2005
and has previously been described elsewhere . Local CDC
staffs, who are trained on data upload and management, create
electronic records in CRIMS for each patient who tests positive for
HIV. Staffs receive annual refresher training. Patient records
contain information on demographic characteristics, contact
information (including both permanent and temporary residential
addresses), sexual and drug use risk behaviors, likely transmission
routes, medical histories, and laboratory test results . For this
study, we included all adult individuals (over 15 years old) who
received a confirmed HIV diagnosis between January 1, 2006 and
December 31, 2012. All HIV screening is done in accordance with
national HIV policy. Provider-initiated testing and counseling
(PITC) has been in place in hospitals since 2007.
The primary outcome of interest was the proportion of newly
diagnosed HIV/AIDS individuals who received baseline CD4 cell
count testing within 6 months of diagnosis. Data were described by
the median (interquartile range, IQR) and the distribution across
four CD4 cell count categories (,200, 200349, 350500, and $
500). Demographic characteristics were analyzed using
chisquared statistics for dichotomous and categorical variables.
Univariate and multivariate logistic regression models were used
to assess the factors associated with not receiving a timely CD4 cell
count. Variables with p,0.10 under univariate analysis were
retained for multivariate modeling using stepwise selection, and
95% confidences intervals were estimated using these models.
Results with a two-sided p,0.01 were considered statistically
significant. All data analyses were performed using SAS Version
9.3 (SAS Institute, Cary, NC, USA).
This study was a secondary data analysis using existing Chinese
government HIV/AIDS CRIMS data. All subjects signed a
general informed consent upon enrollment to CRIMS indicating
that their data, after removing personal identifiers, could be used
in statistical analyses and/or epidemiological research studies.
Therefore, no additional study specific informed consent was
necessary for this current study. Patient records and information
were de-identified prior to analysis. This study protocol was
reviewed and approved by the Institutional Review Board of the
National Center for AIDS/STD Control and Prevention, Chinese
Center for Disease Control and Prevention (approval
Between January 1, 2006 and December 31, 2012, there were
394,294 individuals newly diagnosed with HIV infection in China.
Patients under 15 years of age (N = 5,798) were excluded from the
study cohort. Of the remaining 388,496 newly diagnosed
individuals, 221,980 (57.1%) patients received a baseline CD4
cell count within 6 months of HIV diagnosis over the six-year
study period (Table 1).
The number of newly identified HIV cases with measured
baseline CD4 counts more than doubled between 2006 and 2012,
increasing from 35,087 to 81,416. The proportion of newly
diagnosed individuals who received a baseline CD4 cell count test
within 6 months increased from 20.0% in 2006 to 76.9% in 2012.
National policies recommend CD4 cell count testing within 14
days after diagnosis of HIV infection. Our study found that the
proportion of newly diagnosed individuals who received baseline
CD4 cell count testing within 14 days increased from 10.9% in
2006 to 46.1% in 2012 (Table 1).
The median baseline CD4 cell count of individuals who
received timely testing over the study period was 294 cells/ml
(IQR: 130454). Over half of the patients (N = 130,442, 58.8%)
had baseline CD4 cell counts ,350 cells/ml, and 76,582 patients
(34.5%) had baseline CD4 cell counts ,200 cells/ml. Less than a
quarter of patients (N = 43,547, 19.6%) had baseline CD4 cell
counts $500 cells/ml (Table 1).
The median baseline CD4 cell count increased slightly by each
calendar year over the study period from 221 cells/ml (IQR: 63
410) in 2006 to 314 cells/ml (IQR: 159460) in 2012. The
percentage of individuals with baseline CD4 cell counts ,200
cells/ml, indicating advanced disease, decreased from 46.9% in
2006 to 30.7% in 2012. The percentage of individuals diagnosed
with baseline CD4 cell counts $500 cells/ml, indicating a recent
acquisition of HIV infection, has remained relatively stable
Characteristics associated with receiving baseline CD4 cell
count testing within 6 months were being female, being married,
having attained middle school education or higher, having
acquired HIV through male-to-male sexual contact or commercial
blood plasma donation, and being diagnosed with HIV infection
at a voluntary counseling and testing (VCT) clinic (Table 2). A
total of 34,248 newly diagnosed individuals (8.8%) died within 6
months after HIV diagnosis. Of these individuals, 23,661 (69.1%)
had not received CD4 cell count testing.
In the univariate logistic regression model, factors associated
with baseline CD4 cell count testing within 6 months of HIV
diagnosis were age group, gender, marital status, education level,
ethnicity, employment as a migrant worker, route of HIV
transmission, site of HIV diagnosis, and year of HIV diagnosis
No. (%) of subjects with
baseline CD4 cell count
Year of HIV diagnosis
Single, divorced, or widowed 175776
Married or lives with partner 201596
Middle school or above 231092
Primary school or below 145077
Farmer or rural laborer 178391
Minority group 117896
Route of HIV infection
Heterosexual contact 222148
Male-to-male sexual contact 44840
Injection drug use 76815
Sexual contact and injection drug 5030
Blood (plasma) donation 17204
Site of HIV diagnosis
VCT centers 110360
Detention centers 47218
*Includes laborer, unemployed, businessman, student, public servant, and unclear.
**Includes targeted intervention project, physical examination for sex workers, and unclear.
***Defined as having migrated from the registered region of residence to another region for at least six months.
In the multivariate logistic regression model (Table 2),
predictors for not receiving CD4 cell count testing with 6 months
included being male (OR: 1.17, 95% CI: 1.151.19), age 55 years
or older (OR: 1.03, 95% CI: 1.001.06), educational attainment of
primary school or below (OR: 1.30, 95% CI: 1.281.32),
occupation as a farmer or rural laborer (OR: 1.16, 95% CI:
1.151.18), route of HIV transmission classified as injecting drug
use (OR: 2.07, 95% CI: 2.022.12) or sexual contact and injecting
drug use (OR: 1.87, 95% CI: 1.761.99), HIV diagnosis in a
hospital (OR: 1.91, 95% CI: 1.881.95) or a detention center (OR:
1.75, 95% CI: 1.701.80), and being a migrant worker (OR: 1.55,
95% CI: 1.531.58). Factors associated with timely CD4 testing
included being married or cohabiting with a partner (OR: 0.87,
95% CI: 0.860.89), being of Han ethnicity (OR: 0.76, 95% CI:
0.740.77), and route of HIV transmission classified as
male-tomale sexual contact (OR: 0.62, 95% CI: 0.600.64) or commercial
blood plasma donation (OR: 0.83, 95% CI: 0.810.87).
Baseline CD4 cell counts were also analyzed by the route of
HIV infection and the year of reporting (Table 3). There were
significant differences in the distributions of CD4 cell counts by the
routes of HIV infection and by the year of HIV diagnosis
(heterosexual contact: x2 = 119.63, p,0.01; male-to-male sexual
contact: x2 = 21.07, p,0.01; IDUs: x2 = 191.85, p,0.01; and
commercial blood plasma donation: x2 = 66.95, p,0.01).
Individuals infected through heterosexual contact and commercial blood
plasma donation were more likely to have baseline CD4 cell
counts ,200 cells/ml than individuals infected by male-to-male
sexual contact, injection drug use, or sexual contact and injection
The median baseline CD4 cell counts for all age groups
increased slightly from 2006 to 2012 (Figure 1). However, the
median baseline CD4 cell count for patients 45 years and older
remained below 250 cells/ml over the study period. The median
baseline CD4 cell counts of patients by route of transmission show
none-to-little increase over the study period (Figure 2). Individuals
infected through heterosexual contact and through commercial
blood plasma donation had considerably lower median baseline
CD4 cell counts than other subgroups.
The aim of our study was to identify the proportion of
HIVpositive individuals in China who received baseline CD4 testing
within 6 months and characteristics associated with failing to
receive testing within 6 months. CD4 cell count measurements are
a standard component of HIV testing algorithms to monitor
disease progression. Few past studies in China  have evaluated
access to baseline CD4 cell count testing, and this is the first study
to present results on a national scale.
In the era of Treatment as Prevention, early HIV detection,
timely monitoring of disease progression, and early linkage to
ART are critical steps to curbing the spread of HIV [25,26,27,28].
In the United States, about 77% of HIV-diagnosed individuals are
linked to care within 34 months, and 51% were retained in
ongoing care . With effective interventions such as the
addition of case management, the proportion of HIV-positive
patients linked to ongoing care can be significantly increased
compared to those who receive the standard of care . As
China continues to develop and expand its national AIDS
programs, including the NFATP, it will be critical to have regular
assessment and monitoring of the programs ability to link newly
identified HIV-positive individuals to timely CD4 testing and
To monitor the implementation of the national AIDS programs,
NCAIDS developed annual quantitative targets of core program
elements, including the proportion of people known to be living
with HIV whose CD4 cell counts were monitored at least once a
year, to determine anti-retroviral therapy eligibility . For
individuals nationwide diagnosed with HIV and AIDS, this
proportion rose from 45.3 and 10.1% in 2007 to 54.2 and
62.5% in 2009, respectively . Expanding on this previous
finding, this current study shows that significant progress has also
been made in increasing baseline CD4 cell count testing among
HIV newly diagnosed individuals, as evidenced by the increase in
CD4 cell count testing within 6 months from 20.0% in 2006 to
76.9% in 2012. The increases in CD4 monitoring of both new
HIV cases and previously diagnosed cases were facilitated by
structural expansions of the national AIDS programs and increases
in the availability of testing materials/equipment [20,31].
National policies recommend that the blood draw for the
baseline CD4 cell count test should be completed at the first
follow-up visit, which is scheduled at 14 days following the
diagnosis. In our study, about 53.7% of individuals diagnosed in
2012 did not receive baseline CD4 cell count testing by the 14-day
benchmark, and 23.1% did not receive CD4 cell count testing
within 6 months. We identified several individual-level risk factors
for failing to receive CD4 cell count testing within 6 months: age
55 years or older, male, primary school education or below, route
of HIV transmission categorized as injection drug use or combined
sexual contact and injection drug use, being diagnosed at a
hospital or a detention center, and being a migrant worker. Some
population-level factors are also likely to influence the obtainment
and timing of CD4 testing. Until recent years, many county
hospitals did not have the CD4 cell count testing equipment. In
several regions with very low HIV prevalence, some counties and
municipalities only had one CD4 detection machine for the entire
area. This was likely to have delayed CD4 cell count testing for a
small propotion of newly diagnosed HIV-positive individuals.
Other population-level factors may include stigma and long
distances between residences and clinics .
In our study, the majority of newly HIV diagnosed individuals
were infected through heterosexual contact (Table 2). This is in
accordance with recent literature indicating that sexual
transmission has become the dominant mode of HIV transmission in
China [23,33,34]. Over 60% of these individuals had baseline
CD4 cell counts ,350 cells/ml over the study period (Table 3),
which is a higher proportion than those infected by male-to-male
sexual contact or injection drug use. While HIV in China was
historically driven by epidemics among injection drug users
(IDUs), China will need to adjust to the challenges of facing an
HIV epidemic that is predominantly spread by sexual contact.
The group with the highest proportion (over 75%) of CD4 cell
counts ,350 cells/ml were individuals infected through
commercial blood plasma donation. In the mid-1990s, there were major
outbreaks of HIV through unsafe commercial blood and plasma
donations [35,36]. The extent of the epidemic was identified
through large-scale targeted screening interventions among former
paid plasma donors .
The two populations who had the highest median baseline CD4
counts were IDUs and men who have sex with men (MSM). This
suggests that outreach efforts to reach these high-risk populations
have produced some success in promoting early and regular HIV
screening. However, MSM had the highest percentage of timely
CD4 testing (78.7%) while IDUs had the lowest percentage
(34.9%) when comparing subpopulations by route of transmission.
Past research studies have similarly noted that MSM present with
higher median CD4 levels compared to other risk groups . In
our study cohort, the relative success in linking HIV-positive MSM
to timely CD4 testing may also be due to a comprehensive
prevention and control program in sixty-one cities from 2008 to
2009 targeted towards MSM. This program was carried out with
the support of MSM community groups. This program led to
policies and additional ongoing intervention programs that address
HIV prevention, HIV diagnosis and CD4 cell count testing among
The barriers for IDUs to access medical care are
welldocumented . In China, many IDUs are engaged in migrant
work, have unstable lifestyles, experience stigma and
discrimination from health providers, and face the fear of arrest due to the
illegality of drug use in China . Our study noted a slight
increase of CD4 cell count levels in IDUs over the study period. In
recent years, several intervention measures been taken to decrease
illicit drug use and to strengthen prevention and control of HIV
transmission among IDUs [39,40]. Another significant strategy for
engaging the HIV-positive IDU population in regular care is to
expand access to methadone maintenance treatment, which has
been shown to independently promote linkage to HIV care and
Our study found that older patients were more likely to present
at late disease stages, which has been noted previously in the
literature . There is currently very limited research [43,44] on
elderly HIV patients in China, who are not typically considered a
vulnerable population for contracting HIV. According to data in
CRIMS, the number of newly diagnosed individuals who were 55
years old or older has significantly increased in recent years
[unpublished data, NCAIDS, 2013], as it has in the United States.
Further studies are needed to explore issues related to the
diagnosis and treatment of elderly HIV-positive patients in China.
Perhaps due to the implementation of the national AIDS
programs  the proportion of patients with advanced HIV
disease (CD4 count ,200 cells/ml) has declined slightly since 2007.
Of the 221,963 individuals who received timely baseline CD4
testing, the proportion of patients diagnosed late with HIV has
declined slightly over the study period from 2006 to 2012. In our
study cohort, 34.5% of individuals (N = 76580) had baseline CD4
counts of ,200 cells/ml and 58.8% (N = 130434) had baseline
CD4 counts of ,350 cells/ml (Table 1). Late diagnosis and late
ART initiation are strongly associated with negative health
outcomes, including suboptimal CD4 increases with treatment, a
high rate of opportunistic infections, and increased risk of
mortality . Early identification of HIV and prompt monitoring
are critical to improving patient outcomes and reducing disease
Our study has several limitations. First, all data is reported by
local providers and may have not been uploaded to the national
databases in a timely manner. While providers and CDC staff
review the data for completeness and accuracy, there may be some
errors in the database. Second, in most cases, the route of infection
was self-reported by the individual, and some misreporting may
have occurred due to stigma, particularly for the categories of
male-to-male sexual contact and injection drug use. Third, while
we attempted to reduce the influence of confounding variables by
using multivariate analysis, it remains possible that there was
confounding by unmeasured variables. Fourth, our study analysis
did not assess disease progression of the newly diagnosed HIV/
AIDS patients by clinical staging or viral load testing. This
information is available elsewhere in CRIMS; however, a full
discussion of monitoring strategies over the study period is beyond
the scope of this paper. Finally, our study did not exclude
individuals who died between their diagnosis and the 6-month
benchmark for timely CD4 testing. These patients were included
in the 8% of the study cohort who were indicated as lost to
followup and subsequently categorized as not having received timely
CD4 testing. A study that only assesses individuals who were still
living 6 months after HIV diagnosis may produce higher rates of
timely CD4 testing.
The risk factors identified in this study should guide future
intervention strategies to increase early HIV diagnosis and CD4
cell count testing among key populations. In recent years, an
increasing number of HIV cases have been identified at VCT
clinics at local CDC sites, which have higher rates of linkage to
baseline CD4 testing. Regional strategies that have achieved
success in reducing loss to follow up and increasing linkage to care
have included in-parallel Western blot confirmation testing and
baseline CD4 testing (Yunnan) and compressing the timeframe
from screening, confirmation, and CD4 testing (Guangxi).
This studys evaluation of baseline CD4 cell count testing after
HIV diagnosis provides a valuable reference for further increasing
testing coverage and linkage to care. Despite significant
improvement, a high proportion (23.1%) of HIV-positive patients still
failed to receive timely CD4 count testing in 2012, the last year of
the study. To shorten the time to CD4 cell count testing and to
improve access to regular testing and treatment, there should be
efforts to dramatically improve referrals and integration of patient
tracking between the health facilities responsible for patient
followup, CD4 cell count testing, and ART delivery.
The authors thank all of the health care and laboratory staff who
participated in data collection for this study and conducted CD4 baseline
Disclaimer: The opinions expressed herein reflect the collective views
of the co-authors and do not necessarily represent the official position of
the National Center for AIDS/STD Control and Prevention, Chinese
Center for Diseases Control and Prevention. Funding organizations had no
role in the design and conduct of the study; collection, management,
analysis, and interpretation of the data; and preparation, review, or
approval of the manuscript.
Conceived and designed the experiments: HT YM ZW. Performed the
experiments: HT JH JX LW QQ. Analyzed the data: HT. Contributed
reagents/materials/analysis tools: HT JH JX LW QQ. Wrote the paper:
HT CS ZW. Intepreted results: RD. Edited and revised manuscript: RD.
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