Cancer is a leading cause of death among people living with HIV/AIDS (PLWHA). We conducted a systematic review and meta-analysis to evaluate prevalence of cancer risk factors among Chinese PLWHA based on 102 articles. Random effects meta-analysis was used to calculate the summary prevalence estimate (sPrev) and 95% confidence interval (CI) for each cancer risk factor by demographic group. Overall, the sPrev for each risk factor among Chinese PLWHA was: 41.1% (95% CI: 35.3–46.9%) for current smoking; 30.3% (95% CI: 23.3–37.4%) for current alcohol consumption; 24.4% (95% CI: 14.7–30.2%) for overweight and obesity; 12.5% (95% CI: 10.6–14.3%) for hepatitis B virus infection; 29.1% (95% CI: 23.6–34.5%) for hepatitis C virus infection; 33.9% (95% CI: 24.3–43.5%) for high-risk human papillomavirus infection from cervical samples and 78.6% (95% CI: 69.4–87.7%) from anal samples; 2.7% (95% CI: 0.7–4.7%) for Epstein-Barr virus (EBV) immunoglobulin M (IgM) positivity, 94.7% (95% CI: 90.7–98.8%) for EBV IgG positivity and 25.6% (95% CI: 12.4–38.8%) for EBV DNA positivity; 14.9% (95% CI: 12.4–17.4%) for human herpes virus 8 infection. The prevalence of major cancer risk factors was high among PLWHA in China, suggesting an urgent need for interventions to reduce cancer risk in this high-risk group.
Highly active antiretroviral therapy (HAART) or combination antiretroviral therapy (cART) has drastically reduced mortality in people living with HIV/AIDS (PLWHA)1,2,3. For PLWHA, cancer is now one of the leading causes of death with higher incidence of both AIDS-defining cancers (ADCs) and non-AIDS-defining cancers (NADCs) compared with the general population4,5,6,7,8. In particular, NADCs have shown increasing incidence and account for a rising proportion of all cancers in this population4. China has implemented HAART nationally since 2003. In a Chinese cohort, substantially elevated standardized incidence ratios of NADCS and ADCs were observed, and cancers occurred at a younger age for PLWHA compared to the general population9. Accumulated evidence suggests that HIV-induced immunodeficiency and prevalent risk factors other than HIV infection independently contribute to the increased cancer risk among PLWHA10, 11. The major risk factors associated with leading causes of cancer deaths include tobacco use (associated with lung, colorectal, stomach, and liver cancer), alcohol consumption (colorectal and liver cancer), overweight/obesity (breast and colorectal cancer), and viral infections (liver, stomach, and cervical cancer)12, 13. Numerous independent studies have reported prevalence of cancer risk factors among PLWHA in China. However, the researches vary in time and geographic areas, and do not provide a comprehensive overview of cancer risk factors epidemics for PLWHA in China. We conducted a meta-analysis among PLWHA in China to describe the prevalence of major cancer risk factors including tobacco smoking, alcohol consumption, overweight and obesity, and cancer-related viral infections such as hepatitis B virus (HBV), hepatitis C virus (HCV), human papillomavirus (HPV), Epstein-Barr virus (EBV) and human herpes virus 8 (HHV8). Prevalence estimates among Chinese PLWHA were compared with the general population or uninfected comparison groups from the same study when available.
The process of study selection
The process of selection of publications and the numbers of articles for each cancer risk factor are presented in Table 1. A total of 3,955 peer-reviewed research articles were identified from four databases: PubMed (219), CNKI (2,381), Wanfang Data (586), and CQVIP (769). We excluded 3,407 articles after screening titles and abstracts. Among the remaining 548 studies (101 in English and 447 in Chinese), we further excluded 446 studies during full-text review for the following reasons: 171 were studies with an irrelevant population, 138 had no prevalence estimate, 33 did not present original data, 44 were reviews, 39 had a small sample size (less than 100), and 21 were redundant articles. Finally, 102 eligible publications (35 in English and 67 in Chinese) contributed to the meta-analyses14,15,16,17,18,19,20,21,22,23,24,25,26,27,28,29,30,31,32,33,34,35,36,37,38,39,40,41,42,43,44,45,46,47,48,49,50,51,52,53,54,55,56,57,58,59,60,61,62,63,64,65,66,67,68,69,70,71,72,73,74,75,76,77,78,79,80,81,82,83,84,85,86,87,88,89,90,91,92,93,94,95,96,97,98,99,100,101,102,103,104,105,106,107,108,109,110,111,112,113,114,115. One additional study with unique data on HIV uninfected population was included for comparison analysis116.
Characteristics of eligible publications
Table 2 shows the characteristics of the eligible articles. Ninety-two cross-sectional studies, 7 prospective cohort studies38, 52, 60, 80, 94, 100, 101, 2 retrospective cohort studies68, 79 and 1 intervention trial36 were included. Most studies (99) were based in clinics or hospitals for PLWHA recruitment, 2 were population-based72, 73 and 1 study sampled was recruited from jail75. The 102 eligible studies covered 20 provinces and 4 municipalities in China. The median sample size for PLWHA was 295 [interquartile range (IQR): 178–551]. Seventy-five articles reported the median or mean age, and the median of the median or mean age was 37.2(IQR: 34.0–41.0). Of the 95 articles reporting gender distribution, the median proportion of male was 72.6% (IQR: 61.3–86.9%). Of the 16 articles reporting the proportions of MSM, the median was 79.1% (IQR: 63.9–100.0%). Of the 23 articles reporting the proportions of IDU, the median was 74.8% (IQR: 40.4–100.0%). Of 26 articles reporting the proportions on ART, the median was 67.5% (IQR: 45.3–100.0%).
Prevalence estimates for cancer risk factors
Table 3 presents the group-specific sPrev estimates for each cancer risk factor among PLWHA and the corresponding prevalence in the Chinese general population. Selected forest plots for important cancer risk factors are shown in Fig. 1. Moreover, Table 4 presents the results comparing the prevalence between PLWHA and HIV uninfected groups if data were available from the same studies.
A total of twenty-six articles reported prevalence of smoking among PLWHA. Overall, the sPrev for current smoking was 41.1% (95% CI: 35.3–46.9%, I 2 = 96.0%) in PLWHA based on the meta-analysis of 21 studies. The sPrev of current smoking was 63.2% (95% CI: 39.7–86.8%) for male PLWHA and was 3.4% (95% CI: 2.2–4.6%) for females, based on the 5 studies with gender-specific prevalence. Overall, the sPrev of ever and former smoking was 51.9% (95% CI: 42.8–61.1%) based on 5 studies and 13.9% (95% CI: 0.3–27.6%) based on 3 studies, respectively (Table 3). Significantly higher smoking prevalence was observed in PLWHA than in HIV uninfected subjects when compared in the same studies (Table 4).
Thirty-two publications reported prevalence of alcohol consumption among PLWHA. Overall, the sPrev for current alcohol consumption was 30.3% (95% CI: 23.3–37.4%, I 2 = 98.6%) based on the meta-analysis of 25 studies. Gender-specific estimates showed that the sPrev of current alcohol consumption was 26.9% (95% CI: 18.5–35.4%, I 2 = 91.8%) in male PLWHA based on 5 studies and was 3.3% (95% CI: 1.2–5.4%, I 2 = 67.8%) in females based on 3 studies. MSM presented a current drinking sPrev of 35.7% (95% CI: 18.9–52.5%) based on 3 studies while IDUs presented a current drinking sPrev of 13.1% (95% CI: 8.3–17.9%) based on 2 studies. Overall, the sPrev of ever and former alcohol drinking was 64.3% (95% CI: 60.8–67.7%) and 17.8% (95% CI: 3.6–32.0%), respectively (Table 3). Six studies compared the prevalence of alcohol consumption between PLWHA and HIV negative controls, 5 of which reported no significant difference while 1 reported a lower prevalence in HIV positive MSM than in HIV negatives (33.8% vs. 50.0%, P = 0.004) (Table 4).
Overweight and obesity
Six studies reported the prevalence of overweight and obesity (BMI ≧ 24 kg/m2) among PLWHA, with a sPrev of 24.4% (95% CI: 14.7–30.2%, I 2 = 94.3%) (Table 3).
Hepatitis B virus infection
Twenty-nine articles reported the prevalence of HBV infection defined as HBsAg seropositivity in PLWHA. The sPrev of HBsAg was 12.5% (95% CI: 10.6–14.3%, I 2 = 96.1%), 10.4% (95% CI: 8.1–12.8%, I 2 = 66.2%) and 13.4% (95% CI: 11.0–15.8%, I 2 = 89.0%) in overall, female and male groups, respectively. The highest sPrev of HBsAg was among IDUs (32.8%, 95% CI: 0.0–70.7%, I 2 = 99.7%) (Table 3). In a study reporting comparisons with HIV uninfected group, HBsAg prevalence in PLWHA was also higher in IDU group (18.9% vs. 11.3%, P = 0.013) (Table 4).
Hepatitis C virus infection
Forty-two publications reported the prevalence of HCV infection defined as HCV antibody seropositivity. Based on the meta-analysis of 31 studies, the overall HCV sPrev was 29.1% (95% CI: 23.6–34.5%, I 2 = 99.5%). Male PLWHA showed a sPrev of 47.1% (95% CI: 32.2–62.0%, I 2 = 99.8%) based on 15 studies, while female PLWHA had a sPrev of 29.9% (95% CI: 23.2–36.6%, I 2 = 98.4%) based on 16 studies. The highest HCV prevalence was found in IDU group with a sPrev of 83.4% (95% CI: 63.8–100.0%, I 2 = 99.8%) (Table 3). Higher prevalence was found in HIV infected IDUs comparing to HIV-negative participants in the same study (Table 4).
Human papillomavirus infection
Nine studies reported prevalence of HPV infection in PLWHA. The number of studies for each group-specific meta-analysis ranged from 2 to 4. For cervical samples, the HPV sPrev of both any type and high-risk type was 42.0% (95% CI: 37.7–46.3%, I 2 = 34.3%) and 33.9% (95% CI: 24.3–43.5%, I 2 = 90.2%), respectively. For anal samples, the sPrev among male PLWHA of any type of HPV was 78.6% (95% CI: 69.4–87.7%, I 2 = 81.5%), and the sPrev of high-risk type was 52.1% (95% CI: 27.9–76.2%, I 2 = 96.3%). Similar sPrev was observed among HIV positive MSM (Table 3). All comparisons between PLWHA and HIV uninfected group reported significantly higher prevalence of HPV in PLWHA from the same studies (Table 4).
Epstein-Barr virus infection
Nine publications presented the prevalence of Epstein-Barr virus infection. The number of studies for meta-analysis ranged from 1 to 4 when stratified by EBV testing method and demographic groups. Immunoglobulin M (IgM) was tested in 4 studies and the sPrev was 2.7% (95% CI: 0.7–4.7%, I 2 = 89.7%). IgG was tested in 2 studies, and the sPrev in overall, female and male groups was 94.7% (95% CI: 90.7–98.8%, I 2 = 85.5%), 92.5% (95% CI: 88.3–96.7%, I 2 = 61.1%) and 96.8% (95% CI: 93.6–100.0%, I 2 = 71.9%), respectively. DNA from peripheral blood was tested in 2 studies, and the overall sPrev was 25.6% (95% CI: 12.4–38.8%, I 2 = 90.4%). One study reported the prevalence of 27.1% (95% CI: 16.7–37.6%) in female and 34.2% (95% CI: 27.4–41.0%) in male PLWHA for EBV DNA positivity (Table 3). One study tested DNA in saliva from PLWHA and the prevalence was 82.0% (95% CI: 77.2–86.8%), which was higher than the prevalence in uninfected comparison group (30.0%) (Table 4).
Human herpes virus 8 infection
Four articles reported the prevalence of HHV8 infection in PLWHA, of which 3 studies had serum antibody and one had saliva DNA tested. The prevalence of saliva DNA positivity was 14.3% (95% CI: 12.4–17.4%). For serum antibody, the sPrev in overall, female, male and IDU groups was 14.9% (95% CI: 12.4–17.4%, I 2 = 0.0%), 12.1% (95% CI: 0.0–25.3%, I 2 = 92.9%), 17.7% (95% CI: 8.3–27.2%, I 2 = 85.0%) and 16.3% (95% CI: 0.0–35.7%, I 2 = 97.0%), respectively. The highest serum HHV8 prevalence was among MSM (32.3%, 95% CI: 24.2–40.4%) (Table 3). Significantly higher prevalence was consistently found in PLWHA than in the HIV-negative comparison groups from the same studies (Table 4).
Sensitivity analyses and publication bias
We recalculated each sPrevomi for all studies except the “omitted” one in turn, with the results of full meta-analyses named as sPrevall. The influence was evaluated by |sPrevomi - sPrevall|/sPrevall. All observed influences were less than 15% in our sensitivity analyses. Influences greater than 10% could be found in smoking among females (3.4% for all studies versus 3.1% for studies with higher potential for bias omitted) and males (63.2% vs. 55.4%), alcohol consumption among males (26.9% vs. 30.2%), overweight and obesity (22.4% vs. 25.8%), and HCV infection among IDUs (83.4% vs. 93.0%).
In our meta-analysis, substantial publication bias was significantly observed by the Egger test and/or the Begg test in estimating the overall sPrev of smoking (P-value for Egger test was 0.028, P-value for Begg test was 0.057), the overall sPrev of alcohol consumption (P Egger = 0.002, P Begg = 0.007), the overall sPrev of HBV infection (P Egger = 0.791, P Begg = 0.018), and the sPrev of HCV infection overall (P Egger = 0.141, P Begg = 0.014), in females (P Egger = 0.015, P Begg = 0.344), and in males (P Egger = 0.095, P Begg = 0.621).
To our knowledge, this is the first comprehensive meta-analysis to report the summary prevalence of cancer risk factors among PLWHA in China. We found that Chinese PLWHA had higher prevalence of smoking, alcohol consumption, and virus infections including HBV, HCV, HPV, EBV and HHV8, but had lower prevalence of overweight and obesity when compared with the HIV-negative participants from the same studies and the Chinese general population.
For such two modifiable behavioral risk factors as tobacco and alcohol use, Chinese PLWHA showed high prevalence of tobacco smoking and alcohol drinking overall and especially among males. For example, the smoking prevalence is 53.3% for general Chinese men117, while the sPrev is even higher, reaching 63.2% for male PLWHA. Such elevated smoking prevalence in HIV infected people was also found in independent Chinese studies comparing with HIV-negative participants24, 35, and in a meta-analysis in western countries with lower smoking prevalence in general population118. The sPrevs also varied by group-specific analyses, with certain subgroups at higher risk in tobacco and alcohol use. The overall sPrev of alcohol drinking is close to the prevalence from Chinese general population (30.3% vs. 28.8%)119 while MSM showed slightly higher sPrev (35.7%) and IDUs showed significantly lower estimate (13.1%). As group I carcinogens defined by IARC, tobacco smoking and alcohol consumption are not only associated with a series of human cancers, but also with other important chronic diseases. Based on our summarized estimates, the high prevalence of tobacco and alcohol use especially among male PLWHA suggested the need for an effective and more targeted intervention in smoking and drinking behaviors as well as a close observation of their roles in HIV and cancer disease progression to reduce morbidity and to improve quality of life in this aging population with prolonged life expectancy.
The prevalence of cancer-related viral infections, including HBV, HCV, HPV, EBV and HHV8 infection, are significantly higher in PLWHA than in general Chinese population120,121,122,123,124,125,126, shown by the results from both meta-analyses and independent studies. By demographic group, 10.4–13.4% of PLWHA were HBsAg positive, and 29.1–47.1% were HCV antibody positive. Moreover, the highest prevalence of HBV (32.8%) and HCV (83.4%) infection were both found in IDUs, probably due to the shared transmission route with HIV. For female PLWHA, the sPrev of both any type of HPV (42.0%) and high-risk type of HPV (33.9%) from cervical samples were higher than the prevalence in Chinese general population aged 15–60 years122, 123. Moreover, we found that in anal samples collected from male PLWHA, the HPV prevalence was very high no matter whether they were MSM or not. These observations call attention since HPV infection is also a risk factor for anal cancer. The high seropositivity of EBV-IgG was close to the prevalence reported earlier in the Chinese general population (97.6%)125. Although the latter statistic might be limited to experimental conditions and in need of update, it is believed that EBV infection is very common among adults127. Moreover, several studies suggested higher detection rate of EBV DNA among HIV-infected subjects compared to HIV-negatives, suggesting potentially more active viral application in immune-suppressed population110, 128, 129. Last but not least, the overall seroprevalence of HHV8 infection was 14.9%, higher than the prevalence in the Chinese general population126, with the highest prevalence found in MSM (32.3%, 95% CI: 24.2–40.4%).
The overall prevalence of overweight and obesity among PLWHA was 22.4% (95% CI: 14.7–30.2%), lower than the prevalence of 42.6% in Chinese general population119. This is similar with the observations in western countries that the obesity prevalence was lower in HIV population118. We need to further observe the change in weights in PLWHA to have a better understanding and balance in control of both the HIV wasting syndrome and risk for obesity-related cancers and chronic diseases.
A meta-analysis was recently published on prevalence of risk factors for NADCs among PLWHA in western high-income countries118, which, consistent with our analysis, also observed higher prevalence of cancer risk factors among PLWHA than the general population. However, the prevalence level seems to be different between PLWHA in western countries and in China. Compared with PLWHA in western countries, PLWHA in China seemed to have higher prevalence in alcohol consumption (30.3% versus 24.0%), HCV (29.1–47.1% versus 23.0–28.0%) and HBV (10.4–13.4% versus 4.0–5.0%) infection, but lower prevalence in smoking (41.1% versus 54.0%), overweight and obesity (22.4% versus 53.0%) and HPV infection (cervical high-risk types: 33.9% versus 46.0%, anal high-risk types: 52.1% versus 66.0%). Thus, the spectrum of cancers among PLWHA in China might be different from that in western countries and further investigations and interventions might be targeted to different high-risk groups.
Substantial heterogeneity across subgroups was significantly observed with I 2 values larger than 90%. This was expected since heterogeneity could be found in almost all ‘overall’ groups, because we could not know the proportion of genders or behavioral characteristics in these study populations across publications. So was the case in ‘male’ groups, which could have different proportions of heterosexual male, MSM and IDU. Meanwhile, extensive heterogeneity still existed in specific demographic groups such as female, MSMs and IDUs. This could be attributable to many potential factors including study design, sampling method, geographical regions, study period, age, ethnicity, the definition or method of measurement for risk factors, differences in CD4+ and the length of time in ART, etc118, 130. Insufficient number of studies has limited our further stratification analysis. However, random effects models were used to minimize the impact of heterogeneity on precision and provided rational approximations of pooled prevalence estimates in our meta-analyses. Sources of heterogeneity should be further explored in the future with more research for specific subgroups.
Several limitations in our study should be noted. First, there might be some information bias since the methods for measuring these risk factors might vary across studies. Most (69.2%) studies did not give a clear definition of smoking habits (e.g., ever smoking: have smoked at least 100 cigarettes in life; Current smoking: smoked within the past 30 days) or did not have a precise measurement for smoking dose or frequency, while only 50% of studies presented the range of time (past 30 days or a day) for current alcohol drinking. Although we tried to extract information from reference studies using standardized definitions, misclassification might still exist since not every study gave a clear definition for each risk factor. Also, the testable HPV subtypes varied across studies, and therefore, underestimation of HPV prevalence might have occurred in studies with fewer testable HPV subtypes. Second, the representativeness of our meta-analyses is compromised since it covered 24 but not all 31 provinces or municipalities in China, underscoring the need for expanded research and surveillance efforts on cancer risk factors among PLWHA all over the country. Third, comparability was not considered across different sources of data due to time lags among studies. Some risk factors may present a temporal trend, some may not. For those with an increasing or decreasing trend, it may have compromised the comparison. Fourth, as prevalence estimates of cancer risk factors can vary with characteristics including age, lack of matching for age and other factors also limited the validity of the comparisons between PLWHA and the general population. However, consistent results were still observed when stratified roughly by age where possible (Supplemental Table S1). Fifth, substantial publication bias was observed according to rigorous publication bias tests, and might be attributable to several factors, including the presence of extensive heterogeneity, which we have discussed above131, 132. The association between behavioral changes such as smoking and alcohol consumption and severity of HIV patients might lead to underestimation of prevalence of cancer risk factors among PLWHA.
Despite these limitations, the present study provides a broad overview of prevalence of cancer risk factors among PLWHA in China. Both in comparison with the Chinese general population and with the uninfected comparison groups, the studies reach a wide consensus on higher prevalence of cancer risk factors among PLWHA. Along with the management of HIV individuals and ART program, interventions to reduce cancer risk factors should also be implemented in this population. Cancer prevention measures in PLWHA should include smoking cessation, HBV and HCV treatment, vaccination against HBV and HPV, annual cervical and anal Pap tests and cancer screening according to relevant guidelines4, 133,134,135,136,137,138. Furthermore, a better understanding of cancer risk attributable to specific factors in different HIV infected groups is needed to develop strategies in preventing cancer.
We searched for peer-reviewed research articles published in English and Chinese from the following databases: PubMed, China National Knowledge Infrastructure (CNKI), Wanfang Data and Chinese Scientific Journals Fulltext Database (CQVIP). Using the Medical Subject Headings (MeSH) terms ‘China’ or ‘Taiwan’ with ‘HIV,’ ‘HIV Infections’ or ‘Acquired Immunodeficiency Syndrome’, the search also included MeSH terms for the specific cancer risk factors as follows: smoking (‘Smoking’ or ‘Tobacco Products’ or ‘Tobacco’ or ‘Tobacco Use’), alcohol consumption (‘Alcohol Drinking’ or ‘Alcoholism’ or ‘Alcoholic Intoxication’), overweight or obesity (‘Overweight’ or ‘Obesity’ or ‘Body Mass Index’ or ‘Body Weight’), HBV (‘Hepatitis B’), HCV (‘Hepatitis C’), HPV (‘Papillomavirus Infections’ or ‘Papillomaviridae’), EBV (‘Epstein-Barr Virus Infections’), and HHV8 (‘Herpesvirus 8, Human’). We also searched those MeSH terms and their abbreviations of each risk factor under the condition of ‘all fields’ in each database. Due to the large number of studies published on HBV and HCV infections among PLWHA in China, we restricted published data from January 1, 2013 to February 29, 2016 in order to use the latest published prevalence of HBV and HCV infections. For other cancer risk factors, data published from database inception to February 29, 2016 were included in the analyses.
One author (Jin Z-Y) identified relevant articles, excluding those with unrelated titles and abstracts before obtaining full-text references. Two independent authors (Jin Z-Y and Liu X) conducted full-text review. Cross-sectional, case-control, prospective or retrospective cohort and intervention trial studies were included. Studies with sample size greater than 100 were considered to have a sufficiently stable prevalence estimate to be qualified for inclusion in the study. Studies lacking original data for the numerator or denominator of the prevalence estimate were excluded. If information from one study had been published for more than once, we chose the publication with more detailed information such as prevalence estimates stratified by specific demographic groups, studies with a larger sample size, or those most recently updated.
Data were extracted and organized using Microsoft Excel (Version 2010, Microsoft Corp., Redmond, WA, USA). For each risk factor, the number of PLWHA with known status was recorded as the denominator and the number of positive subjects was recorded as the numerator. The participants with unknown status were excluded from the calculation. If an article contained more than one of the mentioned risk factors, we kept all of them. If the PLWHA were stratified into different groups such as females, males, men who have sex with men (MSM) or injection drug users (IDU), we included data from each subgroup for prevalence estimate. The definitions of smoking and drinking status including “ever/never”, “former/current” were based on the descriptions in the original studies when a clear definition is not available. We also extracted prevalence estimates for HIV uninfected comparison groups if data were available from the same study. Other information including the first author’s name, year of publication, study site, original study design, sampling frame, calendar years of research, major information for participants including the mean or median age, percentage of males, MSM, IDU, treatment with antiretroviral therapy (ART), and the measurement of risk factors were also extracted.
We also extracted prevalence estimates for cancer risk factors among the general population from the most representative surveys. For tobacco smoking, alcohol consumption, overweight and obesity, prevalence estimates were extracted from a national survey, which was carried out in Chinese adults (aged 18 years and over with the median age in the range from 45 to 49 years) at 162 disease surveillance points (DSPs) from 31 provinces in 2010117, 119. For HBV and HCV infections, prevalence estimates were obtained from a national serosurvey in 2006, of which participants were local residents aged 1–59 years (the median age was in the range from 15 to 59 years for HBV and in the range from 15 to 20 years for HCV) living in 31 provinces with 160 DSPs120, 121. For HPV infection, prevalence estimates were acquired from a nationwide investigation of female subjects aged 15–60 years in 37 Chinese cities in 2012, a review (age ranging from 15 to 59 years) and a population-based study among men aged 25–65 years (the median age was 43 years)122,123,124. For EBV infection, the prevalence estimate was extracted from a 1989 study by Liu125. For HHV8 infection, the prevalence estimate was from a systematic review and meta-analysis published in 2012126.
PLWHA were stratified into overall, female, male, MSM, and IDU demographic groups when such subgroups were available. The ‘Overall’ group represents PLWHA not restricted by gender or HIV transmission category (i.e., did not include a research on specific group by gender or HIV transmission category). Similarly, the ‘male’ group implies that PLWHA were not restricted by HIV transmission category. A meta-analysis of prevalence was performed for each risk factor by demographic group if there was more than one study included. Heterogeneity tests across subgroups were examined by Q-test (P < 0.1 refers to statistically significant heterogeneity) and I 2 values139, 140. Random effects models were used because of significant heterogeneity across subgroups141, 142. DerSimonian and Laird method (D-L) was applied to estimate the summary prevalence estimate (sPrev) and its 95% confidence interval (CI) for each risk factor143. If only one study was presented for the specific subgroup, we showed the single prevalence and its 95% CI. In sensitivity analyses, each sPrev was recalculated excluding studies evaluated as having higher potential for bias. Lastly, we performed a publication bias test when the meta-analysis included more than 10 studies144, 145. Publication bias was assessed through the Egger weighted regression and Begg rank correlation method (P < 0.1 represents statistically significant publication bias)146, 147. All the analyses were conducted by Stata 12.0 (Stata Corp LP).
Reniers, G. et al. Mortality trends in the era of antiretroviral therapy: evidence from the Network for Analysing Longitudinal Population based HIV/AIDS data on Africa (ALPHA). AIDS (London, England) 28(Suppl 4), S533–542, doi:10.1097/qad.0000000000000496 (2014).
Granich, R. et al. Trends in AIDS Deaths, New Infections and ART Coverage in the Top 30 Countries with the Highest AIDS Mortality Burden; 1990–2013. PloS one 10, e0131353, doi:10.1371/journal.pone.0131353 (2015).
Granich, R., Williams, B. & Montaner, J. Fifteen million people on antiretroviral treatment by 2015: treatment as prevention. Current opinion in HIV and AIDS 8, 41–49, doi:10.1097/COH.0b013e32835b80dd (2013).
Mitsuyasu, R. T. Non-AIDS-defining cancers. Topics in antiviral medicine 22, 660–665 (2014).
Calabresi, A. et al. Incidence of AIDS-defining cancers and virus-related and non-virus-related non-AIDS-defining cancers among HIV-infected patients compared with the general population in a large health district of Northern Italy, 1999–2009. HIV medicine 14, 481–490, doi:10.1111/hiv.12034 (2013).
Gopal, S. et al. Moving forward in HIV-associated cancer. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 32, 876–880, doi:10.1200/jco.2013.53.1376 (2014).
Hleyhel, M. et al. Risk of non-AIDS-defining cancers among HIV-1-infected individuals in France between 1997 and 2009: results from a French cohort. AIDS (London, England) 28, 2109–2118, doi:10.1097/qad.0000000000000382 (2014).
Hleyhel, M. et al. Risk of AIDS-defining cancers among HIV-1-infected patients in France between 1992 and 2009: results from the FHDH-ANRS CO4 cohort. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 57, 1638–1647, doi:10.1093/cid/cit497 (2013).
Zhang, Y. X., Gui, X. E., Zhong, Y. H., Rong, Y. P. & Yan, Y. J. Cancer in cohort of HIV-infected population: prevalence and clinical characteristics. Journal of cancer research and clinical oncology 137, 609–614, doi:10.1007/s00432-010-0911-y (2011).
Engels, E. A. et al. Elevated incidence of lung cancer among HIV-infected individuals. Journal of clinical oncology: official journal of the American Society of Clinical Oncology 24, 1383–1388, doi:10.1200/jco.2005.03.4413 (2006).
Borges, A. H., Dubrow, R. & Silverberg, M. J. Factors contributing to risk for cancer among HIV-infected individuals, and evidence that earlier combination antiretroviral therapy will alter this risk. Current opinion in HIV and AIDS 9, 34–40, doi:10.1097/coh.0000000000000025 (2014).
Torre, L. A. et al. Global cancer statistics, 2012. CA: a cancer journal for clinicians 65, 87–108, doi:10.3322/caac.21262 (2015).
Boffetta, P. & Hashibe, M. Alcohol and cancer. The Lancet. Oncology 7, 149–156, doi:10.1016/s1470-2045(06)70577-0 (2006).
Yao, N. et al. Antiretroviral therapy adherence among HIV/AIDS patients in Xi’an. Chin J AIDS STD 21, 184–188 (2015).
Wei, H. X. et al. Compliance of antiviral therapy and influencing factors in people living with HIV/AIDS in Nanjing. Chin J Epidemiol 37, 672–676 (2015).
Pu, Y. Analysis of 184 dual infection cases of TB/HIV. Modern Preventive Medicine 38, 2007–2008 (2011).
Xiao, Y. K., Ji, G. P., Liu, A. W., Tian, C. C. & Li, H. An analysis of adherence and its influencing factors among AIDS patients receiving ART in Anhui province. Chin J AIDS STD 20, 489–491 (2014).
Nurbiya, A. et al. Research of dietary patterns and KAP in HIV/AIDS infectors/patients in Xinjiang, 2013. Bull Dis Control Prev 29, 24–27 (2014).
Zhang, T. J., He, N., Ding, Y. Y., Jiang, Q. W. & Wood, C. Antibody responses to lytic and latent human herpesvirus 8 antigens among HIV-infected patients in central China. Bioscience trends 6, 122–129, doi:10.5582/bst.2012.v6.3.122 (2012).
Luo, X. F. et al. Tobacco use among HIV-infected individuals in a rural community in Yunnan Province, China. Drug and alcohol dependence 134, 144–150, doi:10.1016/j.drugalcdep.2013.09.023 (2014).
Bao, M. J., Dong, N., Zhang, L., Li, H. W. & Lu, H. Z. Survey and analysis of depression and social support of people infected with HIV. Chinese Nursing Research 29, 471–473 (2015).
Sun, W., Wu, M., Qu, P., Lu, C. M. & Wang, L. Psychological well-being of people living with HIV/AIDS under the new epidemic characteristics in China and the risk factors: a population-based study. International journal of infectious diseases: IJID: official publication of the International Society for Infectious Diseases 28, 147–152, doi:10.1016/j.ijid.2014.07.010 (2014).
Cheng, W. et al. The prevalence and relevant factors of hyperglycemia in AIDS patients receiving antiretroviral therapy in a single center. Chin J Intern Med 53, 446–449 (2014).
Cheng, S. H., Chu, F. Y., Lin, Y. S. & Hsueh, Y. M. Influence of age and CD4+ T cell counts on the prevalence of genital human papillomavirus infection among HIV-seropositive men who have sex with men in Taiwan. Journal of medical virology 84, 1876–1883, doi:10.1002/jmv.23413 (2012).
Cheng, S. H., Chu, F. Y., Wang, C. C. & Hsueh, Y. M. Screening and risk factors for anal cancer precursors in men infected with HIV in Taiwan. Journal of medical virology 86, 193–201, doi:10.1002/jmv.23825 (2014).
Zhang, H. Y. et al. The diversity of human papillomavirus infection among human immunodeficiency virus-infected women in Yunnan, China. Virology journal 11, 202, doi:10.1186/s12985-014-0202-3 (2014).
Wu, P. Y. et al. Metabolic syndrome among HIV-infected Taiwanese patients in the era of highly active antiretroviral therapy: prevalence and associated factors. The Journal of antimicrobial chemotherapy 67, 1001–1009, doi:10.1093/jac/dkr558 (2012).
Luo, X., Pan, D. M., Sang, J., Zheng, D. & Liu, L. J. Quality of Life of HIV/AIDS Patients in Ba’nan District at Chongqing. Chin J Derm Venereol 28, 276–278 (2014).
Dong, B. Q., Wang, X. W., Liu, W. & Liu, F. Y. Study on TB/HIV co-infection prevalence rate and affected factors among HIV/AIDS and TB patients. Journal of Applied Preventive Medicine 12, 193–197 (2006).
Li, L. et al. A study on lipids and C-reactive protein in HIV-infected patients. Chin J AIDS STD 17, 111–114 (2011).
Zhou, Y. Q. et al. The quality of life among people at the age of 50 years or above living with HIV/AIDS in Yunnan province. Chin J AIDS STD 21, 485–487, 492 (2015).
Tsai, M. S. et al. Reduced bone mineral density among HIV-infected patients in Taiwan: prevalence and associated factors. Journal of microbiology, immunology, and infection=Wei mian yu gan ran za zhi 47, 109–115, doi:10.1016/j.jmii.2012.08.026 (2014).
Zhou, J. R., Lu, X. M. & Li, B. L. The analesis of risk factors among AIDS patients complicated with tuberculosis. Zhejiang Clinical Medical Journal 17, 1485–1487 (2015).
Jiang, A. R. et al. The influence of HIV related lipodystrophy on life quality among AIDS patients with antiretroviral treatment. Chin J Dis Control Prev 18, 490–492 (2014).
Su, P. Y., Tao, F. B., Hao, J. H., Huang, K. & Zhu, P. Mental health and risk behavior of married adult HIV/AIDS subjects derived from paid blood donation in the rural of Anhui Province. Journal of Hygiene Research 39, 739–742 (2010).
Xie, Y. G. et al. Impact of nursing intervention on treatment compliance and survival quality among AIDS patients. Chin J Public Health 31, 1495–1497 (2015).
Zhao, T. T., Wei, B., Liang, H., Luo, H. Y. & Tang, X. Y. Influence factors of IHDS scores and its correlation with MMSE scale in minority AIDS patients. Chin J Public Health 28, 216–217 (2012).
Lin, R. Y., Li, H. & Liu, M. Pathogenesis characteristics of patients with HIV infection complicated with pulmonary tuberculosis and analysis of risk factors. Medical Journal of National Defending Forces in Southwest China 25, 734–737 (2015).
Zhang, Z. K., Sun, Y. H., Wu, H. Y. & Zhou, J. B. A study on Self-rated health and its influencing factors in HIV/AIDS people in the rural area of Fuyang city. Chin J Behavioral Med Sci 17, 37–40 (2008).
Gu, X. D., Zhang, H. W. & Wu, H. Clinical analysis of antiretroviral treatment of 506 HIV-infected patients. Chin J AIDS STD 19, 390–392 (2013).
Wang, C. S. et al. Effects of HIV infection on prognosis of HCV infected former blood donors. Journal of Zhengzhou University (Medical Sciences) 46, 53–56 (2011).
Lin, B., Sun, X. G., Lin, L., Wang, Z. Y. & Fu, J. H. Investigation on Adherence to Antiretroviral Therapy and Influence Factors of AIDS Patients in Shandong Province. Prev Med Trib 16, 207–208 (2010).
Ge, R., Luo, J. Y., Xu, W. X. & Zhu, W. T. Study on HAART adherence and related influencing factors among HIV/AIDS patients in Jiaxing City. Chin J Dis Control Prev 19, 206–208 (2015).
Li, J. et al. Influencing factors of drug treatment compliance among patients with HIV/AIDS in Jinan city of China. Journal of Shandong University (Health Science) 52, 106–110 (2014).
Liu, H. W. et al. Study on the immunological improvement of treatment and the influencing factors among AIDS patients receiving HAART in Henan Province. Chin J Dis Control Prev 18, 843–846 (2014).
Li, T. Z., Dai, L. L., Li, Z. C. & Wu, H. Clinical study of factors related to liver damage in people living with HIV/AIDS. Chin J AIDS STD 15, 252–253 (2009).
Muessig, K. E. et al. Suboptimal antiretroviral therapy adherence among HIV-infected adults in Guangzhou, China. AIDS care 26, 988–995, doi:10.1080/09540121.2014.897912 (2014).
Luo, X. F. et al. Alcohol use and subsequent sex among HIV-infected patients in an ethnic minority area of Yunnan Province, China. PloS one 8, e61660, doi:10.1371/journal.pone.0061660 (2013).
Hu, Y. et al. Anal human papillomavirus infection among HIV-infected and uninfected men who have sex with men in Beijing, China. Journal of acquired immune deficiency syndromes (1999) 64, 103–114, doi:10.1097/QAI.0b013e31829b6298 (2013).
Yang, C. B., Gu, X. D., Luo, X. W., Liang, C. & Cen, Y. H. Effectiveness of Highly Active Antiretroviral Therapy for Injection Drug Users with HIV/AIDS:A report of 102 cases. Chinese General Practice 13, 3188–3190 (2010).
Jin, H. et al. Risks and predictors of current suicidality in HIV-infected heroin users in treatment in Yunnan, China: a controlled study. Journal of acquired immune deficiency syndromes (1999) 62, 311–316, doi:10.1097/QAI.0b013e31827ce513 (2013).
Yen, Y. F. et al. HIV infection risk among injection drug users in a methadone maintenance treatment program, Taipei, Taiwan 2007–2010. The American journal of drug and alcohol abuse 38, 544–550, doi:10.3109/00952990.2012.702171 (2012).
Zhang, Y. Z., Ma, P., Zhou, J. F. & Wang, J. Application of NRS 2002 for nutritional screening in patients with AIDS. Chongqing Medicine 42, 2313–2314, 2317 (2013).
Dong, W. Y. et al. Multi-variate Logistic regression analysis of influencing factors of the depression in the HIV-infected out-patients. Chinese Journal of New Clinical Medicine 04, 429–433 (2011).
Zhou, Y. et al. Rates of HIV, syphilis, and HCV infections among different demographic groups of female sex workers in Guangxi China: evidence from 2010 national sentinel surveillance data. AIDS care 25, 1433–1441, doi:10.1080/09540121.2013.772282 (2013).
Pan, H. X., Huang, Q. F., Luan, Y., Liang, X. J. & Yu, L. B. Analysis of sentinel surveillance results of HIV, HCV and syphilis in drug users in Nanning during 2012–2014. Chin J Health Lab Tec 25, 3918–3919, 3923 (2015).
Shen, Q. F. et al. Relationship between HCV and Liver Injury among HIV-positives Receiving Methadone Maintenance Treatment in Dehong, Yunnan, province. Chin J AIDS STD 21, 926–929, 938 (2015).
Dong, Y. et al. Hepatitis B virus and hepatitis C virus infection among HIV-1-infected injection drug users in Dali, China: prevalence and infection status in a cross-sectional study. Archives of virology 160, 929–936, doi:10.1007/s00705-014-2311-0 (2015).
Zhou, L. et al. A research on HBV co-infection among new report HIV infected population in Taizhou. Chinese Primary Health Care 28, 71–74 (2014).
Liu, Y. et al. Hepatitis B virus infection in a cohort of HIV infected blood donors and AIDS patients in Sichuan, China. Journal of translational medicine 12, 164, doi:10.1186/1479-5876-12-164 (2014).
Zhang, F. et al. HIV, hepatitis B virus, and hepatitis C virus co-infection in patients in the China National Free Antiretroviral Treatment Program, 2010–12: a retrospective observational cohort study. The Lancet. Infectious diseases 14, 1065–1072, doi:10.1016/s1473-3099(14)70946-6 (2014).
Chen, X. et al. Prevalence of hepatitis B virus and hepatitis C virus in patients with human immunodeficiency virus infection in Central China. Archives of virology 158, 1889–1894, doi:10.1007/s00705-013-1681-z (2013).
Chen, Y. P., Pai, T. R., Liang, H. & Xu, Y. F. The analysis and clinical value of HBV, HCV and TP test results among 126 HIV infected patients. Int J Lab Med 37, 112–114 (2016).
Wu, Z. Q. et al. The analysis HCV, HBV and TP infection among HIV patients. Jiangsu Med J 41, 944–945 (2015).
Pan, H., Mao, S. G., Liu, F. Y., Yan, H. L. & Wen, Q. Analysis of co-infection of hepatitis B, hepatitis C virus and syphilis in AIDS patients. Chin J Health Lab Tec 25, 3705–3706 (2015).
Ye, Y., Su, H. M., Yang, A. K. & Li, Y. D. The results of HBV, HCV and HGV infection test among HIV infected population in Puer city. Soft Science of Health 27, 581–584 (2013).
Li, Y. et al. The clinical distribution of 994 HIV infection patients and statistical analysis of HIV and HCV co-infection. Int J Lab Med 34, 2474–2475 (2013).
Pererdun, M., Zhang, Y. X., Maimaitili, W., Pai, H. J. & Hamulati, W. Prevalence and risk factors of HIV/HCV co-infection in HIV/AIDS patients in Xinjiang, China. Chin J AIDS STD 21, 477–480 (2015).
Zhang, S. X., Su, S. L., Lin, B., Sun, X. G. & Fu, J. H. Epidemiological analysis of HIV and HCV co-infection in Shangdong. Chin J AIDS STD 19, 110–113 (2013).
Zhang, T. J., Tully, D. C. & Zhou, S. j. & He, N. Characteristics of HCV co-infection among HIV infected individuals from an area with high risk of blood-borne infections in central China. PloS one 9, e94219, doi:10.1371/journal.pone.0094219 (2014).
Zhao, R. et al. Epidemiological distribution and genotype characterization of hepatitis C virus and HIV co-infection in Wuhan, China, where the prevalence of HIV is low. Journal of medical virology 85, 1712–1723, doi:10.1002/jmv.23650 (2013).
Dong, C. et al. The impact of social factors on human immunodeficiency virus and hepatitis C virus co-infection in a minority region of Si-chuan, the People’s Republic of China: a population-based survey and testing study. PloS one 9, e101241, doi:10.1371/journal.pone.0101241 (2014).
Liu, Y., Zhao, J., Shen, T., Lu, F. M. & Lu, Q. J. Effect of HCV/HIV co-infection on the concentration of serum zinc. Acta Nutrimenta Sinica 36, 40–44 (2014).
Zhou, Y. B. et al. The geographic distribution patterns of HIV-, HCV- and co-infections among drug users in a national methadone maintenance treatment program in Southwest China. BMC infectious diseases 14, 134, doi:10.1186/1471-2334-14-134 (2014).
Hsieh, M. H. et al. Hepatitis C virus infection among injection drug users with and without human immunodeficiency virus co-infection. PloS one 9, e94791, doi:10.1371/journal.pone.0094791 (2014).
Liu, J., Zhu, J. J., Wen, J. X. & Lu, X. Y. Investigation on the concurrent infection of HCV and TP among people with HIV in Changji prefecture. Chin J Health Lab Tec 25, 4314–4315 (2015).
Ng, M. H. et al. High prevalence but low awareness of hepatitis C virus infection among heroin users who received methadone maintenance therapy in Taiwan. Addictive behaviors 38, 2089–2093, doi:10.1016/j.addbeh.2013.01.010 (2013).
Zhang, L., Zhang, D., Chen, W., Zou, X. & Ling, L. High prevalence of HIV, HCV and tuberculosis and associated risk behaviours among new entrants of methadone maintenance treatment clinics in Guangdong Province, China. PloS one 8, e76931, doi:10.1371/journal.pone.0076931 (2013).
Li, Y. et al. Combination Antiretroviral Therapy Is Associated With Reduction in Liver Fibrosis Scores in HIV-1-Infected Subjects. Medicine 95, e2660 (2016).
Mijiti, P. et al. Prevalence and predictors of anaemia in patients with HIV infection at the initiation of combined antiretroviral therapy in Xinjiang, China. International journal of STD & AIDS 26, 156–164, doi:10.1177/0956462414531935 (2015).
Pan, Y. J., Zhu, M. L., Pan, K. N., Yu, D. J. & Zhang, Y. L. Analysis of other pathogens infection in HIV/AIDS patients. Chin J Health Lab Tec 24, 1955–1957 (2014).
Duan, X. et al. Distribution and Clinical Features of AIDS in Adult Patients under Treatment in Jiangxi Province. Journal of Nanchang University (Medical Sciences) 54, 91–95 (2014).
Tang, Y. F. & Yang, J. Y. Co-infection of HIV and HBV, HCV, TP in Liangshan. Sichuan Medical Journal 34, 1947–1948 (2013).
Wang, Q. L., Lin, M. H. & Wang, Z. L. Clinical epidemiology of HIV/AIDS subjects co-infection in patients with HCV and/or HBV. Anhui Medical Journal 36, 583–586 (2015).
He, Y. M. The clinical features of AIDS patients with HBV and HCV infection. J Medical Forum 36, 87–88 (2015).
Liu, J. et al. The liver function of HBV and HCV co-infection among HIV patients in Kunming. Chin J AIDS STD 19, 376 (2013).
Zheng, Y. F. et al. Studies on clinical epidemiology of 1153 naïve HIV/AIDS patients in Shanghai. Chin Prev Med 14, 190–193 (2013).
Zhang, Y. et al. The epidemiological features in primary diagnosis of 1243 HIV/AIDS patients from 2005 to 2013 in Xi’an City. Chin J Dis Control Prev 19, 200–202 (2015).
Shen, Y. Z. et al. Serological survey of viral hepatitis markers among newly diagnosed patients with HIV/AIDS in China. HIV medicine 14, 167–175, doi:10.1111/j.1468-1293.2012.01048.x (2013).
Lee, K. Y. et al. Therapeutic drug monitoring and pharmacogenetic study of HIV-infected ethnic Chinese receiving efavirenz-containing antiretroviral therapy with or without rifampicin-based anti-tuberculous therapy. PloS one 9, e88497, doi:10.1371/journal.pone.0088497 (2014).
Cao, Y. et al. Prevalence and risk factors for chronic kidney disease among HIV-infected antiretroviral therapy-naive patients in mainland China: a multicenter cross-sectional study. Nephrology (Carlton, Vic.) 18, 307–312, doi:10.1111/nep.12031 (2013).
Feng, X. et al. Epidemiological analysis of HIV/AIDS patients in Yunnan provincial general hospital. China Modern Doctor 51, 17–19 (2013).
Li, H. B. et al. Clinical characteristics of patients infected HIV in general hospital: Analysis of 133 cases. Med J West China 25, 68–71 (2013).
Kou, H. J. et al. Comparison of nevirapine plasma concentrations between lead-in and steady-state periods in Chinese HIV-infected patients. PloS one 8, e52950, doi:10.1371/journal.pone.0052950 (2013).
Wang, Y. F., Xiong, J. F. & Yang, X. L. The analysis HCV, TP and HSV-2 infection among HIV patients in Guiyang. Journal of Aerospace Medicine 25, 970–972 (2014).
Xiao, M. M., Wang, Y., Shao, H., Zhang, Y. & Li, P. Investigation of HCV co-infection among HIV-1 infected patients in the South of Anhui. Laboratory Medicine 29, 705–707 (2014).
Liu, J. et al. Analysis on hepatitis C virus infection and related factors among newly reported HIV infections in Henan province. Chin J Epidemiol 35, 935–938 (2014).
Zhao, M. et al. The effectiveness of one-stop service model on adherence in MSM infected with HIV/AIDS: A pilot study. Chin J AIDS STD 19, 574–579 (2013).
An, M. H. et al. Study on the rates of infection and spontaneous clearance on HCV among HIV-infected men who have sex with men in China. Chin J Epidemiol 34, 15–18 (2013).
Guo, X. F., Li, J. & Dai, W. D. Study of human papillomavirus infection and cervical intraepithelial lesion in HIV/AIDS. Prog Obstet Gynecol 22, 565–567 (2013).
Zhang, Y. X. et al. Analvsis of cervical HPV infection in HIV positive Chinese women. Prog Obstet Gynecol 47, 185–190 (2012).
Luo, L. L., Chen, S. H., Xiong, Y. & Cai, H. B. The relationship between expression of P16(INK4a) protein and HPV infection in HIV-positive women. Journal of Chinese Oncology 19, 600–604 (2013).
Yu, C. T. et al. High prevalence of anal human papillomavirus infection and associated risky behaviors in men infected with human immunodeficiency virus in Taiwan. AIDS and behavior 17, 1211–1218, doi:10.1007/s10461-012-0173-6 (2013).
Li, X. et al. Anal HPV/HIV co-infection among Men Who Have Sex with Men: a cross-sectional survey from three cities in China. Scientific reports 6, 21368, doi:10.1038/srep21368 (2016).
Yang, K. F., Liu, J. H. & Li, L. J. Clinical analysis of 157 AIDS patients. J of Pub Health and Prev Med 26, 118–120 (2015).
Zhang, J. J. et al. Therapeutic efficacy of 731 naive AIDS patients in Beijing. Infect Dis Info 27, 347–349 (2014).
Hu, S. H., Liu, W., Xu, Y. H. & Fan, S. L. Analysis on the clinical characteristics of 217 AIDS patients in a general hospital. Chinese Journal of Social Medicine 31, 438–440 (2014).
Wu, C. et al. Results of detection of Epstein-Barr virus DNA in peripheral blood of HIV/AIDS patients. China Tropical Medicine 12, 609–611 (2012).
Zhou, S. J. et al. DNA sequence analysis of functional C-terminus of carcinogeneous latent membrane protein-1 of Epstein-Barr virus in HIV-infected patients. Fudan Univ J Med Sci 38, 518–521 (2011).
Shi, H. P. et al. Detection of Epstein-Barr Virus in the saliva of human Immunodeficiency Virus Infected Patients from Yunnan Province,China. Journal of Kunming Medical University 33, 144–146 (2012).
He, N. et al. Multiple viral coinfections among HIV/AIDS patients in China. Bioscience trends 5, 1–9 (2011).
Yang, P. R., Guo, S. X., Tan, X. H. & Yang, L. Research on co-infections of HIV and human herpesvirus-8 among the Uygur high-risk groups in a city, Xinjiang. Chin J Prev Med 43, 960–964 (2009).
Li, C. W. et al. Nested-PCR detection of cytomegalovirus and herpesviruses 6,7 and 8 in saliva from human immunodeficiency virus-infected subjects. J Pract Stomatol 30, 265–266 (2014).
Lee, Y. M., Chuang, S. Y., Wang, S. F., Lin, Y. T. & Chen, Y. M. Epidemiology of human herpesvirus type 8 and parvovirus B19 infections and their association with HIV-1 among men who have sex with men and injection drug users in Taiwan. Journal of microbiology, immunology, and infection=Wei mian yu gan ran za zhi 47, 233–238, doi:10.1016/j.jmii.2013.01.006 (2014).
Yang, C. K. et al. Prevalence and predictors of syphilis and herpes simplex type 2 virus (HSV-2) infections among HIV-infected men who have sex with men in Jiangsu province. Acta Universitatis Medicinalis Nanjing (Natural Science) 33, 672–675 (2013).
Zhang, T. et al. Prevalence of human herpesvirus 8 and hepatitis C virus in a rural community with a high risk for blood-borne infections in central China. Clinical microbiology and infection: the official publication of the European Society of Clinical Microbiology and Infectious Diseases 17, 395–401, doi:10.1111/j.1469-0691.2010.03287.x (2011).
Zhang, M. et al. Cross-sectional survey on smoking and smoking cessation behaviors among Chinese adults in 2010. Zhonghua Yu Fang Yi Xue Za Zhi 46, 404–408 (2012).
Park, L. S., Hernandez-Ramirez, R. U., Silverberg, M. J., Crothers, K. & Dubrow, R. Prevalence of non-HIV cancer risk factors in persons living with HIV/AIDS: a meta-analysis. AIDS (London, England) 30, 273–291, doi:10.1097/qad.0000000000000922 (2016).
Chinese center for disease control and prevention. Report On Chronic Disease Risk Factor Surveillance In China, 2010. Beijing: Military Medical Science Press (2012).
Liang, X. et al. Epidemiological serosurvey of hepatitis B in China–declining HBV prevalence due to hepatitis B vaccination. Vaccine 27, 6550–6557, doi:10.1016/j.vaccine.2009.08.048 (2009).
Chen, Y. S. et al. A sero-epidemiological study on hepatitis C in China. Chin J Epidemiol 32, 888–891 (2011).
Wang, R. et al. Nationwide prevalence of human papillomavirus infection and viral genotype distribution in 37 cities in China. BMC infectious diseases 15, 257, doi:10.1186/s12879-015-0998-5 (2015).
Li, J., Huang, R., Schmidt, J. E. & Qiao, Y. L. Epidemiological features of Human Papillomavirus (HPV) infection among women living in Mainland China. Asian Pacific journal of cancer prevention: APJCP 14, 4015–4023 (2013).
Liu, M. et al. Prevalence, incidence, clearance, and associated factors of genital human papillomavirus infection among men: a population-based cohort study in rural China. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 23, 2857–2865, doi:10.1158/1055-9965.epi-14-0365 (2014).
Liu, Y. T. A serological study on anti-CMV and anti-EBV antibodies in population of Beijing, Changzhi Shanxi and Yichang Hubei. Chin J Epidemiol 10, 277–281 (1989).
Zhang, T. et al. Human herpesvirus 8 seroprevalence, China. Emerging infectious diseases 18, 150–152, doi:10.3201/eid1801.102070 (2012).
Cohen, J. I. Epstein-Barr virus infection. The New England journal of medicine 343, 481–492, doi:10.1056/nejm200008173430707 (2000).
Wang, C. Z., Chen, Y. Y. & He, Y. Study on Changes of Epstein-Barr in HIV Infected Patients after Highly Active Antiretroviral Therapy. Journal of medical forum 29, 4–7 (2008).
van Baarle, D. et al. High prevalence of Epstein-Barr virus type 2 among homosexual men is caused by sexual transmission. The Journal of infectious diseases 181, 2045–2049, doi:10.1086/315521 (2000).
Zhuang, X. et al. HIV and HCV prevalence among entrants to methadone maintenance treatment clinics in China: a systematic review and meta-analysis. BMC infectious diseases 12, 130, doi:10.1186/1471-2334-12-130 (2012).
Schwarzer, G., Antes, G. & Schumacher, M. Inflation of type I error rate in two statistical tests for the detection of publication bias in meta-analyses with binary outcomes. Statistics in medicine 21, 2465–2477, doi:10.1002/sim.1224 (2002).
Tang, J. L. & Liu, J. L. Misleading funnel plot for detection of bias in meta-analysis. Journal of clinical epidemiology 53, 477–484 (2000).
Niaura, R., Chander, G., Hutton, H. & Stanton, C. Interventions to address chronic disease and HIV: strategies to promote smoking cessation among HIV-infected individuals. Current HIV/AIDS reports 9, 375–384, doi:10.1007/s11904-012-0138-4 (2012).
Lifson, A. R. & Lando, H. A. Smoking and HIV: prevalence, health risks, and cessation strategies. Current HIV/AIDS reports 9, 223–230, doi:10.1007/s11904-012-0121-0 (2012).
Deeken, J. F. et al. The rising challenge of non-AIDS-defining cancers in HIV-infected patients. Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 55, 1228–1235, doi:10.1093/cid/cis613 (2012).
Tyerman, Z. & Aboulafia, D. M. Review of screening guidelines for non-AIDS-defining malignancies: evolving issues in the era of highly active antiretroviral therapy. AIDS reviews 14, 3–16 (2012).
Pinzone, M. R., Berretta, M., Cacopardo, B. & Nunnari, G. Epstein-barr virus- and Kaposi sarcoma-associated herpesvirus-related malignancies in the setting of human immunodeficiency virus infection. Seminars in oncology 42, 258–271, doi:10.1053/j.seminoncol.2014.12.026 (2015).
Smith, C. & Khanna, R. The Development of Prophylactic and Therapeutic EBV Vaccines. Current topics in microbiology and immunology 391, 455–473, doi:10.1007/978-3-319-22834-1_16 (2015).
Higgins, J. P. & Thompson, S. G. Quantifying heterogeneity in a meta-analysis. Statistics in medicine 21, 1539–1558, doi:10.1002/sim.1186 (2002).
Higgins, J. P., Thompson, S. G., Deeks, J. J. & Altman, D. G. Measuring inconsistency in meta-analyses. BMJ (Clinical research ed.) 327, 557–560, doi:10.1136/bmj.327.7414.557 (2003).
Fleiss, J. L. The statistical basis of meta-analysis. Statistical methods in medical research 2, 121–145 (1993).
DerSimonian, R. & Laird, N. Meta-analysis in clinical trials. Controlled clinical trials 7, 177–188 (1986).
DerSimonian, R. & Laird, N. Meta-analysis in clinical trials revisited. Contemporary clinical trials 45, 139–145, doi:10.1016/j.cct.2015.09.002 (2015).
Sterne, J. A., Gavaghan, D. & Egger, M. Publication and related bias in meta-analysis: power of statistical tests and prevalence in the literature. Journal of clinical epidemiology 53, 1119–1129 (2000).
Anzures-Cabrera, J. & Higgins, J. P. Graphical displays for meta-analysis: An overview with suggestions for practice. Research synthesis methods 1, 66–80, doi:10.1002/jrsm.6 (2010).
Egger, M., Davey Smith, G., Schneider, M. & Minder, C. Bias in meta-analysis detected by a simple, graphical test. BMJ (Clinical research ed.) 315, 629–634 (1997).
Begg, C. B. & Mazumdar, M. Operating characteristics of a rank correlation test for publication bias. Biometrics 50, 1088–1101 (1994).
This study was funded by Natural Science Foundation of China (NSFC) (grant no: 81361120385; 81373062) and Shanghai Municipal Health and Family Planning Commission (grant no: GWTD2015S05; 15GWZK0101; 15GWZK0801).
The authors declare that they have no competing interests.
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Jin, ZY., Liu, X., Ding, YY. et al. Cancer risk factors among people living with HIV/AIDS in China: a systematic review and meta-analysis. Sci Rep 7, 4890 (2017). https://doi.org/10.1038/s41598-017-05138-x
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