Epidemiological Temporal Trends of Opportunistic Infections and Mortality Rates Among Hospitalized HIV/AIDS Patients: A Retrospective Study in Beijing, China (2012-2022)

doi:10.21203/rs.3.rs-4853484/v1

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Epidemiological Temporal Trends of Opportunistic Infections and Mortality Rates Among Hospitalized HIV/AIDS Patients: A Retrospective Study in Beijing, China (2012-2022)

https://doi.org/10.21203/rs.3.rs-4853484/v1

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HIV-associated opportunistic infections (OIs) continue to pose significant challenges in the management of HIV/AIDS patients, influencing hospitalization rates and mortality outcomes. This retrospective study aimed to assess the spectrum of OIs and epidemiological temporal trends among inpatient HIV/AIDS cases at Beijing You'an Hospital from 2012 to 2022.Clinical data of HIV-infected inpatients were analyzed to evaluate the prevalence of OIs, incidence rates, and mortality rates associated with these infections over an 11-year period.Among 10,316 hospitalized HIV/AIDS patients, tuberculosis (18.3%) and Pneumocystis pneumonia (PCP) (15.3%) were the most common OIs. Over time, a significant decline in the incidence of PCP (from 23.8% in 2012 to 14.7% in 2022, p < 0.05) and tuberculosis (from 23.8% to 7.4%) was observed. Conversely, the incidence of nontuberculous mycobacterial (NTM) infections increased (from 0.3% to 2.7%, p < 0.01). Overall in-hospital mortality rate among HIV patients decreased from 5.5% to 2.1% (p < 0.05) during the study period, with a notable decline in PCP-associated mortality (from 9.2% to 4.1%). The study highlights shifting trends in the epidemiology of OIs among hospitalized HIV/AIDS patients, attributed partly to the widespread use of antiretroviral therapy. Despite declining mortality rates overall, PCP remains a significant contributor to in-hospital mortality among HIV-infected individuals, emphasizing the ongoing need for targeted interventions in managing these infections.

Health sciences/Medical research/Epidemiology

Health sciences/Diseases/Infectious diseases/Hiv infections

HIV

HIV-associated opportunistic infections

Mortality

Epidemiology

As a major global public health problem, human immunodeficiency virus(HIV) has claimed 40.1 million lives so far and has continued to spread in all countries around the world(1); By the end of 2021, there were an estimated 38.4 million people living with HIV worldwide. By the end of 2020, there were 1.053 million people living with HIV in China, with a total of 351000 reported deaths(2).

Although there is no cure for HIV infection, with the popularization of antiretroviral (ART) drugs and the publicity of AIDS related prevention knowledge, AIDS infection has become a controllable chronic disease. To achieve the global goal of ending AIDS by 2030, 95% of people living with HIV should be diagnosed, 95% should receive antiretroviral treatment, and 95% of people living with AIDS should achieve virology suppression. In the past 20 years, to prevent the spread risk of AIDS, China has constantly formulated and updated policies and regulations on injecting drug abuse and blood products and provided free antiretroviral treatment(3). Preliminary results have been achieved, but more efforts are needed to reach the above standards.

Opportunistic infection (OIs) is still the main cause of hospitalization of AIDS infected people. At present, there are few epidemiological reports on opportunistic infections among AIDS patients in China(4–6), and they have not been updated in recent years. With the change of HIV subtypes and the emergence of antiretroviral drug resistance(7–10), the opportunistic infection spectrum is also changing.

Therefore, this study aims to comprehensively evaluate the trend of changes in the opportunistic infection spectrum of HIV inpatients using representative HIV inpatient samples from a nationally renowned infectious disease hospital, providing a basis for clinical diagnosis and empirical treatment.

Data Source and Study Design

This study was a retrospective cross-sectional study of all hospitalized patients with a discharge diagnosis of AIDS who were hospitalized in the Beijing You'an Hospital, a well-known and the largest North China specialized hospital for infectious diseases, from January 2012 and October 2022, and admitted inpatients were collected from all over the country. We examined the trends in the epidemiology and outcomes of the spectrums of opportunistic infections and the outcome among HIV hospitalizations using discharge data. The data contains deidentified information regarding each hospitalization, including patient demographic characteristics, admission status, discharge diagnoses, procedures, comorbid conditions, and outcomes.The study protocol was approved by the Clinical Research Ethics Committee of Beijing You'an Hospital Affiliated to Capital Medical University. Informed consent was waived due to the retrospective nature of this study.

Opportunistic infections and Outcome

The diagnosis of OIs was taken in accordance with the guideline recommended by the United States Center for Disease Control and Prevention (CDC)(11). Opportunistic infections assessed included Mycobacterium tuberculosis (TB), Nontuberculous mycobacterial (NTM), Pneumocystis pneumonia (PCP), Cytomegalovirus (CMV), Candidiasis, Cryptococcosis, Penicillium Marneffei, Cerebral Toxoplasmosis, Progressive multifocal leukoencephalopathy (PML). The primary outcome of interest was the trends in the prevalence and outcomes such as in-hospital mortality among 2 subgroups of HIV, such as HIV with PCP, and HIV with TB.

Statistical Analysis

We analyzed trends in the prevalence of demographic, clinical characteristics and in-hospital mortality. We performed subgroup analyses by OIs. The Mann Kendall test was used to analyze the trend. Continuous values are reported as mean ± standard error of the mean and compared using analysis of Student t test. Categorical variables were reported as a number and/or percentage and compared using the chi-squared test. A 2-tailed P < .05 was considered statistically significant. Statistical analyses were performed using the R Software V.4.0.3 (Free Software Foundation, Boston, Massachusetts, USA).

Characteristics of the Study Cohort

From January 2012 to August 2022, Beijing You'an Hospital admitted 10316 patients infected with HIV/AIDS. Out of these, 9612 (93.2%) were male patients and 704 (6.8%) were female patients. The mean age for HIV patients was 39.5 ± 12.8 years, and male patients were significantly younger than female patients (39.1 ± 12.6 vs. 45.2 ± 14.5 years). The most common opportunistic infection in HIV hospitalized patients was tuberculosis (18.3%), followed by PCP (15.3%), followed by CMV (7.4%), Cryptococcosis (3.8%), Candidiasis (2.2%), NTM (1.1%), Cerebral Toxoplasmosis (0.7%), Penicillium marneffei (0.7%), PML (0.5%) (Table 1). Among HIV hospitalizations, no significant statistical difference was observed in the incidence of opportunistic infections between male and female patients.

Table 1

Demographic Characteristics and Prevalence of OIs
Characteristics	Total (%)	Male (%)	Female (%)
n	10316	9612(93.2)	704(6.8)	p
age(years) (mean (SD))	39.49 (12.79)	39.07 (12.56)	45.20 (14.45)	< 0.001
Age(years)(%)				< 0.001
< 20	135 (1.3)	96 (1.0)	39 (5.5)
20–40	5814 (56.4)	5624 (58.5)	190 (27.0)
40–60	3590 (34.8)	3221 (33.5)	369 (52.4)
≥ 60	777 (7.5)	671 (7.0)	106 (15.1)
Cryptococcosis(%)	388 (3.8)	356 (3.7)	32 (4.5)	0.303
PCP (%)	1577 (15.3)	1468 (15.3)	109 (15.5)	0.924
TB(%)	1889 (18.3)	1777 (18.5)	112 (15.9)	0.098
NTM (%)	114 (1.1)	107 (1.1)	7 (1.0)	0.917
CMV (%)	760 (7.4)	713 (7.4)	47 (6.7)	0.514
EB(%)	110 (1.1)	105 (1.1)	5 (0.7)	0.446
Cerebral Toxoplasmosis (%)	69 (0.7)	66 (0.7)	3 (0.4)	0.563
Candidiasis(%)	228 (2.2)	208 (2.2)	20 (2.8)	0.295
Penicillium marneffei (%)	68 (0.7)	63 (0.7)	5 (0.7)	1.000
PML(%)	56 (0.5)	48 (0.5)	8 (1.1)	0.051
In-Hospital Mortality (%)	274 (2.7)	255 (2.7)	19 (2.7)	0.795

Among 1889 HIV coinfected TB patients, the highest proportion of intrapulmonary TB (49.6%), followed by intrapulmonary + extrapulmonary TB (29.4%), extrapulmonary TB (21.0%)(Fig. 1A); In 388 HIV patients with cryptococcal infection, the most common site of infection was the central nervous system(CNS)(83.5%), followed by cryptococcal pneumonia (9.8%), and a few patients had cutaneous cryptococcal infection(Fig. 1B); Among HIV patients coinfected with CMV infection, the types of infection include CMV retinitis (48.6%), CMV encephalitis (2.6%), other CMV infections(48.8%)( Fig. 1C).

In 3531 patients with opportunistic HIV infection of the respiratory system, the etiological agents of infection were, in that order, Pneumocystis (44.7%), Mycobacterium tuberculosis (42.3%), Cryptococcus (10.0%), and Nontuberculous mycobacteria (3.2%) (Fig. 1D). Contributing etiologies for 362 HIV cases with CNS infection included Mycobacterium tuberculosis (43.1%), Toxoplasma (19.1%), Cryptococcus (16.9%), CMV (5.5%), and PML (1.5%) (Fig. 1E).

Trends of the prevalence of Opportunistic infections in patients with HIV hospitalizations

We analyzed trends in age, sex ratio, and incidence of opportunistic infections among patients with HIV over an 11-year period (Table 2). Mann-Kendall trend test showed that the age of hospitalized HIV patients increased year by year during the study period (p for trend < 0.05), especially the proportion younger than 20 years decreased significantly. No significant trends were observed in the sex ratio of HIV patients.

Table 2

Trends in the Clinical and Demographic Characteristics of the Study Cohort
	2012	2013	2014	2015	2016	2017	2018	2019	2020	2021	2022	p value for trend
n	366	538	785	874	1097	1236	1180	1305	786	1145	1004
age (mean (SD))	40.00 (13.33)	38.62 (12.33)	37.95 (12.73)	38.37 (12.21)	37.85 (12.69)	38.10 (12.36)	39.11 (11.95)	40.09 (12.63)	40.44 (12.49)	41.29 (13.46)	42.32 (13.78)	< 0.001
Age(years) (%)												< 0.001
< 20	9 (2.5)	9 (1.7)	13 (1.7)	15 (1.7)	25 (2.3)	15 (1.2)	12 (1.0)	12 (0.9)	7 (0.9)	11 (1.0)	7 (0.7)
20–40	183 (50.0)	301 (55.9)	484 (61.7)	506 (57.9)	667 (60.8)	752 (60.8)	676 (57.3)	713 (54.6)	423 (53.8)	601 (52.5)	508 (50.6)
40–60	141 (38.5)	197 (36.6)	229 (29.2)	293 (33.5)	330 (30.1)	394 (31.9)	420 (35.6)	486 (37.2)	297 (37.8)	422 (36.9)	381 (37.9)
≥ 60	33 (9.0)	31 (5.8)	59 (7.5)	60 (6.9)	75 (6.8)	75 (6.1)	72 (6.1)	94 (7.2)	59 (7.5)	111 (9.7)	108 (10.8)
Female (%)	38 (10.4)	55 (10.2)	47 (6.0)	65 (7.4)	75 (6.8)	77 (6.2)	55 (4.7)	75 (5.7)	60 (7.6)	83 (7.2)	74 (7.4)	< 0.001
Cryptococcosis(%)	6 (1.6)	8 (1.5)	25 (3.2)	55 (6.3)	66 (6.0)	41 (3.3)	55 (4.7)	41 (3.1)	18 (2.3)	43 (3.8)	30 (3.0)	< 0.001
PCP (%)	87 (23.8)	105 (19.5)	158 (20.1)	177 (20.3)	175 (16.0)	184 (14.9)	144 (12.2)	157 (12.0)	96 (12.2)	146 (12.8)	148 (14.7)	< 0.001
TB(%)	87 (23.8)	157 (29.2)	206 (26.2)	222 (25.4)	279 (25.4)	233 (18.9)	177 (15.0)	235 (18.0)	107 (13.6)	112 (9.8)	74 (7.4)	< 0.001
NTM (%)	0 (0.0)	0 (0.0)	0 (0.0)	0 (0.0)	3 (0.3)	12 (1.0)	14 (1.2)	21 (1.6)	12 (1.5)	25 (2.2)	27 (2.7)	< 0.001
CMV (%)	30 (8.2)	26 (4.8)	57 (7.3)	71 (8.1)	61 (5.6)	88 (7.1)	105 (8.9)	113 (8.7)	71 (9.0)	78 (6.8)	60 (6.0)	0.005
EB(%)	5 (1.4)	12 (2.2)	2 (0.3)	1 (0.1)	8 (0.7)	14 (1.1)	21 (1.8)	12 (0.9)	3 (0.4)	22 (1.9)	10 (1.0)	< 0.001
Cerebral Toxoplasmosis (%)	1 (0.3)	3 (0.6)	3 (0.4)	4 (0.5)	9 (0.8)	25 (2.0)	4 (0.3)	10 (0.8)	7 (0.9)	2 (0.2)	1 (0.1)	< 0.001
Candidiasis (%)	42 (11.5)	52 (9.7)	36 (4.6)	20 (2.3)	6 (0.5)	3 (0.2)	5 (0.4)	16 (1.2)	13 (1.7)	15 (1.3)	20 (2.0)	< 0.001
Penicillium marneffei (%)	0 (0.0)	1 (0.2)	4 (0.5)	14 (1.6)	8 (0.7)	8 (0.6)	11 (0.9)	7 (0.5)	6 (0.8)	5 (0.4)	4 (0.5)	0.04
PML (%)	6 (1.6)	4 (0.7)	8 (1.0)	14 (1.6)	5 (0.5)	10 (0.8)	3 (0.3)	4 (0.3)	2 (0.3)	0 (0.0)	0 (0.0)	< 0.001
In-Hospital Mortality (%)	20 (5.5)	20 (3.7)	21 (2.7)	18 (2.1)	42 (3.8)	27 (2.2)	24 (2.0)	32 (2.5)	27 (3.4)	22 (1.9)	21 (2.1)	< 0.001

Our study results also show that the prevalence of major OIs in patients with HIV hospitalizations declined over the period of 11 years. Over a period of 11 years, we noted a progressive decline in rates of PCP among HIV hospitalizations from 23.8% in 2012 to 14.7% in 2022 (p < 0.05) (Table 2). A significant decrease was also observed in the TB infection rate, from 23.8–7.4%. Moreover, the incidence of PML decreased from 1.6–0.0% (P < 0.05). Notably, the incidence of comorbid NTM infection among hospitalized HIV patients increased year by year, reaching 2.7% by 2022 (P < 0.05). The incidence of other opportunistic infections did not change significantly over the study period.

Trends of In-Hospital Mortality in patients with HIV hospitalizations

Overall, in-hospital mortality was 2.7% among HIV patients, 7.5% among HIV patients with PCP, and 2.8% among HIV patients with TB. From 2012 to 2022, there was a yearly decreasing trend in in-hospital mortality among HIV hospitalized patients, from 5.5–2.1% (p < 0.05) (Table 2). Subgroup analysis revealed that in-hospital mortality decreased from 9.2–4.1% in patients with complicated PCP, and the same decreasing trend was observed in patients with TB, from 12.6–2.7%( Fig. 2), however, the trend was not statistically significant(p > 0.05).

This study retrospectively observed the changes in the opportunistic infection spectrum of AIDS patients admitted to Beijing You'an Hospital from 2012 to 2022, representing the situation in North China. The proportion of women in this study population is 6.8%, which is lower than previous studies(4–6) and shows a decreasing trend year by year; The average age is 39.5 ± 12.8 years old, which is similar to the research results from North China (39.2 ± 11.4)(6) and higher than the patients in Sichuan (34 years old)(5). The trend test shows that the age of hospitalized AIDS patients has increased year by year in the past 10 years, especially the proportion of patients younger than 20 years old has declined significantly.

With the widespread use of antiretroviral therapy, the life expectancy of HIV-positive individuals receiving this treatment globally has shown improvement(12), leading to an extension of the lifespan of existing HIV patients. Furthermore, the implementation of national policies for the prevention and control of HIV, along with increased public awareness through dissemination of knowledge about HIV transmission routes, has contributed to an enhanced understanding of high-risk behaviors associated with HIV infection(3, 13). Early prevention, detection, and treatment have also played a significant role in increasing the average age of HIV patients.

In recent years, there has been an annual decline in the prevalence of female HIV-infected individuals, possibly due to alterations in the predominant modes of HIV transmission. The probabilities of HIV infection through blood transmission, mother-to-child transmission, and illicit drug injection have markedly reduced(14–16). Presently, sexual transmission has emerged as the primary route of HIV transmission, with an escalating proportion of HIV cases transmitted through male-to-male sexual contact(15). Enhancing monitoring and prevention endeavors targeting men who have sex with men will be a pivotal focal point in future HIV control and prevention strategies.

This study aimed to analyze common opportunistic infection sites. As anticipated, nearly half of the patients with tuberculosis infections also suffer from extrapulmonary tuberculosis, with central nervous system infection being the predominant pathogen (43.10%). Previous research(17) has indicated that HIV increases the risk of extrapulmonary tuberculosis infection. These findings highlight the importance of diagnosing and treating extrapulmonary tuberculosis in hospitalized HIV patients. Furthermore, in this study, the majority of HIV-infected patients with Cryptococcus infection exhibited central nervous system involvement (83.5%), significantly higher than the proportion of cryptococcal meningitis among the overall cryptococcal infection patients (45.88%)(18). From another perspective, among the pathogens causing central nervous system infections in HIV-infected individuals, Cryptococcus infection ranks second only to Mycobacterium tuberculosis and Toxoplasma gondii.

Regarding the most common opportunistic infections, the results of this study indicate a gradual decrease in the proportion of infections caused by Mycobacterium tuberculosis and Pneumocystis jirovecii over the past decade, which is consistent with previous internationally related research findings(19–21). An observational study(19) conducted in the United States assessed the incidence of HIV-associated Pneumocystis pneumonia (PCP) from 2002 to 2014. The results revealed a significant decrease in incidence from 6.7% in 2002 to 3.5% in 2014 (p < 0.001). Although the incidence of PCP in this study remained higher than that in the United States, it also exhibited a consistent annual decline. Additionally, both the in-hospital mortality rates attributed to tuberculosis infection and PCP showed a decreasing trend. As previously mentioned, with the widespread use of antiretroviral drugs, not only has the number of AIDS-stage patients decreased, but also the in-hospital mortality of patients has significantly reduced.

This study presents its initial findings on the emerging trend of incidence rates concerning opportunistic infections within the Chinese population. Alongside the evident declining trajectory observed in the occurrence of frequently encountered opportunistic infections, a progressive reduction in mortality rates among individuals diagnosed with HIV has also been noted. This underscores the efficacy of the nation's efforts in HIV prevention and treatment. However, the overall incidence rate, coupled with the inpatient fatality rate, persists at levels warranting careful consideration. Timely disease detection and the prompt initiation of antiretroviral therapy remain pivotal measures in preemptively addressing hospitalizations associated with AIDS-related complications.

Competing interests

The authors declare no competing interests.

Funding

This study was not supported by funding projects.

Author Contribution

T.L., M.X. and S.J. collected data, performed statistical analysis, and drafted the final manuscript. T.L. and M.X. conceived the idea of the study, collected data, and revise the final manuscript. All authors approved the final version of the manuscript.

Data Availability

The datasets used and/or analysed during the current study available from the corresponding author on reasonable request.

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You are reading this latest preprint version

Epidemiological Temporal Trends of Opportunistic Infections and Mortality Rates Among Hospitalized HIV/AIDS Patients: A Retrospective Study in Beijing, China (2012-2022)

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Version 1

Abstract

Figures

Introduction

Materials and methods

Data Source and Study Design

Opportunistic infections and Outcome

Statistical Analysis

Results

Characteristics of the Study Cohort

Trends of the prevalence of Opportunistic infections in patients with HIV hospitalizations

Trends of In-Hospital Mortality in patients with HIV hospitalizations

Discussion

Conclusions

Declarations

Competing interests

Funding

Author Contribution

Data Availability

References

Additional Declarations

Status:

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