People Living With HIV have a prolonged virus shedding duration even with anti-SARS-CoV-2 treatment：a retrospective cohort study in Wuhan, China

doi:10.21203/rs.3.rs-4978525/v1

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Research Article

People Living With HIV have a prolonged virus shedding duration even with anti-SARS-CoV-2 treatment：a retrospective cohort study in Wuhan, China

https://doi.org/10.21203/rs.3.rs-4978525/v1

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Objective

This study aimed to investigate the clearance of SARS-CoV-2 in people living with HIV (PLWH) after receiving anti-SARS-CoV-2 treatment and the relevant factors.

Methods

A retrospective investigation was conducted based on clinical data of patients with anti-SARS-CoV-2 treatment between December 2022 and June 2023. The patients were categorized into PLWH and HIV-negative groups. Basic information, comorbidity, COVID-19 severity, white blood cell count, lymphocyte count, anti-SARS-CoV-2 medicine, steroid usage, and SARS-CoV-2 virus shedding duration were collected. The Kaplan-Meier curve was employed to compare virus shedding rates, and multivariate logistic regression and Cox regression analyses were utilized to identify factors influencing SARS-CoV-2 virus shedding duration.

Results

A total of 149 patients with COVID-19 (32 PLWH and 117 HIV-negative individuals) were enrolled in the study. The median estimated virus shedding duration for PLWH group and HIV-negative group are 21 days and 14 days, respectively (P < 0.001). The virus shedding rates at the 5th day were 15.63% and 60.68% (P < 0.001), and at the 28th day were 87.50% and 97.44% (P = 0.019) for PLWH and HIV-negative groups, respectively. Multivariate logistic regression analysis showed that HIV infection (OR = 0.026, 95% CI: 0.004–0.159) and lymphocyte count at admission (OR = 4.341, 95% CI: 1.536–12.265) were independent factors influencing virus shedding at 5th day (P < 0.05). Compared to the mild COVID-19 group, the moderate and severe groups had significant impacts on virus shedding at both the 5th and the 28th day (P < 0.05). Multivariate Cox regression analysis revealed that age (OR = 0.977, 95% CI: 0.963–0.991), HIV infection (OR = 0.351, 95% CI: 0.197–0.626), duration of anti-SARS-CoV-2 therapy initiation (OR = 0.827, 95% CI: 0.786–0.871), and lymphocyte count (OR = 1.999, 95% CI: 1.372–2.914) were independent factors influencing SARS-CoV-2 virus shedding duration at the 28th day (P < 0.05). Compared to the mild COVID-19 group, the moderate, severe, and critically ill groups had statistically significant impacts on nucleic acid conversion (P < 0.001).

Conclusion

PLWH with COVID-19 had a prolonged virus shedding duration even with anti-SARS-CoV-2 treatment, which could lead to more opportunities to accumulate multiple mutations and induce resistance to anti-SARS-CoV-2 medicines.

SARS-CoV-2

virus shedding duration

HIV

lymphocyte count

Since the emergence of SARS-CoV-2 in 2019, it has posed a significant threat and impact on human health and daily life globally, especially for people living with HIV (PLWH), due to their compromised immune function.[1] Our former study in Wuhan and a study in England had shown that PLWH have a higher mortality than general population after infected with SARS-CoV-2.[2, 3]Even with antiretroviral therapy (ART) for undetected HIV viral load, HIV infection can still affect the immune response to the SARS-CoV-2, thereby affecting the clearance of the virus.[4]

Viral shedding, as a crucial indicator for assessing infectivity and determining disease progression,[5] exhibits significant heterogeneity in clinical research results due to the virus's biological characteristics, host factors, and the immunity of infected individuals (whether through previous infection or vaccination). Studies indicated that the duration of SARS-CoV-2 Delta variant viral shedding is 14.6–17.0 days,[6] while the duration of Omicron variant ranging from 9.06 to 12.04 days.[7] The small molecule anti-SARS-CoV-2 medicines could significantly shortened virus shedding duration, effectively reducing the severity and mortality rate in COVID-19 patients. [8] However, current researches on the virus shedding duration of SARS-CoV-2 primarily focuses on patients with normal immune function. The data among immunocompromised groups, such as PLWH, are largely missing, prompting our attention.

Therefore, this study aimed to compared the viral shedding duration of SARS-CoV-2 among PLWH and HIV-negative individuals after receiving anti-SARS-CoV-2 treatment. The study also analyzed the factors influencing the virus shedding of SARS-CoV-2.

Patients:

Patients with COVID-19 included in this study were inpatients in the infectious diseases department of Zhongnan hospital between December 2022 and June 2023. All inpatients received routine detection for HIV antibody on admission. Inclusion criteria: patient who met the diagnostic criteria and severity classification for COVID-19 referring to the "Diagnosis and Treatment Protocol for Novel Coronavirus Infection (the tenth edition)"[9]; The exclusion criteria were as follows: (1) without anti-SARS-CoV-2 treatment; (2) lack of SARS-CoV-2 nucleic acid test results; (3) anti-SARS-CoV-2 treatment duration < 5 days; (4) Loss to follow-up; Then based on the HIV infection status, the included patients were divided into PLWH and the HIV negative group. This study was approved by the hospital's ethics committee(2024146K), and all participants provided informed consent.

Data Collection:

Clinical data for the enrolled patients were collected from electronic medical record system, including age, gender, comorbidity, white blood cell and lymphocyte counts at admission, time of anti-SARS-CoV-2 medicine administration, time for clearance of the SARS-CoV-2 nucleic acid.

Research Methods:

The oropharyngeal swabs samples were collected for SARS-CoV-2 nucleic acid testing using RT-PCR to detect the cycle threshold (Ct) values of the SARS-CoV-2 virus ORF1ab and N genes. When both the Ct values of the virus ORF1ab gene and N gene in the same sample were greater than 35, the result was determined as negative. The duration of anti-SARS-CoV-2 therapy initiation referred to the interval (days) between onset of symptoms and the first administration of anti-SARS-CoV-2 medicines [9]; The virus shedding duration referred to the interval (days) from the first appearance of symptoms to the first negative nucleic acid test. Starting from the duration of anti-SARS-CoV-2 therapy initiation, nucleic acid samples were collected every 5 days until the clearance of the virus or continuously collected for 28 days.

Statistical Methods

Statistical analysis was conducted by SPSS 26.0 software. If the data did not follow a normal distribution, it was represented by the median (interquartile range) [M (P25, P75)]. Non-parametric tests (Mann-Whitney U test) were used for intergroup comparisons. Categorical variables were presented as counts (%), and intergroup comparisons were made using the χ2 test. Univariate and multivariate logistic regression analyses were employed to identify factors influencing virus shedding duration. Kaplan-Meier method was used to depict the COVID-19 virus shedding rate and median virus shedding duration. A multivariate Cox regression model was used to assess factors influencing virus shedding duration. A significance level of P < 0.05 was considered statistically significant.

Characteristics of enrolled patients

During the investigation period, a total of 189 patients were diagnosed with COVID-19. After exclusion of 20 patients without anti-SARS-CoV-2 treatment, 15 patients lack of virus nucleic acid test results, 3 patients with anti-SARS-CoV-2 treatment duration < 5 days, 2 patients were lost follow-up, total 149 patients were finally enrolled, all of them received three doses of the vaccine for COVID-19. Among them, 32 were PLWH and 117 were HIV-negative patients. All patients were treated with anti-SARS-CoV-2 medicines including Nirmatrelvir/Ritonavir, Simnotrelvir/Ritonavir, Azvudine or Molnupiravir.

The PLWH were significantly younger than the HIV-negative patients (P < 0.001), and they were also predominantly male (P = 0.006) and had a higher proportion of critical COVID-19 type (P = 0.006). Compared to HIV-negative patients, the enrolled PLWH had less comorbidities and lower lymphocyte counts (P = 0.002). The time from the onset of symptoms to the first use of anti-SARS-CoV-2 medicines in PLWH was later than that in HIV-negative patients (P = 0.005), and the SARS-CoV-2 shedding duration in PLWH was longer than that in HIV-negative patients (P < 0.001). The SARS-CoV-2 shedding rates of PLWH for the 5th day (P < 0.001) and the 28th day (P = 0.019) were lower than those of HIV-negative patients. (Table 1.)

Table 1

Clinical characteristics of enrolled patients
	HIV (+) (n = 32)	HIV(-)(n = 117)	P-value
Age, years	40.5(31–54)	68(54–75)	< 0.001
Gender [n (%)]
Male	28(87.50%)	72(61.54%)	0.006
Female	4(12.50%)	45(38.46%)
Comorbidities [n (%)]△	13(40.63%)	83(70.94%)	0.002
Types of COVID-19 [n (%)]
Mild	3(9.38%)	3(2.56%)	0.080
Moderate	17(53.13%)	69(58.97%)	0.550
Severe	8(25.00%)	43(36.75%)	0.210
Critical	4(12.50%)	2(1.71%)	0.006
White blood cell count(10⁹/L)	3.40(2.41–6.35)	5.21(4.05–7.04)	0.060
Lymphocyte counts (10⁹/L)	0.56(0.34–0.82)	0.8(0.6–1.2)	0.002
Time of first antiviral drug administration(days)	11(4.25–16.75)	7(5–10)	0.005
Virus shedding duration(days)	21.5(15.5–30.0)	14.0(12.0–17.0)	< 0.001
Virus shedding status on the 5th day [n (%)]	5(15.63%)	71(60.68%)	< 0.001
Virus shedding status on the 28th day [n (%)]	28(87.50%)	114(97.44%)	0.019
antivirus drugs [n (%)]
Nirmatrelvir/Ritonavir	8 (25%)	32 (27.35%)	0.790
Azvudine	18 (56.25%)	68 (58.12%)	0.850
Simnotrelvir/Ritonavir	7 (21.88%)	20 (17.09%)	0.530
Molnupiravir	4 (12.50%)	5 (4.27%)	0.080
Glucocorticoids [n (%)]	10 (31.25%)	47 (40.17%)	0.360
antiretroviral therapy [n (%)]	19 (59.38%)	-
△ Including cardiovascular disease, diabetes, chronic lung, liver and kidney disease, cancer

SARS-CoV-2 shedding status after 5 days of anti-SARS-CoV-2 treatment

The SARS-CoV-2 virus shedding rates on the 5th day of treatment among PLWH was 15.63%, and 60.68% for HIV-negative patients. The concurrent HIV infection (OR = 0.026, 95% CI: 0.004–0.159) and lymphocyte count upon admission (OR = 4.341, 95% CI: 1.536–12.265) were independent influencing factors for virus shedding (P < 0.05). Compared to the mild COVID-19 classification group, both moderate and severe classifications had a statistically significant impact on virus shedding (P < 0.05). However, the use of different anti-SARS-CoV-2 medicines for COVID-19, including Nirmatrelvir/Ritonavir, Simnotrelvir/Ritonavir, Azvudine, and Molnupiravir, did not show statistical significance (P > 0.05), as shown in Table 2.

Table 2

Risk factors for SARS-CoV-2 virus shedding status after 5 days of anti-SARS-CoV-2 treatment
	OR	95% CI	P-value
Age, years	0.971	0.941–1.003	0.072
Gender	1.098	0.449–2.686	0.837
HIV infection	0.026	0.004–0.159	0.000
Comorbidities△	1.405	0.48–4.115	0.535
Time of first administration of antiviral drugs for COVID-19	1.199	1.069–1.346	0.056
COVID-19 classification
Mild	ref	ref	0.042
Moderate	0.023	0.001–0.431	0.012
Severe	0.013	0.001–0.266	0.005
Critical	0.000	0.000	0.998
White blood cell count(10⁹/L)	1.093	0.922–1.296	0.306
Lymphocyte count(10⁹/L)	4.341	1.536–12.265	0.006
antivirus drugs
Nirmatrelvir/Ritonavir	ref	ref	0.735
Azvudine	0.773	0.291–2.051	0.605
Simnotrelvir/Ritonavir	1.041	0.261–4.156	0.955
Molnupiravir	2.133	0.286–15.889	0.460
Glucocorticoids	1.010	0.371–2.749	0.984
△ Including cardiovascular disease, diabetes, chronic lung, liver and kidney disease, cancer

Risk factors associated with SARS-CoV-2 shedding duration

The median SARS-CoV-2 shedding duration of PLWH and HIV-negative patients was 21 days and 14 days, respectively(P < 0.001), as shown in Fig. 1. The age (OR = 0.977, 95% CI: 0.963–0.991), HIV infection (OR = 0.351, 95% CI: 0.197–0.626), duration of anti-SARS-CoV-2 therapy initiation (OR = 0.827, 95% CI: 0.786–0.871), and lymphocyte count at admission (OR = 1.999, 95% CI: 1.372–2.914) were independent factors for the virus shedding duration. Compared to the mild COVID-19 classification group, the moderate, severe, and critical classification groups all showed significant impacts on the virus shedding (P < 0.001), as shown in Table 3.

Table 3

Risk factors associated with Virus shedding duration in COVID-19 Patients
	OR	95.0% CI	P-value
Age, years	0.977	0.963–0.991	0.001
Gender	1.179	0.777–1.79	0.438
HIV infection	0.351	0.197–0.626	0.000
Comorbidities△	0.922	0.566–1.502	0.743
Time of first administration of antiviral drugs for COVID-19	0.827	0.786–0.871	0.000
COVID-19 classification
Mild	ref	ref	0.000
Moderate	0.047	0.015–0.143	0.000
Severe	0.058	0.017–0.192	0.000
Critical	0.004	0-0.029	0.000
White blood cell count	1.055	0.977–1.139	0.170
Lymphocyte count	1.999	1.372–2.914	0.000
Glucocorticoids	0.926	0.597–1.436	0.730
△ Including cardiovascular disease, diabetes, chronic lung, liver and kidney disease, cancer

Understanding the virus shedding status after SARS-CoV-2 infection and associated influencing factors is crucial, especially for PLWH. Due to compromised immune function, PLWH are prone to opportunistic infections, and the situation becomes even more complex and challenging after contracting COVID-19. Our findings indicate that PLWH experience a prolonged virus shedding duration even with anti-SARS-CoV-2 therapy.

The most studies about the virus shedding duration of PLWH with COVID-19 were focus on without anti-SARS-CoV-2 treatment. A study in South Africa showed that the natural virus shedding duration for PLWH after contracting COVID-19 (18.5 days) was longer than the general population (11.3 days).[10] Another prospective cohort study showed that SARS-CoV-2 shedding duration was 27 days in PLWH with CD4⁺ counts < 200 cells/µL, which were significantly differed from the general population(7days).[11] The heterogeneity in these results may be attributed to different viral strains and variations in the immune status of the PLWH included in the studies. According to our knowledge, the limited research was performed for the impact of anti-SARS-CoV-2 therapy on the SARS-CoV-2 shedding duration in PLWH. A study in Henan, China, showed that the average virus shedding duration for 12 PLWH individuals infected with SARS-CoV-2 (Delta variant) was 32.36 ± 2.64 days. But the data was not compared with HIV-negative patients. [12] Our research found that even with anti-SARS-CoV-2 treatment, the average virus shedding duration for PLWH was 21 days, significantly longer than the general population. We also revealed that the virus shedding rates for PLWH after 5 days and 28 days of treatment were 15.63% and 87.50%, respectively, significantly lower than the HIV-negative group. This may be due to the direct impact of HIV infection on immune cells such as CD4⁺ T lymphocytes and monocytes, leading to a continuous reduction in their numbers. Furthermore, HIV chronic infection indirectly results in the loss of CD8⁺ T lymphocyte function and abnormal immune activation of B lymphocytes.[13] The immune deficiency caused by HIV infection mitigates the inflammatory storm induced by SARS-CoV-2, weakening the body's ability to clear the virus and prolonging the survival time of SARS-CoV-2 in hosts with impaired immune function.[14] This could lead to an increased risk of virus accumulation and mutations, potentially complicating treatment or inducing vaccine immune escape. [15, 16]

Our former study revealed that HIV infection and low lymphocyte count are associated with prolonged virus shedding duration. HIV infection-induced immunodeficiency and low lymphocyte count may help PLWH avoid severe immune storm attacks during SARS-CoV-2 infection.[17-19] It has been reported that most patients experience a significant decrease in lymphocytes after SARS-CoV-2 infection, with a more severe decrease in the deceased group, indicating that a low lymphocyte count may impact the prognosis of COVID-19 patients.[20, 21] The lymphocyte count in COVID-19 patients shows a trend of two decreases: the first decrease occurs in the early stages of infection when lymphocytes are depleted or distributed to organs for tissue infiltration, and the second decrease may be due to the inhibition of the immune system, especially acquired immune function, resulting in a decline in lymphocyte count and worsening of the patient's condition. Therefore, for immunocompromised patients infected with SARS-CoV-2, dynamic monitoring of peripheral blood lymphocyte count, and where possible, monitoring of lymphocyte subsets, are recommended to assess the patient's immune function status.[22]

Furthermore, we found that the delayed duration of anti-SARS-CoV-2 therapy initiation is also an adverse factor influencing virus clearance. This is consistent with the results of a multicenter cohort study from Germany, they found that anti-SARS-CoV-2 treatment later than five days after diagnosis were significantly associated with the longer viral shedding.[23] The earlier anti-SARS-CoV-2 treatment initiation is crucial especially for high-risk groups such as the elderly and immunocompromised patients like PLWH, to reduce viral replication and minimize disease severity and mortality risk.

The severity classification of COVID-19 is further found to be associated with prolonged virus shedding duration. Compared to mild cases, the virus shedding duration for moderate, severe, and critical COVID-19 cases is extended, aligning with previous research.[24, 25] This could be due to a more severe immune imbalance and a stronger "cytokine" storm in severe/critical patients, leading to a longer virus shedding duration and exacerbating the condition.[26] Additionally, our study found that age is associated with prolonged virus shedding duration, consistent with the findings of previous studies.[27-29] This association may be attributed to the higher prevalence of comorbidity, multi-organ dysfunction, and weakened immune function in elderly patients, leading to a diminished ability to clear the virus.

Due to the prolonged virus shedding duration in immunocompromised patients after SARS-CoV-2 infection, persistent positive virus results may occur. Therefore, it is currently recommended to extend the use of anti-SARS-CoV-2 medicines for such patients based on the relief of clinical symptoms and nucleic acid testing for SARS-CoV-2.[22] In our study, we had appropriately extended the duration of use for anti-SARS-CoV-2 medicines and found that commonly used anti-SARS-CoV-2 medicines, including small molecule drugs (Nirmatrelvir/Ritonavir, Simnotrelvir/Ritonavir) and RNA virus inhibitors (Molnupiravir, Azvudine) did not significantly differ in their impact on virus shedding duration. That may relate to the relatively small sample size included.

This study has some limitations. Firstly, it only included hospitalized patients, excluding outpatient cases, which may result in data bias. Secondly, limitations in sampling and differences in the technical expertise of sampling and detection personnel may introduce confounding factors, leading to false negatives due to sampling or false positives due to testing. Thirdly, our study did not collect information on patients neutralizing antibody level for SARS-CoV-2. Additionally, the small sample size of HIV-infected individuals hindered further analysis, including the impact analysis of ART drugs and opportunistic infections on the prolonged virus shedding duration in PLWH after contracting COVID-19. Further research with an expanded sample size is needed for further investigation.

In conclusion, our study revealed that PLWH with COVID-19 had a prolonged virus shedding duration even with anti-SARS-CoV-2 treatment, which could lead to more opportunities to accumulate multiple mutations and induce resistance to anti-SARS-CoV-2 medicines.

Ethics approval

This study protocol was approved by the Institutional Review Board at Zhongnan Hospital of Wuhan University (approval number: [2024146K]) and was in accordance with the Declaration of Helsinki revised in 1983.

Consent to participate

Informed consent is waived because all personally identifiable information in the text has been omitted.

Not applicable.

Consent for publication

Not applicable.

Availability of data and materials

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

Competing interests

None.

Funding

This independent research was supported by Non-profit Central Research Institute Fund of Chinese Academy of Medical Sciences (2020-PT320-004) and the Gilead Sciences Research Scholars Program in HIV.

Authors' contributions

In the terms of Author contributions:

Ke Liang, Shi Zou, Hengning Ke conceptualized the study. Qian Du, Li Xu, Qianhui Chen, Wei Guo, Jie Liu, Shihui Song, Miao Tan and Yuting Tan contributed to data collection. Qian Du and Songjie Wu performed the data analysis. Qian Du wrote the manuscript. All authors have accessed and verified the underlying data. All authors have full access to all the data in the study. The corresponding authors had final responsibility for the decision to submit for publication.

Acknowledgements

Authors thanks all participants in this study.

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No competing interests reported.

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People Living With HIV have a prolonged virus shedding duration even with anti-SARS-CoV-2 treatment：a retrospective cohort study in Wuhan, China

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Abstract

Objective

Methods

Results

Conclusion

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Introduction

Materials and Methods

Patients:

Data Collection:

Research Methods:

Statistical Methods

Results

Characteristics of enrolled patients

SARS-CoV-2 shedding status after 5 days of anti-SARS-CoV-2 treatment

Risk factors associated with SARS-CoV-2 shedding duration

Discussion

Conclusion

Declarations

References

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