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Official websites use. Share sensitive information only on official, secure websites. This article was submitted to Molecular Psychiatry, a section of the journal Frontiers in Psychiatry. The use, distribution or reproduction in other forums is permitted, provided the original author s and the copyright owner s are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms. Premature biological aging, assessed by shorter telomere length TL and mitochondrial DNA mtDNA alterations, has been reported among people with major depressive disorders or psychotic disorders. However, these markers have never been assessed together among people who inject drugs PWIDs , although mental disorders are highly prevalent in this population, which, in addition, is subject to other aggravating exposures. We next performed a multivariate analysis to identify risk factors associated with being diagnosed with a major depressive episode MDE or a psychotic syndrome PS. In total, and PWIDs with and without psychiatric conditions were analyzed. TL attrition was even stronger when PWIDs cumulated at least two episodes of major depressive disorders. On the other hand, no difference was observed in mtDNA alterations between groups. The telomeric age difference with drug users without a diagnosis of psychiatric condition was estimated during 4. Keywords: drug use, depression, psychotic syndrome, telomere shortening, mitochondrial DNA, hepatitis C virus, aging. Psychiatric conditions among people who inject drugs PWIDs are of great concern. Moreover, the type of substance is also an important factor to take into consideration, psychosis being more frequent among methamphetamine users 4 — 7 , while heroin users are more prone to depression 8 , 9. Both mental disorders and substance use have been identified as risk factors for premature morbidities and mortalities, increased psychosocial distress, and an increased risk of blood-borne viral acquisition and transmission Among the comorbidities, cardiovascular impairment, insulin resistance, and neurodegenerative disorders 11 — 13 are frequent. Depressive disorders have been associated with higher levels of inflammatory and metabolic markers, which also increase the risk of developing cardiovascular diseases and type II diabetes Schizophrenia has also been associated with an increased risk of cardiovascular diseases, diabetes, and high blood pressure Biomarkers of cellular aging have been associated with many of these conditions. In some situations, they constitute early markers of disease development, enabling early interventions to prevent their progression. Mitochondria are essential for adenosine triphosphate production, which provides the necessary energy for cell functions. They have their own DNA, a small and circular molecule of 16, bp coding for 13 proteins of the respiratory chain. A cell contains hundreds to thousands of mitochondria, which in turn contain 1—10 mtDNA molecules; the number of molecules varies depending on cell type and energy requirement. MtDNA is highly susceptible to genetic damages mainly because of its proximity to the respiratory chain, which produces oxygen radicals, nucleotide repair mechanisms less effective than the nuclear ones, and the absence of protective histone scaffolds. Cell response to mitochondrial injuries is to increase the number of mtDNA per cell in order to compensate for the mutated ones. Up to a certain threshold, altered mitochondria can also be eliminated through mitophagy, but a clonal expansion of the mutated molecule can be overtaken that results in a mitochondrial function that is no longer sustained Quantification of mitochondrial copy number content MCN and its subsequent decrease and the rates of mtDNA mutations and deletions MDD have been proposed as a proxy for mitochondrial dysfunction and markers of cellular aging 20 , Similarly, TL attrition was identified as a marker of premature aging. Each telomere consists of 3—20 kb of a sequence of six repeated nucleotides — TTAGGG —, positioned at the ends of chromosomes, protecting them from degradation. They are synthesized by the telomerase, an RNA-dependent DNA polymerase, found in the stem and progenitor cells but missing in somatic cells, with the exception given to immature lymphocytes. Physiologically, telomeres shorten with age, but this process can be accelerated by individual and environmental factors. These markers of premature cellular aging have been extensively studied among patients with psychiatric conditions. Among subjects with depressive symptoms, MCNs in blood have yielded discordant results: reports found it increased 22 — 24 , decreased 25 , 26 , or without any change 27 , 28 when compared to healthy subjects. Leukocyte TL, however, was almost unanimously found to be shortened among depressed subjects 22 , 28 — 31 , while this association is still discussed among people with psychotic disorders Among drug users, decreases in MCN and increases in mtDNA damage have been reported among opiate-addicted patients 33 , while methamphetamine has been shown to induce mitochondrial damages in vitro 34 , Moreover, 4,bp common deletion, which is highly associated with aging, was never investigated in these populations Finally, TL has been shown to be shortened in leucocytes of drug-addicted subjects Nevertheless, a comprehensive evaluation of three age-related biomarkers that include MCN, MDD, and TL, has never been studied, to our knowledge, among a population with substance use disorders and co-occurring mental illness. In a recent study among injecting heroin users in Vietnam, we reported that one-third of them were suffering from psychiatric conditions, with a current major depressive episode MDE and psychotic syndromes PSs accounting for This project had the primary objective to evaluate the impact of a community-based intervention for HIV screening and treatment among PWIDs to control HIV transmission in Hai Phong, Vietnam and consisted of 4 annual respondent-driven sampling surveys and biannual visits for those enrolled in the cohorts In a face-to-face interview, community workers gathered information on socio-demographic data and drug use. If necessary, psychiatric treatments were initiated. For the present study, we included PWIDs who had banked blood samples and who had a psychiatric interview Supplementary Figure 1. Similarly, the population with PS included both those with a current or a lifetime PS. Briefly, 2. In each plate, one calibrator, one control, and one no template control were added. The plate was valid if the calibrator and control were within the expected range and no amplification occurred in the no template well. The sample was valid if the Ct value did not exceed Each plate contained one DNA extract from plasma considered as a control and a no template control. Validation of the amplification followed the sample rules for MCN. Telomere length was measured by a real-time PCR, using a technique described elsewhere Each plate contained standards for telomere sequence ranging from 1. Poly substance use included any excessive alcohol consumption, daily heroin injection, or frequency of methamphetamine consumption greater than or equal to 4 times a month Population characteristics are given as frequencies and percentages for categorical variables or mean values with standard deviation SD for numerical variables. In multivariate analysis, associations between psychiatric conditions MDE and PS and age-related biomarkers were assessed by binomial logistic regression, using MCN, MDD, and TL as continuous variables and adjusted for possible confounding factors i. Therefore, the selection of the variables was based on a literature review rather than a statistical criterion. These factors were related to heroin, methamphetamine, and alcohol consumption, which are risk factors for psychiatric disorders and have shown their potency to accelerate aging 37 , 46 , We also tested HIV and HCV infections as they have been both linked with neuropsychiatric outcomes and accelerated aging 46 , 48 , We also included ARV and methadone treatments, because they are able to induce immuno-inflammatory anomalies, which can accelerate premature cellular aging 50 , 51 and direct inhibitory effect on enzymatic processes. At last, we included age and sex, which have both been linked with TL and mitochondrial dysfunctions: TLs are shortened with age and are longer in women than in men 52 ; mitochondrial dysfunction is accumulated with age No multiple testing correction was done. Final models were selected in a forward stepwise manner, using the smallest Akaike Information Criterion. The odds for any psychiatric condition depending on TL continuous variable were given for 0. Overall, subjects had a consultation with a psychiatrist between August and April In total, twenty subjects were excluded from the analysis because of incomplete data, and thirteen were also excluded because they had an isolated suicidal risk. In total, subjects were diagnosed with at least one psychiatric condition and had no diagnosis of psychiatric condition and were defined as our control population. A patient flowchart is available in Supplementary Figure 1. Out of the PWIDs with a psychiatric condition, People who inject drugs with any psychiatric condition differed from PWIDs with no psychiatric condition. Notably, they were older, injected heroin for longer, smoked methamphetamine more often, used street methadone more frequently, had excessive alcohol consumption more often, and were less committed to their methadone program. However, the use of other drugs cannabis, cocaine, amphetamine, ecstasy, and ketamine was very limited and did not differ significantly between the two groups data not shown. The prevalence rates of viral infections between the two groups were similar; more than two-thirds of HIV-infected participants were receiving first-line ARV treatment Table 2. Reasons to invalidate the data were unmet quality control criteria and no blood sample available. These differences were not significant Table 3. Tested vs. LSM, least square mean. Neither MCN nor MDD was associated with any psychiatric disorder in multivariate analyses when adjusted for confounders data not shown. Therefore, we performed two analyses stratified on the subject of HCV status. Excessive alcohol consumption and not receiving methadone were associated risk factors of MDE aOR: 3. Values in bold are statistically significant. Herein, we reported that among the canonical age-related biomarkers, telomere attrition was associated with mental depression episodes and PSs in HCV-infected PWID, while mitochondrial genotoxicity markers were not. Meanwhile, such an association was not observed among HCV-uninfected subjects. Given a conservative approach to fix a 59 bp telomere loss per chromosome and per year of life 54 , the telomere age of the PWID with one MDE can be considered 4. TL attrition is related to accelerated biological aging and therefore a risk factor for age-related diseases, such as cardiovascular diseases, diabetes, atherosclerosis, neurodegenerative diseases, cancer. Overall, TL attrition increased the risk of frailty and mortality 11 , Telomere length attrition was one of the earliest described markers of premature aging, often a consequence of low-grade inflammation and oxidative stress Yet, in neuropsychiatric diseases, many studies have evidenced immune dysfunctions, such as increased systemic and brain pro-inflammatory cytokine, increased C-reactive protein concentrations in peripheral blood, and the infiltration of peripheral immune cells through the blood-brain barrier, microglial activation, and increased peripheral innate immunity activity 57 , Therefore, mental disorders are associated with an increase in oxidative stress and impairment of immuno-inflammation homeostasis. Many studies have previously analyzed the link between TL and mental disorders in adults who do not use drugs. Depression, in particular, has been extensively investigated. Nearly all studies on the subject matter have found shorter TL to be associated with MDE 22 , 59 — 62 , with few exceptions Meanwhile, PS and schizophrenia have been studied less often and have produced more heterogeneous results: finding decrease 61 , 64 , 65 , increase 32 , 66 , or no change 67 , 68 in TL when compared to the control group. However, two meta-analyses found a slight association between shorter TL and schizophrenia 65 , More recently, a meta-analysis that includes 14, subjects confirmed that shorter TL was associated with any psychiatric disorder; the association with depression remained significant when subgroup analyses were performed, while the association with PS was no longer significant Herein, we reported the same association among HCV-infected PWIDs but with additional aggravating factors, such as multiplicity of depression episodes. Furthermore, the multivariate analysis showed excessive alcohol consumption as a risk factor for mental disorders as previously reported 71 , Mental disorders are listed among the extra-hepatic symptoms of HCV infection Heroin use has been related to immune impairment in the brain and increased neuroinflammatory response; moreover, studies have revealed TL attrition and decreased telomerase activity in the blood of heroin users when compared to controls 37 , 75 , Methamphetamine use also showed an increase in oxidative stress and inflammation in the brain and has recently been associated with a shorter TL among HIV-positive subjects 46 , Ultimately, PWIDs belong to a population that is poly exposed to multiple risk factors that possibly play a role in the underlying and damaging processes that drive telomere shortening and premature biological aging. Mitochondrial dysfunctions assessed through mtDNA alterations have also been proposed as markers for premature aging. Previous reports have shown inconsistent results in terms of MCN in blood between depressed and controls. The same trends were reported for cell-free circulating MCN ccf-MCN in plasma, which has been proposed as a more accurate biomarker for mitochondrial disruption, with decreased 79 or increased 24 ccf-MCN. Only a few studies have looked for MCN in the blood of schizophrenic patients; they have found a slight decrease in MCN among patients when compared to the controls 80 — 82 ; although no difference in ccf-MCN was observed Studies on mtDNA integrity, i. Additionally, we did not find any difference in MDD between the two populations. This study has limitations. First, the MINI used in this study did not diagnose anxiety conditions, which are highly prevalent among PWIDs and which have been previously associated with premature aging Second, we did not have a group of non-drug users with or without mental disorders that would have been useful in positioning our findings in a broader context. Thirdly, aging markers were analyzed in whole blood DNA extracts. Fourth, the mtDNA integrity did not encompass the point mutation rate, as it required sequencing techniques. Finally, the participants were recruited outside the healthcare system and they did undergo clinical examination. Consequently, comorbidities and other polymedications were not recorded and could not be used as confounding variables in the various analyses. We, therefore, suggest that this subset of PWIDs with mental disorders is at higher risk of age-related diseases because of premature TL attrition rather than mtDNA alterations, particularly among those who are suffering from depression. The raw data supporting the conclusions of this article will be made available by the authors, without undue reservation. NN and PM: methodology. MD and AV: formal analysis. MD and J-PM: data curation, and writing—original draft preparation. All authors have read and agreed to the published version of the manuscript. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article, or claim that may be made by its manufacturer, is not guaranteed or endorsed by the publisher. This section collects any data citations, data availability statements, or supplementary materials included in this article. As a library, NLM provides access to scientific literature. Front Psychiatry. Find articles by Nicolas Nagot. Find articles by Laurent Michel. Find articles by Sao Mai Le. Find articles by Huong Thi Duong. Find articles by Roselyne Vallo. Find articles by Delphine Rapoud. Find articles by Hoang Thi Giang. Find articles by Catherine Quillet. Find articles by Nham Thi Tuyet Thanh. Find articles by Khuat Thi Hai Oanh. Find articles by Vu Hai Vinh. Find articles by Jonathan Feelemyer. Find articles by Philippe Vande Perre. Find articles by Khue Pham Minh. Find articles by Didier Laureillard. Find articles by Don Des Jarlais. Received Dec 31; Accepted May 12; Collection date Total of PWID with psychiatric condition Open in a new tab. Click here for additional data file. Similar articles. Add to Collections. Create a new collection. Add to an existing collection. Choose a collection Unable to load your collection due to an error Please try again. Add Cancel. Major depressive episode MDE. Patient with several psychiatric conditions. Heroin, number of years practicing injection. Heroin, frequency of injection during the month preceding the interview. Methamphetamine, Positive urine test. Methamphetamine, number of years of consumption. Methamphetamine, frequency of consumption during the month preceding the interview. Methadone Positive urine test. Excessive alcohol consumption. Major depressive episode and psychotic syndrome. Telomere length continuous. Heroin, frequency of consumption per month ref : less than daily. Alcohol ref: no excessive consumption. Methadone ref: currently receiving methadone. Heroin, frequency of consumption per month ref: less than daily.
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Mental Disorders Are Associated With Leukocytes Telomere Shortening Among People Who Inject Drugs
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Mental Disorders Are Associated With Leukocytes Telomere Shortening Among People Who Inject Drugs
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