Abstract
Few studies have explored the relationship between antibiotic exposure and sleep in newlyweds. We applied the actor–partner interdependence moderation model to estimate the relationships of antibiotic exposure with nighttime sleep duration (weekday, weekend, and average sleep durations) and daytime sleepiness in newlyweds. We found that 99.0% of the 2698 enrolled individuals were exposed to at least one antibiotic. Among the newlyweds, exposure to florfenicol (β, − 0.077; 95% confidence interval [CI], − 0.143, − 0.011), exposure to chloramphenicols (− 0.086 [− 0.160, − 0.011]), and exposure to veterinary antibiotics (VAs) (− 0.106 [− 0.201, − 0.010]) were negatively associated with weekday sleep duration. Florfenicol, chloramphenicols, and VAs were also inversely related to average sleep duration in the newlyweds. Ciprofloxacin and cyadox exposure was significantly associated with an increase of 0.264 (0.030, 0.497) and (0.375 [0.088, 0.663]) Epworth Sleepiness Scale (ESS) scores in the newlyweds, respectively. Gender moderated the actor–partner effects of erythromycin and tetracyclines on the newlyweds’ weekday sleep duration and ESS scores. Overall, exposure to florfenicol, chloramphenicols, and VAs shortened weekday and average sleep durations of newlyweds. Exposure to ciprofloxacin and cyadox promoted daytime sleepiness. Gender moderated the actor–partner effects of specific antibiotics on the weekday sleep duration and ESS scores of the newlyweds.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
Data will be available from the corresponding authors on reasonable request.
Code availability
The software has been licensed.
References
Anh HQ, Le TPQ, Da Le N, Lu XX (2021) Antibiotics in surface water of East and Southeast Asian countries: a focused review on contamination status, pollution sources, potential risks, and future perspectives. Sci Total Environ 764:142865. https://doi.org/10.1016/j.scitotenv.2020.142865
Baranowski WJ (2011) Clarithromycin-induced hypersomnia in children. Int J Clin Pharmacol Ther 49:297–299. https://doi.org/10.5414/cpp49297
Ben Y, Fu C, Hu M, Liu L (2019) Human health risk assessment of antibiotic resistance associated with antibiotic residues in the environment: a review. Environ Res 169:483–493. https://doi.org/10.1016/j.envres.2018.11.040
Ben Y, Hu M, Zhong F, Du E (2022) Human daily dietary intakes of antibiotic residues: dominant sources and health risks. Environ Res 212:113387. https://doi.org/10.1016/j.envres.2022.113387
Besedovsky L, Schmidt EM, Linz B, Diekelmann S (2017) Signs of enhanced sleep and sleep-associated memory processing following the anti-inflammatory antibiotic minocycline in men. J Psychopharmacol 31:204–210. https://doi.org/10.1177/0269881116658991
Billings ME, Hale L, Johnson DA (2020) Physical and social environment relationship with sleep health and disorders. Chest 157:1304–1312. https://doi.org/10.1016/j.chest.2019.12.002
Binks HGEV, Gupta C, Irwin C (2020) Effects of diet on sleep: a narrative review. Nutrients 12:936. https://doi.org/10.3390/nu12040936
Bowers SJ, Vargas F, Gonzalez A, He S (2020) Repeated sleep disruption in mice leads to persistent shifts in the fecal microbiome and metabolome. PLoS ONE 15:e0229001. https://doi.org/10.1371/journal.pone.0229001
Carvalho IT, Santos L (2016) Antibiotics in the aquatic environments: a review of the European scenario. Environ Int 94:736–757. https://doi.org/10.1016/j.envint.2016.06.025
Chang D, Mao Y, Qiu W, Wu Y (2023) The source and distribution of tetracycline antibiotics in China: a review. Toxics 11:214. https://doi.org/10.3390/toxics11030214
Chu L, Wang H, Su D, Zhang H (2022) Urinary antibiotics and dietary determinants in adults in Xinjiang. West China Nutrients 14:4748. https://doi.org/10.3390/nu14224748
Enginar N, Eroglu L, Ulak G (1991) The effect of ofloxacin on pentobarbital-induced sleep in mice. Pharmacol Biochem Behav 40:65–67. https://doi.org/10.1016/0091-3057(91)90321-r
Ermer AE, Proulx CM (2022) The association between relationship strain and emotional well-being among older adult couples: the moderating role of social connectedness. Aging Ment Health 26:1198–1206. https://doi.org/10.1080/13607863.2021.1910786
Faulkner DV, Cantley ML, Kennedy DG, Elliott CT (2022) MRM(3)-based UHPLC-MS/MS method for quantitation of total florfenicol residue content in milk and withdrawal study profile of milk from treated cows. Food Chem 379:132070. https://doi.org/10.1016/j.foodchem.2022.132070
Gandhi KD, Mansukhani MP, Silber MH, Kolla BP (2021) Excessive daytime sleepiness: a clinical review. Mayo Clin Proc 96:1288–1301. https://doi.org/10.1016/j.mayocp.2020.08.033
Gao H, Shu Q, Chen J, Fan K (2019) Antibiotic exposure has sex-dependent effects on the gut microbiota and metabolism of short-chain fatty acids and amino acids in mice. mSystems 4:e00048-00019. https://doi.org/10.1128/mSystems.00048-19
Garcia RL, Kenny DA, Ledermann T (2015) Moderation in the actor-partner interdependence model. Pers Relat 22:8–29. https://doi.org/10.1111/pere.12060
Geng M, Liu K, Huang K, Zhu Y (2020) Urinary antibiotic exposure across pregnancy from Chinese pregnant women and health risk assessment: repeated measures analysis. Environ Int 145:106164. https://doi.org/10.1016/j.envint.2020.106164
Golomb BA, Koslik HJ, Redd AJ (2015) Fluoroquinolone-induced serious, persistent, multisymptom adverse effects. BMJ Case Rep 2015:bcr2015209821. https://doi.org/10.1136/bcr-2015-209821
Gunn HE, Buysse DJ, Matthews KA, Kline CE (2017) Sleep-wake concordance in couples is inversely associated with cardiovascular disease risk markers. Sleep 40:zsw028. https://doi.org/10.1093/sleep/zsw028
Han M, Yuan S, Zhang J (2022) The interplay between sleep and gut microbiota. Brain Res Bull 180:131–146. https://doi.org/10.1016/j.brainresbull.2021.12.016
Hao H, Guo W, Iqbal Z, Cheng G (2013) Impact of cyadox on human colonic microflora in chemostat models. Regul Toxicol Pharmacol 67:335–343. https://doi.org/10.1016/j.yrtph.2013.08.011
Heath AM, Haszard JJ, Galland BC, Lawley B (2020) Association between the faecal short-chain fatty acid propionate and infant sleep. Eur J Clin Nutr 74:1362–1365. https://doi.org/10.1038/s41430-019-0556-0
Hou L, Fu Y, Zhao C, Fan L (2022) Ciprofloxacin and enrofloxacin can cause reproductive toxicity via endocrine signaling pathways. Ecotoxicol Environ Saf 244:114049. https://doi.org/10.1016/j.ecoenv.2022.114049
Hu Y, Zhu Q, Wang Y, Liao C (2022) A short review of human exposure to antibiotics based on urinary biomonitoring. Sci Total Environ 830:154775. https://doi.org/10.1016/j.scitotenv.2022.154775
Huang C, Lei H, Liu C, Wang Y (2022) Acute and subchronic exposure of cyadox induced metabolic and transcriptomic disturbances in Wistar rats. Toxicology 482:153367. https://doi.org/10.1016/j.tox.2022.153367
Jitaru M, Turliuc MN (2022) The moderator role of interpersonal emotion regulation on the associations between commitment, intimacy, and couple satisfaction. Int J Environ Res Public Health 19:10506. https://doi.org/10.3390/ijerph191710506
Kayani MUR, Yu K, Qiu Y, Shen Y (2021) Environmental concentrations of antibiotics alter the zebrafish gut microbiome structure and potential functions. Environ Pollut 278:116760. https://doi.org/10.1016/j.envpol.2021.116760
Kecklund G, Axelsson J (2016) Health consequences of shift work and insufficient sleep. BMJ 355:i5210. https://doi.org/10.1136/bmj.i5210
Kische H, Ewert R, Fietze I, Gross S (2016) Sex hormones and sleep in men and women from the general population: a cross-sectional observational study. J Clin Endocrinol Metab 101:3968–3977. https://doi.org/10.1210/jc.2016-1832
Klein EY, Milkowska-Shibata M, Tseng KK, Sharland M (2021) Assessment of WHO antibiotic consumption and access targets in 76 countries, 2000–15: an analysis of pharmaceutical sales data. Lancet Infect Dis 21:107–115. https://doi.org/10.1016/s1473-3099(20)30332-7
Lecomte A, Barateau L, Pereira P, Paulin L (2020) Gut microbiota composition is associated with narcolepsy type 1. Neurol Neuroimmunol Neuroinflamm 7:e896. https://doi.org/10.1212/NXI.0000000000000896
Lee PH, Macfarlane DJ, Lam TH, Stewart SM (2011) Validity of the International Physical Activity Questionnaire Short Form (IPAQ-SF): a systematic review. Int J Behav Nutr Phys Act 8:115. https://doi.org/10.1186/1479-5868-8-115
Lee S, Martire LM, Damaske SA, Mogle JA (2018) Covariation in couples’ nightly sleep and gender differences. Sleep Health 4:201–208. https://doi.org/10.1016/j.sleh.2017.10.009
Li R, Wang H, Shi Q, Wang N (2017) Effects of oral florfenicol and azithromycin on gut microbiota and adipogenesis in mice. PLoS ONE 12:e0181690. https://doi.org/10.1371/journal.pone.0181690
Liu K, Zhang J, Geng M, Zhu Y (2020) A stable isotope dilution assay for multi-class antibiotics in pregnant urines by LC–MS/MS. Chromatographia 83:507–521. https://doi.org/10.1007/s10337-020-03866-3
Lyu J, Yang L, Zhang L, Ye B (2020) Antibiotics in soil and water in China-a systematic review and source analysis. Environ Pollut 266:115147. https://doi.org/10.1016/j.envpol.2020.115147
Maier L, Goemans CV, Wirbel J, Kuhn M (2021) Unravelling the collateral damage of antibiotics on gut bacteria. Nature 599:120–124. https://doi.org/10.1038/s41586-021-03986-2
Maranges HM, McNulty JK (2017) The rested relationship: sleep benefits marital evaluations. J Fam Psychol 31:117–122. https://doi.org/10.1037/fam0000225
Martinez A, Subbiah S, Stonum P, Brooks T (2020) Characterization of serotonin following exposure to antibiotics in white-tailed deer. Gen Comp Endocrinol 285:113265. https://doi.org/10.1016/j.ygcen.2019.113265
Moulin-Sallanon M, Millet P, Rousset C, Zimmer L (2005) Chloramphenicol decreases brain glucose utilization and modifies the sleep-wake cycle architecture in rats. J Neurochem 93:1623–1632. https://doi.org/10.1111/j.1471-4159.2005.03167.x
Mulder M, Radjabzadeh D, Kiefte-de Jong JC, Uitterlinden AG (2020) Long-term effects of antimicrobial drugs on the composition of the human gut microbiota. Gut Microbes 12:1795492. https://doi.org/10.1080/19490976.2020.1791677
Nakamaru-Ogiso E, Miyamoto H, Hamada K, Tsukada K (2012) Novel biochemical manipulation of brain serotonin reveals a role of serotonin in the circadian rhythm of sleep-wake cycles. Eur J Neurosci 35:1762–1770. https://doi.org/10.1111/j.1460-9568.2012.08077.x
Nicolaides NC, Vgontzas AN, Kritikou I, Chrousos G. (2020). HPA axis and sleep. Endotext. https://www.ncbi.nlm.nih.gov/pubmed/25905298
Nonaka K, Nakazawa Y, Kotorii T (1983) Effects of antibiotics, minocycline and ampicillin, on human sleep. Brain Res 288:253–259. https://doi.org/10.1016/0006-8993(83)90101-4
Ogawa Y, Miyoshi C, Obana N, Yajima K (2020) Gut microbiota depletion by chronic antibiotic treatment alters the sleep/wake architecture and sleep EEG power spectra in mice. Sci Rep 10:19554. https://doi.org/10.1038/s41598-020-76562-9
Palleja A, Mikkelsen KH, Forslund SK, Kashani A (2018) Recovery of gut microbiota of healthy adults following antibiotic exposure. Nat Microbiol 3:1255–1265. https://doi.org/10.1038/s41564-018-0257-9
Palma-Alvarez RF, Duque-Yemail J, Ros-Cucurull E, Robles-Martinez M (2020) Quinolone-induced psychosis: an updated review. Actas Esp Psiquiatr 48: 126–137. https://www.ncbi.nlm.nih.gov/pubmed/32905605
Pérez-Carbonell L, Mignot E, Leschziner G, Dauvilliers Y (2022) Understanding and approaching excessive daytime sleepiness. Lancet 400:1033–1046. https://doi.org/10.1016/s0140-6736(22)01018-2
Petitjean F, Buda C, Me J, David M (1979) The effect of chloramphenicol on sleep in cat – comparison with thiamphenicol, erythromycine, and oxytetracycline. Psychopharmacology 66:147–153. https://doi.org/10.1007/BF00427622
Prattala R, Paalanen L, Grinberga D, Helasoja V (2007) Gender differences in the consumption of meat, fruit and vegetables are similar in Finland and the Baltic countries. Eur J Public Health 17:520–525. https://doi.org/10.1093/eurpub/ckl265
Ramirez J, Guarner F, Bustos Fernandez L, Maruy A (2020) Antibiotics as major disruptors of gut microbiota. Front Cell Infect Microbiol 10:572912. https://doi.org/10.3389/fcimb.2020.572912
Rana A, Singh S, Deshmukh R, Kumar A (2020) Pharmacological potential of tocopherol and doxycycline against traumatic brain injury-induced cognitive/motor impairment in rats. Brain Inj 34:1039–1050. https://doi.org/10.1080/02699052.2020.1772508
Rosenberg R, Babson K, Menno D, Morris S (2022) Test-retest reliability of the Epworth Sleepiness Scale in clinical trial settings. J Sleep Res 31:e13476. https://doi.org/10.1111/jsr.13476
Schwartz DJ, Langdon AE, Dantas G (2020) Understanding the impact of antibiotic perturbation on the human microbiome. Genome Med 12:82. https://doi.org/10.1186/s13073-020-00782-x
Sen P, Molinero-Perez A, O’Riordan KJ, McCafferty CP (2021) Microbiota and sleep: awakening the gut feeling. Trends Mol Med 27:935–945. https://doi.org/10.1016/j.molmed.2021.07.004
Shao S, Pan W, Wang B, Liu Y (2023) Association between antibiotic exposure and the risk of infertility in women of childbearing age: a case-control study. Ecotoxicol Environ Saf 249:114414. https://doi.org/10.1016/j.ecoenv.2022.114414
Shao Y, Wang Y, Yuan Y, Xie Y (2021) A systematic review on antibiotics misuse in livestock and aquaculture and regulation implications in China. Sci Total Environ 798:149205. https://doi.org/10.1016/j.scitotenv.2021.149205
Smith RP, Easson C, Lyle SM, Kapoor R (2019) Gut microbiome diversity is associated with sleep physiology in humans. PLoS ONE 14:e0222394. https://doi.org/10.1371/journal.pone.0222394
Spaggiari G, Romeo M, Casarini L, Granata ARM (2022) Human fertility and sleep disturbances: a narrative review. Sleep Med 98:13–25. https://doi.org/10.1016/j.sleep.2022.06.009
Sun Y, Kong Z, Song Y, Liu J (2022) The validity and reliability of the PHQ-9 on screening of depression in neurology: a cross sectional study. BMC Psychiatry 22:98. https://doi.org/10.1186/s12888-021-03661-w
Tracy EL, Putney JM, Papp LM (2022) Empty nest status, marital closeness, and perceived health: testing couples’ direct and moderated associations with an actor-partner interdependence model. Fam J Alex Va 30:30–35. https://doi.org/10.1177/10664807211027287
Wang H, Wang N, Wang B, Fang H (2016) Antibiotics detected in urines and adipogenesis in school children. Environ Int 89–90:204–211. https://doi.org/10.1016/j.envint.2016.02.005
Wang Z, Wang Z, Lu T, Chen W (2022) The microbiota-gut-brain axis in sleep disorders. Sleep Med Rev 65:101691. https://doi.org/10.1016/j.smrv.2022.101691
Wen J, Geng S, Zhu L, Yao X (2023) Urinary antibiotic concentrations in preschool children from eastern China and health risk assessment. Environ Sci Pollut Res Int 30:82547–82559. https://doi.org/10.1007/s11356-023-28209-1
Wierzbiński P, Hubska J, Henzler M, Kucharski B (2023) Depressive and other adverse CNS effects of fluoroquinolones. Pharmaceuticals 16:1105. https://doi.org/10.3390/ph16081105
Yang H, Ye DM, Lin ZZ, Lin XY (2023) Young people exposure to antibiotics: implication for health risk and the impact from eating habits of takeaway food. Sci Total Environ 902:166377. https://doi.org/10.1016/j.scitotenv.2023.166377
Yao C, Wang Z, Jiang H, Yan R (2021) Ganoderma lucidum promotes sleep through a gut microbiota-dependent and serotonin-involved pathway in mice. Sci Rep 11:13660. https://doi.org/10.1038/s41598-021-92913-6
Zhang J, Liu X, Zhu Y, Yang L (2020) Antibiotic exposure across three generations from Chinese families and cumulative health risk. Ecotoxicol Environ Saf 191:110237. https://doi.org/10.1016/j.ecoenv.2020.110237
Zhang J, Liu Z, Song S, Fang J (2022) The exposure levels and health risk assessment of antibiotics in urine and its association with platelet mitochondrial DNA methylation in adults from Tianjin, China: a preliminary study. Ecotoxicol Environ Saf 231:113204. https://doi.org/10.1016/j.ecoenv.2022.113204
Zhong S, Wu X, Zhang D, Du S (2022) Antibiotics in urine from general adults in Shenzhen, China: demographic-related difference in exposure levels. Sci Total Environ 843:157070. https://doi.org/10.1016/j.scitotenv.2022.157070
Acknowledgements
We sincerely thank all the newlyweds, staff, and administrators in the study. Our study was financially supported by the National Natural Science Foundation of China (82073578), the Research Level Improvement Plan of Anhui Medical University (2019xkjT006), and the Research Fund for Scientific Research Level Improvement Plan of Anhui Medical University (2022xkjT007).
Funding
This work was supported by the National Natural Science Foundation of China (82073578), the Research Level Improvement Plan of Anhui Medical University (2019xkjT006), and the Research Fund for Scientific Research Level Improvement Plan of Anhui Medical University (2022xkjT007).
Author information
Authors and Affiliations
Contributions
LG contributed to conceptualization, investigation, methodology, data curation, formal analysis, writing—original draft, revision, and editing; YN and BW contributed to conceptualization, investigation, and methodology; LK, SY, and YT contributed to investigation; PZ and SS contributed to conceptualization, investigation, and supervision; FT contributed to funding acquisition, project administration, supervision, and validation; KL contributed to conceptualization, funding acquisition, project administration, supervision, writing—review and editing.
Corresponding author
Ethics declarations
Ethics approval
The protocols were approved by the Anhui Medical University Committee on the Ethics of Human Research (20189999) and complied with the Declaration of Helsinki.
Consent to participate
Informed consent was signed from all newlyweds included in the study.
Consent for publication
Newlyweds included in the study agreed to publish their data.
Competing interests
The authors declare no competing interests.
Additional information
Responsible Editor: Lotfi Aleya
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Gu, L., Ni, Y., Wang, B. et al. Antibiotic exposure associated with nighttime sleep duration and daytime sleepiness in newlyweds. Environ Sci Pollut Res 31, 6350–6371 (2024). https://doi.org/10.1007/s11356-023-31475-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11356-023-31475-8