Anemia in patients ten years after bariatric surgery

Anemia in patients ten years after bariatric surgery | Research Square window.SnipcartSettings = { analytics: { enabled: false } }; (function() { var accessVector = localStorage.getItem('access_vector') || ''; window.dataLayer = window.dataLayer || []; if (accessVector) { window.dataLayer.push({ user: { profile: { profileInfo: { snid: accessVector } } } }); } })(); (function(w,d,s,l,i){w[l]=w[l]||[];w[l].push({'gtm.start':new Date().getTime(),event:'gtm.js'});var f=d.getElementsByTagName(s)[0],j=d.createElement(s),dl=l!='dataLayer'?'&l='+l:'';j.async=true;j.src='https://www.googletagmanager.com/gtm.js?id='+i+dl;f.parentNode.insertBefore(j,f);})(window,document,'script','dataLayer','GTM-K279D39R'); Browse Preprints In Review Journals COVID-19 Preprints AJE Video Bytes Research Tools Research Promotion AJE Professional Editing AJE Rubriq About Preprint Platform In Review Editorial Policies Our Team Advisory Board Help Center Sign In Submit a Preprint Cite Share Download PDF Article Anemia in patients ten years after bariatric surgery Klas Sjöberg, Mimmi Karlsson, Johan Ottosson This is a preprint; it has not been peer reviewed by a journal. https://doi.org/ 10.21203/rs.3.rs-3920388/v1 This work is licensed under a CC BY 4.0 License Status: Published Journal Publication published 09 Nov, 2024 Read the published version in International Journal of Obesity → Version 1 posted 9 You are reading this latest preprint version Abstract Background Obesity, i.e., BMI above 35, affects more than 10% of the global population. Bariatric surgery is an efficient way to treat this condition. Unfortunately, there is a risk for nutritional deficiencies. The number of studies after a longer time span are scarce. The aim of this study was to determine the occurrence of anemia five and ten years after bariatric surgery and how it was related to substitution therapy. Patients and methods Registry data from individuals having primary bariatric surgery in the Scandinavian Obesity Surgery Registry (SOReg) from 2007 to 2022 and with a follow-up at five or ten years was retrieved. Demographic data including weight, as well as method of surgery, Hb levels, supplementation, PPI use and stomal ulcerations were recorded. Results In total, 59 557 individuals (mean age 41 years, range 18-74, 76% women) could be included. The majority, 86%, had undergone laparoscopic Roux-en-Y gastric bypass. After five years 2 838/13 944 women (20.3%) and 456/4 049 men (11.2%) had anaemia. After ten years 644/3 400 women (18.9%) and 178/947 men (18.8%) had anaemia. The use of oral iron increased from 40 to 45% and the need for parenteral iron intake increased from 5 to 11%. Conclusions Anaemia is a significant but manageable condition five and ten years after bariatric surgery. Despite prescription of oral iron supplements to 45% ten years after surgery the Hb levels could still not be fully restored. Consequently, the importance of follow-up visits and continuous supplementation is emphasized. Health sciences/Signs and symptoms/Digestive signs and symptoms Biological sciences/Physiology/Metabolism/Feeding behaviour Anemia bariatric surgery complications follow-up hemoglobin Figures Figure 1 Introduction The prevalence of obesity is increasing worldwide. Between the years 1975 and 2014 the global age-standardized prevalence of obesity, defined as body mass index (BMI) ≥ 30 kg/m², has increased from 3.2–10.8% in men, and from 6.4–14.9% in women ( 1 ). In 2014, 2.3% of the world’s men and 5.0% of the world’s women were severely obese i.e ., with a BMI ≥ 35 kg/m² ( 1 ). Obesity is in turn a risk factor for a range of health issues e.g. , the metabolic syndrome, type 2 diabetes, hypertension, hyperlipidaemia, and cardiovascular disease, as well as a risk factor for cancer ( 2 , 3 ) and a shorter life expectancy compared to the overall population ( 4 ). Many trials and programs have been initiated with the aim to reduce BMI and at the same time reduce the health risks associated with obesity. Bariatric surgery has proven to be the most efficient treatment in reducing and then keeping a lower BMI over time. ( 2 ) On average 5 000 bariatric surgeries are carried out in Sweden each year. The positive outcomes after bariatric surgery are well documented with reduced cardiovascular disease, improvement or even remission of type 2 diabetes as well as protection against development of type 2 diabetes ( 2 , 5 ). The Swedish Obese Subjects (SOS) study, a prospective controlled trial, has among other things shown a decrease in overall mortality as well as a decrease in the risk of cancer after bariatric surgery in obese subjects ( 6 , 7 ). The Scandinavian Obesity Surgery Registry (SOReg) is a national research and quality register that started in 2007 covering virtually all bariatric surgical procedures in Sweden. The register is continuously validated, and registrations have been shown to have very high validity ( 8 ). More than 80 000 operations have been registered, and follow-up visits are registered at 6 weeks, 1 year, 2 years, 5 years, and 10 years after the operation. At the follow-ups, the coverage rate varies between 40 and 95%. The complications second to bariatric surgery vary with the surgical methods used. However, surgical complications as well as dysmotility may occur in all types of surgical procedures. These side effects include bowel obstruction, stomal ulcerations, and gallstone problems ( 9 ). Several other adverse effects after bariatric surgery have been described. These include increased mental illness sometimes with suicidal tendencies or risk of alcohol dependence, and furthermore deficiencies of various nutrients, that among others risk resulting in an increased incidence of anemia ( 10 , 11 ). Patients going through bariatric surgery have an increased risk of anemia already after a shorter period of follow-up. Furthermore, the anemia resumes after standard substitution is given ( 12 ). Regardless of the cause of anemia the condition eventually leads to fatigue and weakness. Anemia has also been associated with a lower quality of life (QoL) ( 13 ). In patients that have undergone bariatric surgery the risk for anemia in the long run, i.e. , after five and ten years, has been scarcely investigated. In a larger group of 959 patients (where 85% were female) that underwent laparoscopic Roux-en-Y gastric bypass 51% had iron deficiency ten years later. The mean hemoglobin (Hb) levels decreased from 135 to 116 g/l ( 14 ). In another investigation with the same time span 47% of 348 patients had iron deficiency with a Hb fall from 138 to 124 g/l after 36 months ( 15 ). In a Norwegian study iron deficiency (based on ferritin levels) occurred in 44% of 530 patients after 10–15 years. The Hb levels were divided into subgroups making comparisons with other reports difficult ( 16 ). Based on the published data this far it would be valuable to follow-up these results in a larger cohort with follow-up according to present guidelines. The purpose of this study was to determine the occurrence of anemia after bariatric surgery in a national cohort over a longer time span and how it was related to substitution therapy, and complications. Patients and Methods Data has been retrieved from the Scandinavian Obesity Surgery Registry (SOReg) database collected until December 2022. All patients in the SOReg database who had undergone primary bariatric surgery ( i.e. , Roux-en-Y gastric bypass (GBY), Sleeve Gastrectomy (SG) or a Bilio-pancreatic diversion with duodenal switch (DS)) with a follow-up period of at least five years were included. In other words, only patients that had gone through bariatric surgery between January 2007 and December 2017 were included. Patients with bariatric surgery before the age of 18, with a registered date of death before a five-year follow-up period, creatinine above 250, and pregnancy in close proximity to their five- or ten-year follow-up were excluded. Before exclusion the population consisted of 60 895 individuals. See Fig. 1 . Demographic data regarding sex, age at the time of surgery and surgical method was registered. At five- and ten-years follow-up weight, BMI, smoking habits, mean Hb levels, percentage with anaemia and supplementary treatment was also retrieved. Treatment with proton pump inhibitors (PPI) and stomal ulcerations were also recorded since these factors can also affect Hb levels. Anemia was defined according to WHOs definition in which the blood cell level (Hb) is under 120 g/L for women and under 130 g/L for men ( 17 ). The study was approved by the Swedish Ethical Review Authority (protocol number 2020–02233). The study is registered-based with anonymized data prior to analysis. Results The study comprised 59 557 individuals, mean age 41 at the time of surgery, range 18–74, 76% women. See Table 1. The majority (86%) had undergone GBY in the total population as well as in the two subgroups with follow-up at five years (88%) and at ten years (98%). As expected, the overall Hb mean level was lower at the five years follow-up compared to preoperative Hb. However, there was no difference in Hb levels between the subgroups with follow-up at five and ten years. Since registration of the Hb levels were not possible in SOReg between 2007 and 2011 only 50% in the group prior to surgery had any Hb level stated. At five- and ten-years follow-up the percentages were 62 and 54%, respectively. The subgroups that had undergone follow-up at five and ten years after surgery consisted of 29 236 (49%) and 8 047 patients (14%), respectively. See Table 1. The percentage with anaemia was 18.3 in the whole group after five years compared to 4.1% prior to surgery. The mean Hb levels in the total population of women at ten years follow-up were 129.1 g/L and for men 140.5 g/L, respectively. The mean Hb in the groups with anaemia was 108.5 and 108.8 g/L for women and 119.4 and 117.8 g/L for men after five and ten years, respectively. See Table 2. For the total population with a registered ten-year follow-up, as well as for the men and women separately, more patients used supplementary treatment with iron after ten years than after five years. The use of oral iron went from 40 to 45% at follow-up at ten years and the need for parenteral iron intake went from 5 to 11% at follow-up at ten years. See table 3. In both women and men, more patients needed substitution with iron as time went by. In both women and men, the substitution with oral iron differed, 44 compared to 50% in women and 25 to 37% in men after five and ten years, respectively. The corresponding numbers for parenteral iron were 6 compared to 12% in women and 2 to compared 5% in men, respectively. See Table 4A and B. Furthermore, substitution with multivitamins and vitamin D was also substantial as well as B12 for obvious reasons. See Tables 3 and 4. The prevalence of stomal ulceration was 1–2% in all groups. The use of PPI was 14% after ten years compared to 10% after five years. See Table 5. After ten years in women with anaemia 76 out of 644 patients (12%) were treated with PPI and in men 29 out of 178 (16%) were treated with PPI. Discussion The purpose with bariatric surgery is to achieve weight loss and gain health benefits, but at the same time the surgery increases the risk of utritional deficiencies. One of the more potentially serious complications is anaemia. The percentage with anaemia increased from 4.1 before surgery to 18.9% after 10 years. Since the incidence of anaemia increases with age this could very well be caused by multimorbidity in an aging population. However, in a Danish study (based on cut-off levels 117 g/l for women and 134 g/l for men, respectively) the percentage with anaemia at 40–49 years of age was 8.1% and 3.9% in women and men, respectively compared to 4.4% and 6.8% in the age group 50–59, respectively ( 18 ). Consequently, even though the Hb levels in the present study could be maintained to some degree, anaemia per se was apparent after a longer follow-up period. Even though the Hb levels drop to some extent in the present study, the proportion of patients with anaemia does not increase to any major extent over time compared to other studies based on patients that have been operated with bariatric surgery. In an older study from 1998 47% had anaemia and the Hb levels decreased from 138 to 124 g/l after ten years ( 15 ). In 2014 another study found anaemia in 51% with a fall in Hb from 135 to 116 g/l ( 14 ), also after ten years. The Hb levels found in the present study was 141 g/l prior to surgery and 132 g/l after ten years (129 g/l in women and 140 g/l for men, respectively). Anaemia was more frequent in women (19%) compared to 16% in a recently published Norwegian study. The occurrence of anaemia in men cannot be compared since the definition for anaemia for men differs in the two populations ( 16 ). Consequently, even though the preoperative level was slightly higher in the present study it seems as if the Hb level can be kept at a rather normal level despite the potential effects of bariatric surgery. This is probably due to an increased awareness among the health care professionals responsible for the follow-up visits. The information to patients about the importance of supplementary treatment with iron and other supplements after bariatric surgery also seems to be satisfactory. However, to maintain homeostasis a large minority must be prescribed different types of supplements. The need for substitution is not reduced as time goes by. In contrast, the group that is prescribed iron or folic acid increases over the years – even after ten years. However, this population is not regaining the blood level prior to surgery over time. This indicates that the prescribed doses of iron might be insufficient or that other causes than iron deficiency could be present. This suggests that a more accurate investigation of the cause of anaemia in this population in the first years after surgery should be undertaken and hopefully result in a higher Hb level than what has been achieved with the current guidelines. Consequently, to prevent complications, a regular follow-up over a longer time span is mandatory. With a structured follow-up individuals with any signs of malnutrition can be identified and referred for accurate treatment. The follow-up can also be a control station to make sure that the individuals have understood the importance of a lifelong substituting therapy post bariatric surgery to reduce the risk of anaemia and other malabsorptive conditions in the future. It can be assumed that not all patients attend their follow-up visits. In view of the risk for malnutrition and anaemia in particular it is important to emphasize for the patient that regular visits are valuable to maintain health and quality of life. The incidence of diagnosed stomal ulceration is low and even if it is underdiagnosed it is unlikely to contribute to development of anaemia to any major degree. The use of PPI is high, especially among women after ten years where 13% were prescribed PPI. In view of the nature of the surgery that results in a vast reduction of acid production per se this treatment does probably not play any major role in the development of anaemia. This is in line with the observation that the percentage of patients with PPI treatment did not differ between anaemic and non-anaemic patients. The indication for PPI treatment is not registered in SOReg but include reflux disease and upper GI pain. The cause of anaemia after bariatric surgery is more likely to be found in altered anatomy and/or poor nutritional intake. A strength with the present study is that almost all patients that have undergone bariatric surgery in the country have been included. As a result, the number of included patients is, to the best of our knowledge, the highest this far for a bariatric operated cohort. The long follow-up period covering a decade is also valuable and gives information about the risks over a longer time span. An important limitation of this study is that Hb has not been registered for all patients at all three time-points. This is due to the fact that Hb was introduced as a variable in SOReg 2012 and consequently no patients registered during the first five years has a preoperative Hb. The other factor of importance is that Hb is not a mandatory variable and patients can be registred in SOReg without Hb. It has not been possible to correct this problem with at dropout analysis since the only source of data come from SOReg in his study. Another limitation is that we only have information about the Hb and not the iron or ferritin levels. Our findings can hence not give any clear indication to all possible causes leading to anaemia. Another limitation is that the supplementary treatment with “multivitamin” can be both with or without iron. This group with multivitamin supplementation is thus stated separately from those with oral iron supplementation. However, multivitamin on the Swedish market contain only small amounts of iron, up to 15 mg/day in recommended doses. Furthermore, as in all registries, not all parameters are recorded and consequently data is missing. On the other hand, the large group may still provide information that makes the conclusions generalizable. Finally, despite the high number of participants, where many patients have been registered at all three occasions, it is not a retrospectively collected prospective study but instead a cross-sectional study comparing three independent groups of patients. In view of the many participants, we consider it is still possible to draw conclusions about the occurrence of anaemia in patients that had undergone bariatric surgery. To conclude, bariatric surgery is an effective measure to obtain weight loss and improved metabolic control. Despite regular follow-up visits and prescription of adequate substitution, anaemia is a significant but treatable problem and seems to be less pronounced compared to other reports. Regular check-up on a yearly basis is recommended to avoid serious complications such as untreated anaemia. However, even though supplements are prescribed to a substantial subgroup it has not been possible to fully restore the Hb levels to their original levels. Adjustments of the doses or in some cases a more thorough investigation of the underlying causes could be contemplated. In these patients several causes behind anaemia could be present at the same time. In view of the large minority requiring substitution, it is recommended that the importance of regular follow-up visits is emphasized, and that the medication is maintained over time. In view of the high incidence of anaemia after such a long time span as ten years it is extra important to be aware of the substantial risk for development of anaemia and malabsorption as time goes by. A patient that has gone through surgery for a better health should not have to risk developing other diseases instead that impairs the quality of life. Conclusions Anaemia is a significant but still manageable condition five and ten years after bariatric surgery. However, despite prescription of oral iron supplements to 45% of the patients ten years after surgery the Hb levels could still not be fully restored. Consequently, the importance of follow-up visits and continuous evaluation of the need for supplementation is emphasized. Declarations Competing Interests There are no competing financial interests in relation to the present study. Author contributions All authors were responsible for the design of the study. JO provided the data and. MK extracted and analysed the data. MK wrote the manuscript under supervision of KS and JO provided feedback on the manuscript. Acknowledgements We want to thank the Foundations at Skåne University Hospital for financial support. Data availability statement The data in this study has been retrieved from the SOReg registry (SOReg (uu.se)), the Scandinavian Obesity Surgery Registry. References NCD Risk Factor Collaboration. 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Prevalence of Anemia and Related Deficiencies 10 Years After Gastric Bypass—a Retrospective Study. Obesity Surgery 2015;25:1019–1023. Lucca U, Tettamanti M, Mosconi P, Apolone G, Gandini F, Nobili A, et al. Association of Mild Anemia with Cognitive, Functional, Mood and Quality of Life Outcomes in the Elderly: The “Health and Anemia” Study. PLoS One 2008 April;3(4): e1920. Obinwanne KM, Fredrickson KA, Mathiason MA, Kallies KJ, Farnen JP, Kothari SN. Incidence, treatment, and outcomes of iron deficiency after laparoscopic Roux-en-Y gastric bypass: a 10-year analysis. J Am Coll Surg. 2014;218(2):246–52. Brolin RE, Gorman JH, Gorman RC, Petschenik AJ, Bradley LJ, Kenler HA, Cody RP. Are vitamin B12 and folate deficiency clinically important after roux-en-Y gastric bypass? J Gastrointest Surg. 1998 Sep-Oct;2(5):436–42. Sandvik J, Kverndokk Bjerkan K, Græslie H, Lihaug Hoff DA, Johnsen G, Klöckner C, et al. Iron Deficiency and Anemia 10 Years After Roux-en-Y Gastric Bypass for Severe Obesity. Front Endocrinol (Lausanne). 2021;12:679066 https:// apps.who.int/iris/bitstream/handle/10665/85839/WHO_NMH_NHD_MNM_11.1_eng.pdf Ryberg-Nørholt J, Frederiksen H, Nybo M. Changing reference intervals for haemoglobin in Denmark: Clinical and financial aspects. Biochem Med (Zagreb) 2017;27(3):030702 https://doi.org/10.11613/BM.2017.030702 Tables Tables 1-5 are available in the Supplementary Files section. Additional Declarations There is NO conflict of interest to disclose Supplementary Files Table1Characteristicsofthestudypopulation.xlsx Table 1 Characteristics of the study population prior to bariatric surgery, and at follow-up at five and ten years, respectively Table2Hblevelsandpercentwithanemia.xlsx Table 2 Hemoglobin levels and percent with anemia prior to surgery, and at follow-up at five and ten years, respectively Table3Supplementarytreatment.xlsx Table 3 Supplementary treatment reported in the populations with five- and ten-years follow-up Table4Supplemetarytreatmentinmenandwomen.xlsx Table 4 A Supplementary treatment reported in the populations with five- and ten-years follow-up in women Table 4 B Supplementary treatment reported in the populations with five- and ten-years follow-up in men Table5SupplementarytreatmentwithPPIandstomalulcers.xlsx Table 5 Supplementary treatment with PPI and stomal ulcer registered as a complication in the population with 5- and 10-years follow-up Cite Share Download PDF Status: Published Journal Publication published 09 Nov, 2024 Read the published version in International Journal of Obesity → Version 1 posted Editorial decision: revise 28 Feb, 2024 Review # 2 received at journal 26 Feb, 2024 Reviewer # 2 agreed at journal 13 Feb, 2024 Review # 1 received at journal 11 Feb, 2024 Reviewer # 1 agreed at journal 09 Feb, 2024 Reviewers invited by journal 05 Feb, 2024 Submission checks completed at journal 05 Feb, 2024 First submitted to journal 02 Feb, 2024 Editor assigned by journal 02 Feb, 2024 You are reading this latest preprint version Research Square lets you share your work early, gain feedback from the community, and start making changes to your manuscript prior to peer review in a journal. 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Also discoverable on Platform About Our Team In Review Editorial Policies Advisory Board Help Center Resources Author Services Accessibility API Access RSS feed Manage Cookie Preferences © Research Square 2026 | ISSN 2693-5015 (online) Privacy Policy Terms of Service Do Not Sell My Personal Information {"props":{"pageProps":{"initialData":{"identity":"rs-3920388","acceptedTermsAndConditions":true,"allowDirectSubmit":false,"archivedVersions":[],"articleType":"Article","associatedPublications":[],"authors":[{"id":271135141,"identity":"35dfed46-7286-411f-be4e-68c66d49073d","order_by":0,"name":"Klas 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19:42:04","extension":"xlsx","order_by":1,"title":"","display":"","copyAsset":false,"role":"supplement","size":12860,"visible":true,"origin":"","legend":"\u003cp\u003eTable 1 Characteristics of the study population prior to bariatric surgery, and at follow-up at five and ten years, respectively\u003c/p\u003e","description":"","filename":"Table1Characteristicsofthestudypopulation.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-3920388/v1/1788fe02914c9c35635bdeca.xlsx"},{"id":50815350,"identity":"72cad16c-c187-418b-9681-61e0668ceee9","added_by":"auto","created_at":"2024-02-07 19:42:04","extension":"xlsx","order_by":2,"title":"","display":"","copyAsset":false,"role":"supplement","size":10927,"visible":true,"origin":"","legend":"\u003cp\u003eTable 2 Hemoglobin levels and percent with anemia prior to surgery, and at follow-up at five and ten years, respectively\u003c/p\u003e","description":"","filename":"Table2Hblevelsandpercentwithanemia.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-3920388/v1/a2f71b8b525dfb227d6d6a91.xlsx"},{"id":50815355,"identity":"8699ae12-b3cd-43fa-9258-0c0145ffba91","added_by":"auto","created_at":"2024-02-07 19:42:04","extension":"xlsx","order_by":3,"title":"","display":"","copyAsset":false,"role":"supplement","size":10496,"visible":true,"origin":"","legend":"\u003cp\u003eTable 3 Supplementary treatment reported in the populations with five- and ten-years follow-up\u003c/p\u003e","description":"","filename":"Table3Supplementarytreatment.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-3920388/v1/deacea206641a9e2e2fe3778.xlsx"},{"id":50815352,"identity":"ffc00fa3-04a4-48bd-aae1-10c8bb69f180","added_by":"auto","created_at":"2024-02-07 19:42:04","extension":"xlsx","order_by":4,"title":"","display":"","copyAsset":false,"role":"supplement","size":11542,"visible":true,"origin":"","legend":"\u003cp\u003eTable 4 A Supplementary treatment reported in the populations with five- and ten-years follow-up in women\u003c/p\u003e\n\u003cp\u003eTable 4 B Supplementary treatment reported in the populations with five- and ten-years follow-up in men\u003c/p\u003e","description":"","filename":"Table4Supplemetarytreatmentinmenandwomen.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-3920388/v1/d58fce4d7777eb9f61885d86.xlsx"},{"id":50815354,"identity":"ffa9cb85-1eb5-4aac-ad50-ea2c251fb52f","added_by":"auto","created_at":"2024-02-07 19:42:04","extension":"xlsx","order_by":5,"title":"","display":"","copyAsset":false,"role":"supplement","size":10538,"visible":true,"origin":"","legend":"\u003cp\u003eTable 5 Supplementary treatment with PPI and stomal ulcer registered as a complication in the population with 5- and 10-years follow-up\u003c/p\u003e","description":"","filename":"Table5SupplementarytreatmentwithPPIandstomalulcers.xlsx","url":"https://assets-eu.researchsquare.com/files/rs-3920388/v1/275d6c2a36fbd9f8dde0c182.xlsx"}],"financialInterests":"There is \u003cb\u003eNO\u003c/b\u003e conflict of interest to disclose","formattedTitle":"Anemia in patients ten years after bariatric surgery","fulltext":[{"header":"Introduction","content":"\u003cp\u003eThe prevalence of obesity is increasing worldwide. Between the years 1975 and 2014 the global age-standardized prevalence of obesity, defined as body mass index (BMI)\u0026thinsp;\u0026ge;\u0026thinsp;30 kg/m\u0026sup2;, has increased from 3.2\u0026ndash;10.8% in men, and from 6.4\u0026ndash;14.9% in women (\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e). In 2014, 2.3% of the world\u0026rsquo;s men and 5.0% of the world\u0026rsquo;s women were severely obese \u003cem\u003ei.e\u003c/em\u003e., with a BMI\u0026thinsp;\u0026ge;\u0026thinsp;35 kg/m\u0026sup2; (\u003cspan citationid=\"CR1\" class=\"CitationRef\"\u003e1\u003c/span\u003e). Obesity is in turn a risk factor for a range of health issues \u003cem\u003ee.g.\u003c/em\u003e, the metabolic syndrome, type 2 diabetes, hypertension, hyperlipidaemia, and cardiovascular disease, as well as a risk factor for cancer (\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e, \u003cspan citationid=\"CR3\" class=\"CitationRef\"\u003e3\u003c/span\u003e) and a shorter life expectancy compared to the overall population (\u003cspan citationid=\"CR4\" class=\"CitationRef\"\u003e4\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eMany trials and programs have been initiated with the aim to reduce BMI and at the same time reduce the health risks associated with obesity. Bariatric surgery has proven to be the most efficient treatment in reducing and then keeping a lower BMI over time. (\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e) On average 5 000 bariatric surgeries are carried out in Sweden each year. The positive outcomes after bariatric surgery are well documented with reduced cardiovascular disease, improvement or even remission of type 2 diabetes as well as protection against development of type 2 diabetes (\u003cspan citationid=\"CR2\" class=\"CitationRef\"\u003e2\u003c/span\u003e, \u003cspan citationid=\"CR5\" class=\"CitationRef\"\u003e5\u003c/span\u003e). The Swedish Obese Subjects (SOS) study, a prospective controlled trial, has among other things shown a decrease in overall mortality as well as a decrease in the risk of cancer after bariatric surgery in obese subjects (\u003cspan citationid=\"CR6\" class=\"CitationRef\"\u003e6\u003c/span\u003e, \u003cspan citationid=\"CR7\" class=\"CitationRef\"\u003e7\u003c/span\u003e).\u003c/p\u003e \u003cp\u003eThe Scandinavian Obesity Surgery Registry (SOReg) is a national research and quality register that started in 2007 covering virtually all bariatric surgical procedures in Sweden. The register is continuously validated, and registrations have been shown to have very high validity (\u003cspan citationid=\"CR8\" class=\"CitationRef\"\u003e8\u003c/span\u003e). More than 80 000 operations have been registered, and follow-up visits are registered at 6 weeks, 1 year, 2 years, 5 years, and 10 years after the operation. At the follow-ups, the coverage rate varies between 40 and 95%.\u003c/p\u003e \u003cp\u003eThe complications second to bariatric surgery vary with the surgical methods used. However, surgical complications as well as dysmotility may occur in all types of surgical procedures. These side effects include bowel obstruction, stomal ulcerations, and gallstone problems (\u003cspan citationid=\"CR9\" class=\"CitationRef\"\u003e9\u003c/span\u003e). Several other adverse effects after bariatric surgery have been described. These include increased mental illness sometimes with suicidal tendencies or risk of alcohol dependence, and furthermore deficiencies of various nutrients, that among others risk resulting in an increased incidence of anemia (\u003cspan citationid=\"CR10\" class=\"CitationRef\"\u003e10\u003c/span\u003e, \u003cspan citationid=\"CR11\" class=\"CitationRef\"\u003e11\u003c/span\u003e). Patients going through bariatric surgery have an increased risk of anemia already after a shorter period of follow-up. Furthermore, the anemia resumes after standard substitution is given (\u003cspan citationid=\"CR12\" class=\"CitationRef\"\u003e12\u003c/span\u003e). Regardless of the cause of anemia the condition eventually leads to fatigue and weakness. Anemia has also been associated with a lower quality of life (QoL) (\u003cspan citationid=\"CR13\" class=\"CitationRef\"\u003e13\u003c/span\u003e). In patients that have undergone bariatric surgery the risk for anemia in the long run, \u003cem\u003ei.e.\u003c/em\u003e, after five and ten years, has been scarcely investigated. In a larger group of 959 patients (where 85% were female) that underwent laparoscopic Roux-en-Y gastric bypass 51% had iron deficiency ten years later. The mean hemoglobin (Hb) levels decreased from 135 to 116 g/l (\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e). In another investigation with the same time span 47% of 348 patients had iron deficiency with a Hb fall from 138 to 124 g/l after 36 months (\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e). In a Norwegian study iron deficiency (based on ferritin levels) occurred in 44% of 530 patients after 10\u0026ndash;15 years. The Hb levels were divided into subgroups making comparisons with other reports difficult (\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e). Based on the published data this far it would be valuable to follow-up these results in a larger cohort with follow-up according to present guidelines.\u003c/p\u003e \u003cp\u003eThe purpose of this study was to determine the occurrence of anemia after bariatric surgery in a national cohort over a longer time span and how it was related to substitution therapy, and complications.\u003c/p\u003e"},{"header":"Patients and Methods","content":"\u003cp\u003eData has been retrieved from the Scandinavian Obesity Surgery Registry (SOReg) database collected until December 2022. All patients in the SOReg database who had undergone primary bariatric surgery (\u003cem\u003ei.e.\u003c/em\u003e, Roux-en-Y gastric bypass (GBY), Sleeve Gastrectomy (SG) or a Bilio-pancreatic diversion with duodenal switch (DS)) with a follow-up period of at least five years were included. In other words, only patients that had gone through bariatric surgery between January 2007 and December 2017 were included. Patients with bariatric surgery before the age of 18, with a registered date of death before a five-year follow-up period, creatinine above 250, and pregnancy in close proximity to their five- or ten-year follow-up were excluded. Before exclusion the population consisted of 60 895 individuals. See Fig.\u0026nbsp;\u003cspan refid=\"Fig1\" class=\"InternalRef\"\u003e1\u003c/span\u003e.\u003c/p\u003e \u003cp\u003eDemographic data regarding sex, age at the time of surgery and surgical method was registered. At five- and ten-years follow-up weight, BMI, smoking habits, mean Hb levels, percentage with anaemia and supplementary treatment was also retrieved. Treatment with proton pump inhibitors (PPI) and stomal ulcerations were also recorded since these factors can also affect Hb levels. Anemia was defined according to WHOs definition in which the blood cell level (Hb) is under 120 g/L for women and under 130 g/L for men (\u003cspan citationid=\"CR17\" class=\"CitationRef\"\u003e17\u003c/span\u003e).\u003c/p\u003e \u003cp\u003e The study was approved by the Swedish Ethical Review Authority (protocol number 2020\u0026ndash;02233). The study is registered-based with anonymized data prior to analysis.\u003c/p\u003e"},{"header":"Results","content":"\u003cp\u003eThe study comprised 59 557 individuals, mean age 41 at the time of surgery, range 18\u0026ndash;74, 76% women. See Table\u0026nbsp;1. The majority (86%) had undergone GBY in the total population as well as in the two subgroups with follow-up at five years (88%) and at ten years (98%). As expected, the overall Hb mean level was lower at the five years follow-up compared to preoperative Hb. However, there was no difference in Hb levels between the subgroups with follow-up at five and ten years. Since registration of the Hb levels were not possible in SOReg between 2007 and 2011 only 50% in the group prior to surgery had any Hb level stated. At five- and ten-years follow-up the percentages were 62 and 54%, respectively.\u003c/p\u003e \u003cp\u003eThe subgroups that had undergone follow-up at five and ten years after surgery consisted of 29 236 (49%) and 8 047 patients (14%), respectively. See Table\u0026nbsp;1.\u003c/p\u003e \u003cp\u003eThe percentage with anaemia was 18.3 in the whole group after five years compared to 4.1% prior to surgery. The mean Hb levels in the total population of women at ten years follow-up were 129.1 g/L and for men 140.5 g/L, respectively. The mean Hb in the groups with anaemia was 108.5 and 108.8 g/L for women and 119.4 and 117.8 g/L for men after five and ten years, respectively. See Table\u0026nbsp;2.\u003c/p\u003e \u003cp\u003eFor the total population with a registered ten-year follow-up, as well as for the men and women separately, more patients used supplementary treatment with iron after ten years than after five years. The use of oral iron went from 40 to 45% at follow-up at ten years and the need for parenteral iron intake went from 5 to 11% at follow-up at ten years. See table 3.\u003c/p\u003e \u003cp\u003eIn both women and men, more patients needed substitution with iron as time went by. In both women and men, the substitution with oral iron differed, 44 compared to 50% in women and 25 to 37% in men after five and ten years, respectively. The corresponding numbers for parenteral iron were 6 compared to 12% in women and 2 to compared 5% in men, respectively. See Table\u0026nbsp;4A and B. Furthermore, substitution with multivitamins and vitamin D was also substantial as well as B12 for obvious reasons. See Tables\u0026nbsp;3 and 4.\u003c/p\u003e \u003cp\u003eThe prevalence of stomal ulceration was 1\u0026ndash;2% in all groups. The use of PPI was 14% after ten years compared to 10% after five years. See Table\u0026nbsp;5. After ten years in women with anaemia 76 out of 644 patients (12%) were treated with PPI and in men 29 out of 178 (16%) were treated with PPI.\u003c/p\u003e"},{"header":"Discussion","content":"\u003cp\u003eThe purpose with bariatric surgery is to achieve weight loss and gain health benefits, but at the same time the surgery increases the risk of utritional deficiencies. One of the more potentially serious complications is anaemia. The percentage with anaemia increased from 4.1 before surgery to 18.9% after 10 years. Since the incidence of anaemia increases with age this could very well be caused by multimorbidity in an aging population. However, in a Danish study (based on cut-off levels 117 g/l for women and 134 g/l for men, respectively) the percentage with anaemia at 40\u0026ndash;49 years of age was 8.1% and 3.9% in women and men, respectively compared to 4.4% and 6.8% in the age group 50\u0026ndash;59, respectively (\u003cspan citationid=\"CR18\" class=\"CitationRef\"\u003e18\u003c/span\u003e). Consequently, even though the Hb levels in the present study could be maintained to some degree, anaemia \u003cem\u003eper se\u003c/em\u003e was apparent after a longer follow-up period.\u003c/p\u003e \u003cp\u003eEven though the Hb levels drop to some extent in the present study, the proportion of patients with anaemia does not increase to any major extent over time compared to other studies based on patients that have been operated with bariatric surgery. In an older study from 1998 47% had anaemia and the Hb levels decreased from 138 to 124 g/l after ten years (\u003cspan citationid=\"CR15\" class=\"CitationRef\"\u003e15\u003c/span\u003e). In 2014 another study found anaemia in 51% with a fall in Hb from 135 to 116 g/l (\u003cspan citationid=\"CR14\" class=\"CitationRef\"\u003e14\u003c/span\u003e), also after ten years. The Hb levels found in the present study was 141 g/l prior to surgery and 132 g/l after ten years (129 g/l in women and 140 g/l for men, respectively). Anaemia was more frequent in women (19%) compared to 16% in a recently published Norwegian study. The occurrence of anaemia in men cannot be compared since the definition for anaemia for men differs in the two populations (\u003cspan citationid=\"CR16\" class=\"CitationRef\"\u003e16\u003c/span\u003e). Consequently, even though the preoperative level was slightly higher in the present study it seems as if the Hb level can be kept at a rather normal level despite the potential effects of bariatric surgery. This is probably due to an increased awareness among the health care professionals responsible for the follow-up visits. The information to patients about the importance of supplementary treatment with iron and other supplements after bariatric surgery also seems to be satisfactory.\u003c/p\u003e \u003cp\u003eHowever, to maintain homeostasis a large minority must be prescribed different types of supplements. The need for substitution is not reduced as time goes by. In contrast, the group that is prescribed iron or folic acid increases over the years \u0026ndash; even after ten years. However, this population is not regaining the blood level prior to surgery over time. This indicates that the prescribed doses of iron might be insufficient or that other causes than iron deficiency could be present. This suggests that a more accurate investigation of the cause of anaemia in this population in the first years after surgery should be undertaken and hopefully result in a higher Hb level than what has been achieved with the current guidelines.\u003c/p\u003e \u003cp\u003eConsequently, to prevent complications, a regular follow-up over a longer time span is mandatory. With a structured follow-up individuals with any signs of malnutrition can be identified and referred for accurate treatment. The follow-up can also be a control station to make sure that the individuals have understood the importance of a lifelong substituting therapy post bariatric surgery to reduce the risk of anaemia and other malabsorptive conditions in the future. It can be assumed that not all patients attend their follow-up visits. In view of the risk for malnutrition and anaemia in particular it is important to emphasize for the patient that regular visits are valuable to maintain health and quality of life.\u003c/p\u003e \u003cp\u003eThe incidence of diagnosed stomal ulceration is low and even if it is underdiagnosed it is unlikely to contribute to development of anaemia to any major degree. The use of PPI is high, especially among women after ten years where 13% were prescribed PPI. In view of the nature of the surgery that results in a vast reduction of acid production \u003cem\u003eper se\u003c/em\u003e this treatment does probably not play any major role in the development of anaemia. This is in line with the observation that the percentage of patients with PPI treatment did not differ between anaemic and non-anaemic patients. The indication for PPI treatment is not registered in SOReg but include reflux disease and upper GI pain. The cause of anaemia after bariatric surgery is more likely to be found in altered anatomy and/or poor nutritional intake.\u003c/p\u003e \u003cp\u003eA strength with the present study is that almost all patients that have undergone bariatric surgery in the country have been included. As a result, the number of included patients is, to the best of our knowledge, the highest this far for a bariatric operated cohort. The long follow-up period covering a decade is also valuable and gives information about the risks over a longer time span. An important limitation of this study is that Hb has not been registered for all patients at all three time-points. This is due to the fact that Hb was introduced as a variable in SOReg 2012 and consequently no patients registered during the first five years has a preoperative Hb. The other factor of importance is that Hb is not a mandatory variable and patients can be registred in SOReg without Hb. It has not been possible to correct this problem with at dropout analysis since the only source of data come from SOReg in his study. Another limitation is that we only have information about the Hb and not the iron or ferritin levels. Our findings can hence not give any clear indication to all possible causes leading to anaemia. Another limitation is that the supplementary treatment with \u0026ldquo;multivitamin\u0026rdquo; can be both with or without iron. This group with multivitamin supplementation is thus stated separately from those with oral iron supplementation. However, multivitamin on the Swedish market contain only small amounts of iron, up to 15 mg/day in recommended doses. Furthermore, as in all registries, not all parameters are recorded and consequently data is missing. On the other hand, the large group may still provide information that makes the conclusions generalizable. Finally, despite the high number of participants, where many patients have been registered at all three occasions, it is not a retrospectively collected prospective study but instead a cross-sectional study comparing three independent groups of patients. In view of the many participants, we consider it is still possible to draw conclusions about the occurrence of anaemia in patients that had undergone bariatric surgery.\u003c/p\u003e \u003cp\u003eTo conclude, bariatric surgery is an effective measure to obtain weight loss and improved metabolic control. Despite regular follow-up visits and prescription of adequate substitution, anaemia is a significant but treatable problem and seems to be less pronounced compared to other reports. Regular check-up on a yearly basis is recommended to avoid serious complications such as untreated anaemia. However, even though supplements are prescribed to a substantial subgroup it has not been possible to fully restore the Hb levels to their original levels. Adjustments of the doses or in some cases a more thorough investigation of the underlying causes could be contemplated. In these patients several causes behind anaemia could be present at the same time. In view of the large minority requiring substitution, it is recommended that the importance of regular follow-up visits is emphasized, and that the medication is maintained over time. In view of the high incidence of anaemia after such a long time span as ten years it is extra important to be aware of the substantial risk for development of anaemia and malabsorption as time goes by. A patient that has gone through surgery for a better health should not have to risk developing other diseases instead that impairs the quality of life.\u003c/p\u003e"},{"header":"Conclusions","content":"\u003cp\u003eAnaemia is a significant but still manageable condition five and ten years after bariatric surgery. However, despite prescription of oral iron supplements to 45% of the patients ten years after surgery the Hb levels could still not be fully restored. Consequently, the importance of follow-up visits and continuous evaluation of the need for supplementation is emphasized.\u003c/p\u003e"},{"header":"Declarations","content":"\u003cp\u003e \u003ch2\u003eCompeting Interests\u003c/h2\u003e \u003cp\u003eThere are no competing financial interests in relation to the present study.\u003c/p\u003e \u003c/p\u003e\u003ch2\u003eAuthor contributions\u003c/h2\u003e \u003cp\u003eAll authors were responsible for the design of the study. JO provided the data and. MK extracted and analysed the data. MK wrote the manuscript under supervision of KS and JO provided feedback on the manuscript.\u003c/p\u003e\u003ch2\u003eAcknowledgements\u003c/h2\u003e \u003cp\u003eWe want to thank the Foundations at Sk\u0026aring;ne University Hospital for financial support.\u003c/p\u003e\u003ch2\u003eData availability statement\u003c/h2\u003e \u003cp\u003eThe data in this study has been retrieved from the SOReg registry (SOReg (uu.se)), the Scandinavian Obesity Surgery Registry.\u003c/p\u003e"},{"header":"References","content":"\u003col\u003e\u003cli\u003e\u003cspan\u003eNCD Risk Factor Collaboration. Trends in adult body-mass index in 200 countries from 1975 to 2014: a pooled analysis of 1698 population-based measurement studies with 19\u0026middot;2 million participants. Lancet 2016;387:1377\u0026ndash;96.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSj\u0026ouml;str\u0026ouml;m L. 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Association of Mild Anemia with Cognitive, Functional, Mood and Quality of Life Outcomes in the Elderly: The \u0026ldquo;Health and Anemia\u0026rdquo; Study. PLoS One 2008 April;3(4): e1920.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eObinwanne KM, Fredrickson KA, Mathiason MA, Kallies KJ, Farnen JP, Kothari SN. Incidence, treatment, and outcomes of iron deficiency after laparoscopic Roux-en-Y gastric bypass: a 10-year analysis. J Am Coll Surg. 2014;218(2):246\u0026ndash;52.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eBrolin RE, Gorman JH, Gorman RC, Petschenik AJ, Bradley LJ, Kenler HA, Cody RP. Are vitamin B12 and folate deficiency clinically important after roux-en-Y gastric bypass? J Gastrointest Surg. 1998 Sep-Oct;2(5):436\u0026ndash;42.\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eSandvik J, Kverndokk Bjerkan K, Gr\u0026aelig;slie H, Lihaug Hoff DA, Johnsen G, Kl\u0026ouml;ckner C, et al. Iron Deficiency and Anemia 10 Years After Roux-en-Y Gastric Bypass for Severe Obesity. Front Endocrinol (Lausanne). 2021;12:679066\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003ehttps://\u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003eapps.who.int/iris/bitstream/handle/10665/85839/WHO_NMH_NHD_MNM_11.1_eng.pdf\u003c/span\u003e\u003cspan address=\"http://apps.who.int/iris/bitstream/handle/10665/85839/WHO_NMH_NHD_MNM_11.1_eng.pdf\" targettype=\"URL\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003c/span\u003e\u003c/li\u003e \u003cli\u003e\u003cspan\u003eRyberg-N\u0026oslash;rholt J, Frederiksen H, Nybo M. Changing reference intervals for haemoglobin in Denmark: Clinical and financial aspects. Biochem Med (Zagreb) 2017;27(3):030702 \u003cspan class=\"ExternalRef\"\u003e\u003cspan class=\"RefSource\"\u003ehttps://doi.org/10.11613/BM.2017.030702\u003c/span\u003e\u003cspan address=\"10.11613/BM.2017.030702\" targettype=\"DOI\" class=\"RefTarget\"\u003e\u003c/span\u003e\u003c/span\u003e\u003c/span\u003e\u003c/li\u003e\u003c/ol\u003e"},{"header":"Tables","content":"\u003cp\u003eTables 1-5 are available in the Supplementary Files section.\u003c/p\u003e"}],"fulltextSource":"","fullText":"","funders":[],"hasAdminPriorityOnWorkflow":false,"hasManuscriptDocX":true,"hasOptedInToPreprint":true,"hasPassedJournalQc":"","hasAnyPriority":false,"hideJournal":false,"highlight":"","institution":"","isAcceptedByJournal":true,"isAuthorSuppliedPdf":false,"isDeskRejected":"","isHiddenFromSearch":false,"isInQc":false,"isInWorkflow":false,"isPdf":false,"isPdfUpToDate":true,"isWithdrawnOrRetracted":false,"journal":{"display":true,"email":"[email protected]","identity":"international-journal-of-obesity","isNatureJournal":false,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"ijo","sideBox":"Learn more about [International Journal of Obesity](http://www.nature.com/ijo/)","snPcode":"41366","submissionUrl":"https://mts-ijo.nature.com/cgi-bin/main.plex","title":"International Journal of Obesity","twitterHandle":"@intjobesity","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"ejp","reportingPortfolio":"Nature AJ","inReviewEnabled":true,"inReviewRevisionsEnabled":false},"keywords":"Anemia, bariatric surgery, complications, follow-up, hemoglobin","lastPublishedDoi":"10.21203/rs.3.rs-3920388/v1","lastPublishedDoiUrl":"https://doi.org/10.21203/rs.3.rs-3920388/v1","license":{"name":"CC BY 4.0","url":"https://creativecommons.org/licenses/by/4.0/"},"manuscriptAbstract":"\u003cp\u003eBackground\u003c/p\u003e\n\u003cp\u003eObesity, i.e., BMI above 35, affects more than 10% of the global population. Bariatric surgery is an efficient way to treat this condition. Unfortunately, there is a risk for nutritional deficiencies. The number of studies after a longer time span are scarce. The aim of this study was to determine the occurrence of anemia five and ten years after bariatric surgery and how it was related to substitution therapy.\u003c/p\u003e\n\u003cp\u003ePatients and methods\u003c/p\u003e\n\u003cp\u003eRegistry data from individuals having primary bariatric surgery in the Scandinavian Obesity Surgery Registry (SOReg) from 2007 to 2022 and with a follow-up at five or ten years was retrieved. Demographic data including weight, as well as method of surgery, Hb levels, supplementation, PPI use and stomal ulcerations were recorded.\u003c/p\u003e\n\u003cp\u003eResults\u003c/p\u003e\n\u003cp\u003eIn total, 59 557 individuals (mean age 41 years, range 18-74, 76% women) could be included. The majority, 86%, had undergone laparoscopic Roux-en-Y gastric bypass. After five years 2 838/13 944 women (20.3%) and 456/4 049 men (11.2%) had anaemia. After ten years 644/3 400 women (18.9%) and 178/947 men (18.8%) had anaemia. The use of oral iron increased from 40 to 45% and the need for parenteral iron intake increased from 5 to 11%.\u003c/p\u003e\n\u003cp\u003eConclusions\u003c/p\u003e\n\u003cp\u003eAnaemia is a significant but manageable condition five and ten years after bariatric surgery. Despite prescription of oral iron supplements to 45% ten years after surgery the Hb levels could still not be fully restored. Consequently, the importance of follow-up visits and continuous supplementation is emphasized.\u003c/p\u003e","manuscriptTitle":"Anemia in patients ten years after bariatric surgery","msid":"","msnumber":"","nonDraftVersions":[{"code":1,"date":"2024-02-07 19:41:59","doi":"10.21203/rs.3.rs-3920388/v1","editorialEvents":[{"type":"communityComments","content":0},{"type":"decision","content":"revise","date":"2024-02-28T17:05:12+00:00","index":"","fulltext":""},{"type":"editorInvitedReview","content":"This content is not available.","date":"2024-02-26T12:00:22+00:00","index":2,"fulltext":"This content is not available."},{"type":"reviewerAgreed","content":"This content is not available.","date":"2024-02-13T12:16:41+00:00","index":2,"fulltext":"This content is not available."},{"type":"editorInvitedReview","content":"This content is not available.","date":"2024-02-11T14:06:30+00:00","index":1,"fulltext":"This content is not available."},{"type":"reviewerAgreed","content":"This content is not available.","date":"2024-02-09T17:50:57+00:00","index":1,"fulltext":"This content is not available."},{"type":"reviewersInvited","content":"","date":"2024-02-05T13:17:40+00:00","index":"","fulltext":""},{"type":"checksComplete","content":"","date":"2024-02-05T11:25:27+00:00","index":"","fulltext":""},{"type":"submitted","content":"International Journal of Obesity","date":"2024-02-02T09:49:07+00:00","index":"","fulltext":""},{"type":"editorAssigned","content":"","date":"2024-02-02T09:49:07+00:00","index":"","fulltext":""}],"status":"published","journal":{"display":true,"email":"[email protected]","identity":"international-journal-of-obesity","isNatureJournal":false,"hasQc":false,"allowDirectSubmit":false,"externalIdentity":"ijo","sideBox":"Learn more about [International Journal of Obesity](http://www.nature.com/ijo/)","snPcode":"41366","submissionUrl":"https://mts-ijo.nature.com/cgi-bin/main.plex","title":"International Journal of Obesity","twitterHandle":"@intjobesity","acdcEnabled":true,"dfaEnabled":true,"editorialSystem":"ejp","reportingPortfolio":"Nature AJ","inReviewEnabled":true,"inReviewRevisionsEnabled":false}}],"origin":"","ownerIdentity":"563b8425-5046-40f0-905a-e7edd126d54b","owner":[],"postedDate":"February 7th, 2024","published":true,"recentEditorialEvents":[],"rejectedJournal":[],"revision":"","amendment":"","status":"published-in-journal","subjectAreas":[{"id":28575975,"name":"Health sciences/Signs and symptoms/Digestive signs and symptoms"},{"id":28575976,"name":"Biological sciences/Physiology/Metabolism/Feeding behaviour"}],"tags":[],"updatedAt":"2024-11-10T08:06:31+00:00","versionOfRecord":{"articleIdentity":"rs-3920388","link":"https://doi.org/10.1038/s41366-024-01675-4","journal":{"identity":"international-journal-of-obesity","isVorOnly":false,"title":"International Journal of Obesity"},"publishedOn":"2024-11-09 05:00:00","publishedOnDateReadable":"November 9th, 2024"},"versionCreatedAt":"2024-02-07 19:41:59","video":"","vorDoi":"10.1038/s41366-024-01675-4","vorDoiUrl":"https://doi.org/10.1038/s41366-024-01675-4","workflowStages":[]},"version":"v1","identity":"rs-3920388","journalConfig":"researchsquare"},"__N_SSP":true},"page":"/article/[identity]/[[...version]]","query":{"redirect":"/article/rs-3920388","identity":"rs-3920388","version":["v1"]},"buildId":"qtupq5eGEP_6zYnWcrvyt","isFallback":false,"isExperimentalCompile":false,"dynamicIds":[84888],"gssp":true,"scriptLoader":[]}