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Emerging travel group named sabre hospitality’s distribution partner.

UAE-based online travel company Emerging Travel Group has formed a distribution partnership with hotel technology provider Sabre Hospitality.

The collaboration will integrate Emerging Travel Group's platforms with Sabre's SynXis technology platform.

This is expected to result in increased revenue opportunities and streamlined distribution processes for hoteliers.

The alliance will enable hoteliers to benefit from Emerging Travel Group's distribution channels and global exposure.

This includes access to RateHawk, a business-to-business (B2B) platform that connects more than 80,000 travel professionals, retail travel agents, and API partners across 120 markets.

RateHawk also offers RateHawk Premier, a concierge service tailored for high-net-worth travellers.

Hotel partners connecting to Emerging Travel Group via SynXis will gain the ability to manage their inventory, availability, rates, and promotions from one distribution point.

Emerging Travel Group direct supply head Simone Large said: “Emerging Travel Group has a comprehensive list of integrations, however, adding SynXis is pivotal in the development of our direct supply strategy and will help us increase our global coverage.

“By integrating with SynXis, we will be better positioned to increase our portfolio with diverse high-quality properties of hotel chains, which are particularly sought after by our retail customers while enabling hoteliers to expand their visibility among this high-valued segment.”

In addition to RateHawk, Emerging Travel Group also operates the ZenHotels and Roundtrip brands.

With more than 3,000 employees, has a presence in more than 80 countries.

It has offices in cities including Dubai, Wilmington, Singapore, London, Berlin, Lisbon, Warsaw, and Limassol.

Last month, Wyndham Hotels & Resorts extended its agreement with Sabre Hospitality, reaffirming the latter as its exclusive global central reservation system provider.

"Emerging Travel Group named Sabre Hospitality’s distribution partner" was originally created and published by Hotel Management Network , a GlobalData owned brand.

The information on this site has been included in good faith for general informational purposes only. It is not intended to amount to advice on which you should rely, and we give no representation, warranty or guarantee, whether express or implied as to its accuracy or completeness. You must obtain professional or specialist advice before taking, or refraining from, any action on the basis of the content on our site.

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• Emerging role of environmental pollutants in inflammatory bowel disease risk, outcomes and underlying mechanisms
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• http://orcid.org/0000-0001-7171-0139 Maria Manuela Estevinho 1 , 2 ,
• Vishal Midya 3 ,
• http://orcid.org/0000-0001-5058-5527 Shirley Cohen-Mekelburg 4 , 5 ,
• http://orcid.org/0000-0002-6880-5759 Kristine Højgaard Allin 6 , 7 ,
• http://orcid.org/0000-0002-2337-2902 Mathurin Fumery 8 ,
• Salome Pinho 9 , 10 , 11 ,
• http://orcid.org/0000-0001-6472-249X Jean-Frederic Colombel 12 ,
• http://orcid.org/0000-0003-4729-1485 Manasi Agrawal 6 , 12
• 1 Department of Gastroenterology , Unidade Local de Saúde Gaia Espinho , Vila Nova de Gaia , Portugal
• 2 Department of Biomedicine, Unit of Pharmacology and Therapeutics , Faculty of Medicine, University of Porto , Porto , Portugal
• 3 Department of Environmental Medicine and Climate Science , Icahn School of Medicine at Mount Sinai , New York , New York , USA
• 4 Division of Gastroenterology and Hepatology , University of Michigan Medicine , Ann Arbor , Michigan , USA
• 5 VA Center for Clinical Management Research , VA Ann Arbor Health Care System , Ann Arbor , Michigan , USA
• 6 Center for Molecular Prediction of Inflammatory Bowel Disease (PREDICT), Department of Clinical Medicine , Aalborg University , Copenhagen , Denmark
• 7 Department of Gastroenterology and Hepatology , Aalborg University Hospital , Aalborg , Denmark
• 8 Department of Gastroenterology , CHU Amiens and PériTox, UMR-I 01 INERIS, Picardie Jules Verne University , Amiens , France
• 9 i3S, Institute for Research and Innovation in Health , Porto , Portugal
• 10 ICBAS-School of Medicine and Biomedical Sciences , Porto , Portugal
• 11 Faculty of Medicine, University of Porto , Porto , Portugal
• 12 The Dr. Henry D. Janowitz Division of Gastroenterology , Icahn School of Medicine at Mount Sinai , New York , New York , USA
• Correspondence to Dr Manasi Agrawal, The Dr. Henry D. Janowitz Division of Gastroenterology, Icahn School of Medicine at Mount Sinai, New York, New York, USA; manasi.agrawal{at}mountsinai.org

Epidemiological and translational data increasingly implicate environmental pollutants in inflammatory bowel disease (IBD). Indeed, the global incidence of IBD has been rising, particularly in developing countries, in parallel with the increased use of chemicals and synthetic materials in daily life and escalating pollution levels. Recent nationwide and ecological studies have reported associations between agricultural pesticides and IBD, particularly Crohn’s disease. Exposure to other chemical categories has also been linked with an increased risk of IBD. To synthesise available data and identify knowledge gaps, we conducted a systematic review of human studies that reported on the impact of environmental pollutants on IBD risk and outcomes. Furthermore, we summarised in vitro data and animal studies investigating mechanisms underlying these associations. The 32 included human studies corroborate that heavy and transition metals, except zinc, air pollutants, per- and polyfluorinated substances, and pesticides are associated with an increased risk of IBD, with exposure to air pollutants being associated with disease-related adverse outcomes as well. The narrative review of preclinical studies suggests several overlapping mechanisms underlying these associations, including increased intestinal permeability, systemic inflammation and dysbiosis. A consolidated understanding of the impact of environmental exposures on IBD risk and outcomes is key to the identification of potentially modifiable risk factors and to inform strategies towards prediction, prevention and mitigation of IBD.

• CROHN'S DISEASE
• ULCERATIVE COLITIS
• EPIDEMIOLOGY
• INFLAMMATION
• INTESTINAL MICROBIOLOGY

https://doi.org/10.1136/gutjnl-2024-332523

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Introduction

Inflammatory bowel disease (IBD), encompassing Crohn’s disease (CD) and ulcerative colitis (UC), is a chronic immune-mediated disease primarily involving the gastrointestinal tract. IBD was first reported in Western countries in the late 18th to mid-19th centuries, coinciding with the Industrial Revolution and a major ecologic shift towards the modern environment. A similar pattern has been observed in developing and recently developed countries in Asia and Africa, where IBD has increased in incidence following modernisation and urbanisation in the 1990s–2000s. 1 Globally, the estimated number of IBD cases increased from 3.3 million in 1990 to 4.9 million in 2019, a rise of 47.5%, 2 accounting for over $25 billion in annual direct healthcare costs in the USA. 3 Therefore, IBD is a global public health concern. 2 While both genetic and non-genetic risk determinants are implicated, the aetiology of IBD remains inadequately elucidated, a roadblock to IBD prediction and prevention efforts. Genome-wide association studies have identified over 200 loci associated with IBD, but less than a third of cases are attributed to genetics alone, further supporting the role of the environment in IBD onset and outcomes. 4 Uncovering how environmental factors influence IBD onset and disease course could ultimately inform strategies towards mitigation of risk and disease progression. 5 The imperative to delve into this topic is heightened considering the increasing levels of global pollution and environmental contaminants (eg, air pollutants and industrial chemicals) over the last decades, resulting from unregulated modernisation and industrialisation. 6 It is also relevant to acknowledge that changes in exposure patterns are associated with climate change and widening health disparities, pertinent concerns in the current era. In this systematic review, we summarise the available human studies on the impact of environmental pollutants on IBD risk and outcomes. Additionally, we compile available in vitro and animal studies data on underlying mechanisms and identify knowledge gaps.

Systematic review

We conducted this systematic review after registration in the International Prospective Register of Systematic Reviews (PROSPERO, registration number: CRD42024524629), following the Preferred Reporting Items for Systematic Reviews guidance for data extraction and reporting. 7 Our research question was formulated using the ‘Population, Intervention, Comparison and Outcome’ (PICO) 8 methodology. The population of interest was healthy individuals at risk of developing IBD (prospective cohorts) or individuals with IBD (retrospective cohorts, genome-wide association studies or studies evaluating the impact of exposure on disease outcomes); the intervention or exposure of interest, was specific environmental pollutants; the comparator was individuals without IBD diagnosis/outcomes; and the endpoints were the development of IBD or IBD-related outcomes.

Literature search

Three online databases (MEDLINE, Web of Science and Scopus) were searched for studies addressing the PICO. The query used for PubMed was pollutants or pesticides or particulate matter (PM) or heavy metals or per- and polyfluoroalkyl substances (PFAS) or PM 2.5 or PM 10 AND inflammatory bowel disease or Crohn’s disease or ulcerative colitis or intestinal inflammation. The search included studies published in databases whose inception dates up to 29 April 2024. In addition, the references of articles identified as being relevant were reviewed for further published data matching the PICO question. Screening and selection of studies were done by two authors (MME and MA) using Rayyan, and discrepancies were resolved by a third arbitrator (VM).

Inclusion and exclusion criteria

Original research studies were included if they evaluated the impact of specific environmental pollutants, either in utero or throughout life, on healthy individuals at risk of developing IBD or on patients diagnosed with IBD, across all ages, in both urban and rural areas of developed and developing regions. Studies not meeting the inclusion criteria, as well as those focussing solely on diet or other exposures, reviews, case reports, guidelines or editorials, were excluded. No restrictions were imposed based on language. We excluded studies on exposure to plastics in this review due to the unique physical and chemical properties of these pollutants, challenges associated with their measurement and the limited available human data on plastic exposure and IBD at present.

Data extraction and quality assessment

The following information was extracted from the studies: citation details, characteristics of the study population, follow-up duration, details on the exposure, tools used to assess exposure (eg, biomarkers, surveys), study outcomes (incidence/prevalence of IBD, disease characteristics or outcomes), studied confounders and assessment of exposure-response (if available). The reporting quality of the studies was evaluated independently by two reviewers (MME and MA) using the Strengthening the Reporting of Observational Studies in Epidemiology (STROBE) criteria, 9 considering 22 parameters for cohort and case-control studies. For ecological studies and genome-wide association studies, only the criteria relevant to those specific designs were evaluated.

Narrative review

We summarised data on the impact of pollutants on intestinal inflammation, relevant to IBD, from in vitro and animal model studies using a narrative approach. The studies included in the narrative review were gathered through a non-systematic search on PubMed. The search query used was ‘pollutants or pesticides or particulate matter (PM) or heavy metals or PFAS or PM 2.5 or PM 10 AND ((in vitro) or (in vivo)) and (intestinal inflammation)’. References from clinical studies included in our systematic review and prior review papers on the subject were also considered.

Categories of pollutants: characteristics, sources and distribution

A pollutant is any chemical substance that appears in an organism or the environment at levels exceeding permissible limits. 10 These compounds are typically known for their widespread distribution, and, along with their byproducts, they can persist in and interact with the environment for extended periods. Pollutants can be categorised based on different parameters, for example, sources, physical and chemical properties and impact on environmental and human health. 10 Considering the source, pollutants may be classified into (1) water pollutants (eg, chemicals, microbial contaminants, algal toxins, pharmaceuticals and personal care products); (2) air pollutants (eg, industrial and agricultural emissions, vehicle exhaust and smoking); (3) soil pollutants (eg, -cidal agents, heavy metals and industrial byproducts) and (4) others (comprising light, noise, radioactive, thermal and microbial pollutants). 11 Pollutants can also be grouped based on chemical composition (inorganic vs organic), boiling point (volatile or non-volatile) and ability to undergo biomagnification through the food chain based on their fat solubility. 11 Highly persistent organic pollutants include PFAS, pesticides and polycyclic aromatic hydrocarbons (PAH), the former representing a highly persistent group of thousands of fluorinated compounds, ‘forever chemicals’, that are used extensively in industries, in household and personal items, food and packaging. 12 In this review, based on a composite 13 of the above features as well as available data, chemical pollutants were classified into the following subtypes: (1) heavy and transition metals; (2) air pollutants, including PM (fine inhalable particles 14 subdivided according to their sizes in PM 2.5 , PM 2.5–10 and PM 10 13 ), gaseous molecules (nitrogen oxides—NO x , sulphur dioxide—SO 2 , carbon monoxide—CO and ozone—O 3 ), volatile organic compounds and greenhouse gases (carbon dioxide—CO 2 , methane—CH 4 , nitrous oxide—N 2 O and fluorinated gases); (3) industrial compounds and organic pollutants (including PFAS, PAH, solvents and flame retardants); (4) -cidal agents (pesticides, herbicides and insecticides).

Summary of literature search

The systematic search yielded 3743 results. Of these, 583 duplicates were excluded, and 3128 records were eliminated based on inclusion and exclusion criteria ( figure 1 ). We included 32 studies in the final qualitative systematic review. Study characteristics and main results are presented in online supplemental table 1 . Of these, 12 were case-control studies, 12 14–24 seven were retrospective cohort analyses, 25–31 four were ecological analyses, 32–35 four were cross-sectional, 36–39 three were prospective cohort studies, 40–42 and two were genome-wide association studies. 43 44 These studies pertained to the following categories of specific pollutants: heavy metals or transition metals (n=5), 14–16 31 40 air pollutants (n=16), 17–21 25–27 32–34 36 39 41 43 44 industrial compounds and organic pollutants (n=10) 12 22–24 28–30 35 37 38 or pesticides (n=1). 42 . 25 studies reported on CD and UC risk, while five reported on UC alone 15 17 29 36 44 and one on CD 32 alone; the paediatric population was the focus of one study. 27 . Six studies analysed the impact of pollutants on disease course. 25 32 34 36 39 41 Online supplemental table 2 summarises the STROBE assessment for all studies.

Supplemental material

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Preferred Reporting Items for Systematic Reviews and Meta-Analyses flowchart of studies’ selection.

Impact of pollutants on IBD risk

In this section, we summarise the results of the human studies focussing on the impact (harmful, null or protective) of specific pollutants on IBD risk ( figure 2 ).

Summary of the main findings in each pollutant category. As, arsenic; CO, carbon monoxide; Cu, copper; CD, Crohn’s disease; IBD, inflammatory bowel disease; Fe, iron; Pb, lead; Hg, mercury; NO 2 , nitrogen dioxide; NO x , nitrogen oxides; OC, organochlorine; OP, organophosphate; Ox, oxidants, O3, ozone; PM, particulate matter; PFAS, per- and poly-fluoroalkyl substances; PAH, polycyclic aromatic hydrocarbons; Se, selenium; SO 2 , sulphur dioxide; UC, ulcerative colitis; Zn, zinc.

Heavy metals or transition metals

It is important to acknowledge that while some metals are essential as nutrients (cobalt (Co), copper (Cu), chromium (Cr), iron (Fe), magnesium (Mg), manganese (Mn), molybdenum (Mo), nickel (Ni), selenium (Se) and zinc (Zn)), others (arsenic (As), cadmium (Cd), chromium (Cr), lead (Pb) and mercury (Hg)) are considered systemic toxicants and human carcinogens. Additionally, all metals can be toxic at some level, depending on several factors, including the dose, route of exposure, chemical species and characteristics of the exposed individuals.

Five studies investigated the impact of metal exposure on IBD risk. The methods used to assess exposure were variable: two studies evaluated the quality of water consumed by the study population (at the region 40 and district level, 31 at or shortly after diagnosis), while others measured metals in colon biopsies, deciduous teeth 16 and hair samples. 14 Notably, only the last two matrices allowed for measuring metals at a high temporal resolution, with the analysis of tooth dentine being the only one that generates temporal profiles of uptake during foetal growth. 45 The study on teeth 16 evaluated exposures from the second trimester of pregnancy until 6 months after birth, while the hair 14 analyses using 3–4 cm of hair proximal to the scalp allowed for the assessment of exposure in adulthood, reflecting exposure up to 4 months before sampling. In all studies, individuals who developed IBD had higher concentrations of metals than healthy controls. An association between measured heavy metals and IBD was reported in three studies. 15 31 40 The specific profile of heavy metals varied across studies; Pb, Cu 15 16 and Fe 15 31 were associated with IBD risk in more than one study. Conversely, three studies 14 15 40 reported higher levels of Zn in individuals without IBD relative to those with IBD. The reporting quality of the studies was moderate-high for all studies, apart from one online supplemental table 2 ), 15 which provided a less detailed description of the recruitment process and did not address bias or confounders. Also, most did not provide information regarding sample size calculation due to the exploratory nature of these studies.

Air pollutants

The impact of air pollution on the risk of IBD was estimated in 10 studies 17–21 26 27 33 43 44 , of which two studies 17 44 focused on UC outcomes. The methodology for exposure assessment was variable: four used land use regression modelling, 19 20 43 44 , two used surveys 18 32 and the remaining used geographic information systems (GIS) and satellite monitoring data. Four studies 17 19 43 44 reported that higher levels of PM 2.5 were associated with UC risk, and one study 26 reported an association with IBD overall. When limiting the analysis to paediatric-onset IBD, there was no impact of PM 2.5 exposure. 27 Conversely, in a nested case-control study 20 with a smaller sample size, the opposite association was reported, with lower levels of PM 2.5 in individuals with IBD compared with those without IBD (adjusted OR of 0.24 (95% CI 0.07 to 0.81) per 5 lg/m 3 ). One study 19 reported a positive association between PM 2.5–10 and PM 10 and the risk of UC in a dose-dependent manner. On the other hand, another study reported null findings. 44

With respect to other air pollutants, based on GIS data, nitrogen oxides were reported to be significantly associated with the risk of UC in one study 19 and CD in another. 21 In another GIS-based analysis of air pollutants, oxidant levels during pregnancy and childhood were recognised as risk factors for paediatric-onset IBD, but null associations were reported for exposure to other gases. 27 Regarding reporting quality, 4 of the 15 studies did not provide detailed information on recruitment criteria, patients’ selection, data collection and analysis or management of confounders and sources of bias. 17 25 33 39

Industrial compounds and organic pollutants

We identified 10 relevant studies in this subgroup, of which seven studied the impact of exposure to PFAS on IBD. 12 22 23 28–30 38 In a nested case-control analysis 12 of military recruits, higher concentrations of the PFAS mixture (consisting of nine PFAS chemicals) up to 10 years before IBD diagnosis were associated with an increased risk of both CD and UC in a dose-dependent manner. In other studies focussing on specific legacy, PFAS identified associations between individual PFAS chemicals (perfluorooctanoic acid (PFOA) 23 28–30 and perfluorooctane sulfonate (PFOS) 23 ) and the risk of UC, with a dose–response relationship reported in two of them. 28 30 Conversely, in another report from the Nurses’ Health Study, inverse associations were identified between the levels of three legacy PFAS (PFOA, PFOS and perfluorodecanoic acid (PFDA)) and the risk of CD, while no association was found for UC. 22 Of note, the median PFAS level in this cohort was lower than the national average. Two 35 38 other analyses reported null associations between PFAS and IBD based on zip code-level exposure data.

Regarding other industrial contaminants, one case-control study 24 identified a higher risk of UC in men exposed to silica dust in a time-dependent manner, while the risk of CD was higher in exposed women. Exposure to electronic waste (discarded electronic devices and equipment) enriched with polycyclic aromatic hydrocarbon compounds has been associated with systemic inflammatory changes in children (increased absolute lymphocyte and monocyte counts, lower serum levels of CD4 + T cells, increased B cells and sialyl Lewis A concentrations), although their impact on IBD as an outcome is not known. 37 The reporting quality of the studies addressing industrial and organic contaminants was adequate.

One study 42 prospectively determined exposure to specific pesticides among agricultural workers and families using questionnaires. Exposure to organochlorine (OC) and organophosphate (OP) insecticides was associated with elevated hazards of IBD, particularly dieldrin (adjusted HR (aHR) 1.59, 95% CI 1.03 to 2.44), toxaphene (aHR 1.56, 95% CI 1.05 to 2.32) and terbufos (aHR 1.53, 95% CI 1.19 to 1.96), without a clear exposure-response trend. The reporting quality was adequate.

Impact of pollutants on IBD-related outcomes

Data on the impact of specific pollutants on IBD-related outcomes is more limited. Six studies examined the impact of air pollutants on disease course (both CD and UC: n=4, 25 34 39 41 CD: n=1, 32 UC: n=1 36 ). The studies that assessed IBD exacerbations based on hospitalisation 25 34 39 or outpatient visits 36 found a positive association with air pollutant emissions. A dose–response association was reported between total air pollutants and IBD-related hospitalisations 35 and between daily outpatient visits for UC and PM 2.5 concentrations. 36 Exposure to PM 2.5 and NO x was associated with an increased risk of enterectomy or all-cause mortality in a prospective analysis of over 4700 individuals with IBD. 41 In this study, a concentration–response relationship was observed; patients exposed to each IQR increase in pollutants such as PM 2.5 , NO x , NO 2 and PM 10 experienced a 10%–16% higher risk of enterotomy and all-cause mortality. An ecological study 32 reported a higher CD-related mortality rate in zip codes with higher exposure to SO 2 ; however, no association was found for PM 2.5 . CO was also reported to increase the risk of hospitalisations, particularly due to UC. 25 39 On the other hand, the role of O 3 is not clear. 25 39

Association between pollutants and gut inflammation: data from in vitro and animal studies

Here, we summarise available data on mechanisms underlying the impact of different exposures on gut inflammation, based on in vitro data and animal studies ( figure 3 ).

Proposed underlying mechanisms mediating IBD risk with exposure to environmental pollutants: a summary of in vitro data and in vivo animal studies. Al, aluminium; Ag, silver; As, arsenic; Cd, cadmium; Cr, chromium; Cu, copper; IL, interleukin; Pb, lead; MPO, myeloperoxidase; Ni, nickel; PM, particulate matter; PFAS, per- and polyfluoroalkyl substances; PFOS, perfluorooctane sulfonate; PFOA, perfluorooctanoic acid; PI3K-PKB/Akt, phosphoinositide-3-kinase-protein kinase B/Akt; ROS, reactive oxygen species; SCFA, short-chain fatty acids; TNF, tumour necrosis factor.

Exposure to different metals (Al, 46 Cd, 47 Ni, 48 Ag, 49 Hg, 50 Pb, 51 Cr 52 and As 53 ) was shown to induce a proinflammatory phenotype in intestinal epithelial cells (increased expression of interleukin (IL)-1β, 53 54 IL-17α, 53 IL-8, 53 tumour necrosis factor(TNF)-α, 47 54 IL-6, 54 IL-4, 54 IL-10 49 and IL-18 49 ). Also, exposure to metals like Al and Cd has been shown to impact cell death and renewal, increase gut permeability and exacerbate experimental colitis in mice. 55 56 Other mechanisms have also been proposed, including reduced gut microbiota diversity, altered composition (eg, decreased abundance of Akkermansia with chronic exposure to Al, Cd, Cr, Cu and Pb 52 ) and changes in metabolic function that may, in turn, affect the host’s immune and metabolic responses. 51 In addition, exposure to Pb, Cu and Fe, for instance, may also directly induce inflammatory responses and cause oxidative stress. 51 57 A recent exploratory pilot analysis examined the complex connection among metals, microbiome and intestinal inflammation. This analysis revealed that exposure to certain metals during pregnancy, combined with specific bacterial types during childhood (termed metal-microbial cliques), correlated with elevated faecal calprotectin levels, a marker of subclinical inflammation. 58 Conversely, Zn seems to have a protective role, improving the antioxidant and immune capacities and reducing apoptosis of intestinal epithelial cells in animal models. 59 Recent reports suggest that exposure to Pb may secondarily induce changes in Cu, Fe and Zn levels, 60 broadening further the complexity and relevance of metal exposure.

PM, specifically PM 2.5 which has the highest penetration ability, is the most studied air pollutant. In mouse models, exposure to PM 2.5 alters circulating cytokine levels (decrease in Th17, 61 increase in TNF-α, 61 IL-1β 62 and IL-6 62 ). Also, PM 2.5 is reported to impact the gut microbiome in several animal models, decreasing bacterial diversity and changing the firmicutes/bacteroidetes ratio 63 and microbial metabolic pathways. 62 PM 2.5 also promotes oxidant-dependent activation of the nuclear factor kappa B (NF-κB) pathway, with downstream disruption of tight junctions, and increases the permeability of human Caco-2 cell monolayers. 63 However, two-dimensional models, like Caco-2 cells, may not accurately reflect the characteristics of native cells, particularly regarding the expression of receptors and transporters. Using a three-dimensional model that incorporates stromal cells and extracellular matrix, Woodby et al 64 have shown that chronic exposure to PM affects gut redox homeostasis and decreases the levels of cell–cell adhesion proteins (zonula occludens protein-1 and claudin-1). Moreover, other reports have demonstrated that PM can accelerate chemically induced colonic tumour formation in murine models, a process that relies on the phosphoinositide 3-kinase (PI3K)/AKT pathway. 65 This finding may be relevant considering the increased risk of colorectal cancer in patients with IBD with active inflammation. Finally, PM 10 was demonstrated to interfere with calcium signalling, absorption and digestion pathways, exacerbating pre-existing intestinal inflammation in an organoid model. 66

Industrial compounds, byproducts and organic pollutants

In mice studies, exposure to PFAS was associated with a decrease in firmicutes/bacteroidetes ratio, a decrease in Clostridiales, Enterobacteriale and Lactobacillales and a loss of gut barrier integrity due to a reduction in short-chain fatty acid production and intestinal tight junction proteins (zonula occludens-1, occludin and claudin-1). 67 Others have demonstrated increased expression of proinflammatory cytokines (particularly IL-6, TNF-α and IL-1β) and the expansion of systemic CD4 + T cells with PFOS. 68 This compound was also reported to increase neutrophil recruitment to the intestine of zebrafish larvae, which was later validated in 2,4,6-trinitrobenzene sulfonic acid (TNBS)-induced colitis in mice. 68 Studies conducted on bivalves using multiomics analyses suggested that the peroxisome proliferator-activated receptor-mediated lipid metabolism (Toll-like receptors/myeloid differentiation primary response 88/NF-kB and PI3K-Akt-mTOR) and the autophagy pathways likely mediate PFOA-associated immunotoxicity. 69 These pathways coordinate cellular responses to environmental stimuli, cell growth and proliferation, and immune regulation. 69

Furthermore, evidence from human metabolomics suggests that PFAS exposure impacts important cellular metabolic pathways, including lipid, amino acid, carbohydrate/glycans, nucleotide, energy metabolism and glycan biosynthesis, which may suggest the effects of PFAS exposure on cellular energy and membrane disruption that can be potentially associated with pathological processes. 70 Also, levels of PFOS and PFOA in human serum samples are associated with altered IgG glycosylation in both children and adults. 71 Several glycosylation abnormalities have been described in IBD as, for example, defects in N-glycan branching of mucosal T cells from UC, leading to T-cell hyperactivation and increased disease severity. 72 More recently, in a pilot analysis of the PFAS mixture in dried blood spots from neonates, an estimate of prenatal exposure, PFAS levels were associated with faecal calprotectin at 3 years of age, particularly in the offspring of women with IBD. 73

Data regarding the mechanistic effects of other contaminants such as benzo[a]pyrene, 74 polychlorinated biphenyls, ammonia 75 and triclocarban 76 are few. However, in line with PFAS data, exposure to these chemicals increases the expression of IL-6, TNF-α and IL-1β and leads to altered intestinal permeability.

Recent preclinical evidence supports the impact of diverse pesticides on the intestinal mucosa. Phosalone 77 and chlorpyrifos, 78 OP pesticides, were reported to increase oxidative stress, TNF-α, IL-1β and IL-6 levels and to decrease intestinal permeability in mice. Similarly, exposure to avermectin and pyrethroid pesticides (fenpropathrin and deltamethrin) was found to increase oxidative stress and inflammation and to compromise the integrity of the intestinal barrier in carp 79 and mice. 80 Recently, a study used an innovative approach combining publicly available databases, zebrafish chemical screens, machine learning and mouse preclinical models to test for the effects of over 200 chemicals on intestinal inflammation. 81 Of the 20 top candidate chemicals to induce intestinal inflammation, 11 were -cidal agents; two herbicides (flumetralin and propyzamide) and two pesticides (azinphos-methyl and phorate) boosted TNBS-induced intestinal inflammation in zebrafish. Propyzamide was also found to induce colon shortening and intestinal inflammation (promoting T H 1 and T H 17 cell differentiation and increased expression of IL-17+ T cells) in mice. 81

We systematically summarised 32 human studies on environmental pollutants relevant to IBD risk and outcomes. Overall, these studies support an association between heavy and transition metals, air pollutants, industrial contaminants, insecticides and an increased risk of IBD. In contrast, Zn exposure may be protective against IBD. Limited data suggests that IBD outcomes, such as hospitalisations, are more prevalent with increased exposure to air contaminants. Studies with comparable study designs will be important to clarify, as well as quantify, the impact of pollutants on IBD. Based on animal models and in vitro data, most of these pollutants promote intestinal inflammation through changes in the gut microbiome, loss of intestinal barrier function and systemic inflammation. Globally, the reporting quality of the studies was adequate.

Heavy and transition metals play vital roles in biological processes, including as enzyme cofactors and electron transporters. Thus, any dyshomeostasis in these metals can disrupt metabolic and physiological functions. Both case-control 14–16 and cohort 31 40 studies demonstrated associations between metals and IBD, with individuals exposed to elevated concentrations of Mn, Hg, As, Pb and Fe at a greater risk of IBD. These findings are supported by evidence from a pilot study on deciduous teeth and an exploratory analysis of healthy children, the latter reporting an interaction between prenatal metal exposure and microbiome signatures towards downstream intestinal inflammation. 58 In line with this, preclinical studies have shown both direct and microbiome-related effects of metals on the microbial metabolic profile, intestinal permeability, cytokine milieu and systemic immune dysregulation. 82 In contrast, Zn appears to decrease the risk of IBD. 15 This has biological plausibility considering Zn’s anti-inflammatory and antioxidant effects in animal studies. 59 Furthermore, this is corroborated by two large prospective cohort studies in which an inverse relationship between dietary Zn intake and the risk of CD was detected. Yet, no such association was observed for UC. 83

With respect to air pollutants, which may be inhaled or ingested, five of the seven reports 19 37 41 42 that investigated the effect of PM 2.5 19 37 41 42 reported a harmful association with IBD, particularly with UC. 43 44 This association is supported by the proinflammatory effects of PM 2.5 in the intestinal tract in in vitro and animal studies. The association of PM 2.5 with UC but not with CD, highlighted in some studies, may be related to perturbation of colonic microbiota composition by air pollutants and warrants further study. Other air pollutants, such as total oxidant agents, 27 NO 21 and SO 2 , 21 may be particularly relevant in early life. 84 Indirect data also supports this framework. In a population-based cohort study, early-life exposure to agricultural land use was associated with increased CD risk, while exposure to greenspace and biodiversity was protective. 85 These exposures may modulate NO and SO 2 levels, mainly from vegetable crops, fertilisers or livestock. Certainly, exposures during the early life period, which extends from the prenatal period to early childhood, are critical to microbiome establishment, immune maturation and the risk of IBD later in life. 85–88 Exposures in adulthood may be relevant to older-onset IBD. 89 Studies exploring the effects of pollutants at different stages of life are likely to be relevant, particularly towards honing prediction and prevention strategies. The impact of air pollutants on adverse IBD outcomes such as hospitalisation, 25 34 39 surgery 41 and mortality 32 are consistent with those pertaining to other immune-mediated diseases, such as rheumatoid arthritis 90 and emphasise the importance of mitigation strategies.

The importance of industrial contaminants has increased, not only because their sources are proliferating but also because some have long-lasting persistence, rising over time. 12 Among these, the most relevant are PFAS, a family of over 8000 synthetic chemicals widespread in the environment. The adverse effects of PFOS and PFOA on gut homeostasis are consistently reported in animal and in vitro studies, as well as in recent analyses of human serum samples and neonatal dried blood spots. This knowledge and the PFAS association with a broad range of conditions, 91 including cancer and immunotoxicity, have been recognised by European and American agencies and authorities. 91 However, not all epidemiological studies reported an association between PFAS levels and IBD risk. This highlights the importance of studying PFAS (and other pollutants) in totality, such as a mixture, rather than measuring individual compounds, such as legacy PFAS. 12 Furthermore, delineating the impact of PFAS on gut mucosal integrity and permeability by assessing its effects on mucosal glycocalyx composition and microbiota functions is relevant. This approach can provide insights into the underlying causes of the transition from health to inflammation associated with the onset of IBD.

With respect to pesticides, their detrimental impact on intestinal mucosa has been reported in numerous in vitro and animal studies. However, only one clinical study explored the role of pesticides in modulating the risk of IBD. Although this prospective study found a positive association with OC and OP insecticides, the exposure was measured using questionnaires, making it subjective and prone to recall bias. 42 While more objective exposure assessments are needed, two recent population-based studies 85 92 indirectly support the role of pesticides as risk factors. The first, from the Danish population, identified that early life exposure to agricultural land use was linked to a higher risk of CD. 85 The second, which evaluated French farmers, identified some agricultural activities in which pesticides are commonly applied, like fruit arboriculture and crop farming, to be more strongly associated with IBD risk. 92

While reporting important findings for specific pollutants, this review also highlights knowledge gaps ( figure 4 ). Regarding metals, these include the limited number of human studies with relatively small sample sizes and the absence of individual-level and long-term assessments of exposures in many cases. Further, there are few tools available to establish concentration–effect relationships. Future work is also needed to understand the interactive effects of multiple metals or metal mixtures and to unravel the dysregulation in foetal metal biodynamics (eg, altered rhythmicity, a biomarker of metal homeostasis and a concept different from exposure). 93 The complex relationship between metals and the gut microbiome is also just beginning to be understood. Even though the existing evidence for air pollutants is robust, there is a need for more comprehensive exposure assessments, accounting for the dynamics introduced by environmental policies and understanding how exogenous exposure to air pollutants exacerbates the effect of endogenous pollutants like pesticides and PFAS. Concerning industrial products, although several clinical studies address PFAS, using advanced laboratory techniques and statistical models is crucial to detecting meaningful immunological effects and conducting valid risk assessments. Regarding in vitro and in vivo animal studies, little evidence exists for other PFAS compounds other than PFOS and PFOA. The impact of relevant industrial contaminants like hydrogen sulphide, triclocarban, ammonia and flame retardants on gut inflammation remains to be explored. Regarding -cidal agents, it remains difficult to evaluate past and time-varying exposures, dose-effect measures, and the role of unexplored vectors such as soil. There is a paucity of data for other agents, such as pharmaceutical products and endocrine disruptors.

Main findings of the review.IBD, inflammatory bowel disease; PFAS, per- and polyfluoroalkyl substances.

Overall, the measurement of exposure biomarkers with high temporal resolution, particularly in preclinical biological samples and the application of advanced measurement techniques and composite data analysis are needed to clearly delineate the impact of environmental pollutants on IBD. This approach may also provide insights into the role of different environmental insults in different stages of life and clarify whether the timing of exposure may be more critical than the duration. Mechanistic data using IBD models, rather than extrapolation from other models, will provide granular insights into IBD pathogenesis. Finally, it is important to note that variables beyond environmental pollutants, such as genetic, epigenetic and dietary factors, are likely to modulate IBD risk and outcomes via direct and interaction effects, highlighting the complexity of IBD pathogenesis. For example, the effect of smoking on health outcomes is modulated by genetic variants that influence its metabolism. 94 95 Future multiomic analyses will uncover gene–pollutant interactions in the context of IBD.

Finally, it is key to advance and upscale the field of bioremediation, identifying microorganisms, enzymes and inert compounds that may help eliminate or, at least, neutralise pollutants. These transdisciplinary approaches will provide evidence towards effective prevention strategies in regulatory and clinical contexts, as well as provide a framework towards understanding environmental impacts on other immune-mediated diseases. In the meantime, based on current knowledge and in line with international recommendations, it is crucial to minimise harmful exposures through modification of production processes, use of less toxic materials, implementation of conservation techniques, reuse and upcycling. Such practices, at individual and societal levels, are likely to be relevant towards improving health outcomes overall.

Ethics statements

Patient consent for publication.

Not applicable.

Ethics approval

Acknowledgments.

The authors thank Jill Gregory, Certified Medical Illustrator, Icahn School of Medicine at Mount Sinai, New York, for the illustrations.

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X @ShirleyCoMekMD, @KristineAllin, @Matfum, @manasiagrawalmd

Contributors All authors planned and formatted the review. MME conducted the literature search and data integration. MME, VM, SC-M and MA drafted the manuscript. MME, VM, SC-M, KHA, MF, SP, J-FC and MA conducted critical revision of the manuscript for important intellectual content. MA is responsible for the overall content as guarantor.

Funding MA is supported by the National Institute of Diabetes and Digestive and Kidney Diseases (K23DK129762-02), the International Organisation for the Study of Inflammatory Bowel Disease and the Crohn’s and Colitis Foundation Litwin IBD Pioneers Award. KHA is supported by the Danish National Research Foundation (DNRF148) and the Novo Nordisk Foundation (NNF23OC0086595).

Competing interests MF reports receiving lecture/consultant fees from Abbvie, Ferring, Tillots, MSD, Biogen, Amgen, Fresenius, Hospira, Sandoz, Pfizer, Bristol Myers Squibb, Celgene, Gilead, Boehringer, Eli Lilly, Nordic-Pharma, Arena, Galapagos, Janssen and Takeda. JFC reports receiving research grants from AbbVie, Janssen Pharmaceuticals and Takeda; receiving payment for lectures from AbbVie, Amgen, Allergan, Ferring Pharmaceuticals, Shire and Takeda; receiving consulting fees from AbbVie, Amgen, Arena Pharmaceuticals, Boehringer Ingelheim, Bristol Myers Squibb, Celgene Corporation, Eli Lilly, Ferring Pharmaceuticals, Galmed Research, Glaxo Smith Kline, Geneva, Iterative Scopes, Janssen Pharmaceuticals, Kaleido Biosciences, Landos, Otsuka, Pfizer, Prometheus, Sanofi, Takeda, TiGenix and hold stock options in Intestinal Biotech Development.MA reports consulting for Douglas Pharmaceutical.

Provenance and peer review Commissioned; externally peer reviewed.

Supplemental material This content has been supplied by the author(s). It has not been vetted by BMJ Publishing Group Limited (BMJ) and may not have been peer-reviewed. Any opinions or recommendations discussed are solely those of the author(s) and are not endorsed by BMJ. BMJ disclaims all liability and responsibility arising from any reliance placed on the content. Where the content includes any translated material, BMJ does not warrant the accuracy and reliability of the translations (including but not limited to local regulations, clinical guidelines, terminology, drug names and drug dosages), and is not responsible for any error and/or omissions arising from translation and adaptation or otherwise.

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World Tour Merge・Travel Game 4+

Town adventure by merging gems, soloband games ltd, designed for ipad.

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Ellie always dreamed of more, but she lived in a provincial town with her parents and her faithful dog Max. Her days seemed monotonous, and she longed for exciting adventures. Then, on her birthday, Ellie received an unexpected gift from her parents – a ticket to her dream journey! It was a ticket to travel the world, and she could take only one companion. Without hesitation, she chose her loyal friend, Max. From that moment on, an incredible adventure began. Ellie and Max traveled through different countries, met interesting people, and explored new cultures. They strolled on the Himalayas, marveled at ancient castles in Europe, and savored exotic cuisine in Asia. The journey turned into a real dream adventure for Ellie. She realized that the world is so diverse and wonderful that she wanted to learn even more. And while it was time to return home, she knew that her adventures had only just begun. With Max by her side and new friends in different corners of the world, Ellie knew that her life would never be dull and predictable again. - Join Ellie on an exciting journey as you explore various captivating locations! - Get to know intriguing characters and uncover their hidden mysteries! - Immerse yourself in the top-notch merging game with a plethora of fascinating mechanics! - Collect awesome rewards! - Engage in thrilling activities!

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Carnival Cruise Line debuts first Solar Eclipse Cruise, opens first wave of itineraries for Summer 2026

Royal Caribbean’s Star of the Seas takes center stage to deliver ultimate family vacation

GoTürkiye appoints Hilal Demirel New York Director of the Turkish Ministry of Culture and Tourism

Carter Hospitality Group appoints Hospitality Operations Director

The Hospitality Show announces 2024 sustainability programming, initiatives

Avion Hospitality appoints Dan Peterson Senior Vice President of Operations

UK’s ICO launches new tool to generate privacy notices for the hospitality sector

The First Roma by The Pavilions Hotels & Resorts partners with Parco di Roma Golf Club to launch Ultimate Golf Getaway

Up Norway teams up with Havila Voyages for sustainable luxury land and sea journey on Norwegian Coast

How do you handle car accidents involving tourists

Qatar Airways acquires 25 per cent stake in Airlink

Aer Lingus Regional expands network from Glasgow with service to Cork

Crystal Resto appointed Director of Sales & Marketing at Hyatt Regency Grand Reserve Puerto Rico

Grand Hotel Courmayeur Mont Blanc accepted into Preferred Hotels & Resorts L.V.X. Collection

Hospitable unveils suite of new features to help self-managers professionalize and scale 

TripStax bolsters commitment to client data protection with ISO certification and SOC2 audit

CAI 2024 Conference: Madeira, the European Capital of the cruise industry

El Mangroove, Autograph Collection hosts 2nd Sustainable Gastronomic Congress

ELEVAT3 launches Sales & Marketing division

Allied Market Research: Vacational rental market to reach $279.5b. globally

Now open: Four Seasons Resort Mallorca at Formentor welcomes guests

talixo signs agreement with Flight Centre Travel Group to provide global transfers for business travel

Travelex launches new redesigned app for the Travelex Money Card, powered by Mastercard

DMC NexusTours leads the way to offer carbon-neutral transfers

Luxury projects dominate as Middle East hotel pipeline expands slightly YOY

Russian tourism to Abu Dhabi on the rise, fuelled by premium experiences

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Business travel made smooth

Build a successful business with simplified business travel. Roundtrip allows you to plan every step of a business trip simply and easily. From booking travel services at special rates to managing an itinerary, you'll be free to focus on what really matters.

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Discover how roundtrip can help your business, until teleportation is invented, organise your business travel with roundtrip, absolutely free free today, free tomorrow, free forever, travel managers.

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Finance team

As a corporate travel manager, you know how stressful business trips can be. Keeping travel records in order, last-minute changes and cancellations, and finding a suitable hotel and flight that fits within a tight budget - it can really be challenging!

We feel your pain. And we’ve built your solution. Roundtrip is here to radically simplify your travel planning. Our user-friendly tools support travel managers like you by automating travel plans and policies. Here’s how:

Select hotels fast, based on any parameters

Reduced special rates and a wide inventory mean you can find the perfect option that fits with your travel policies.

Choose to pay how you like: by invoice, credit card, payment link, or on the spot at check-in — whatever suits your company’s financial regulations best.

Add your travel policies

You can use your company’s travel policies when booking. Grant your employees specific rights for working in the system.

Create employee profiles

Employee profiles ensure that their specific details load automatically when they book, avoiding potential errors with check-in or flights.

Use settings for several legal entities

Book hotels, airline tickets, and transfers from different legal entities or affiliates with ease.

Downloadable invoices and reports

Get the documents you need anytime and in any format that you like.

Create cost centers for efficient trip allocations

Manage your bookings and expenses efficiently with our easy-to-use tools.

Get 24/7 support

We’re here for you. Speaking over 12 languages, our 24/7 support team is standing by to answer questions, check bookings, and resolve issues when they occur. Plus, a dedicated Account Manager will help you throughout your entire journey.

Empower your employees to book

Give your employees access to Roundtrip by an invitation link or through the mass upload tool. They can then book for themselves, and you can see their order history.

Roundtrip is part of the Emerging Travel Group

Emerging Travel Group (ETG) is a global leader in online travel. We have been changing the travel industry since 2010, creating one of the most high-tech systems in the world for the B2C, B2B, B2A and CTM segments.

The Emerging Travel Group’s Mission

We strive to create, distribute, and operate the most convenient travel products. We constantly innovate and break the rules of the highly complex travel industry to make travel more widely available for individuals, more rewarding for professionals, and simpler for everyone.

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User-friendly

A dedicated sales manager will show you how simple it is to use Roundtrip. They'll go the extra mile to guarantee you have the best possible experience.

Take advantage of the best rates for hotels, airlines, transfers and car rentals. We scan offers worldwide to find the most competitive prices for you.

Your Roundtrip Account Manager is committed to your success. Like having a personal friend in the travel industry, they are your one-stop-shop for all your travel questions and concerns.

Talk with actual people (not robots) when you need help. Speaking over 12 languages, our 24/7 support team is here for you.

A Business Traveler’s Guide to Maximizing an Airport Layover

Celebrating 100,000 Direct Contracts with Roundtrip

10 Best Practices for Corporate Planners to Overcome Common Travel Mishaps

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Roundtrip is part of the Emerging Travel Group, one of the world's fastest growing travel holding companies. Join us to soar above the stars!

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