Impact of night-shift work on the prevalence of erosive esophagitis in shipyard male workers

After the industrial revolutions, the concept of shift work emerged, and the type of work was divided into day and night shifts. In a recent population survey, 18 % of the US labor force works in some form of shift work (Mcmenamin 2007). Among the companies in South Korea, 20 % have adopted shift work and 80 % of those companies that have adopted shift work have adopted a 12-h day shift (Son et al. 2008). Working at night can affect health in various manners because it disrupts the circadian rhythm (Knutsson 2003). Almost all physical functions, including the control of appetite and digestion, are regulated by the circadian rhythm (Knutsson 2010).

Gastroesophageal reflux disease (GERD) is a condition developed when the reflux of stomach contents causes troublesome symptoms and/or complications (Vakil et al. 2006). Its prevalence is known to be 10–20 % in the Western world and <5 % in Asia. The most common symptoms are heartburn, regurgitation, and dysphagia. GERD symptoms cause a large burden among employers because of the high absence rate and poor performance (Locke et al. 1997).

Recent studies have indicated that disruption of the circadian system, such as due to shift work, is an important contributory factor in numerous important pathological conditions, including gastrointestinal diseases (Erren and Reiter 2009). Although many studies have investigated the association between shift work and gastrointestinal disorders, these have focused on peptic ulcer disease or unspecific gastrointestinal symptoms (Lundell et al. 1999). A strong evidence links shift work to peptic ulcer disease (Knutsson 2003). However, only one study investigated the association between shift work and GERD; this study used a questionnaire to diagnose GERD (Li et al. 2008). To date, therefore, no study has been published that has examined the possible association between night-shift work and GERD by using endoscopy. Erosive esophagitis (EE) is a complication of GERD that can be easily detected on endoscopy and can be used as an objective criterion for the diagnosis of GERD (Vakil et al. 2006). In this study, we assessed the impact of night-shift work and other factors on the prevalence of EE among shipyard male workers in South Korea, to clarify the association between night-shift work and GERD.

Most of the characteristics of the workers who had worked on night shifts were similar to those of the workers who had never worked night shifts (Table 1). However, the workers with night-shift work were less likely to have received education for ≥13 years (P < 0.001).

EE was detected in 8.8 % (530/6040) of the workers who underwent EGD. Table 2 presents the ORs and 95 % confidence interval (CI) of EE with night-shift work adjusted for suspected confounders. In the multiple logistic regression models controlled for multiple covariates, including age, BMI, smoking status, alcohol consumption, educational level, marital status, and H. pylori infection, night-shift work was associated with EE (OR 1.41; 95 % CI 1.03–1.94). Obesity, smoking, and alcohol consumption of ≥140 g/week were significantly associated with EE (OR 1.76; 95 % CI 1.40–2.21; OR 1.97; 95 % CI 1.49–2.62; OR 1.51; 95 % CI 1.22–1.87, respectively). In comparison, H. pylori infection was negatively associated with EE (OR 0.29; 95 % CI 0.24–0.35). No significant interaction was observed between night-shift work and any of the potential confounding variables.

In this study, the prevalence of EE was 8.8 %, which is similar to the prevalence rates of 6.7, 7.9, and 7.6 % in previous Korean studies (Kim et al. 2011a, b; Shim et al. 2009; Lee et al. 2011) and 6.4 % in a Chinese study (Zou et al. 2011), but lower than the prevalence rates of 15.5 and 11.8 % in Western populations (Ronkainen et al. 2005; Zagari et al. 2008).

Li et al. conducted a cross-sectional investigation among outpatients in ten hospitals in China in order to elucidate the epidemiology of gastrointestinal reflux disease symptoms (Li et al. 2008). The study used the Chinese version of the reflux disease questionnaire to diagnose GERD. The researchers showed that night-shift work was significantly associated with GERD. The results were compatible with those of the present study. However, as the study was not designed to evaluate the relationship between night-shift work and GERD, night-shift variables were not described. Furthermore, the study population was not representative of a healthy working population.

No plausible pathophysiological mechanism has been proposed to explain the relationship between night-shift work and GERD. A disrupted circadian rhythm may result from desynchronization of the environment, such as shift work, gene polymorphism, or physiological aging (Konturek et al. 2011). The circadian system controls gut motility, gastric acid secretion, maintenance and restoration of the protective mucosal barrier, production of digestive enzymes, and the immunological system of the gastrointestinal tract (Konturek et al. 2011). Klupinska et al. reported that circulating melatonin levels were significantly lower in patients with the erosive form of GERD than in patients with the non-erosive reflux form (Klupinska et al. 2006). Konturek et al. suggested the possible dose-dependent protective role of melatonin in preventing reflux-induced changes in the esophageal mucosa. Melatonin is an important regulator of circadian system (Konturek et al. 2011). Several mechanisms of action of melatonin on GERD were proposed. Melatonin increases reduced esophageal sphincter pressure, blood flow, and anti-inflammatory molecules in the esophageal mucous and decreases gastric acid secretion (Kandil et al. 2010; Konturek and Konturek 2007).

In addition to the disruption of the circadian system, irregular dietary habit, which is common among shift workers, could lead GERD. Yamamichi et al. reported a correlation between GERD and dietary habits such as having dinner a few hours before going to bed, eating midnight snacks, frequently skipping breakfast, and quick eating (Yamamichi et al. 2012). If these dietary habits are the main causes of GERD in night-shift workers, we could prevent and manage GERD by dietary habit modification. Unfortunately, we did not investigate dietary habits in this study.

BMI was not associated with night-shift work in this study. Although some previous studies showed that BMI was positively associated with night-shift work, most of these studies included female subjects such as nurses (Ramin et al. 2015; Peplonska et al. 2015; Amani and Gill 2013), whereas the present study included only male workers. Some studies with male subjects showed no or negative association between BMI and night-shift work (Fesharaki et al. 2014; van Amelsvoort et al. 2004; Nakamura et al. 1997). Further studies to investigate whether interaction between night-shift work and sex exists with respect to their effect on obesity are required. In comparison, BMI was significantly associated with EE in our study as in most previous studies (Hampel et al. 2005; El-Serag et al. 2007). A recent meta-analysis demonstrated a positive association between BMI and the presence of EE, especially in men. Several hypotheses have been proposed to explain the relationship between obesity and EE. Increased intra-abdominal pressure and subsequent esophageal acid exposure, which are hormonal factors related to adiposity, and increased transient lower esophageal sphincter (LES) relaxation were associated with obesity in previous studies (El-Serag et al. 2006, 2007; Wu et al. 2007).

Smoking was not associated with night-shift work in this study. In a recent study with 4685 Koreans, Cho et al. reported that smoking was not associated with night-shift work (Cho et al. 2013). However, most of the previous studies reported a positive association between smoking and night-shift work (Ramin et al. 2015; Fesharaki et al. 2014; Van Amelsvoort et al. 2004; Peplonska et al. 2015; Nicholson et al. 1999). To clarify the cause of the discrepant results, additional studies are needed. However, smoking was significantly associated with EE in the present study. Some previous studies reported a positive relationship between smoking and EE (Chiba et al. 2012; Kim et al. 2011a, b). Cigarette smoking has been reported to prolong esophageal acid clearance times with hyposalivation, provoke acid reflux, and reduce LES pressure (Kahrilas and Gupta 1989; Kahrilas et al. 1990).

In accordance with previous reports, alcohol consumption was significantly associated with EE in our study (Chiba et al. 2012; Kim et al. 2011a, b). Excessive alcohol intake has been reported to promote acid regurgitation by reducing LES pressure and slowing both esophageal motility and gastric emptying (Kaufman and Kaye 1978; Keshavarzian et al. 1990; Mincis et al. 1995).

In comparison, H. pylori infection was negatively associated with EE, which is consistent with previous reports (Chung et al. 2011; Kim et al. 2008; Unal et al. 2006; Nordenstedt et al. 2007). These results suggest that H. pylori-associated inflammation plays a role in the prevention of the development of EE. However, the association between H. pylori and EE is complex and remains incompletely defined.

To the best of our knowledge, this is the first study to evaluate the relationship between night-shift work and EE. The reflux diagnostic questionnaire has some limitation to detect GERD because of its low specificity of 50 % (Li et al. 2008). Hence, instead of a using questionnaire, the present study used endoscopic findings to diagnose GERD.

Our study has several limitations. First, we did not investigate the history of reflux-inducing habits such as supine position after meals and meals before bedtime. In addition, we did not investigate the possibility that dietary habits, including fat, chocolate, and caffeine intakes are associated with GERD. These dietary factors can confound the association between night-shift and EE. Second, inter-operator variability of EGD in the assessment of esophagitis could occur. To minimize this, we used the LA classification, which is the most thoroughly evaluated classification for esophagitis and widely used. Third, the study participants were healthy male workers with the same occupational backgrounds. Therefore, it was difficult to generalize our findings to encompass women or other working groups owing to selection bias. Finally, our study is cross-sectional; hence, we could not investigate the causality between night-shift work and GERD.

Our study revealed that night-shift work is a risk factor for GERD, and avoidance of night-shift work should be considered a primary prevention strategy for GERD. Physicians should pay attention to night-shift work as a risk factor when managing GERD. New studies that take into consideration history of reflux-inducing habits as variables are required to confirm the association between night-shift work and GERD.