Exercise-Related Transient Abdominal Pain (ETAP)

3.1 Pain Sensation and Severity

Morton and Callister [1] studied almost 600 cases of ETAP and observed that the sensation of the pain was significantly related to its severity. The pain was described as sharp or stabbing when severe, and cramping, aching, or pulling when less intense. Progression to sharp and stabbing pain with increasing pain severity has been observed subsequently in other epidemiological studies [12], clinical trials [16], and case reports [17].

When Morton and Callister questioned individuals from six sports about their experience of ETAP in the past year, symptomatic individuals reported the severity as 5.6 ± 0.2 out of 10 at its worst, resulting in 76 % having to reduce their exercise intensity when the pain was present and 12 % to stop exercise altogether [1]. In a study that targeted a single running event, sufferers rated the pain as 3.6 ± 0.1 out of 10, forcing 36 % to slow down and 6 % to stop entirely [12]. Although the pain is mostly benign, it can clearly be detrimental to performance and may compromise sports participation for some individuals [1, 12].

3.2 Pain Location

In approximately 80 % of cases, the pain is described as localized rather than vague and diffuse [1, 12]. While the pain is mostly localized during an episode, it may occur in any region of the abdomen [1, 12], with pain in the mid- to upper-abdomen, especially along the costal border, being the most common site as shown in Fig. 1 [1, 2, 3, 12, 18, 19]. Right side pain has been reported as up to twice as common as left side pain [12, 16], although left side pain may be more prevalent among the young [1, 5, 11].

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3.3 Intra-Individual Frequency and Pain Reproducibility

Approximately half of the 600 symptomatic individuals surveyed by Morton and Callister [1] claimed ETAP occurred in less than 10 % of exercise sessions, and 82 % indicated it occurred no more than 20 % of the time.

The reproducibility of ETAP has been explored in two laboratory-based studies [20, 21]. Plunkett and Hopkins [21] reported poor reproducibility of the condition, although only ten subjects were involved in the study. Morton et al. [20] exercised 23 symptomatic individuals on a treadmill on two different days after consuming large volumes of fluid and found 64 % experienced ETAP in both trials, 23 % experienced ETAP in one trial, and only 13 % did not experience ETAP on either occasion. The intra-class correlation between the two trials was significant for the mean pain severity (r = 0.66, p < 0.01) but not peak severity (r = 0.41). The authors suggested that the between-days reliability of the pain was acceptable for repeated measure design studies, but they acknowledged that the subjective, transient, and partially unpredictable nature of the phenomenon makes studying the condition challenging [16, 20, 21, 22].

3.4 Shoulder Tip Pain

As far back as 1951, Sinclair [2] reported an association between ETAP and shoulder tip pain (STP). In his observations on 123 athletes, 28 (23 %) reported STP in association with ETAP and in all but one case the STP was on the same side of the torso as ETAP. The significance of this observation is that the shoulder tip region—extending from the lateral third of the trapezius border to the acromion process—is the referred site for pain arising from tissue innervated by the phrenic nerve [23], which includes the diaphragm and neighboring structures. The association between STP and ETAP is informative regarding the etiology of ETAP, as discussed below.

While difficult to delineate as referred pain, Morton and Callister [1] questioned individuals about ‘non-injury-related’ shoulder pain in their study of ETAP in six sports. Fourteen percent reported experiencing sharp, well localized pain in the shoulder tip region characteristic of referred STP [23], and those who were susceptible to ETAP were significantly (p < 0.01) more likely to report STP. Further, STP was most common in the same sports as ETAP, albeit approximately 4–5 times less common than ETAP [11]. STP was only reported by 5 % of the 848 participants questioned by Morton et al. [12] at a running event, as compared with 27 % for ETAP, but the two conditions were significantly related. In both studies, STP was rated as more severe than ETAP but was not related to ETAP in a particular region of the torso.

4.1 Personal Characteristics

In an article that appeared in the British Medical Journal in 1945 [24], the author asserted that some individuals are more susceptible to ETAP than others, which could be attributed to anatomical, physiological, or mechanical factors. Subsequently, investigations of a variety of personal characteristics on the experience of ETAP have been conducted [1, 5, 12, 25].

Several studies have demonstrated that the young are most susceptible to ETAP [1, 2, 26]. Morton and Callister [11] reported 77 % of active individuals under the age of 20 years experienced the pain compared with only 40 % of individuals over the age of 40 years. Both the prevalence and severity of ETAP have been shown to significantly decrease with increasing age [11, 12]. Confounding the observation that ETAP decreases with increasing age might be a reduction in activity levels, however these studies targeted an active population. While the young appear more susceptible to the pain, Kugelmass [5] reported it to be relatively uncommon before the age of 10 years.

Conflicting reports exist regarding the influence of sex on ETAP. ETAP was reported four times more frequently by females in a study by ter Steege et al. [14] of gastrointestinal complaints during long distance running. Other studies of gastrointestinal symptoms during running have also reported a higher prevalence of ETAP among females [4, 27]. Rehrer et al. [4] reported 41 % of females experienced ETAP during an ultra-marathon event compared with only 17 % of males, although the difference was not statistically significant as only 12 females participated in the event. Conversely, two studies by Morton and colleagues [1, 12] found no gender differences in the experience of ETAP when other potentially confounding factors such as age were controlled for. As the studies by Morton and colleagues [11, 12] involved a comparably larger number of cases, the weight of the current evidence suggests that there is little or no effect of gender on ETAP.

A high level of physical conditioning may decrease the experience of ETAP [2, 3]; however, the ailment is not unknown among well trained and even elite athletes [10, 12, 15]. Morton and Callister [1] observed well conditioned individuals to be as likely to report experiencing ETAP within the past year as less conditioned individuals and also to report pain of a similar severity, although better conditioned individuals reported experiencing the pain less frequently. Hence, training status might have some prophylactic benefits but in some athletes the possibility of experiencing ETAP cannot be eliminated [3].

The influence of body type and posture on ETAP has been investigated in several studies [1, 5, 11, 12, 25]. Body mass index was not related to ETAP in either of the large epidemiological studies conducted by Morton and colleagues [1, 11, 12]. Recognizing the limitations of body mass index as a surrogate for body type, Morton and Callister [25] investigated the relationship between somatotype and the experience of ETAP in 159 active young people (mean age = 18.6 years). ETAP was unrelated to somatotype, which conflicted with an early report by Kugelmass [5], who observed children with an ectomorphic disposition to be most afflicted by the pain. However, the two studies [5, 25] did concur that individuals with poor postural alignment were more predisposed to the pain. Morton and Callister [25] found individuals with kyphosis were more susceptible to ETAP (p < 0.01) and the extent of kyphosis and lordosis influenced the pain severity (p < 0.05). The implications of these observations are discussed below when considering the etiology of the pain.

4.2 Mode of Exercise

As described previously, the experience of ETAP varies for different sporting activities, with running consistently being reported as most provocative of the condition [1, 2, 6, 10, 11, 12, 26, 28]. It has been concluded that ETAP is most prevalent in activities that involve repetitive torso movement, involving either vertical translation or longitudinal rotation, especially when the torso is in an extended posture [1, 29]. These conditions are all met in running, which explains the high prevalence of ETAP in this activity. Swimming extends the torso and involves repetitive rotation with the torso extended, accounting for a modest prevalence of ETAP. Cycling, in which the prevalence of ETAP is comparatively low, flexes the torso and involves relatively little movement.

Exercise intensity has been suggested to influence ETAP [2, 15, 28] although the pain can clearly occur during activities of low intensity such as horse riding [1]. Morton et al. [12] reported 31 % of runners experienced the pain during a walk/run event compared with only 16 % of walkers. Controlling for factors such as the age of the participants, the runners were 3.5 times more likely to report the pain than the walkers. As running also differs from walking in its movement characteristics, this would confound the potential effect of exercise intensity. Among the runners in this study, the occurrence or severity of ETAP was unrelated to the time to complete the event, suggesting exercise intensity was not important [12].

4.3 Pre-Exercise Ingestion

Consuming food or drink before exercise has consistently been reported to evoke ETAP [1, 2, 10, 11, 12]. Consequentially, laboratory-based studies that have endeavoured to take measurements of the pain have required subjects to eat and/or drink before exercise to provoke its manifestation [2, 6, 16, 20, 22].

Fifty-two percent of respondents surveyed by Morton and Callister [1] perceived eating before exercise to provoke ETAP, and 38 % claimed that drinking before exercise provoked the pain. Sinclair [2] reported that the postprandial state could induce ETAP in 30 out of 35 cases compared with only 19 cases when prior feeding did not occur. Approximately half of the individuals who reported developing ETAP during the run/walk event studied by Morton et al. [12] claimed the pain developed shortly after ingesting fluid at a drink station. Further, an analysis of the pre-event meal of the 848 participants in this event showed a positive relationship between the volume of food and drink consumed relative to body weight and the experience of ETAP. Interestingly, ETAP was unrelated to the nutritional content of the pre-event meal with regards to carbohydrate (sugar and starch), fat, protein, water, or total energy. However, a limitation of this study was that participants were not asked whether they periodically experienced the pain and so analyses could not be performed on the symptomatic individuals only.

Two studies have shown that the composition of ingested fluid influences the experience of ETAP, with hypertonic fluids being most provocative [20, 21]. Plunkett and Hopkins [21] compared the consumption of large volumes of water, an isotonic solution, and a hypertonic solution on the experience of ETAP during treadmill running. They found that the isotonic solution evoked fewer symptoms of ETAP than water (p < 0.05) but the hypertonic trial was more provocative than both (p < 0.01). Similarly, Morton et al. [20] found a hypertonic beverage to be significantly more provocative of ETAP than isotonic and hypotonic beverages, with 83 % of subjects developing the pain after consuming the hypertonic solution compared with 70 % in the other two trials. Other studies have suggested a connection between the carbohydrate content of ingested fluid and the experience of ETAP [4, 28].

While fluid consumption appears to provoke ETAP, fluids may be better tolerated with practice. Reliability testing conducted by Morton et al. [20], which involved subjects exercising on several occasions after consuming large volumes of fluid, found that the experience of ETAP decreased in the later trials. Just as the gut may be trainable with regards to digesting and absorbing fluids during exercise [30], this may suggest that sufferers of ETAP might benefit from practicing fluid consumption during exercise.

4.4 Inadequate Warm-up and Cold Ambient Conditions

Inadequate warm-up prior to exercise and cold ambient conditions have been suggested to provoke ETAP [3, 12, 24, 31]; however, these claims are based on anecdotal observations. For example, Capps [3] claimed that 40 out of 60 competitors in a cross-country running event that occurred in an ambient temperature of −9 °C were forced out of the event due to ETAP. Morton et al. [12] reported that equal numbers of competitors developed ETAP during the first, middle, and final third of a 14-km running event, suggesting that inadequate warm-up was not an important contributor. At this time, the influence of these factors is inconclusive and requires further clarification.

5.1 Diaphragmatic Ischemia

In 1941, Capps [3] proposed that ETAP was caused by ischemia of the diaphragm. In support of this theory are sensations associated with innervation of the diaphragm. The diaphragm is mostly innervated by the phrenic nerve, which refers pain to the shoulder tip region, but the peripheral portions of the diaphragm are supplied by the lower six intercostal nerves, which could account for sharp and well localized pain in the subcostal region [34, 35].

The main evidence against this theory is that ETAP can be induced by activities of low respiratory demand, such as horse, camel, and motorbike riding, where ischemia of the diaphragm is improbable [1, 2, 36]. Further, this theory does not account for ETAP in regions of the abdomen other than the subcostal border. Finally, it has been questioned whether in non-diseased individuals the diaphragm muscle would become ischemic and fatigue before the muscles of the limbs, as this would imply central fatigue precedes peripheral fatigue [37].

Interestingly, in a study that predated Capps’ theory, diaphragmatic movements were monitored during an episode of ETAP using a fluoroscopic technique and were found to be full and unrestricted [6]. More recently, Morton and Callister [16] required subjects to perform a flow-volume loop while experiencing ETAP and found no compromise in any spirometry measures. They had hypothesized that lung function would be impaired, especially inhalation, if the diaphragm was ischemic [16]. In conclusion, diaphragmatic ischemia is an unlikely etiology of ETAP.

5.2 Mechanical Stress on the Visceral Ligaments

Historically, the most widely accepted theory on the causation of ETAP has centred on mechanical stress being placed upon the visceral ligaments that support the abdominal viscera, especially the liver and stomach, via attachments to the diaphragm. The theory was first proposed at least as far back as the 1920s [3, 7], but was popularized by Sinclair [2] in 1951.

This theory explains several features of ETAP, most notably the high prevalence of ETAP in activities that are ‘jolting’ in nature yet of low respiratory demand such as horse riding [1, 2, 36]. Further, consuming food and fluid prior to exercise could provoke ETAP by the increased gastric mass loading the visceral ligaments [2]. Plunkett and Hopkins [21] argued that increased gastric mass would also result when consuming hypertonic beverages [20, 21, 28] due to these fluids slowing gastric emptying and thereby maintaining a larger gastric mass. As the visceral ligaments attach to the diaphragm, the theory could also explain the experience of STP. Less well established observations that lend credibility to the visceral ligament theory include the alleged therapeutic effect of body inversion or wearing a supportive belt around the abdomen [2, 21].

While the visceral ligament theory accounts for many of the characteristics of ETAP, it has been argued that there are several aspects of the pain that the theory cannot explain [38]. The observation of ETAP low in the abdomen is not consistent with the theory. Further, it is unclear why ETAP would be prevalent in swimming as this activity is not ‘jolting’ in nature and occurs in a prone position [1, 3]. It would be expected that increasing adipose stores within the greater and lesser omentum would contribute to an increased susceptibility to ETAP, as these structures attach via mesentery directly to the stomach [34], yet ETAP appears unrelated to body mass index [11, 12] or endomorphy [25]. Finally, as the ligaments are extensions of the abdominal viscera, pain arising from them would likely be visceral in nature, which is typically dull, medial and poorly localized [39], in contrast to ETAP, which is mostly sharp, lateral and well localized [1, 12].

In conclusion, the visceral ligament theory explains several features of ETAP such as its high prevalence in ‘jolting’-type activities and its relation to the post-prandial state. However, the theory has shortcomings relating to the documented pain distribution and characteristics, as well as the observation that ETAP can occur in non-‘jolting’ activities.

5.3 Gastrointestinal Disturbances

ETAP has been commonly referred to as a gastrointestinal disturbance [4, 10, 13, 15, 27, 28, 40, 41, 42] and is commonly the most prevalent symptom reported in studies of gastrointestinal complaints during exercise [4, 15]. Despite being labeled a gastrointestinal disturbance, the etiology of the pain from a gastrointestinal perspective is poorly defined [15, 41, 43].

The few reports that have offered a gastrointestinal explanation for ETAP have focused on the pain originating from gut ischemia [13, 15, 36, 44] or distension [36]. Supportive of an ischemic explanation for the pain, splanchnic blood flow decreases by up to 80 % during exercise [13, 41]. Indeed, gut ischemia has been observed in otherwise healthy subjects, but only during maximal exercise [45], unlike ETAP which can occur during lower intensity activities.

The main reason ETAP has been labeled a gastrointestinal disturbance is due to its association with the post-prandial state [1, 2, 10, 12, 21], yet the pain is commonly experienced when no food or drink is consumed for several hours before exercise [20, 21]. More importantly, the established characteristics of ETAP are dissimilar to gastrointestinal pain, which is typically described as medial, diffuse and colicky [6, 39]. Silen [39] observed that people with gastrointestinal discomfort tend to writhe the torso to obtain pain relief, which is unlike ETAP that is relieved by reducing movement [1, 2, 12, 21, 22].

In conclusion, while ETAP is commonly considered a gastrointestinal complaint, elements of the pain are not consistent with a gastrointestinal origin.

5.4 Muscular Cramp

In the two large epidemiological studies by Morton and colleagues [1, 12] (see Table 1), approximately one in four sufferers of ETAP described the sensation of the pain as ‘cramping’. They suggested that a muscular cramp could explain several of the features of ETAP, such as the pain occurring throughout the abdomen, and suggested the theory warranted further investigation. Subsequently, Morton and Callister [22] measured localized electromyographic (EMG) activity while ETAP was present, as muscular cramp is associated with high levels of EMG activity [46, 47]. EMG activity was not elevated at the site of ETAP during an episode of the pain, which convincingly discredited the muscular cramp theory.

5.5 Median Arcuate Ligament Syndrome

ETAP has been referred to in the literature as median arcuate ligament syndrome [48, 49]. The median arcuate ligament is a fibrous arch that unites the crura of the diaphragm on either side of the aortic hiatus. In some people, the ligament inserts low and crosses the proximal portion of the celiac axis, which can cause compression and ischemic-related epigastric pain, especially post-prandially and during expiration [50]. While the condition does not explain several of the characteristic of ETAP, such as its manifestation in other regions of the abdomen, the anatomical abnormality leading to the syndrome is surprisingly common, being present in approximately 16 % of individuals and 30 % of young people [48].

5.6 Neurogenic Pain

The experience of ETAP appears to be affected by poor posture, especially in the thoracic region [5, 25]. Kugelmass [5] was the first to make this observation and he suggested that poor posture might affect ETAP by altering the mechanics of the abdominal structures responsible for the pain. However, Morton and Aune [51] noted that palpating specific vertebrae in the T8–12 region, which innervates the abdominal wall, could reproduce symptoms of ETAP. ETAP could be exactly reproduced in 8 of 17 subjects assessed, and the site at which the subjects reported ETAP corresponded to the dermatome arising from the nerve root being palpated. Hence, they suggested that a neurogenic origin of ETAP should be considered.

Other reports of ETAP-like symptoms in the literature have implicated the nervous system. For example, slipping rib syndrome, in which hypermobility of the eighth, ninth and/or tenth rib results in trauma to the adjacent intercostal nerve, is a documented but often undiagnosed source of upper abdominal pain similar in nature to ETAP [52, 53, 54, 55, 56, 57, 58]. Similarly, abdominal wall nerve entrapment, in which the anterior cutaneous branch of an intercostal nerve is compressed at the site at which it reflexes sharply and pierces the abdominal musculature, can produce pain with similar features to ETAP [54, 59, 60, 61, 62]. Finally, spinal tumors and facet joint cysts have been known to produce similar symptoms to ETAP as a result of compressive forces being placed on the intercostal nerves [63, 64].

While a neurogenic explanation does not account for all features of ETAP, such as its relation to the post-prandial state, it is notable that the intercostal nerves can be rendered vulnerable to compression as a result of a reduction in intervertebral disk height that can occur during repetitive, dynamic torso movements such as running [65, 66].

5.7 Irritation of the Parietal Peritoneum

After studying approximately 600 sufferers of ETAP, Morton and Callister [1] suggested that ETAP might be caused by irritation of the parietal peritoneum, which is the outer layer of the peritoneum that adheres to the abdominal wall and underside of the diaphragm. They presented the following evidence for ETAP arising from this tissue: aggravation of the portion of the parietal peritoneum that adheres to the abdominal wall causes sharp, well localized pain similar in nature to ETAP [23, 67]; the portion of the parietal peritoneum that underlays the diaphragm is innervated by the phrenic nerve and gives rise to STP when aggravated [23, 68, 69, 70]; pain arising from the parietal peritoneum is accentuated by movement [39]; the parietal peritoneum traverses the entire abdominal wall which could account for the widespread distribution of ETAP [34, 71]; the parietal peritoneum is most firmly adhered to the abdominal wall along the linear alba and the greatest potential for movement is therefore in the lateral aspects of the abdomen [34]; the tension in the parietal peritoneum is increased with the torso in an extended posture; children have a proportionally larger peritoneal surface area than that of adults which might explain the high prevalence of ETAP in the young [72]; and pain arising from the parietal peritoneum relieves quickly on removal of the stimulus [23] which is similar to that observed for ETAP when activity is ceased [16].

In addition to these observations, several case reports describing ETAP have implicated the parietal peritoneum [73, 74, 75]. Dimeo et al. [73] reported the case of a 29-year-old national class distance runner with severe, recurrent ETAP in the upper right abdominal quadrant during exertion. Laparoscopy showed congenital supernumerary ligaments binding the gallbladder to the abdominal wall. Symptoms of ETAP resolved after cholecystectomy and resection of the adhesions. Similarly, Lauder and Moses [74] reported adhesions between the ascending colon and anterior abdominal wall to be the cause of recurrent ETAP in a 28-year-old triathlete. The pain resolved following surgical intervention. Several authors have also suggested that ETAP is caused by a ‘cecal slap syndrome’ in which the caecum slaps against the anterior abdominal wall during repetitive jolting actions such as running [19, 76].

Morton and Callister [1] suggested that ETAP might result from increased friction between the parietal peritoneum attached to the abdominal wall and the visceral peritoneum that overlays the abdominal viscera. They argued that friction might be increased by the visceral and parietal layers of the peritoneum being forced more firmly together by distension of the stomach, as occurs in the postprandial state, or other abdominal organs such as the liver or large intestine. Further, they suggested that exercise-mediated changes in the quantity or viscosity of the lubricating serous fluid contained within the peritoneal cavity might increase friction. The serous fluid within the peritoneal cavity is in a constant state of flux [71, 77], being derived from splanchnic blood flow, which decreases during exercise [13, 41], and draining into the lymphatic system, which is facilitated by movement of the diaphragm [78, 79, 80]. Interestingly, the fluid in the peritoneal cavity is highly responsive to osmotic gradients between it and its vascular supply [71, 77, 81], which might explain the provocative effect of consuming hypertonic beverages on ETAP [20, 21]. Indeed, results of the study by Morton et al. [20] indicated that consuming hypertonic beverages provoked ETAP for reasons other than just increasing gastric mass due to slowing of gastric emptying.

Recently, Mole et al. [82] found that individuals symptomatic to ETAP had significantly thinner transversus abdominis and poorer functional core stability than asymptomatic individuals. The authors argued that better strength and activation of the abdominal musculature, especially the transversus abdominis, might reduce abdominal content mobility leading to lesser symptoms of ETAP. This observation may lend further support to the parietal peritoneum theory, although it would also support the visceral ligament theory as better core stability might reduce loading on the visceral ligaments.

In summary, many of the characteristics of ETAP are consistent with irritation of the parietal peritoneum, and while speculative, friction on this tissue might be a plausible explanation for ETAP.

5.8 Conclusions

The etiology of ETAP remains speculative, although progress has been made within the past 15 years regarding potential mechanisms. While some long-standing theories seem unlikely in the light of more recent findings, other novel theories have emerged. Indeed, determining the cause of ETAP is the first step towards developing procedures to manage the ailment, if at all possible.