Impact of foliar herbivory on the development of a root-feeding insect and its parasitoid

The majority of studies exploring interactions between above- and below-ground biota have been focused on the effects of root-associated organisms on foliar herbivorous insects. This study examined the effects of foliar herbivory by Pieris brassicae L. (Lepidoptera: Pieridae) on the performance of the root herbivore Delia radicum L. (Diptera: Anthomyiidae) and its parasitoid Trybliographa rapae (Westwood) (Hymenoptera: Figitidae), mediated through a shared host plant Brassica nigra L. (Brassicaceae). In the presence of foliar herbivory, the survival of D. radicum and T. rapae decreased significantly by more than 50%. In addition, newly emerged adults of both root herbivores and parasitoids were significantly smaller on plants that had been exposed to foliar herbivory than on control plants. To determine what factor(s) may have accounted for the observed results, we examined the effects of foliar herbivory on root quantity and quality. No significant differences in root biomass were found between plants with and without shoot herbivore damage. Moreover, concentrations of nitrogen in root tissues were also unaffected by shoot damage by P. brassicae larvae. However, higher levels of indole glucosinolates were measured in roots of plants exposed to foliar herbivory, suggesting that the development of the root herbivore and its parasitoid may be, at least partly, negatively affected by increased levels of these allelochemicals in root tissues. Our results show that foliar herbivores can affect the development not only of root-feeding insects but also their natural enemies. We argue that such indirect interactions between above- and below-ground biota may play an important role in the structuring and functioning of communities.
Introduction
Over the past 20 years, studies exploring community-level processes have been based primarily on bi- and tri-trophic interactions in above-ground systems, usually involving associations among plants, insect herbivores, and their natural enemies such as parasitoids or predators (Price et al. 1980; Turlings et al. 1990; Vet and Dicke 1992; Dicke 1999). While providing valuable data on a range of selective forces shaping community structure and function, these studies have generally ignored biological processes that occur below-ground. Recently, however, it has become apparent that above-ground trophic interactions can be strongly influenced by interactions between the host plant and soil-dwelling organisms (Gange and Brown 1989; Masters and Brown 1992, 1997; Masters et al. 1993; Masters 1995; Gange 2001; Van der Putten et al. 2001; Bardgett and Wardle 2003; Bezemer et al. 2003). For instance, recent studies have shown that soil-dwelling organisms—such as root-feeding insects, arbuscular mycorrhiza fungi, and nematodes—can also influence the growth, development, and behavior of higher trophic levels below-ground, including parasitoids (Masters et al. 2001; Gange et al. 2003; Wurst and Jones 2003; Bezemer et al. 2005; Guerrieri et al. 2005) and even hyperparasitoids in the fourth trophic level (Soler et al. 2005).
It is also known that above-ground herbivory can affect the development of below-ground insect herbivores (reviewed by Blossey and Hunt-Joshi 2003), when the shared host plant has previously been exposed to intense shoot damage. For example, Tindall and Stout (2001) reported that severe damage by insect foliar herbivores was correlated with a significant reduction in the body size of an insect herbivore feeding on root tissues of the same host plant, compared with conspecifics developing on roots of plants without foliar herbivores. Other studies have shown similar effects (Masters et al. 1993; Hunt-Joshi and Blossey 2005). However, the effects of foliar herbivory on the development of natural enemies in the soil, such as predators and parasitoids, remain largely unexplored.
Thus far, the effects of above-ground herbivory on the performance of below-ground consumers have been explained mainly by quantitative changes in the amount of root biomass, when an extreme amount of leaf damage results in partial or complete death of the root system. However, minor levels of shoot damage, while not leading to a significant reduction in root biomass, may still affect the quality of the root tissues influencing the development of root-associated organisms (reviewed in Bezemer and Van Dam 2005). Furthermore, interactions between above- and below-ground herbivores may also be mediated by qualitative changes in the shared host plant. For example, insect herbivory frequently leads to a systemic defense response within the host plant, resulting in enhanced concentrations of secondary plant compounds in plant organs that have not been damaged by herbivory (Karban and Baldwin 1997). Secondary plant compounds commonly have a negative impact on herbivore performance (Karban and Baldwin 1997). Several studies have shown that root herbivory can result in enhanced concentrations of secondary plant compounds in the foliage, although the reverse, e.g., the effects of foliar herbivory on changes in concentrations of root secondary plant compounds, has rarely been reported (reviewed in Bezemer and Van Dam 2005). Moreover, herbivory can induce a stress response within the host plant, which can lead to a reallocation of plant compounds such as carbohydrates and soluble nitrogen between root and shoot tissues, and the concentration of these compounds is known to directly affect insect growth parameters (Masters et al. 1993; Masters and Brown 1997). It is important to stress that the mechanisms described above are not necessarily mutually exclusive.
In this study, we examined the effects of above-ground herbivory on the development and survival of a below-ground insect herbivore and its endoparasitoid. Our study is based on interactions involving a naturally occurring system in Western Europe. The black mustard, Brassica nigra L. (Brassicaceae), is a widely distributed annual crucifer that is common along rivers and on disturbed sites in The Netherlands (Schaminee et al. 1998). It is attacked by several adapted specialist herbivores, including the large cabbage white butterfly, Pieris brassicae L. (Lepidoptera: Pieridae) whose larvae feed on the shoots and flowers of this and related species (Harvey et al. 2003). Mustard plants are also attacked by specialized root-feeding herbivores, including the cabbage root fly, Delia radicum L. (Diptera: Anthomyiidae) (Coaker and Finch 1971). Trybliographa rapae (Westwood) (Hymenoptera: Figitidae) is one of the main parasitoids of D. radicum in Europe (Lahmar 1982). The main aim of this investigation was to determine whether the growth, development, and survival of D. radicum and its endoparasitoid, T. rapae, are affected by foliar herbivory by P. brassicae. We also examined whether above-ground herbivory leads to qualitative and/or quantitative differences in root tissues. We compared levels of root biomass in plants with and without shoot damage, as well as levels of nitrogen in root tissues. Finally, we compared levels of allelochemicals (glucosinolates) in root tissues of plants under the two treatments. We hypothesized that above-ground herbivory by P. brassicae would result in reduced root-plant quality which would negatively affect the performance of D. radicum. Because T. rapae is a koinobiont parasitoid, D. radicum larvae continue feeding and growing during much of the parasitoid–host interaction (reviewed in Harvey 2005). As a consequence of this close association between host and parasitoid, we hypothesized that the effects of P. brassicae on D. radicum would be carried over to T. rapae. Since parasitoids are highly susceptible to very small changes in the quality of the hosts, the effect on the parasitoid should be stronger than that on the host.
Materials and methods
Studied species
Brassica nigra, like other members of the Brassicaceae, possesses potent inducible direct defenses via the production of glucosinolates and their breakdown products; thus, the plant provides excellent potential for the study of multitrophic interactions (Van Dam et al. 2003). Pieris brassicae is a specialist chewing foliar herbivore that feeds on several species of wild and cultivated crucifers. The female butterfly typically lays broods of 7–140 eggs on the underside of a leaf. After hatching, the larvae feed gregariously until the third instar, when they disperse on the food plant. Delia radicum is a specialist chewing root herbivore that feeds on several species of crucifers. Females oviposit near the root-stem interface. The newly hatched maggots feed by boring galleries in the upper roots of the plant. Trybliographa rapae is a fairly specialized solitary koinobiont endoparasitoid that parasitizes L1–L3 instar larvae of D. radicum, as well as several closely related species. Adult parasitoid females forage via antennation, ovipositor probing, and vibrotaxis in order to find their hosts (Vet and Van Alphen 1985). The wasps readily parasitize larvae that are actively feeding in the root galleries but refuse hosts extracted from the root (Jones 1986). Females use their sharp, but flexible, ovipositor to explore infested roots to find hosts and evaluate their quality (Neveu et al. 2000).
Seeds of B. nigra were collected from a single population in the Northwest of Wageningen, The Netherlands. Seeds were surface sterilized and germinated on a bed of glass pearls (pearls of 1 mm diameter). One week after germination, seedlings were transplanted into 1.2-l pots, filled with soil collected from a restoration area that was abandoned in 1996, at De Mossel in Ede, The Netherlands. The sandy loam soil was sieved (2 cm) and mixed with 10% white sand (to improve the drainage of the soil), and sterilized using gamma radiation (25 KGray) to eliminate all soil organisms. The plants were grown in a greenhouse, at 70% relative humidity, at 22 ± 1°C (day) and 16 ± 1°C (night) on a 16-h:8-h day:night cycle. Natural daylight was provided by metal halide lamps (225 μmol s−1 m−2 PAR; 1 lamp per 1.5 m2). Plants were watered daily and supplemented with nutrients (Hoagland solution) once when the plants were 3 weeks old. Pieris brassicae was obtained from the insect culture maintained at the Laboratory of Entomology of Wageningen University, The Netherlands. D. radicum and T.rapae were obtained from insect cultures maintained at the Laboratory of Ecobiology of Insect Parasitoids, of Rennes University, France.
Experimental design and insect measurements
To test the effect of above-ground herbivores on the performance of soil insects, we reared D. radicum and its parasitoid T. rapae on roots of plants previously exposed (treatment) and not exposed (control) to P. brassicae larvae. Twenty-five days after transplanting, three newly hatched L1 larvae of P. brassicae were carefully placed with a small brush on the youngest fully developed leaf of each plant, and enclosed in a cylindrical clip cage (5.5 cm diameter) in order to ensure that the damage was localized. After 3 days, the larvae were moved to another new leaf on the plant. The larvae were allowed to feed for a further 3 days, after which each larva and clip cage was removed. Thus, each foliar-damaged plant was exposed to feeding by three L1 P. brassicae larvae for a total of 6 days. A second set of plants was kept undamaged and served as control. To standardize the possible effects of the clip cages on plant shoots, they were also placed on control plants, following the same methods as for the foliar-damaged plants. A total of 72 plants were used in the experiment (36 plants with and 36 without foliar herbivore damage).
One day after removing the P. brassicae larvae, four L1 D. radicum larvae were introduced to each plant by carefully placing the larvae with a brush onto the soil surface immediately adjacent to the stem. Using a magnifying glass, each plant was carefully checked 30 min after inoculation, to ensure that all the root fly larvae had successfully entered into the soil. For each plant, two of the larvae were healthy and two had been parasitized by T. rapae within approximately the prior 12 h. In a previous study, we reported that there was no significant difference in final root biomass in B. nigra plants with initial densities of five unparasitized D. radicum larvae per plant when compared with undamaged plants (Soler at al. 2005). Furthermore, parasitized larvae consume less plant material and attain smaller final masses than healthy hosts (Grandgirard 2003); thus, we assumed that plant root biomass would not be a limiting factor for root herbivore/parasitoid development. It is also important to stress that larvae of D. radicum are not cannibalistic (A.M. Cortesero, unpublished observations), making it possible for unparasitized and parasitized larvae to share a host plant.
To obtain parasitized D. radicum larvae, approximately 300 first instar larvae were offered to 60 mated T. rapae females over the course of 4 h. To facilitate and ensure high rates of parasitism, a slice of B. napus (turnip) root of 1.5–2 cm in height (15 cm diameter) that had previously been infested with the larvae of D. radicum was offered to the parasitoid females. The larvae were collected from the root after 4 h, and 144 larvae were then transferred to the experimental B. nigra plants. Because direct observations of parasitism are almost impossible in T. rapae, 100 additional larvae from the infested turnip slice were removed and placed on a new turnip, where parasitoid emergence was monitored. From these 100 larvae, 92 T. rapae adults emerged, and none produced D. radicum adults.
Following the below-ground inoculation of unparasitized and parasitized D. radicum larvae, experimental plants were placed individually into large meshed cylindrical cages (height 1 m, diameter 35 cm) to ensure that newly emerged adult flies and wasps did not escape and could be immediately captured. Plants from the two treatments were randomly distributed in the greenhouse and were moved around the room every 2–3 days to avoid any potential effects of positioning on insect development. The cages were checked twice daily (once in the morning and once in the afternoon) to record the emergence of adult flies and parasitoids. Newly emerged adults of D. radicum and T. rapae were collected with an aspirator. At emergence, the following data were recorded: (1) development time between inoculation and adult eclosion in days and (2) adult body size, based on the measurement of hind tibia length in both the herbivore and parasitoid. Hind tibia length has been commonly used as a measure of adult size in many insects, especially parasitoids (Godfray 1994; Harvey et al. 1994; Bezemer and Mills 2003). The hind tibia lengths of D. radicum and T. rapae were measured using a calibrated slide under a stereomicroscope. Adult survival (calculated as the proportion of insects that emerged relative to the number of larvae introduced in each pot) was also recorded.
Plant responses
Because the measurement of glucosinolate and nitrogen concentrations requires the destructive sampling of plants, root samples were taken from an additional set of plants (nine plants per treatment). The plants in the additional set were treated in exactly the same way as the foliar-damaged and control plants described above. Root material was collected 1 h before the other set of experimental plants was inoculated with parasitized and unparasitized D. radicum larvae to evaluate the quality of the control and foliar-damaged plants that larvae encountered after inoculation. After carefully washing the roots of each plant, the fine roots were separated from the main root. Roots less than 1 mm thick were considered fine (with a hair-like appearance) and those thicker than 1 mm were considered to be main roots. The roots were immediately frozen at −80°C, then freeze-dried and ground. Glucosinolate contents were determined using high performance liquid chromatography (HPLC) as described by Van Dam et al. (2004). Nitrogen content was determined using a Carlo Erba/Fisons, type EA1108, CHN analyzer. The total root biomass of the experimental plants was determined at the end of the experiment. The roots of each plant were harvested, oven-dried at 70°C and, subsequently, weighed on a microbalance.
Statistical analysis
The effects of foliar herbivory (with or without) and larval status (parasitized or unparasitized) on survival of D. radicum and T. rapae were tested using a generalized linear mixed model (with binomial distribution and logit link function, including plant as random term). The effects of foliar herbivory on developmental time and hind tibia length of D. radicum and T. rapae were tested using a generalized linear model (with normal distribution and identity link function). The effects of foliar herbivory and root type (primary or secondary roots) on plant quality (nitrogen and glucosinolate levels) were tested using a linear mixed model, including plant as random term to consider that the fine and main roots were sampled from the same plants. To test the effect of foliar herbivory on plant quantity (root biomass), we used analysis of variance. Normality, independence, and homogeneity of variance were checked by inspection of the residuals after model fitting. Analyses were carried out in Statistica and Genstat.
Results
Foliar herbivory significantly affected the survival of the root herbivore D. radicum and its parasitoid T. rapae (Wald = 12.17, P < 0.001). Relative to control plants, the survival of D. radicum and T. rapae decreased by more than 50%, when the host plants were previously exposed to foliar herbivory (Fig. 1), and the effect was qualitatively similar for root herbivore and parasitoid responses indicated by a non-significant interaction term (Wald = 0.49, P = 0.48). There was a significant effect of foliar herbivory on D. radicum and T. rapae adult size, measured as hind tibia length (Wald = 5.88, P = 0.02). Both herbivore and parasitoid adult sizes were reduced in the presence of foliar herbivores on the shared host plant (Fig. 2). Again, the negative effect of foliar herbivory did not differ between host and parasitoid (interaction term Wald = 0.02, P = 0.86). Development times of D. radicum and T. rapae were not significantly affected by foliar herbivory (Wald = 3.34, P = 0.07).
Fig. 1Mean (±SE) survival of D. radicum (herbivore) and T. rapae (parasitoid) on B. nigra plants that had been exposed to foliar herbivory (by P. brassicae) (shaded bars), and on control plants (open bars). Within herbivore and parasitoid, significant differences (P < 0.05) between treatments are indicated by different lettersFig. 2Mean (±SE) hind tibia length of D. radicum (herbivore) and T. rapae (parasitoid) on B. nigra plants that had been exposed to foliar herbivory (by P. brassicae) (shaded bars), and on control plants (open bars). Within herbivore and parasitoid, significant differences (P < 0.05) between treatments are indicated by different letters
Plants under both treatments demonstrated similar root biomass (F1,30 = 0.008, P = 0.92; Fig. 3a). Root-nitrogen levels also did not differ significantly between control plants and plants exposed to foliar herbivory (Table 1). Independent of the treatment, nitrogen levels were significantly lower in secondary than in primary roots (Table 1). Foliar herbivory significantly affected the levels of indole glucosinolates (neoglucobrassicin and glucobrassicin) in the roots (Table 1). In the presence of foliar herbivory, the levels of neoglucobrassicin (Fig. 4a) and glucobrassicin (Fig. 4b) significantly increased in both primary and secondary roots. Independent of the treatment, levels of neoglucobrassicin and glucobrassicin were significantly higher in secondary than in primary roots. Concentrations of gluconasturtin (Fig. 4c) and sinigrin (Fig. 4d) did not differ significantly between the roots of control plants and plants that had been exposed to foliar herbivory (Table 1). Independent of the treatment, gluconasturtin levels were significantly higher in primary than in secondary roots. Sinigrin levels did not differ significantly between primary and secondary roots.
Fig. 3Mean (±SE) root biomass (a) and percentage of nitrogen in primary and secondary roots (b) of Brassica nigra plants that had been exposed to foliar herbivory (by P. brassicae) (shaded bars) and in those of control plants (open bars )Table 1Approximate F-test (F and P values) for the fixed effects and variance component estimates from REML (restricted maximum likelihood); analysis of the effect of foliar herbivory (by P. brassicae) and root-type on nitrogen and glucosinolate levels of B. nigra rootsFactorsNitrogenNeoglucobrassicinGlucobrassicinGluconasturtinSinigrinFPFPFPFPFPFoliar herbivory (1)1.60.215.0<0.00115.3<0.0010.50.41.70.2Root-type (2)28.4<0.00128.5<0.00189.5<0.0014.570.030.0010.9Interaction (1.2)0.40.52.90.080.20.50.70.31.40.2Fig. 4Mean (±SE) levels of glucosinolates (μmol g−1 dry mass) (a neoglucobrassicin, b glucobrassicin, c gluconasturtin, d sinigrin) in primary and secondary roots of Brassica nigra plants exposed to foliar herbivory (by P. brassicae) (shaded bars) and in those of control plants (open bars). Within each root type, significant differences (P < 0.05) between treatments are indicated by different letters
Discussion
This study provides evidence that shoot-feeding insects, via systemic changes in the root quality of the shared host plant, can influence the development of root-feeding insects sharing the host plant. Moreover, the effects can be carried over at least one trophic level higher, affecting the performance of a parasitoid. We found that foliar herbivory was significantly correlated with a reduction in successful development of Deliaradicum and Trybliographarapae. Survival of the herbivore and its parasitoid was two to three times higher on plants that were undamaged above-ground than on plants that were previously exposed to foliar herbivory. In addition, when compared with those on control plants, newly emerged adult D. radicum and T. rapae were significantly smaller when the insects developed on plants that had been initially damaged by foliar herbivores. Several authors have argued that body size is the main target of selection in parasitoids and other insects, because it is correlated with life-history and demographic characters such as searching and mating efficiency, longevity, and fecundity (Godfray 1994; Harvey et al. 1994; Bezemer and Mills 2003; Harvey 2005). Consequently, our results reveal not only that D. radicum and T. rapae suffer from increased mortality on plants previously exposed to foliar herbivory compared with control plants, but that fitness of the surviving adults is also compromised.
In a recent study based on the same multitrophic system, we reported that root herbivory by D. radicum reduced the performance of the foliar feeder P. brassicae (Soler et al. 2005). However, several others found no significant relationship between root herbivory and the performance of above-ground herbivores (Moran and Whitham 1990; Salt et al. 1996; Hunt-Joshi and Blossey 2005), and yet others found a positive relationship (Masters and Brown 1992). These results clearly show that the effects of below-ground herbivores on their above-ground counterparts are likely to be association-specific, although this contrasts with the rather consistent negative effect thus far observed in most reciprocal studies of above-ground herbivory on below-ground insects (this study; Moran and Whitham 1990; Masters and Brown 1992; Salt et al. 1996; Tindall and Stout 2001; Hunt-Joshi and Blossey 2005). More work is clearly required to elucidate possible patterns in interactions between above- and below-ground systems, and to determine whether there are any clear patterns emerging from them.
We also found that the amount of root biomass did not differ significantly between the foliar-damaged and control plants, suggesting that the negative effects of above-ground herbivory by P. brassicae on the development of D. radicum and T. rapae were based on qualitative, rather than quantitative, changes in the root system. Because only three young caterpillars were allowed to feed from the foliage for a limited period of time, the physical amount of shoot tissue removed was negligible (R. Soler, personal observation). Changes in root biomass as a result of source–sink relationships within the plant are likely to occur when above-ground herbivore damage is much more extensive (Hunt-Joshi and Blossey 2005). Root nitrogen levels were also not significantly affected by foliar herbivory, and thus it is highly unlikely that changes in this important (and often limiting) primary plant compound were responsible for the observed effects.
However, levels of indole glucosinolates were significantly increased by about 30% in plants that had been exposed to foliar herbivores. Glucosinolates and their breakdown products, including indoles, have been shown to be involved in reducing plant quality for both generalist and specialist insect herbivores and nematodes (Li et al. 2000; Van Dam et al. 2005). Although indoles constituted only a small fraction of total glucosinolates in the plant (with sinigrin being by far the most prevalent), studies with other secondary compounds have shown that only trace amounts in the diet are required to exert strong effects on the development of herbivores and their parasitoids (Barbosa et al. 1986). Consequently, the negative relationship between above-ground herbivory and the development of D. radicum may be, at least partially, correlated with increased levels of indole glucosinolates in the roots of the shared host plant that were induced by feeding damage from P. brassicae larvae above ground.
It has been well established that allelochemicals in the herbivore’s diet can exhibit negative effects on the morphology, development, size, and survival of their predators and parasitoids (reviewed in Harvey 2005; Ode 2006). T. rapae is a koinobiont parasitoid of D. radicum and, therefore, after being parasitized, Delia larvae continue feeding and growing until the final larval instar has been reached. At this time, the developing parasitoid larvae begin destructive feeding and exponential growth (Harvey et al. 1994). At the end of the host’s larval development, allelochemicals that may be present in the hemolymph and other tissues, such as fat body, are rapidly consumed by the koinobiont parasitoid (Harvey 2005). Due to the tight linkage between host and koinobiont parasitoid development, in our study, increased mortality and reduced adult size observed in the T. rapae adults on plants that had been exposed to foliar herbivory could probably be attributed to a corresponding increased mortality and reduced size of its host D. radicum. Parasitoids, in particular, are highly susceptible to very small changes in the quality of the host’s internal biochemical environment (Harvey 2005). Other studies have shown that parasitoids can be more affected than their hosts by the quality of the host plant (Harvey et al. 2003; Soler et al. 2005). This appears not to be the case in our studied trophic chain, since we found comparable effects of foliar herbivory on the root herbivore and its parasitoid.
In summary, this study has reported that herbivore damage of plant shoots can have significant negative effects on the development of below-ground herbivores and their natural enemies. Combined with the results of a previous study based on the same system, we have demonstrated that these effects are largely reciprocal (Soler et al. 2005). Our research further highlights the importance of integrating the below-ground domain with above-ground systems in order to better understand the myriad of factors that shape the evolution, assembly, and functioning of communities and ecosystems (Wardle et al. 2005). Studies over larger spatial scales have already shown that above-ground herbivores can influence the community structure of the below-ground system and vice-versa (De Deyn and Van der Putten 2005; Wardle et al. 2004). Further studies, combining interactions between above-ground and below-ground communities in a multitrophic framework, and which seek to explore both processes and mechanisms, are required if we are to develop a better understanding of the many complex factors that influence community structure and function.

delia radicum
trybliographa rapae
glucosinolates
above-/below-ground interactions
plant–insect interactions


Children with cerebral palsy exhibit greater and more regular postural sway than typically developing children

Following recent advances in the analysis of centre-of-pressure (COP) recordings, we examined the structure of COP trajectories in ten children (nine in the analyses) with cerebral palsy (CP) and nine typically developing (TD) children while standing quietly with eyes open (EO) and eyes closed (EC) and with concurrent visual COP feedback (FB). In particular, we quantified COP trajectories in terms of both the amount and regularity of sway. We hypothesised that: (1) compared to TD children, CP children exhibit a greater amount of sway and more regular sway and (2) concurrent visual feedback (creating an external functional context for postural control, inducing a more external focus of attention) decreases both the amount of sway and sway regularity in TD and CP children alike, while closing the eyes has opposite effects. The data were largely in agreement with both hypotheses. Compared to TD children, the amount of sway tended to be larger in CP children, while sway was more regular. Furthermore, the presence of concurrent visual feedback resulted in less regular sway compared to the EO and EC conditions. This effect was less pronounced in the CP group where posturograms were most regular in the EO condition rather than in the EC condition, as in the control group. Nonetheless, we concluded that CP children might benefit from therapies involving postural tasks with an external functional context for postural control.
Introduction
Poor postural control has been suggested to underlie the delays and deviations in motor skill acquisition and development observed in children with cerebral palsy (CP) (e.g., Berger et al. 1984; Liao et al. 1997; Liao and Hwang 2003). In particular, children with CP encounter problems during static upright standing in altered sensory environments (Cherng et al. 1999; Rose et al. 2002) and when rapid weight shifts during standing are required, either in gait initiation (Stackhouse et al. 2007) or in reaction to external perturbations (Nashner et al. 1983; Woollacott and Burtner 1996).
Postural control is often assessed by means of posturography, that is, the quantitative analysis of centre-of-pressure (COP) trajectories as measured with a force platform. Several descriptive statistics of the COP time series, which are often derived by averaging out the assumed noisy or random character of postural sway, have been shown to change with various motor, sensory and cognitive processes involved in the control of standing (e.g., Horak 2006; Woollacott and Shumway-Cook 2002). In the past two decades, however, new concepts and methods for studying postural control have been introduced based on the assumption that the act of maintaining an erect posture may be viewed as a stochastic process (Collins and De Luca 1993; Newell et al. 1997; Riley et al. 1999; Frank et al. 2001). Based on these insights, new measures have been developed for examining the time-varying or dynamical characteristics of COP trajectories. These dynamical measures may be more informative with regard to changes in postural control with task constraints, aging or pathology than the more global summary statistics that have been typically employed for this purpose, or at least provide important additional information (see Baratto et al. 2002; Raymakers et al. 2005; Roerdink et al. 2006).
Recent research has suggested that the regularity of COP trajectories is a particularly revealing and theoretically important dynamical measure. As a case in point, Roerdink et al. (2006) found that COP trajectories were more regular (as indexed by reduced sample entropy) in stroke patients than in healthy elderly while COP trajectories became progressively less regular with recovery. These findings may be viewed in line with the notion of pathological regularity versus healthy complexity (e.g., Goldberger 1996, 1997). Moreover, when performing a secondary cognitive task COP trajectories became less regular (Roerdink et al. 2006). The latter finding was replicated in young healthy adults, albeit only in the more attention-demanding eyes closed condition (Donker et al. 2007). Based on these results, a direct relation was proposed between the regularity of COP time series and the amount of attention invested in postural control (or, inversely, between COP regularity and the degree of automatism of postural control; see Donker et al. 2007; Roerdink et al. 2006). In particular, the introduction of a secondary cognitive task withdraws attention from the regulation of posture (i.e., towards the performance of the attention-demanding secondary task), resulting in less regular COP trajectories. This interpretation is in line with the claim and corresponding findings of Wulf and colleagues that adopting an external focus of attention is beneficial for the performance and learning of motor skills, whereas an internal focus of attention (e.g., directing attention to one’s own body and bodily movements) can be detrimental as it may disrupt the ‘automatisms’ with which well-learned skills are normally performed (for a review see Wulf and Prinz 2001; see also Wulf et al. 2001; McNevin and Wulf 2002; McNevin et al. 2003).
When applied to CP children this insight may imply that their postural control may be improved by means of instructions or task conditions that direct their attention away from the regulation of posture itself to its consequences in the world. Providing CP children with concurrent visual feedback about postural sway may help create a more external focus of attention (i.e., the external consequences of postural sway become readily apparent via visual cursor movements). Visual feedback of postural sway provides a functional context for postural control (e.g., minimise cursor movements), which is likely to enhance the performance of the primary task (cf., Lin et al. 1998; Van der Weel et al 1991; Volman et al. 2002). For example, Volman et al. (2002) showed that the quality of reaching movements of the affected arm in children with spastic hemiparesis could be enhanced when reaching to press a light switch to turn on a light (task with functional context) compared to reaching to a marker (non-functional task). We therefore expected that postural control could benefit from postural visual feedback as it constitutes a task with a functional external context for postural control, inducing a more external focus of attention. Although postural visual feedback is sometimes used by physical therapists to train postural control and steadiness (i.e., the ability to maintain a given posture with minimal sway, Nichols 1997), evidence for this practice is limited (e.g., Rougier 2003; Ledebt et al. 2005). The recent conceptual and methodological developments in the analysis of COP trajectories alluded to in the preceding provide an alternative approach for studying the consequences of concurrent visual feedback for postural control and thus of its potential for possible therapeutic applications.
Motivated by this combination of theoretical and practical considerations, the aim of the present study was (1) to compare postural sway fluctuations of children with CP with that of typically developing (TD) children and (2) to investigate the effect of visual information on postural sway in CP children and in TD children. For this purpose, the availability of visual information was manipulated relative to standing with eyes open (EO condition) by means of visual deprivation (standing with eyes closed, EC condition) and external provision of COP feedback (FB condition). Two kinds of measures were used to analyse the COP trajectories recorded during those conditions, the one scale-dependent and the other scale-independent. The conventional, scale-dependent measures pertained to the ‘amount of sway’, whereas the more recent scale-independent measures pertained to the ‘regularity of sway’ (see Methods section for details). We hypothesised that (1) compared to TD children, CP children exhibit a greater amount of sway and more regular sway and (2) concurrent visual feedback (providing a functional external context for postural control, creating a more external focus of attention) decreases both the amount of sway and sway regularity in TD and CP children alike, while closing the eyes (increasing task difficulty through deprivation of visual information, promoting a less automatic mode of postural control) has opposite effects.
Methods
Participants
Ten children with congenital hemiplegia or cerebral palsy (CP children; six boys, four girls; mean age = 7 years, range = 5–11 years), reduced to nine in the analyses (see below) and nine typically developing children (TD children; five boys, four girls; mean age = 8 years, range = 5–11 years) without known motor impairments or movement-related disorders volunteered to participate in the experiment. All children and their parents gave their informed consent prior to participation. The experiment was carried out in compliance with the Helsinki Declaration and was endorsed by the VU University Medical Centre Amsterdam.
Procedure and apparatus
Children stood upright on a 1 m × 1 m custom-made strain gauge force plate1 with their arms hanging relaxed alongside the body. Their feet were placed parallel to the anterior–posterior axis of the force plate and the distance between the feet corresponded to the width of the pelvis. Children wore their own shoes, including ankle-foot ortheses and/or insoles to correct for leg-length discrepancies.
Children participated in three conditions that were presented in random order: standing upright with eyes open (EO condition), standing upright with eyes closed (EC condition) and standing upright with visual COP feedback (FB condition). As explained, the FB condition was introduced to provide an external functional context for postural control, creating a more external focus of attention. To this end, a 2.5 m × 2.5 m vertical screen was placed in front of the child at a distance of 1.3 m. On this screen the force plate was depicted as a 40 cm × 40 cm square onto which the COP was projected as a red dot. The children were asked to keep this dot within the target area, which consisted of a 4 cm × 4 cm square. Deprivation of visual postural sway information was effectuated by blindfolding the children in the EC condition. Trial duration was 60 s. Participants performed each condition once, with the proviso that, as part of a separate study, five CP children performed each condition twice (the first trial was used for further analyses). Because in the latter set of recordings trial duration was 30 s, the first 3,000 samples of all trials were used in the analyses to avoid differences in the reliability of the dependent measures. One CP child did not want to be blindfolded and was therefore excluded from further analyses, which rendered the number of CP children equal to the number of control subjects.
Data analysis
Prior to all analyses, the mean was subtracted from mediolateral and anterioposterior COP trajectories, which transformed the original time series into x and y time series, respectively. Subsequently, x and y time series were bi-directionally filtered (second-order low-pass Butterworth filter, cut-off frequency 12.5 Hz) and the resultant distance time series r was constructed using
(see Prieto et al. 1996), with i = 1, 2, 3,..., N and N indicating the total number of analysed samples in the COP time series (i.e., 3,000 samples).
The ‘amount of sway’ was quantified by means of two conventional, scale-dependent measures (see Prieto et al. 1996). First, the average COP distance to the origin of the mean-centred posturogram was determined by taking the mean of the r time series (i.e., mean amplitude rmean in mm). Second, sway path length (SP in mm) was determined by taking the sum of the distances between consecutive points in the conventional posturogram, using .
To examine the structure of COP trajectories in more detail, independent of its size or scale, x and y were normalised to unit variance by dividing those time series by their respective standard deviations σx and σy, resulting in a normalised posturogram. Subsequently, two scale-independent COP measures were quantified. First, the sway path of the normalised posturogram (SPn) was determined in a similar manner as described above for the conventional posturogram. Because the posturograms were normalised to its size, differences in SPn could only be the result of changes in the structure of the posturogram, with a larger SPn indicating a larger amount of ‘twisting and turning’ or ‘curviness’ in the COP trajectory (cf., Donker et al. 2007). Second, COP regularity was quantified by calculating the sample entropy (cf., Richman and Moorman 2000; Lake et al. 2002; see also Roerdink et al. 2006), which is a slightly improved version of the approximate entropy (cf., Pincus 1991). The sample entropy (SEn) is the negative natural logarithm of an estimate of the conditional probability that subseries (epochs) of length m (in our case, m = 3) that match pointwise within a specific tolerance also match at the next point (for a more formal and detailed explanation see Richman and Moorman (2000; Lake et al. 2002). In other words, smaller SEn values imply more regular COP time series, that is, a greater likelihood that sets of matching epochs in a time series will be followed by another match within a certain tolerance. On the other hand, highly irregular COP time series are characterised by the fact that sets of matching epochs tend to be followed by data samples of different values, resulting in larger SEn estimates. In the present study, SEn was quantified from the r time series, which was first normalised to unit variance. To optimise the choice of the tolerance for a given m (see also Roerdink et al. 2006) we applied the approach of Lake et al. (2002) and selected the median value of the optimal tolerance over all trials (in our case, 0.05). The code used for calculating sample entropy was obtained from PhysioNet2 (Goldberger et al. 2000).
To rule out the possibility that COP trajectories exhibited regular or deterministic patterns by chance, we compared the SEn estimates obtained for the COP trajectories to those obtained for surrogate data (cf., Theiler et al. 1992). We used time-randomisation to preserve the probability distribution of the data (e.g., mean, variance) while destroying the temporal correlations in the data, resulting in very large values for SEn. In contrast, phase-randomisation randomises the phases of the data in the Fourier domain but preserves the probability distribution of the data and its spectral power distribution (cf., Kantz and Schreiber 2004). Consequently, estimates of SEn for phase-randomised COP data should be somewhat increased, although less pronounced as for the time-randomised COP data.
Statistics
A repeated-measures analysis of variance (ANOVA) was conducted on all dependent variables with group as between-subject factor (two levels: CP and TD children) and condition as within-subject factor (three levels: EO, EC and FB conditions). The effect of randomisation was evaluated using a one-way repeated measures ANOVA with the factor randomisation (three levels: original, phase-randomised and time-randomised time series), including each individual time series as a sample. Effect sizes for main and interaction effects are reported as partial eta squared (εp2). Besides significant effects (P < 0.05), also tendencies towards significance (P < 0.10) are reported in view of the limited sample size. Paired-samples t-tests were used for post-hoc analyses of significant condition or randomisation effects. The analyses were performed using SPSS (SPSS, Inc., Chicago IL, USA).
Results
The results (F, P and εp2 values) of the group by condition ANOVA for the dependent COP variables are presented in Table 1. In Fig. 1, the group by condition effects are summarised for all dependent measures. CP children’s sway amplitude was greater than that of TD children (i.e., rmean = 12.8 mm and 5.7 mm, respectively, although this difference was strictly speaking not significant, P = 0.062). Neither a significant main effect of condition nor a significant group by condition interaction effect was observed for rmean. Furthermore, no significant main or interaction effects were observed for the sway path in the conventional posturogram (SP; mean 1,367 mm, standard error 108 mm), whereas the sway path in the normalised posturogram (SPn) differed significantly between groups and conditions in the absence of a significant interaction (see Table 1). Specifically, SPn was significantly larger for the TD children (328) than for the CP children (212). Moreover, post-hoc analysis revealed that concurrent visual feedback significantly increased SPn (310) compared to both standing with eyes open (SPn = 259: t(17) = 2.41, P < 0.05) and standing with eyes closed (SPn = 243: t(17) = 2.49, P < 0.05).
Table 1Main and interaction effects of group (between-subject factor, two levels: CP and TD children) and condition (within-subject factor, three levels: EO, EC and FB) on mean sway amplitude (rmean), sway path of the conventional posturogram (SP), sway path of the normalised posturogram (SPn) and sample entropy (SEn)GroupConditionInteractionF(1, 16)aP-valueεp2F(2, 32)aP-valueεp2F(2, 32)aP-valueεp2rmean4.010.0620.201.35ns0.081.11ns0.06SP1.86ns0.100.13ns0.010.13ns0.01SPn11.11<0.0050.415.12<0.020.242.04ns0.11SEn13.49<0.0050.465.53<0.010.263.230.0560.17ns not significantaIn case the assumption of sphericity was violated, the number of degrees of freedom was adjusted using the Huynh–Feldt method (corrected degrees of freedom are not listed here)Fig. 1Effects of group (CP and TD children, represented by black and grey bars, respectively) and condition (EO, EC and FB) on the ‘amount of sway’ (upper panels, mean sway amplitude rmean and sway path of the conventional posturogram SP) and on the ‘regularity of sway’ (lower panels, sway path of the normalised posturogram SPn and sample entropy SEn; note that lower SEn values imply more regular posturograms). Error bars represent the standard error
As can be seen in Table 1, the main effects of group and condition were both significant for sample entropy, while the group by condition interaction tended towards significance (P = 0.056). SEn was significantly larger for the TD children (1.01) than for the CP children (0.71). Moreover, post-hoc analysis revealed that the FB condition significantly increased SEn (0.98) compared to both standing with eyes open (SEn = 0.86: t(17) = 2.37, P < 0.05) and standing with eyes closed (SEn = 0.83: t(17) = 2.42, P < 0.05). The observed tendency of the group by condition interaction towards significance (see Fig. 1, lower right panel) may be due to the fact that for CP children SEn increased gradually over EO, EC and FB conditions (0.71, 0.73 and 0.76, respectively), whereas in the TD children SEn first reduced in the EC condition (0.93) and then increased for the FB condition (1.21) as compared to standing with eyes open (1.01).
The surrogate analysis revealed that SEn differed significantly with randomisation (F(2, 106) = 2915.90, P < 0.001, εp2 = 0.98). Post-hoc t-tests indicated that SEn differed significantly over all comparisons (all t(53) > 7.2, all P < 0.001), indicating that the regular or deterministic patterns observed in the original data did not occur by chance. SEn was on average (standard error) 0.89 (0.04), 1.06 (0.04) and 3.44 (0.02) for original, phase-randomised and time-randomised COP data, respectively.
Discussion
In the present study we compared posturograms of children with CP with those of TD children under three conditions. Across conditions, we expected the posturograms of CP children to reflect a greater amount of sway and more regular sway than those of TD children (Hypothesis 1). Furthermore, in line with the recently postulated relation between the amount of attention invested in posture and COP regularity, we expected that concurrent visual COP feedback, providing a functional external context for postural control leading to a more external focus of attention, would result in a decrease in both the amount of sway and sway regularity, whereas the EC condition, in which visual information is absent, would have opposite results (Hypothesis 2). The data were largely in agreement with both hypotheses, as will be discussed next. Furthermore, the finding that SEn estimates were significantly increased after time- and phase-randomisation of the original data ruled out the possibility that the regular or deterministic properties observed in the original data occurred by chance.
CP children exhibit greater and more regular sway than TD children
Posturogram characteristics of children with CP differed markedly from those of TD children (see Fig. 1). As expected (Hypothesis 1), the CP children exhibited a larger amount of sway than the TD children. In particular, a near significant (P = 0.062, accompanied by a large effect size) increment in mean sway amplitude (rmean) was observed in the CP children compared to that in the TD children (see Table 1 and Fig. 1). Although, strictly speaking, not significant due to the large interindividual variations, this effect suggests that ‘postural steadiness’ is reduced in CP children, consistent with previous results on balance control in CP children (e.g., Cherng et al. 1999; Ferdjallah et al. 2002; Liao and Hwang 2003; Rose et al. 2002). An interesting and unexpected finding was that the total COP excursion (i.e., SP) did not differ significantly between CP and TD children. In combination with the apparent increase in sway amplitude, this finding hints at the presence of marked differences in the dynamical structure of posturograms between CP and TD children. To expose those differences, we focused on the sway regularity using two scale-independent measures. Scale-independence was achieved by normalising the data to unit variance. As expected, sway path length of the normalised posturogram was significantly reduced in CP children, indicating less ‘twisting and turning’ in the posturogram (see also Donker et al. 2007). Relatedly, resultant COP trajectories of the CP children were more regular than those of the TD children, as indexed by significantly lower sample entropy values. Recently, increased regularity in COP trajectories has been reported for a variety of pathological conditions, including athletes with a sports-related cerebral concussion (Cavanaugh et al. 2005 using approximate entropy), patients with Parkinson’s disease (Schmit et al. 2006 using recurrence quantification analysis) and stroke patients (Roerdink et al. 2006 using sample entropy). These findings are in line with the more general notion of ‘dynamical diseases’ (Glass and Mackey 1988; Belair et al. 1995) and the ‘pathological regularity versus healthy complexity’ hypothesis (Goldberger 1996, 1997; Goldberger et al. 2002; Kyriazis 2003; Lipsitz 2002), according to which less ‘complex’ or more ‘regular’ physiological time series reflect less effective physiological control. In a similar vein, the observed increased COP regularity in CP children may be viewed as the dynamical signature of poor postural control.
Effect of visual information
We further expected that the ‘amount of sway’ would be reduced in the presence of concurrent visual COP feedback, providing a supposedly beneficial functional external context for postural control (cf., Van der Weel et al. 1991; Volman et al. 2002; Wulf and Prinz 2001), as opposed to deprivation of visual information in standing with eyes closed. However, no significant main effects of condition were found for the scale-dependent COP measures (i.e., mean amplitude and sway path, see Table 1). This unexpected result is in line with some recent studies showing that the use of visual COP feedback to facilitate quiet standing has no effect on conventional COP parameters in TD children (Lebiedowska and Syczewska 2000) and healthy elderly and stroke patients (Dault et al. 2003) alike. These findings suggest that participants may require some practice to benefit from visual COP feedback. This may explain why, in spite of the apparent lack of immediate effects, Ledebt et al. (2005) found that balance training with visual feedback improved CP children’s quiet standing ability as well as their functional limits of stability as assessed by a weight-shifting task.
In contrast to the results obtained for the ‘amount of sway’ under the various conditions, the scale-independent measures pertaining to the ‘regularity of sway’ did show significant differences between the FB condition and the EO and EC conditions. This indicates that the dynamical structure of the posturogram must have been different in the FB condition compared to the EO and EC conditions, which was precisely what we anticipated when formulating our expectation that sway would be less regular in the FB condition (i.e., longer sway path of the normalised posturogram and higher sample entropy) and more regular in the EC condition (Hypothesis 2). Sway path of the normalised posturogram was indeed significantly longer with visual feedback than for standing with eyes open  or closed, indicating more twisting and turning (see also Donker et al. 2007). In parallel, sample entropy increased with concurrent visual feedback compared to standing with eyes open and eyes closed. Thus, in spite of the fact that the ‘amount of sway’ did not change significantly over conditions, the observed changes in ‘regularity of sway’ were as expected: sway was more regular in the EC condition and less regular in the FB condition.
Our expectations concerning the ‘regularity of sway’ with conditions were derived from the proposed direct relation between the amount of attention invested in posture and the regularity of COP trajectories (cf., Donker et al. 2007; Roerdink et al. 2006). This interpretation is in line with the insight of Wulf and colleagues that adopting an external focus of attention, i.e., a focus on the consequences of one’s movement in the external world, is beneficial for the performance and learning of motor skills (McNevin et al. 2003; McNevin and Wulf 2002; Wulf and Prinz 2001; Wulf et al. 2001). Specifically, we expected that providing CP children with concurrent visual feedback about postural sway would help shift the focus of attention to the external consequences of postural sway (i.e., cursor movements) by constituting a functional external context for postural control (e.g., minimise cursor movements). Providing a functional context for the task at hand generally enhances its performance (e.g., Lin et al. 1998; Van der Weel et al. 1991; Volman et al. 2002). In line with these notions, we expected that standing with concurrent visual feedback, a functional task inducing a more external focus of attention, would lead to less regular sway compared to the EO condition, whereas standing with eyes closed would lead to more regular sway in the EC condition compared to the EO condition because task difficulty increased due to the absence of visual information. This predicted pattern of results was only found for the TD children and not for the CP children (see lower right panel of Fig. 1). As it turned out, COP regularity in the CP children gradually decreased from the EO condition (most regular), via the EC condition, to the FB condition (least regular). As a result of this difference in group behaviour, a strong tendency towards a significant group by condition interaction on sample entropy was found. From this latter observation one could tentatively infer that CP children’s posture actually improved when standing with eyes closed compared to standing with eyes open. In support of this somewhat counter-intuitive inference, Rose et al. (2002) showed that the percentage of CP children with abnormal sway characteristics did not differ between EO and EC conditions, while the number of sway path outliers even reduced when standing with eyes closed in that particular CP group. Following a similar line of interpretation, Newell et al. (1997) suggested that very young children may create self-induced perturbations when using visual information in controlling posture, a phenomenon which may be particularly prominent in CP children given that the development of proper neural control mechanisms is strongly delayed compared to TD children (viz., Forssberg 1999). From the opposite SEn results between CP and TD children with eyes open and eyes closed it is fair to conclude that postural control in CP children is organised differently than in TD children, especially with regard to the use of normal sway-induced visual information.
It has been suggested that creating an external focus of attention would allow for a more automatic control of movements (e.g., Donker et al. 2007; McNevin and Wulf 2002; Roerdink et al. 2006), which is often found to be more efficient (e.g., Blanchard et al. 2005; McNevin et al. 2003). Although no significant main effect of condition on mean amplitude was found, the finding that during quiet standing with visual COP feedback sample entropy increased (i.e., less regularity in the posturogram) in both TD and CP children supports this idea. Moreover, it corroborates the suggestion that visual COP feedback may be advantageous when seeking to improve postural control, although it must be emphasised again that it requires training (see Ledebt et al. 2005).
Conclusion
The findings of the present study indicate that postural control in CP children is deteriorated compared to TD children, most likely due to a slowed development of neural control mechanisms in CP children. Moreover, visual deprivation (EC condition) influenced sway characteristics differently in CP and TD children, testifying to the altered nature of postural control in CP children. In line with the proposed relation between the amount of attention invested in posture and COP regularity, we found in CP and TD children alike that, compared to the EO and EC condition, COP trajectories were less regular in the presence of visual COP feedback, corresponding to a functional context mediated external shift in the focus of attention. Future studies should examine the merits of adopting an external focus of attention to enhance postural control in CP children in training or therapy, for example by providing visual COP feedback leading to a posture specific functional task or by introducing an attention-demanding secondary cognitive task.

cerebral palsy
regularity
postural control
attention
centre-of-pressure trajectories


Gastrointestinal Endoscopic Terminology Coding (GET-C): A WHO-Approved Extension of the ICD-10

Technological developments have greatly promoted interest in the use of computer systems for recording findings and images at endoscopy and creating databases. The aim of this study was to develop a comprehensive WHO-approved code system for gastrointestinal endoscopic terminology. The International Classification of Diseases, 10th edition (ICD-10), and the ICD-10 clinical modification (ICD-10-CM) were expanded to allow description of every possible gastrointestinal endoscopic term under conditions defined by the WHO. Classifications of specific gastrointestinal disorders and endoscopic locations were added. A new chapter was developed for frequently used terminology that could not be classified in the existing ICD-10, such as descriptions of therapeutic procedures. The new extended code system was named Gastrointestinal Endoscopic Terminology Coding (GET-C). The GET-C is a complete ICD-10-related code system that can be used within every endoscopic database program for all specific endoscopic terms. The GET-C is available for free at http://www.trans-it.org/.
Introduction
Technological developments and the introduction of hospital information systems have greatly promoted interest in the use of computer systems for recording findings and images at endoscopy. Several database systems have been developed for this purpose, most working only as a report generator. These systems are, however, hampered by the lack of a specific code system for endoscopic diagnoses and terminology. As a result of this shortcoming, the composition of reports and storage of data differ considerably between systems. Systems use different database structures and variable terminology and are thus not compatible or comparable.
The International Classification of Diseases (ICD) is designed to promote international comparability in the collection, processing, classification, and presentation of mortality statistics. This ICD is developed, published, and maintained by the World Health Organization (WHO). The system is, in its current setting, not applicable for endoscopy, as it does not include descriptive terminology. However, endoscopic findings are classified according to their appearance. Adequate description of this appearance in uniform terminology is essential for the interpretation of endoscopy reports and allows important conclusions to be made with respect to therapy and prognosis. Thus it is important to uniformly store and code endoscopic findings. This is, however, hampered by the lack of a specific, uniformly applicable code system for endoscopic terminology and findings. In addition, only about 80% of report systems are able to use a code in their database [1].
Different coding systems for medical data are being used. The ICD, 9th edition (ICD-9), and the clinical modification of the ICD-9 (ICD-9-CM) have already been used and proven to be of value in a specific and defined gastrointestinal endoscopic setting [2]. The ICD has been revised periodically to incorporate changes in the medical field. The tenth edition (ICD-10) differs from the ninth edition in several ways, although the overall content is similar. First, the ICD-10 has alphanumeric categories rather than numeric categories. Second, some chapters have been rearranged, some titles changed, and conditions have been regrouped. Third, the ICD-10 has almost twice as many categories as the ICD-9. The ICD-10 has been available since 1992 and was translated into Dutch in 1997 [3]. Other medical specialities, such as oncology and dentistry, have produced an extended code system for their field of interest based on the ICD-10 [4].
The aim of this project is to develop a comprehensive code system for gastrointestinal endoscopic terminology, based on the widely accepted ICD-10 code system, that can be used in any gastrointestinal endoscopic information system.
Methods
As a basis for the new coding system the latest edition of the ICD, the ICD-10, was chosen. The reason for choosing this code system was that a predecessor has already been in use for some gastrointestinal endoscopic databases [2]. In addition, the current version of the ICD is now accepted in a majority of countries throughout the world [5].
Extensions of the ICD-10 are made according to the recommendations of the WHO, without changing the structure of the ICD-10. The first four characters are never changed, but one or more characters are added behind these first four descriptors. In this way it is always possible to delete the extension to come back to the original ICD-10. We used the Dutch translation of the ICD-10. Also, the draft version of the ICD-10-CM of the National Center for Health Statistics (NCHS) was studied, which is available on the Internet [6]. Conflicts with this ICD-10 CM system were avoided, to rule out coding conflicts.
A working group, the TRANS.IT working group, was founded, comprised of representatives from two academic hospitals (Utrecht, Amsterdam) and four general hospitals. This working group used the Endobase III system (Olympus). In this system, the endoscopist can choose among three methods of writing reports. Besides the Minimal Standard Terminology (MST) [7], text-blocks and standard reports are also available. A standard report is a complete report based on a diagnosis or a combination of diagnoses. With text-blocks, different portions of the text are combined to compose a complete report. These two variants enable more rapid generation of reports and are well accepted and widely used in the Netherlands [8].
In the TRANS.IT project group, which was founded as a peer reference group, standard reports, text-blocks, and linkage to the new code system were discussed.
A list of every endoscopic finding, intervention, or complication described using one of the three methods of report writing available for TRANS.IT users was generated. All items on this list were linked to a specific code.
Results
We first generated a list of the different fields necessary for evaluation of endoscopic data (Table 1). The program automatically generated the data during the composition of endoscopic reports. All these fields are necessary to generate a comprehensive anonymous database with endoscopic information for extensive research. In addition, demographic data such as gender and age of patients and specialty of referring doctor are recorded.Table 1Different fields that need a specific code in endoscopic information systemsReason for endoscopyMedication useSedation and medication during endoscopyPreparationProcedure for investigationEndoscopic diagnosis/findingsTherapeutic and diagnostic interventionsHistology resultsTherapy startedAdvice to referring doctorComplications
We included all available standard reports, text-blocks, and diagnoses of Minimal Standard Terminology (MST) accepted by the TRANS.IT group. The endoscopic findings, interventions, and complications were extracted and linked to a specific code. In this way, a total of 316 standard reports and 1571 text-blocks were coded, to assure coding of every item within this project.
In total, 2593 different items were extracted and received a specific code. Of these items, 630 (24%) could be coded with the existing ICD-10. Thus, 1963 new codes were required and added to the ICD-10 system, in order to be able to specifically code every endoscopic term.
The ICD-10 used was originally designed for mortality and discharge statistics. The problem with that design is that the structure used in the ICD-10 is not very detailed. This is true especially for gastrointestinal endoscopic terms, which do not always include a mortality risk but, most of the time, descriptive items essential for prognosis and therapy. For example, specific descriptions of peptic ulcers are relevant for determination of outcome risks, therapy, and prognosis. We therefore introduced the Forrest classification for description of gastric and duodenal ulcers [9]. We thus, for instance, changed the diagnosis K25.2 (acute gastric ulcer with both hemorrhage and perforation) to K25.21 (acute gastric ulcer with spurting bleeding and perforation; Forrest Ia) in the Gastrointestinal Endoscopic Terminology Coding (GET-C; Table 2).Table 2Comparison of ICD-10 and GET-C codes for gastric ulcerICD-10DescriptionGET-CDescriptionK25.0Gastric ulcer, acute with hemorrhageK25.0Gastric ulcer, acute with hemorrhageK25.01Gastric ulcer, acute with spurting bleeding (Forrest Ia)K25.02Gastric ulcer, acute with nonspurting active bleeding (Forrest Ib)K25.1Gastric ulcer, acute with perforationK25.1Gastric ulcer, acute with perforationK25.2Gastric ulcer, acute with both hemorrhage and perforationK25.2Gastric ulcer, acute with both hemorrhage and perforationK25.21Gastric ulcer, acute with spurting bleeding and perforation (Forrest Ia)K25.22Gastric ulcer, acute with nonspurting active bleeding and perforation (Forrest Ib)K25.3Gastric ulcer, acute without hemorrhage or perforationK25.3Gastric ulcer, acute without hemorrhage or perforationK25.31Gastric ulcer, acute with visible vessel (Forrest IIa)K25.32Gastric ulcer, acute nonbleeding with overlying clot (Forrest IIb)K25.33Gastric ulcer, acute with hematin-covered basis (Forrest IIc)K25.34Gastric ulcer, acute with clean ulcer ground (Forrest III)K25.5Gastric ulcer, chronic or unspecified with perforationK25.5Gastric ulcer, chronic or unspecified with perforationK25.6Gastric ulcer, chronic or unspecified with both hemorrhage and perforationK25.6Gastric ulcer, chronic or unspecified with both hemorrhage and perforationK25.61Gastric ulcer, chronic or unspecified with spurting bleeding and perforation (Forrest Ia)K25.62Gastric ulcer, chronic or unspecified with non- spurting active bleeding and perforation (Forrest Ib)K25.7Gastric ulcer, chronic without hemorrhage or perforationK25.7Gastric ulcer, chronic without hemorrhage or perforationK25.71Gastric ulcer, chronic with visible vessel (Forrest IIa)K25.72Gastric ulcer, chronic non-bleeding with overlying clot (Forrest IIb)K25.73Gastric ulcer, chronic with hematin-covered basis (Forrest IIc)K25.74Gastric ulcer, chronic with clean ulcer ground (Forrest III)K25.9Gastric ulcer, unspecified, without hemorrhage or perforationK25.9Gastric ulcer, unspecified, without hemorrhage or perforationK25.91Gastric ulcer, unspecified, with visible vessel (Forrest IIa)K25.92Gastric ulcer, unspecified, nonbleeding with overlying clot (Forrest IIb)K25.93Gastric ulcer, unspecified, with hematin-covered basis (Forrest IIc)K25.94Gastric ulcer, unspecified, with clean ulcer ground (Forrest III)
Besides such an adaptation of the ICD-10 system, endoscopy is still developing and new terms and endoscopic techniques are continuously being created. For example, new disease classifications are being introduced from time to time, such as the semirecent Los Angeles classification for reflux esophagitis [9, 10].
For several fields, there was no ICD-10 code available, and the item thus could not be categorized under an existing ICD-10 code. For example, the procedure for investigation and interventions could not be covered within the ICD-10 or even the ICD-10-CM system. Because these items are essential for good analysis of endoscopic data, a new chapter with the same structure as the ICD-10 was developed. The items in this new chapter start with the letters OG. We chose to categorize therapeutic interventions in this new chapter also because new therapies are developed frequently and can now be adapted.
Adaptations were made in different chapters of the ICD-10. In Chapter 1, Certain Infectious and Parasitic Diseases (A00–B99), the exact locations in the gastrointestinal tract of some specific infections were added. In Chapter 2, Neoplasms (C00–D48), besides the exact locations in the gastrointestinal tract, the endoscopic characteristics of polyps were described and coded in more detail. It is important to register whether a polyp is pedunculated, sessile, or flat or has a villous endoscopic aspect. Also, the number of polyps found in a specific part of the intestine must be coded, because of important diagnostic and therapeutic options for patients and the follow-up of these patients.
In Chapter 9, Diseases of the Circulatory System (I00–I99), hemorrhoids and varices were described according to a classification. Different gradings of protrusion were used for hemorrhoids. Paquet’s endoscopic classification for esophageal varices was coded [11].
Most changes were, however, made in Chapter 11, Diseases of the Digestive System (K00–K93). The description of esophagitis was divided into different origins and severity. Gastric and duodenal ulcers were coded according to the Forrest classification and their specific location in the stomach or duodenum. Gastritis and duodenitis were coded according to their specific location and the endoscopically suspected cause. Inflammatory bowel diseases were coded according to their endoscopic severity and location. Some complications related to gastrointestinal procedures were coded in more detail.
In Chapter 18 symptoms, signs, and abnormal clinical and laboratory findings that are an indication for endoscopic investigations were coded in more detail. In Chapter 21 postoperative situations important for gastrointestinal endoscopic investigations such as gastric and colon operations were extensively coded.
In the new, thirteenth chapter of the GET-C, about 446 new codes were generated. These codes start with the letters OG. The first part of this chapter includes coding of various indications for endoscopy that could not be categorized in the ICD-10. The second part consists of specific codes for detailed locations in the gastrointestinal tract. The third part includes procedures, which are divided into diagnostic and therapeutic procedures. Diagnostic procedures include, for example, sampling of histology and culture specimens. Examples of therapeutic procedures are different kinds of polypectomies, endoscopic mucosal resections, placement of endoprotheses, and dilatation of stenoses. Another aspect of these therapeutic interventions was used for the management of gastrointestinal bleeding such as injection therapy with or without coagulation, band ligations, and clipping. Preparation and procedure for the endoscopic examination are also coded in this chapter.
The extensions of the GET-C were checked by the Dutch translation board of the ICD-10 to preclude any conflicts between the two code systems.
Discussion
The increased use of computer systems in health care and the need for communication between these systems necessitate the availability of generally accepted code systems. Good coding provides epidemiological information for research purposes. Coding is of importance for hospitals and professionals because most of the financial systems used in health care are based on different codes. In addition, good coding makes statistical analysis of different diagnoses and collection of rare diagnoses easier. With an internationally accepted code, it is possible to compare and share information in one field of interest. Most currently used coding systems are regional or national. Only some coding systems, such as the ICD-10, are translated into different languages and used in different countries.
For endoscopic report writing and endoscopic databases, different systems have been developed. These systems are now being used at many hospitals. We used the Endobase III system from Olympus Europe in our project to compose reports and record different codes. The system runs as a network version with different workstations as well as a stand-alone unit.
The Endobase III system enables the generation of reports via three pathways; in addition to standard reports and text-blocks, the latest translated version of the MST is also used to compose an endoscopic report. Thus it is essential that all differently generated data are coded in the same way to enable analysis of the data anonymously. In this system, all standard reports and text-blocks are linked to one or more specific GET-C codes. The choice of a standard report or text-block leads directly to the recording of the correct GET-C code in the Endobase III database. Due to the structure of the MST, the automatic link for it is more complex to realize. We chose to link the diagnoses with the GET-C code, which is separately selected within the MST by the endoscopist at the end of the report. Automatic linking is essential to ensure correct and complete selection of codes and to make the system workable for endoscopists.
In the TRANS.IT project, an anonymous central database of endoscopic investigations was built. In this central database, only coded data instead of free text can be collected, for privacy reasons. After 3 years of use, a database of about 120,000 investigations using the same coding system has been built by this working group. The GET-C system allows the encoding of any data collected during endoscopic investigations and recorded in any endoscopic database. By extending the ICD-10 with respect to the structure developed by the WHO, it is always possible to extract the original ICD-10 code from the GET-C. Thus, it is possible to link the endoscopic database with other health-care systems throughout the world.
Because endoscopy is an evolving medical specialty, new techniques are continuously becoming available. These require new codes, which will be discussed within the TRANS.IT project.
The Dutch Association of Gastroenterologists has accepted the GET-C. The GET-C will be available for use in other systems and was discussed at the WHO Family of International Classifications Network meeting in October 2004 [12]. The GET-C is available for free at http://www.trans-it.org. We hope that this coding system will help to make endoscopic databases and endoscopic report writing programs more meaningful.

international classification of diseases