Multiscale Drivers of Water Chemistry of Boreal Lakes and Streams

The variability in surface water chemistry within and between aquatic ecosystems is regulated by many factors operating at several spatial and temporal scales. The importance of geographic, regional-, and local-scale factors as drivers of the natural variability of three water chemistry variables representing buffering capacity and the importance of weathering (acid neutralizing capacity, ANC), nutrient concentration (total phosphorus, TP), and importance of allochthonous inputs (total organic carbon, TOC) were studied in boreal streams and lakes using a method of variance decomposition. Partial redundancy analysis (pRDA) of ANC, TP, and TOC and 38 environmental variables in 361 lakes and 390 streams showed the importance of the interaction between geographic position and regional-scale variables. Geographic position and regional-scale factors combined explained 15.3% (streams) and 10.6% (lakes) of the variation in ANC, TP, and TOC. The unique variance explained by geographic, regional, and local-scale variables alone was <10%. The largest amount of variance was explained by the pure effect of regional-scale variables (9.9% for streams and 7.8% for lakes), followed by local-scale variables (2.9% and 5.8%) and geographic position (1.8% and 3.7%). The combined effect of geographic position, regional-, and local-scale variables accounted for between 30.3% (lakes) and 39.9% (streams) of the variance in surface water chemistry. These findings lend support to the conjecture that lakes and streams are intimately linked to their catchments and have important implications regarding conservation and restoration (management) endeavors.
Introduction
Surface water chemistry is regulated by a complex suite of processes and mechanisms operating at varying spatial and temporal scales. Early work by lake ecologists focused on the importance of geographic position as a strong predictor of lake water chemistry. For instance, in the early 1900s, Thienemann (1925) and Naumann (1932) developed lake trophic classification schemes that basically recognized differences between lowland, nutrient rich (eutrophic) and alpine, nutrient poor (oligotrophic) ecosystems. Although lake ecologists were early to appreciate the importance of adjacent land type on lake-water chemistry, stream ecologists have addressed the terrestrial–aquatic linkage concept more formally, with streams being regarded as “open systems that are intimately linked with their surrounding landscapes” (e.g., Hynes 1975). However, lake ecologists have recently revisited the landscape position hypothesis and formalized paradigms that recognize more explicitly the importance of landscape position and its significance for describing among-lake variance (e.g., Kratz and others 1997; Soranno and others 1999; Riera and others 2000).
The surrounding landscape (catchment) with its distinct geology, hydrology, and climate clearly influences the physico-chemical features of a specific water body (e.g., Omernik and others 1981; Osborne and Wiley 1988; Allan 1995; Kratz and others 1997; Soranno and others 1999; Riera and others 2000), and several studies have highlighted the links between surface water chemistry and catchment characteristics, particularly in relation to sensitivity to nutrient enrichment and acidification (Vollenweider 1975; Sverdrup and others 1992; Hornung and others 1995). Indeed, water chemistry, both within and among lakes or streams, is considered to be driven by factors acting on both regional and local scales. Regional factors such as climate, geology and weathering are interrelated with other factors such as soil type and land cover/use, whereas local factors, like the input and retention of organic matter, are related to the vegetation type and topographical relief. Hence, a priori, a close linkage is expected between regional- and local-scale factors. Geographic proximity alone is, however, often not sufficient to predict the physical and chemical characteristics of individual streams or lakes, as differences in external processes such as stream hydrology or lake morphometry and water retention time as well as internal processes such as nutrient cycling, and strengths of interactions with the surrounding landscape may singly or in concert confound the importance of regional-scale factors.
Although a number of studies have addressed the importance of land use/type on surface water chemistry, few studies have simultaneously focused on the importance of local and regional factors as determinants of surface water chemistry, and fewer still have addressed the similarities and differences of lake and stream ecosystems. To our knowledge, only one study (Essington and Carpenter 2000) has simultaneously studied the response of stream and lake ecosystems. These authors showed that streams and lakes were surprisingly similar in nutrient cycling, in particular when adjustments were made for water residence time. By concurrently studying stream and lake ecosystems, we hope to better our understanding of the processes and mechanisms that drive surface water chemistry in these different, but certainly not ecologically isolated ecosystems.
We hypothesize that both streams and lakes are strongly linked to the surrounding landscape, and that spatial variation in surface water chemistry is regulated by non-mutually exclusive factors acting on various hierarchical scales depending on landscape type and/or geographic position. Here, we study the effect of regional and local-scale factors on three commonly measured water chemical variables. Acid neutralizing capacity (ANC) was selected to indicate the effect that catchment geology and weathering might have on buffering capacity. Total phosphorus (TP) was selected for its key role in driving ecosystem productivity and because it is biologically active (i.e., is expected to decrease along, e.g., lake chains). Finally, total organic carbon (TOC) was used as a surrogate measure of the importance of allochthonous input from the boreal catchments. The sites used in this study are often natural brown-water systems, with high contents of humic substances.
We attempted to (1) identify and quantify possible sources of variation in surface water chemistry of boreal streams and lakes, (2) determine which environmental factors and which spatial scales are most important in determining the surface water chemistry of boreal streams and lakes, and (3) determine similarities/differences in the factors driving stream/lake water chemistry.
Methods
Study Site
The data set used in this study consists of 390 streams and 361 lakes sampled as part of the Swedish national stream and lake survey in autumn 2000 (Johnson and Goedkoop 2000; Wilander and others 2003) (Fig. 1). A number of factors suggested that this dataset was sufficiently robust for examining among-site similarities/dissimilarities in surface water chemistry of boreal streams and lakes. Firstly, streams and lakes were selected randomly; thus, the samples should be representative of the population of streams and lakes sampled. In selecting lakes, only lakes with surface areas >4 ha were included, and two size classes were used for stratifying stream sites (catchment area classes of 15 to 50 and 50 to 250 km2). Because we were interested in obtaining a depth-integrated measure of surface water chemistry, lakes were sampled during autumn turnover. Hence, sampling started in the northernmost parts of the country and progressed southwards. A more detailed description of stream and lake selection is given in Wilander and others (2003). In this study, we were interested in understanding the effects of local and regional-scale variables on the expected natural variability of selected water chemistry variables. Thus, sites deemed to be affected by liming, acidification (lakes: critical load exceedence of S and N > 0; Rapp and others (2002)) and agriculture/silviculture (catchments with more than 25% defined as arable and affected by clear-cutting, respectively) were not included in this dataset.
Fig. 1Location of the 361 lakes and 390 streams used to assess the influence of geographic position, and regional and local scale factors on surface water chemistry
The streams and lakes can be classified as relatively small (mean stream width = 5 m; mean lake area = 3.27 km2), nutrient poor, ranging from clear to brownwater ecosystems (mean stream abs 420 nm = 0.188; mean lake abs 420 nm = 0.149). The streams and lakes were distributed fairly evenly across the country. Streams were generally situated at a somewhat lower altitude than lakes (201 m a.s.l. for streams and mean altitude = 331 m a.s.l. for lakes). The catchment area of streams was also smaller (mean catchment area = 64 km2) than that of lakes (257 km2), because streams with catchments >250 km2 were not included in the national stream survey.
Water Chemistry
A single, midstream or midlake (approximately 0.5 m depth) water sample was collected in autumn 2000. All water chemistry analyses were done by the SWEDAC (Swedish Board for Accreditation and Conformity Assessment) certified laboratory at the Department of Environmental Assessment, Swedish University of Agricultural Sciences following international (ISO) or European (EN) standards when available. ANC is a measure of the buffering ability of lakes and streams against strong acid inputs. This metric was chosen because it includes humic substances and compensates for their natural variation, i.e., the effect of acid deposition is more pronounced than in other acidification indicators such as pH or sulfate concentration.
Independent Variables
During sampling, sites were classified according to (aquatic) substratum particle size and vegetation; six substrate classes (ranging from silt/clay to block), two classes of detritus (coarse and fine), and 10 classes of riparian land use and vegetation were classified using four categories as: 0%, <5%, 5–50%, and >50% coverage (Table 1). For streams, 50-m reaches (sampling site) of relatively homogeneous substratum were chosen, and the riparian vegetation designated at a 5-m-wide zone on both sides of the sampling site was classified as above. For lakes, 10-m long and 5-m wide littoral areas of relatively homogeneous substratum were chosen and riparian vegetation, designated at a 50-m long and 5-m wide shoreline zone, was classified as above.
Table 1Dependent and independent variables used in RDAVariableUnitLakes (N = 361)Streams (N = 391)a) DependentChemistryAcid neutralizing capacity (ANC)meq l−13.36 (0.09−0.74)0.51 (0.15−0.99)Total phosphorus (TP)μg l−113.17 (2−28)27.42 (2−67)Total organic carbon (TOC)mg l−19.13 (2.02−16.6)10.57 (2.2−21.08)b) IndependentExplained variabilityGeographic positionLakesStreamsLatitudeDecimal degreesAltitudem a.s.l.18.5%(2)2.7%(3)Ecoregions*Dummy variable  Arctic/alpineDummy variable  Northern borealDummy variable  Southern borealDummy variable  BoreonemoralDummy variable  NemoralDummy variableRegional factors  Mean annual discharge (Q)m3 s-11.3%(5)  Wet & Dry NHx deposition  Wet & dry non-seasalt Mg depositionCatchment land use/cover  Urban areas%  Forested areas%  Alpine treeless land cover%55.4%(1)17.3%(2)  Glacier%  Open freshwater bodies%  Marsh/mires%  Arable land%4.6%(3)68%(1)  Pasture%  Alpine forested areas%Local factorsPhysical properties of sample site  Stream width mM2.7%(4)  Lake areakm21.5%(5)  Water temperature°CAquatic substrate**Classified 0−3  Boulder (>250 mm)Classified 0-3  Block (200–250 mm)Classified 0-3  Cobble (60–200 mm)Classified 0-3  Pebble (20–60 mm)Classified 0-3  Silt/clay (0.02 mm)Classified 0-3  Coarse detritusClassified 0-3  Floating leaved vegetationClassified 0-34.6%(4)  Fine leaved submerged vegetationClassified 0-3  PeriphytonClassified 0-3  Fine dead woodClassified 0-3Riparian land use/cover  Deciduous forestClassified 0-3  HeathClassified 0-3  Arable landClassified 0-3  AlpineClassified 0-3  PastureClassified 0-3  MireClassified 0-3  Canopy coverClassified 0-3a) Chemistry variables (n = 3) with mean values and 10th and 90th percentiles in parentheses. b) Environmental variables (n = 38), divided into three subsets, included in the analyses. Also shown are the first five variables (explained variability in %) that could best explain the variability in ANC, TP, and TOC, using RDA and stepwise forward selection with the order of selection shown in parentheses. Note: the middle boreal ecoregion was insignificant in the Monte Carlo permutation test and excluded from the analysis*Six major ecoregions according to the Nordic Council of Ministers (1984)**Classified as percent coverage where no coverage 0 = 0%, very low coverage 1 = <5%, medium coverage 2 = 5–50%, high coverage 3 = >50%
Catchments were classified as percentage land use/vegetation cover according to the same land use categories used for riparian zones. Hence, catchment land use/cover ranged from 0% (all classes) to 100%. Thereby, maximum urban areas in catchments were 10.2% (lakes) and 26.3% (streams), forested areas covered 99.8% in both lake and stream catchments, and alpine treeless cover was very high with 99.7% (lakes) and 99.9% (streams). Glacier areas comprised only 2.3% of total lake catchment areas, but covered 26.6% of stream catchments; other open freshwater bodies in the catchment comprised 19.4% of lake and 28.9% of stream catchments. Maximum marsh or mire land cover was 82.9% for lake and 67.4% for stream catchments, whereas pasture comprised 18.1% (lakes) and 14.2% (streams). Maximum alpine forested area cover was higher in lake (98.7%) than in stream catchments (65.6%), and maximum arable land covered 24.4% of lake and 24.6% of stream catchments.
Ecoregion delineation of Sweden was obtained from the Nordic Council of Ministers (1984). The ecoregions range from the nemoral region in the south to the arctic/alpine complex in the north. The nemoral region is characterized by deciduous forest, mean annual temperatures >6°C, and a relatively long growth period (180–210 d). In contrast, the arctic/alpine complex in the north is characterized by relatively low mean annual temperatures (<2°C) and short growth periods (<140 d). Geographic position descriptors (longitude, latitude, altitude), ecoregion delineation, discharge, deposition variables, land use/vegetation cover descriptors, physical properties (stream width, lake area) as well as aquatic substrate descriptors resulted in a dataset of 60 environmental (independent) variables.
Statistical Analyses
First, detrended correspondence analyses were conducted to obtain the gradient length of both the stream and lake chemistry data. Because the gradient lengths were in both cases ≤1.5 SD, the linear method redundancy analysis (RDA) was used to study the effects of environmental variables representing geographic position and regional- and local-scale factors on stream and lake water chemistry. Moreover, preliminary analyses of water chemistry (total phosphorus concentration) and catchment land use (% agriculture) did not reveal any step changes between the northern and southern regions. RDA was performed on a correlation matrix and is a form of direct gradient analysis (like Principal Components Analysis). In a first step in RDA, the entire set of 60 environmental variables was tested to determine the significance of individual variables using a Monte Carlo permutation test (with 999 unrestricted permutations). Variables that were not significantly correlated with the three water chemistry variables or that were found to co-vary with other environmental variables (i.e., variance inflation factors >100) were removed (n = 22) from the data set.
Variance Partitioning
The remaining 38 explanatory variables were grouped into three subsets to yield ecologically interpretable variance components as follows: (1) variables describing the geographic position (G) of the water body, (2) regional scale (R), and (3) local scale (L) variables (Fig. 2, Table 2). The variation partitioning technique used has been previously described by Borcard and others (1992) and hence we will not go into detail here. In brief, the procedure allows for the variance in the explanatory data set to be partitioned into different variable components through the use of covariables (i.e., variables whose influence is partialled out of the analysis). Initially, this technique was used to partition variation in ecological data sets into environmental and spatial components (e.g., Økland and Eilertsen 1994) and has been extended by incorporating three sets of explanatory variables (e.g., Anderson and Gribble 1998).
Fig. 2Venn diagram (hypothetical model) showing the unique variation, the partial common variation, and the common variation of the three subsets G, R, and L representing the environmental dataTable 2The procedure of variation partitioning of water chemistry (n = 3) in streams (n = 390) and lakes (n = 361) explained by three sets of environmental variables, geographic (G), regional (R), and local (L) in partial redundancy analysis (pRDA)RunEnvironmental variableCovariableλstreamsλlakes1GRLNone0.7510.6512GeoR&L0.0180.0373R&LNone0.7330.6144R&LGeo0.1730.1845GeoNone0.5780.4676RegG&L0.0990.0787G&LNone0.6520.5738G&LReg0.0550.1169RegNone0.6960.53510LocalG&R0.0290.05811G&RNone0.7210.59312G&RLocal0.2700.22113LocalNone0.4800.430aλ = computed eigenvalue in RDA. These numbers are used to calculate the explanatory power of each component (see Table 3)Table 3Calculation of explanatory power of each component in the variance partitioning modelVariation explained by factorsAbbreviation (see Figs. 2 & 3)Calculation (no. of run, Table 2)λstreamsλlakesGeographicG20.0180.037RegionalR60.0990.078LocalL100.0290.058Geographic & regionalGR12–6–20.1530.106Geographic & localGL8–2–100.0080.021Regional & localRL4–6–100.0450.048Geographic, regional & localGRL7–8–(12–6–2)–(4–6–10)0.3990.303Total explainedTotX10.7510.651UnexplainedUXTotV−TotX0.290.349Total varianceTotV1.01.0aAbbreviations refer to the legend in Fig. 2. The figures in the calculation column refer to the runs in Table 2Fig. 3Sources of variation in lake and stream water chemistry, respectively. Column labels indicate the variation (%) in acid neutralizing capacity, total phosphorus, and total organic carbon accounted for by each subset and their combinations
The total variance explained and the unique contributions of each subset and their joint effects were obtained by the following: (1) RDA was run with all three subsets as environmental variables and no covariables to obtain a measure of the total variance, (2) partial RDA was run with one of the three subsets as environmental variables and no covariables, and (3) partial RDA was run with one of the three subsets as environmental variables constrained by the remaining two groups as covariables and reverse. The third step was repeated three times and each subset was treated as environmental variables constrained by the remaining subsets as covariables. This procedure resulted in four runs of RDA for each subset combination or a total of 13 runs of RDA were done for the full set of analyses for each ecosystem (Table 2). With three subsets of environmental data, the total variation of water chemistry was then partitioned into seven components including covariance terms (Fig. 2, Table 3). The variation explained by these subsets is subtracted from the total variation (1.0 in case of RDA) to obtain the unexplained variation.
Stepwise RDA
Stepwise RDA with forward selection was performed with all 38 environmental variables as independent variables and the 3 water chemical variables (ANC; TP and TOC) as dependent variables to determine the best predictors (high R2 values). In this procedure, selected variables are run as co-variables and subsequent variables (step 2 and on) need to explain a significant amount of the residual variance (tested by Monte Carlo permutation).
Redundancy analyses and partial RDA were done using CANOCO for Windows Version 4.5 (Ter Braak and Smilauer 1997–1998). Prior to all statistical analyses (RDA), chemical and deposition variables, stream width, lake area, and altitude were log-transformed and proportional catchment land use/vegetation cover variables were arcsine square-root transformed to achieve normal distribution (SAS).
Results
Variance decomposition using redundancy analysis showed that all independent variables combined explained more than 65% of the total variation in stream and lake surface water chemistry (Table 3). The amount of variation explained was somewhat higher for streams (λstreams = 0.751) compared to lakes (λlakes = 0.651). The largest proportion of variance was explained by the interaction between all three scale factors (Fig. 3).
Both stream and lake surface water chemistry was more influenced by regional-scale factors than either by geographic position or local-scale factors. However, the unique variance explained by geographic position, regional- or local-scale variables was low (<10%) (Fig. 3). For streams, the unique variance explained by regional-level variables (9.9%) was substantially higher than that explained by local-scale variables (2.9%) or geographic position (1.8%). Similarly, for lakes the unique variance explained by regional-scale variables (7.8%) was higher than that explained by local-scale variables (5.8%) and that explained by geographic position (3.8%). Geographic position and regional-scale factors (G&R) were better predictors of surface water chemistry than regional and local (R&L) or geographic position and local (G&L) factors. The strongest interaction was found between geographic position and regional-scale variables. For streams, the interaction between geographic position and regional-scale variables (G&R) explained 15.3% of the variance in stream chemistry. For lakes, the G&R interaction explained 10.6% of the variance in lake chemistry. The relation between geographic position and local-scale variables was much weaker, in particular for streams. The G&L interaction explained 0.8% of the variance in stream and 2.1% of the variance in lake chemistry. The amount of variance explained by the interaction between regional- and local-scale variables was 4.5% for streams and 4.8% for lakes.
Ordination of stream chemistry and environmental variables showed that the primary RDA axis represented a latitudinal gradient (Fig. 4a). Eigenvalues for the first and second RDA axes were 0.685 and 0.056, respectively. Streams situated in alpine forested or alpine treeless catchments were placed on the right side of the ordination, whereas lowland streams situated in pasture and arable landscape in the south (e.g., boreonemoral ecoregion, eco5) with high wet and dry deposition of NHx (WDNHx) were placed to left. ANC and TP were strongly associated with pasture and arable land use and high WDNHx. TOC concentration was positively correlated with forested catchments and habitats with high amounts of coarse detrital matter and negatively correlated with mean annual discharge (Q) and, like lake-TOC, unrelated to arctic/mountainous characteristics. The second RDA axis was related to glacial land cover and whether the stream was located in the southern boreal ecoregion (eco4).
Fig. 4RDA biplot of environmental factors and ANC, TP, and TOC of (A) streams and (B) lakes. 1 = riparian pasture cover; 2 = floating leaved vegetation; 3 = riparian deciduous forest cover; 4 = riparian alpine cover; 5 = riparian heath cover; 6 = boulder; 7 = block; 8 = pebble; 9 = periphyton; 10 = cobble; 11 = fine leaved submerged vegetation; 12 = water temperature; 13 = wet & dry non–sea salt Mg deposition; 14 = riparian arable cover (streams), alpine forest (lakes); eco1 = arctic/alpine ecoregion; eco2 = northern boreal ecoregion; eco4 = southern boreal ecoregion; eco5 = boreonemoral ecoregion; = nemoral ecoregion; WDNHx = Wet & Dry NHx deposition; c_detritus = coarse detritus; f_detritus = fine detritus; FWD = fine wooded debris (substrate); Q = annual mean discharge
All three lake chemistry variables were negatively correlated with the first RDA axis (Fig. 4b). Eigenvalues for the first and second RDA axes were 0.599 and 0.056, respectively. The first RDA axis represented gradients in latitude and catchment/ecoregion. Lakes situated in alpine, treeless catchments at high latitude and altitude were situated to the right, whereas sites situated in forested catchments or catchments with pasture or arable land use were placed to the left in the ordination. Both ANC and TP were positively correlated with the amount of catchment classified as pasture and arable. Moreover, many of these lakes were situated in the boreonemoral ecoregion (eco5), with high wet and dry deposition of NHx (WDNHx). In contrast, lake water total organic carbon (TOC) was associated with forested catchments, with high amounts of coarse detrital matter (c_detritus). The second RDA axis represented gradients in the amount of catchment classified as mire (or bog), in particular the importance of local factors such as substrate type, water temperature, and riparian mire and fine wooded debris (FWD).
Stepwise RDA of stream and lake chemistry as dependent variables and the “single” variables of geographic position and regional and local environmental variables showed that all variables accounted for 65% (lakes) and 75% (streams) of the total variance. The amount of alpine treeless areas in the catchment was the single most important predictor of lake water chemistry (explaining 55.4% of the explained variance). The second variable selected was altitude (18.5%, i.e., the amount of residual variance explained after running the first variable selected, “alpine treeless areas in the catchment,” as a covariable), followed by the amount of arable land in the catchment (4.6%), percent coverage of floating leaved vegetation in the littoral (4.6%), and lake surface area (1.5%). For streams, the five best single predictors of water chemistry were the amount of arable land in the catchment (68%), followed by the amount of alpine treeless areas in the catchment, altitude (2.7%), stream width (2.7%), and mean annual discharge Q (1.3%).
Discussion
Lakes and streams are often perceived as structurally and functionally different ecosystems, and indeed major dissimilarities do exist regarding differences in water movement. For example, streams are characterized by unidirectional, turbulent flow and high flushing rates, whereas lake chemistry is more affected by the timing and frequency of turnover events (e.g., polymictic to dimictic mixing in boreal lakes). Furthermore, obvious differences in nutrient cycling and recycling are expected due to the relative importance of benthic vs. pelagic productivity (Essington and Carpenter 2000). The surface water chemistry of streams is considered to be tightly linked to catchment characteristics, with geomorphology determining soil type and availability of ions through weathering (e.g., Allan 1995). Lakes, on the other hand, have until recently been perceived as separate entities, more isolated than streams from the surrounding landscape (e.g., Kratz and others 1997; Soranno and others 1999; Riera and others 2000; Quinlan and others 2003). Clearly, terrestrial–aquatic linkages are important predictors of surface water chemistry for both streams and lakes, but the strength of this interaction should vary with geologic and hydrologic settings. Thus, the major difference between the River Continuum Concept (Vannote and others 1980) and the concept of lake landscape position (Kratz and others 1997) probably lies in large differences in water residence times between streams and lakes. Given the differences in water movement, in particular flushing rates, one might expect that streams and lakes differ in the external drivers that affect water chemistry. Surprisingly, our findings do not support this conjecture; the major part of the variation in water chemistry in both streams and lakes was explained by all components (i.e., geographic position as well as regional- and local-scale variables), followed by the combination (or interaction) of geographic position and regional-scale factors. These findings support the premise that variability in surface water chemistry is driven by interactions between geographic position and regional factors. Our finding, however, that regional factors alone accounted for a large part of variation in ANC, TP, and TOC indicates the pivotal role that catchment land use/cover plays in determining surface water chemistry.
The finding that the surface water chemistry of streams and lakes could be partly predicted by regional-scale variables, in particular catchment land use (e.g., arable) agrees with the findings of several earlier studies (e.g., Schonter and Novotny 1993; Allan and others 1997). Johnson and others (1997) showed, for example, that urban land use and rowcrop agriculture were important factors in explaining variability in stream water chemistry. Similarly, Hunsaker and Levine (1995) were able to explain more than 40% of the variance in total nitrogen using landscape metrics. In our study, we were interested in analyzing “natural” variability, so we removed sites judged to be affected by agriculture (i.e., sites with >25% of their catchments classified as arable were not included). Hence, our finding that the amount of arable land in a catchment explained nearly 70% of the variability in stream water chemistry was not expected using these data, and implies that even a small-scale agricultural land use within a catchment may affect phosphorus concentration. The importance of a riparian zone has been proposed to be less important in explaining among-site differences in heavily managed catchments (Omernik and others 1981). These authors suggested that the total amount of agriculture and forest in a catchment are more important predictors of water chemistry than the vegetation composition of the riparian zone. Our finding that less than 6% of the variation in surface water chemistry was explained by local factors alone (such as the presence of a riparian zone) supports this conclusion. Furthermore, in contrast to regional-scale factors, only a small amount of the variation was “hidden” in joint effects or interaction terms between regional and local (<8%) and between geographic and local (<3%) variables. Hence, other factors not considered here, such as where the land use is located in the catchment and in relation to the water body, presumably need to be considered. Indeed, studies of small scale or local factors have been shown to be important in modifying larger scale effects, e.g., several studies have shown the ameliorative influence of a vegetated riparian zone (e.g., Cooper 1990; Osborne and Kovacic 1993).
Redundancy analysis showed that the variability in both stream and lake water chemistry was explained by the similar regional- and local-scale variables. For example, as discussed above, the proportion of arable land use in the catchments was a strong predictor of stream water chemistry (68%), followed by alpine, treeless land cover (17.3%). For lake water chemistry, the amount of alpine, treeless land cover was a good predictor (55.4%), followed by altitude (18.5%) and catchment arable land use (4.6%). Clearly, several of the variables in different “local” and “regional” components covary. For instance, the amount of alpine treeless land cover in the region/catchment and stream width are presumably correlated with altitude. However, as demonstrated here, regional factors were better predictors of stream and lake water chemistry and thus contribute largely to the explanatory power of the covariation components.
All three water chemistry variables were strongly correlated with variables representing a latitudinal gradient; for example, sites in the south are more well buffered and nutrient rich compared to sites in the north. This distinct north–south gradient in water chemistry was not unexpected, but can be easily explained by major landscape-level differences between the northern and southern parts of the country. For instance, the legacy of historical processes on present-day distribution patterns of vegetation is clearly visible in Sweden. At approximately 60°N latitude, a marked difference in vegetation occurs, and this ecotone (limes norrlandicus) basically delineates the transition of broad-leaved (e.g., English oak and elm) and coniferous mixed (e.g., Scots pine and spruce) forests in the south from the boreal pine and spruce forests in the north (Nordic Council of Ministers 1984). In addition, the limes norrlandicus ecotone is also correlated with the highest postglacial coastline or the highest level the sea reached after the last ice age and below which fluvial sediments have been deposited. Hence, these two landscape-scale discontinuities in vegetation and soil type can have profound importance for surface water chemistry. Finally, broad-scale climatic differences also exist between the northern and southern parts of the country, which are manifested in differences in discharge regimes. For example, streams in the south are dominated by autumn and winter rains, whereas streams in the north are dominated by snowmelt-driven peaks in runoff during spring (Anonymous 1979).
Given the profound differences in climate, geomorphology, and vegetation between the northern and southern parts of the country, we anticipated discernible differences in the factors driving surface water chemistry. Indeed, the finding that landscape position is important in explaining variability in surface water chemistry has been shown in previous studies (e.g., Johnson 1999), and supports the use of ecoregions to partition natural variability. Ecoregions have been suggested as appropriate ecological units for classification because they are generally perceived as being relatively homogeneous, having similar climate, geology, and other environmental characteristics (Wright and others 1998), and hence are considered as relatively good predictors of spatial patterns of surface water chemistry (e.g., Landers and others 1988; Larsen and others 1988). However, to be an appropriate classification tool, an ecoregion should minimize within and maximize among region variability, and, ideally, knowledge of how both natural and human-induced variability affect ecosystem processes should be known in order to fully assess the adequacy of ecoregions for partitioning natural variability. For example, it is well known that catchment management practices can have profound effects on surface water quality. For instance, whether a catchment is forested (promotes infiltration, high transpiration, and reduces runoff), clear-cut (results in lower infiltration and transpiration and increased runoff), or reforested may singly or in concert affect the water chemistry of aquatic ecosystems (Foster and others 2003).
The results of this study showed the importance of interactions between variables acting on multiple spatial scales on among-lake and stream water chemistry. Somewhat surprising was the finding that the major drivers were similar between lakes and streams, despite the obvious differences in ecosystem types. For instance, in streams nutrients are spiralling downstream, whereas in lakes, nutrient retention is relatively high, depending on lake size and morphometry. Obviously, the chemical composition of a surface water body is a product of a series of mechanisms and processes acting along a scale continuum, i.e., from broad (geographic) to small (local) scales. Moreover, the environmental characteristics of a specific habitat are not random, but are considered to be controlled by macro-scale geomorphic patterns (Frissell and others 1986). Building on this premise, a conceptual framework has been developed where the aquatic (stream) organism assemblage at a site can be seen as a product of a series of filters (e.g., from continental to microhabitat), with each species occurring at a site having passed through these filters (e.g., Tonn and others 1990; Poff 1997). Similarly, surface water chemistry of a particular site is also constrained to some extent by a number of environmental filters. Small-scale systems develop within the constraints set by broad-scale systems of which they are part, and likewise local-scale processes and conditions are generated by broad-scale, geographic patterns and conditions.
The idiosyncrasies of both ecosystems might be suppressed by the effects of large-scale factors. Geographic position functions as a template determining both regional and local factors. At the catchment level, geology controls soil type, weathering determines ion concentrations (and buffering capacity), and climate determines vegetation type (and land use). However, changes in land use (e.g., afforestation of arable to urban) and/or vegetation cover (e.g., deforestation or afforestation of arable land) are sources of catchment variation that might generate high amounts of variability or noise, making it difficult to tease apart components of natural variation from the effects of anthropogenic impact on surface water chemistry. This inherent catchment variation is probably responsible for the large amount of variation explained by regional factors, which may hide the effects of individual features of lakes and streams appearing similar in their response to environmental factors and influences. However, another caveat in addressing issues of “scale-effects” is that the spatial resolution at which observations are made can confound interpretation of scale-related processes (e.g., Minshall 1988; Manel and others 2000). For example, environmental variables such as nutrient concentrations and hydrology are more influenced by regional-scale processes, whereas other variables such as in-stream vegetation cover are more influenced by local control mechanisms (e.g., Allan and others 1997). Our findings of the importance of interactions between geographic position and regional- and local-scale variables support this conclusion.

anc
total phosphorus
toc
geographic position
spatial scale
variation partitioning
partial rda
lentic
lotic


Does ligament balancing technique affect kinematics in rotating platform, PCL retaining knee arthroplasties?

The goal of this prospective, randomized, blinded trial was to determine if ligament balancing techniques for rotating platform TKA affect postoperative knee kinematics. Sixteen patients with unilateral rotating platform TKA consented to participate in this institutional review board approved study. Eight patients were randomly selected to receive ligament balancing with an instrumented joint spreader device and eight patients received ligament balancing using fixed thickness spacer blocks. A single plane shape matching technique was used for kinematic analysis of static deep knee flexion and dynamic stair activities. There were no differences in knee kinematics between groups during static deep flexion activities. The spreader group demonstrated kinematics more similar to the normal knee during the ascending phase of the dynamic stair activity. Knee kinematics in static knee flexion were unaffected by ligament balancing technique, while knees balanced with the spreader demonstrated a medial pivot motion pattern during stair ascent. This medial pivot motion pattern may improve long-term results by more closely replicating normal knee kinematics.
Introduction
Rotating-platform total knee arthroplasty (TKA) has become increasingly popular because this type of design provides good tibiofemoral conformity and low contact stresses without imposing rotational constraint [28]. These designs have been used for well over 20 years with excellent survivorship [10]. Recent kinematic studies of rotating platform knee arthroplasties have shown excellent stability in extension, but frequent anterior translation of the femur with respect to the tibia in flexed postures [6]. These anterior femoral translations may reduce maximum weightbearing flexion [4] and implant longevity [9], and therefore merit further study.
Tibiofemoral translations are influenced by ligament balance [4, 16, 21, 30], muscle and external forces, and implant design. Ligament balance is thought to play a particularly important role in the function of rotating-platform knee arthroplasties, and numerous balancing techniques have been reported [8, 12, 13, 18]. However, no well designed clinical studies of ligament balance and knee kinematics have been reported.
By performing a prospective, randomized, blinded trial of two ligament balancing techniques for rotating platform TKA, we sought to determine if ligament balancing technique affected postoperative knee kinematics. We hypothesized that ligament balancing with a calibrated spreader/balancer would provide better controlled knee kinematics, specifically reduced anterior femoral translations with flexion, than ligament balancing with fixed thickness spacer blocks.
Materials and methods
Sixteen patients with unilateral osteoarthritis of the knee and with no history of knee injuries or trauma consented to participate in this prospective, randomized, blinded, and institutional review board approved study. All subjects received the same rotating platform, PCL-retaining total knee prosthesis (TC-PLUS SB Solution, Plus Orthopedics AG, Rotkreuz, Switzerland, Fig. 1). The subjects were randomly assigned to two groups preoperatively: eight knees received the prosthesis using a ligament balancing technique employing fixed thickness spacer blocks (control group), while the other eight knees received the same prosthesis employing a calibrated spreader/balancer device to equalize the joint gaps and ligament balance in flexion and extension (spreader group) (Fig. 2).
Fig. 1All patients received a rotating platform total knee arthroplasty (TC-PLUS SB Solution, Plus Orthopedics, Rotkreuz, Switzerland)Fig. 2One group of knees was treated using fixed thickness spacer blocks for ligament balancing (control group, left) and the other group was treated using a calibrated tensioning device (spreader group, right)
All surgeries were performed by the senior surgeon (FK) at South–West London Elective Orthopaedic Centre, Epsom, United Kingdom. All study subjects were operated in the supine position under spinal anesthesia and sedation, and each was administered prophylactic antibiotic prior to inflation of the tourniquet. Standard extramedullary and intramedullary instrumentation were used in all knees for preparation of the tibia and femur, respectively. Standard sequential soft-tissue releasing techniques [22, 29] were utilized in the control and spreader groups, which included resection or release of (1) the anterior fibres of PCL, (2) medial and posteromedial capsule, (3) medial osteophytes, and (4) superficial MCL. In the control group spacer blocks were used in extension and 90 degree flexion to guide soft tissue releases to create balanced and equal flexion–extension gaps. In the spreader group a balancer device (laminar spreader, Plus Orthopedics AG) (Fig. 2) was used in extension and 90 degree flexion to guide soft tissue releases to create balanced and equal flexion–extension gaps. Soft-tissue balance was assessed at 0 and 90 degrees of flexion with patella equally subluxed during measurements in both spreader and spacer block groups in order to accommodate appropriate measuring device into the joint space. A standard force of 20 N was applied to the medial and lateral jaws of the balancing device during this technique [23]. The posterior cruciate ligament (PCL) was retained in all knees with a bone block on the proximal tibia, recessing anterior fibers when necessary to achieve suitable balance.
Study subjects were assessed with pre-operative plain anteroposterior and lateral weightbearing radiographs of the knee and immediately postoperative non-weightbearing anteroposterior and lateral weightbearing radiographs. Patients were assessed post-operatively and over an average follow-up time of 11 ± 3 months (range: 7–15 months). The Knee Society Score [14] was employed as the scoring instrument. There were no differences between the control and spreader groups for height, weight, age, sex distribution, preoperative deformity or preoperative clinical scores (Table 1).
Table 1Patient demographics and clinical assessments (mean ± 1SD)ControlSpreaderP valueAge at operation (years)71.0 ± 8.472.2 ± 6.60.96Height (cm)167 ± 7.6165 ± 7.80.65Weight (kg)75.0 ± 22.670.3 ± 12.90.72Sex (M/F)3/54/41.0aVarus/valgus distribution8/07/11.0aPre-op knee score42.1 ± 10.350.0 ± 11.70.13Pre-op function score50.0 ± 18.955.0 ± 20.40.50Post-op knee score90.5 ± 5.993.5 ± 1.80.51Post-op function score81.3 ± 23.488.1 ± 15.10.72Follow-up (months)10.3 ± 3.111.3 ± 2.30.44aFisher’s exact test
Follow-up consisted of clinical and fluoroscopic assessment performed at Mayday University hospital, Croydon, United Kingdom. Fluoroscopic imaging (Siemens Polystar TOP, Siemens AG, Munich, Germany) consisted of (1) weightbearing maximum flexion lunge activity, (2) kneeling on a padded bench to maximum comfortable flexion and (3) a 4 cycles of a step-up/down on a 25 cm step. For the stair activity, the subjects faced the same direction throughout the cycle, therefore, the step-down was a backward motion that reversed the step ascent motion. Patients were instructed on the study activities prior to recording, and were given an opportunity to practice until comfortable. Lateral fluoroscopic views of the knee were recorded in the maximally flexed positions for the lunge and kneeling activities, as were four repeat trials of step-up/down on the stair. The fluoroscopic images were recorded at 15 frames per second onto an S-VHS VCR. Views of calibration targets also were acquired for distortion correction and optical calibration.
The three-dimensional (3D) positions and orientations of the implant components were determined using model based shape matching techniques [3, 5], including previously reported techniques, manual matching, and image space optimization routines (Fig. 3). The fluoroscopic images were digitized and corrected for static optical distortion. The optical geometry of the fluoroscopy system (principal distance, principal point) was determined from images of calibration targets [3, 5]. The implant surface model was projected onto the geometry corrected image, and its 3D pose was iteratively adjusted to match its silhouette with the silhouette of the subject’s TKA components. The results of this shape matching process have standard errors of approximately 0.5° to 1.0° for rotations and 0.5–1.0 mm for translations in the sagittal plane [3, 5].
Fig. 3Model based shape matching techniques are used to determine the three-dimensional pose of the arthroplasty components from fluoroscopic images. The fluoroscopic image shows the outlines, in red, of the implant surface models superimposed in their registered positions. The images along the right margin show medial, lateral, coronal and transverse views of the implant components’ relative orientations
The relative motions of the femoral and tibial components were determined from the 3D pose of each TKA component using the convention of Tupling and Pierrynowski [26]. The locations of condylar contact were estimated as the lowest point on each femoral condyle relative to the transverse plane of the tibial baseplate. Anteroposterior translations of the condyles were computed with respect to the anteroposterior midpoint of the tibial baseplate. Motion of the mobile bearing was not analyzed since the mobile bearing insert was not visible in the X-ray images and could not be tracked without addition of metallic markers.
Researchers were unblinded to subject group membership only after all kinematic data had been produced. Statistical comparisons of the fluoroscopic images were performed (SPSS ver 13, SPSS Inc., Chicago, US) using two-way repeated measures ANOVA with post hoc pair-wise comparisons (Tukey/Kramer) at a 0.05 level of significance. All other parameters were evaluated using non-parametric tests.
Results
Both the Knee Score and the Function Score were slightly lower for the control group (Table 1). This tendency existed pre-operatively but was not statistically significant.
For the maximum kneeling activity, no significant differences were found in knee angles or translations (Table 2). Maximum implant flexion for the control and spreader groups averaged 102° ± 13° and 108° ± 10° (P = 0.34), respectively. Tibial component valgus for the control and spreader groups averaged 0° ± 2° and −1° ± 2° (P = 0.56), respectively. Tibial external rotation for the control and spreader groups averaged −5° ± 7° and −5° ± 6° (P = 0.87), respectively. Medial tibial contact was located 2.7 ± 12.2 and 1.8 ± 8.2 mm (P = 0.87) posterior to the midline of the tibial plateau for the control and spreader groups, respectively. Lateral tibial contact was located at 10.5 ± 11.4 and 11.1 ± 11.8 mm (P = 0.93) posterior to the midline of the tibial plateau for the control and spreader groups, respectively.
Table 2Knee pose during maximum flexion kneeling (mean ± 1SD)GroupFlexion (°)Valgus (°)Tibial Ext. Rot. (°)Medial AP (mm)Lateral AP (mm)Control102.0 ± 12.80.1 ± 2.1−4.7 ± 7.4−2.7 ± 12.2−10.5 ± 11.4Spreader107.9 ± 10.1−0.5 ± 1.8−5.3 ± 6.3−1.8 ± 8.2−11.1 ± 11.8P value0.34 0.56 0.87 0.87 0.93
For the maximum lunge activity, no significant differences were found in knee angles or translations (Table 3). Knee flexion for the control and spreader groups averaged 95° ± 15° and 102° ± 11° (P = 0.36), respectively. Tibial component valgus for the control and spreader groups averaged 0° ± 1° and −1° ± 2° (P = 0.62), respectively. Tibial external rotation for the control and spreader groups averaged −9° ± 6° and −6° ± 7° (P = 0.29), respectively. Medial tibial contact was located 0.3 ± 8.2 mm and 6.7 ± 7.7 mm (p = 0.1.5) posterior to the midline of the tibial plateau for the control and spreader groups, respectively. Lateral tibial contact was located 16.5 ± 8.7 mm and 16.8 ± 9.9 mm (p = 0.96) posterior to the midline of the tibial plateau for the control and spreader groups, respectively.
Table 3Knee pose during maximum flexion lunge (mean ± 1SD)GroupFlexion (°)Valgus (°)Tibial Ext. Rot. (°)Medial AP (mm)Lateral AP (mm)Control95.3 ± 15.1−0.1 ± 1.4−9.6 ± 5.9−0.3 ± 8.2−16.5 ± 8.7Spreader101.6 ± 10.6−0.6 ± 2.1−5.7 ± 7.3−6.7 ± 7.7−16.8 ± 9.9P value0.360.620.290.150.96
For the stair activity, knees in the spreader group exhibited more posterior medial (P = 0.04, RM-ANOVA) and lateral (P < 0.005, RM-ANOVA) condylar contact than the control knees. There was no difference in average tibial rotation between the two groups, and no pair-wise comparisons at specific flexion ranges resulted in significant differences (Fig. 4). On average, both groups of knees had approximately 2° tibial internal rotation at 0° flexion, and rotated to 7° tibial internal rotation at 80° flexion. Medial contact was observed to remain at approximately 2 mm posterior to the AP midpoint from 0° to 50° flexion, then moved anterior to 80° flexion. The control group showed greater anterior translation of medial contact from 50° to 80° flexion than did the spreader group. Lateral contact was more posterior in the spreader group throughout the stair activity. Both groups showed posterior translation of lateral contact of 2–3 mm from 0° to 30° flexion, with very little net translation from 30° to 80° flexion.
Fig. 4Knee motions during the stair activity differed between the control and spreader groups. Condylar positions were significantly more posterior in the spreader group. There were no significant differences in tibial rotation, nor were there significant pair-wise differences for rotations or translations
Tibiofemoral kinematics during the step activity also were compared using average centers of rotation (COR) for femoral motion with respect to the tibial base-plate (Fig. 5) [6]. The COR provides a concise measure of femoral AP translation—if the COR is central (close to 0%), the femur rotates about the center of the tibia with little AP translation. A medial COR (between 0% and +50%) indicates the femur translates posterior with external rotation during flexion. A lateral COR (between −50 and 0%) indicates the femur translates anterior with external rotation during flexion. For the entire step-up/down cycle, the centers of rotation were at 0% (central) and 13% (medial) (P = 0.058) for the control and spreader groups, respectively. When step-up kinematics were compared, the spreader group showed a COR located more medially (28%) than the control group (0%, P < 0.05, Table 4). There was no difference in COR for step-down kinematics (Table 4). Both groups of knees showed tibial internal rotation with knee flexion, 8.5° and 7.6° for the control and spreader groups, respectively. These differences were not statistically significant.
Fig. 5Average centers of rotation for the entire stair activity were in the center of the tibial plateau (0%) for the control group (left) and to the medial side (13%) for the spreader group (right). This difference was not significant (P = 0.058)Table 4Medial/lateral center of rotation (COR) during the stair activity (mean ± 1SD)GroupExtension phase (%)Flexion phase (%)Control−3 ± 19−4 ± 2Spreader28 ± 41−3 ± 3P value<0.05>0.05
None of the subjects demonstrated valgus or varus angles larger than 2 degrees during motion, consequently there was no obvious evidence of condylar lift-off.
Discussion
One goal of TKA is to reproduce normal knee kinematics. Ligament and soft-tissue balance are thought to play critical roles in obtaining optimal kinematic behavior. Theoretical merits of many balancing techniques and instruments have been discussed [13, 25, 27, 30]. This prospective, randomized and blinded study evaluated two ligament balancing techniques with posterior cruciate retaining rotating platform total knee arthroplasty to determine if balancing technique affected knee kinematics. Randomizing patients for surgical treatment and blinding the investigators to group membership until after all data had been processed reduced the potential for selection, measurement, and interpretation bias to affect the study findings. All subjects demonstrated satisfactory knee function based on clinical scores, there were no clinical complications in any knee, and no evidence of condylar lift-off was found during dynamic activity.
The two knee groups exhibited no significant differences in knee kinematics for the weightbearing lunge and passive kneeling activities. This similarity is not unexpected given the posterior cruciate was retained in all knees. It is interesting to note that tibiofemoral AP position in these knees appears to differ from previous reports with mobile bearing knee arthroplasties. Banks et al. [4] reported lunge kinematics for a mixed group of rotating platform and rotating-and-translating arthroplasties during the same lunge activity, and observed 102° average flexion, 7.7° average tibial internal rotation, and 2.2 mm posterior femoral position with respect to the tibial AP midpoint. The control and spreader groups exhibited approximately the same knee angles, but 8.4 and 11.8 mm posterior femoral position, respectively. Greater posterior femoral translation with flexion is suggestive of more physiologic posterior cruciate ligament function and knee mechanics, although there is insufficient information to attribute those translations specifically to surgical technique, implant design, or a combination of factors. The amount of tibial rotation observed in the flexed postures is similar to other previous reports for knee arthroplasties [6, 15] but is much smaller than the amount of tibial rotation observed in healthy knees in similar postures [1, 20].
Ligament balancing technique did affect knee kinematics during the dynamic stair activity. Condylar contact locations were observed to remain more posterior on the tibia and to have a more medial center of rotation during step-up in the spreader group. These findings suggest the spreader balancing technique provided more normal balance or stability to the medial compartment of the knee, resulting in less medial contact translation during the stair activity. Medial contact in the control group was observed to move anterior with flexion on the stair activity, indicating greater functional laxity in that compartment.
Simple comparisons of knee kinematics across groups are possible using the center of rotation characterization. A medial center of rotation has been described in the healthy normal knee [2, 17]. The spreader group showed a medial center of rotation during stair ascent, indicating medial contact did not move significantly while lateral contact moved anterior with knee extension and femoral internal rotation. The control group showed a center of rotation close to the middle of the tibia for the stair activity, indicating that the femur rotated internally during knee extension with little AP translation (medial contact moved posterior and lateral contact moved anterior with extension). The center of rotation in the spreader group knees differed between the ascending (medial COR) and descending (central COR) phases of the step-up/down activity (Table 4). This suggests that the spreader balancing technique provided greater anterior medial stability than the technique employing fixed thickness spacer blocks, but posterior medial stability was equivalent between the two balancing techniques. Banks and Hodge [7] reported on a mixed group of 44 rotating platform and rotating-and-translating mobile bearing knee arthroplasties during the same stair activity, and found average tibial rotations of 9° and average centers of rotation at −19% (lateral). These motions were associated with anterior femoral translation with flexion, which has been observed in numerous knee arthroplasty designs [11, 19, 24]. The knees in the present study showed similar amounts of tibial rotation, but both groups showed centers of rotation that were more medially located. Thus, the knees in this study exhibited less anterior femoral translation with flexion compared to the knees in the previous report, suggesting both balancing techniques provided beneficial tibiofemoral stability compared to the group average of well-functioning mobile-bearing knee arthroplasties.
This double-blinded prospective randomized study used fluoroscopic kinematic measurements to determine if two ligament balancing techniques would affect knee motions in several activities. Kinematics in flexion were similar, with both groups showing a more posterior femoral position than previously has been reported for similar implant designs. Knees operated with a spreader/balancer device showed a more medial center of rotation in ascending a stair activity, and both groups showed average centers of rotation that were more medial than previously had been reported for similar implant designs. Kinematics closer to the normal knee may yield improved knee performance and implant longevity. However, these kinematic differences are clinically insignificant upon short-term follow up, and their long-term significance remains to be studied.

rotating platform
tka
knee kinematics
spreader balancing device
soft tissue balancing
randomized control trial


Twenty-Four Hour Tonometry in Patients Suspected of Chronic Gastrointestinal Ischemia

Background and aims Gastrointestinal tonometry is currently the only clinical diagnostic test that enables identification of symptomatic chronic gastrointestinal ischemia. Gastric exercise tonometry has proven its value for detection of ischemia in this patients group, but has its disadvantages. Earlier studies with postprandial tonometry gave unreliable results. In this study we challenged (again) the use of postprandial tonometry in patients suspected of gastrointestinal ischemia.
Introduction
In patients presenting with postprandial pain, especially when associated with weight loss and positive history for cardiovascular diseases, chronic gastrointestinal ischemia (CGI) should be among the differential diagnosis [1–3]. Vascular anatomic abnormalities can be demonstrated with duplex ultrasound or angiography. However, a stenosis does not necessarily imply ischemia, due to the abundant collateral circulation. We have recently demonstrated that gastric exercise tonometry (GET) allows differentiation between patients with and without gastrointestinal ischemia. GET showed an accuracy of 87% in detection of gastrointestinal ischemia. The patients selected for treatment using GET, are likely to benefit from revascularization techniques [4–9].
Gastric (exercise) tonometry is not widely accepted as a diagnostic technique for gastrointestinal ischemia due to the lack of familiarity with this approach and its time-consuming nature. Twenty-four hour gastrointestinal tonometry with meals is more familiar (resembling 24-h pH measurement) and easier to perform. Over 90% of CGI patients report postprandial, while only 60% report exercise-related, complaints. Ischemic pain after meals in CGI is caused by insufficient increase of postprandial blood flow to balance the increased metabolic demand of the gastrointestinal tract [10]. This indicates that tonometry directly after meals would be the most physiologic approach of measuring ischemia in these patients. However, earlier studies showed unreliable results using tonometry after meals, related to insufficient suppression of gastric acid secretion and dilution effects [11–13]. We therefore started by testing standard meals in vitro and performed a study with healthy subjects using these meals and high-dose proton pump inhibition (PPI) as an optimal gastric acid suppressant [14]. In this study we retrospectively evaluated the additional value of prolonged gastrointestinal tonometry in a group of patients suspected for possible CGI.
Methods
Patients with unexplained chronic abdominal symptoms who were referred for suspected CGI were included in this study. More-common causes of chronic abdominal symptoms had been excluded previously by appropriate diagnostic evaluation. All patients had imaging of the splanchnic arteries [intra-arterial digital substraction multiplane abdominal angiography (DSA) and duplex ultrasound scanning] and GET. Along with this standard diagnostic work up, patients had twenty-four hour (24 h) tonometry testing, directly following GET.
Gastric exercise tonometry (GET)
GET was performed using a standardized protocol, before, during, and after 10 min of submaximal exercise, as described previously with both gastric and jejunal catheters [15]. A maximal gradient was calculated between stomach and arterial PCO2. The criteria for a positive GET (all three required), established in healthy volunteers and a patient cohort, were: (1) a gradient of >0.8 kPa in the stomach after exercise, (2) an increase in gastric PCO2, and (3) an arterial lactate <8 mmol/l [8,15].
Twenty-four hour tonometry testing
A gastric and jejunal tonometer catheter (8 French, Datex Ohmeda, Helsinki, Finland) and a gastric pH meter (pHersaflexTM, internal reference, Medical Measurement Systems, Enschede, the Netherlands) were inserted nasogastrically using fluoroscopy. Intravenous infusion of omeprazole was started with a bolus of 80 mg in 30 min, followed by 8 mg/h, using an infusion pump (Perfusor compact®, B Braun Melsungen AG, Melsungen, Germany). The catheters were connected, respectively, to the Tonocap (Datex Ohmeda, Helsinki, Finland) and the pH recording device (Medical Measurement Systems, Enschede, the Netherlands). The Tonocaps were connected to a computer on which a data-collection program automatically registered the gastric and jejunal PCO2 level every 10 min. The gastric pH was automatically recorded and stored in a datalogger (Medical Measurement Systems, Enschede, the Netherlands), which also allows for real-time reading of the gastric pH.
As soon as the gastric pH was >4.0 for ≥30 min, the first meal was started (t = 0 min). All patients had meals at standard times: breakfast I (08:00), dinner (12:00), liquid compound meal I (15:00), bread meal (18:00), liquid compound meal II (21:00), and breakfast II (08:00 the next day). The breakfast, bread, and dinner meals were standardized. The liquid compound meal consisted of two packages of 200 ml each (Nutridrink®, Nutricia, The Netherlands). The contents and caloric density of each meal used are presented in Table 1. The patients were instructed to eat their meals within 15 min. The consumption of small amounts of liquids (noncarbonated) was allowed and noted, consumption of alcohol-, acid-, and CO2-containing beverages was strictly prohibited. Due to the limited length of the catheters, the subjects were only capable of performing very minor exercise and were allowed to lie down in supine position from 22:00.
Table 1Composition characteristics of the various standard mealsMealCompositionkcal/gBreakfast Fat (16%), proteins (22%), carbohydrates (62%)1.7DinnerFat (16%), proteins (47%), carbohydrates (37%)2.2Bread mealFat (10%), proteins (19%), carbohydrates (71%)1.8Compound solutionFat (35%), proteins (16%), carbohydrates (49%)1.5Percentages of delivered energy (En%); kcal = kilocalories; g = gram.
Diagnosis and treatment
The results of all diagnostic procedures were discussed in a multidisciplinary team. In this team a gastroenterologist, a vascular surgeon, and an interventional radiologist discussed the symptoms, medical history, physical examination, and all diagnostic evaluations, with the exception of the results on 24-h tonometry. The latter therefore did not influence the consensus diagnosis. The multidisciplinary team decided for every patient: (1) no splanchnic stenosis, (2) splanchnic stenosis and no ischemia or (3) splanchnic stenosis and ischemia (i.e. chronic gastrointestinal ischemia, CGI). The gold standard for the diagnosis of chronic gastrointestinal ischemia was a positive outcome after successful revascularization at (long-term) follow-up. The outcome of GET, and consensus diagnosis of the multidisciplinary team were compared to the results of the 24-h tonometry testing.
Definition of a positive (abnormal) 24 h tonometry
The cut-off values established in the previous healthy subjects study were used to define the criteria for the results on 24-h tonometry [9]. These cut-off values were, for the stomach: 12.1, 11.4, and 11.3 kPa for the breakfast (or bread meal), dinner, and compound solution meals, respectively; in the jejunum these threshold values were, respectively, 12.0, 13.6, and 10.6 kPa. The criteria for a positive finding (abnormal result) on 24-h tonometry were: (1) pathologic responses after three or more (standard) meals, or (2) a combination of one or two pathologic responses after (standard) meals combined with a median PCO2 > 8.0 kPa, measured in between meals.
Statistics
Data were expressed as mean (standard deviation) or median (range) when appropriate. The data of the ischemic and non-ischemic patients were compared using Student’s t-test or χ2 testing. Sensitivity, specificity as well as positive and negative predicted values of 24-h tonometry were calculated with the consensus diagnosis as the gold standard.
Results
Patient characteristics
In a period of three years (2002–2005), in 37 patients referred for suspected of CGI, 24-h tonometry along with the standard work-up was performed. Of these, 33 (89%) patients had complete work-up and were included in this study. Mean age was 54 (22–82) years, with eight males and 25 females. Significant splanchnic stenosis were found in 23/33 (69%) patients. A significant single vessel splanchnic stenosis was found in 14/33 (42%) patients [13 celiac artery (CA) and one superior mesenteric artery (SMA)]. A significant stenosis of two splanchnic arteries was found in 9/33 (27%) patients (all CA and SMA stenosis).
All 33 patients had chronic abdominal pain for a mean of 35 months (range 3–120), 24/33 (73%) patients had pain following meals, 11/33 (33%) patients reported pain during or after exercise, 9/33 (27%) patients reported both pain following meals and during, or after, exercise, and 23/33 (70%) patients reported weight loss. The mean weight loss was 11 kg (range 3–28 kg) in 17 months (range 2–120 months); see Table 1.
Gastric exercise tonometry
In 18/31 (58%) patients a gradient of >0.8 was found by GET. In 14/18 (78%) patients this increased gradient was defined as abnormal using the three criteria as previously defined. In four patients a gradient >0.8 kPa was not caused by ischemia: three patients had persistent acid production, and one performed excessive exercise (leading to false positive findings) [8].
Consensus diagnosis of the multidisciplinary team and results after treatment
According to the team the diagnosis of no stenosis (and no ischemia), stenosis but no ischemia, and stenosis with ischemia (CGI) was diagnosed in, respectively, 12 (36%), four (12%) and 17 (52%) patients.
Fifteen patients diagnosed with CGI had treatment: 10 patients surgical and five patients stent-placement therapy. Three patients had no treatment: two patients preferred a conservative approach and one patient proved inoperable due to comorbidity. After a mean follow-up of 55 months (49–85), 12 out of 15 (80%) patients were free of complaints, one patient died immediately after surgical revascularization (multiple organ failure), one patient had partial improvement, and one patient had persistent complaints. The latter patient had a celiac artery release, and was diagnosed as having no CGI after follow-up; this patient had no abnormalities on 24-h tonometry testing; see Table 2.
Table 2Patient characteristics, results of diagnostic tests and conclusionNrAgeSexStenosisPP painPE painGET resultsConsensus diagnosisTreatmentOutcome complaintsFinal conclusion24-h tono results161FNone+−0,5No stenosis, no ischemia–No stenosis, no ischemiaNormal236MCA+−0,4No ischemia–No ischemiaNormal355FCA+−0,7aCGISurgeryFreeCGIAbnormal476MNone−−0,6No stenosis, no ischemia–No stenosis, no ischemiaNormal547MNone−+1,6bNo stenosis, no ischemia–No stenosis, no ischemiaNormal642FCA + SMA−−1,5CGISurgeryFreeCGIAbnormal765FCA + SMA−−2,0CGIConservativeCGIAbnormal877FCA + SMA+−2,2CGISurgeryDied post-op.CGIAbnormal972FSMA++1,8CGIStentFreeCGIAbnormal1041MNone+−2,8cNo stenosis, no ischemia–No stenosis, no ischemiaNormal1172FCA+−1,4CGIStentPartial relieveCGIAbnormal1267FCA−−0,9cNo stenosis, no ischemia–No ischemiaNormal1340FCA−+1,1cCGISurgeryUnchangedNo ischemiaNormal1482MCA + SMA++1,0CGIConservativeCGINormal1554FCA++0,9CGIConservativeCGINormal1626MCA++1,0CGISurgeryFreeCGIAbnormal1758MNone++2,2cNo stenosis, no ischemia–No stenosis, no ischemiaNormal1822FCA+−0,7No ischemia–No ischemiaNormal1942FNone+−1,1dNo stenosis, no ischemia–No stenosis, no ischemiaNormal2048FCA+−1,7CGISurgeryFreeCGINormal2151FCA+−0,7No ischemia–No ischemiaNormal2243FCA + SMA++0,5eCGISurgeryFreeCGIAbnormal2354FCA + SMA−−1,5CGISurgeryFreeCGINormal2476FCA + SMA+−0,6fCGIStentFreeCGIAbnormal2553MNone+−2,0cNo stenosis, no ischemia–No stenosis, no ischemiaNormal2653FCA++1,1CGIStentFreeCGIAbnormal2750FCA−−1,3CGISurgeryFreeCGIAbnormal2861FCA + SMA++1,7CGIStentFreeCGIAbnormal2963FNone+−0,8No stenosis, no ischemia–No stenosis, no ischemiaNormal3024FCA++1,3CGISurgeryFreeCGIAbnormal3174FCA + SMA−−0,8No ischemia–No ischemiaNormal3241FNone+−1,2dNo stenosis, no ischemia–No stenosis, no ischemiaNormal3363FNone+−0,0No stenosis, no ischemia–No stenosis, no ischemiaAbnormalPP = postprandial, PE = post-exercise, M = male, F = female; CA = celiac artery, SMA = superior mesenteric artery; GET = gastric exercise tonometry, result presented as gradient (in kPa); 24-h tono = twenty-four hour tonometry; CGI = chronic gastrointestinal ischemia.a false negative GETb acid production during GETc false positive GETd no CO2 raise during GETe abnormal jejunal gradient during GETf minor exercise during GET
Twenty-four hour tonometry
The 24-h tonometry was well tolerated in all patients, no medical or technical problems occurred. In 28/33 (85%) patients tonometric measurements were performed in both stomach and jejunum, in 5/33 (15%) patients only stomach measurements were performed (in all five patients placement of jejunal tonometry catheter failed); see Fig. 1. In 8/33 (24%) patients a dose reduction of the compound solution was necessary, due to patient’s inability to consume the normal dosage. The overall gastric acid suppression was good, with a gastric pH > 4 during 94.8% (range 71–100%) of the time. Pathological peaks during 24-h tonometry coexisting with periods of pH < 4, were defined as non-pathologic peaks.
Fig. 1 Individual curves of results of 24-h tonometry in a non-ischemic (A) and an ischemic patient (B). Individual curves of a non-ischemic patient (A) and an chronic gastrointestinal ischemia patient (B); on the horizontal axis the time from 0 to 24 h, on the vertical axis PCO2 from 0 to 20 in kilopascal (kPa); curves: PCO2 values measured every 10 min in stomach
(□), jejunum
(×) and four meals spread over the 24 h period (*)
The fasting baseline of stomach and jejunal PCO2 measurements were significantly higher in the ischemic patients compared to the non-ischemic patients group. The jejunal PCO2 peaks after breakfast and dinner were significantly higher in the ischemic patients compared to the non-ischemic patients; see Tables 3 and 4.
Table 3Results of 24-h tonometry in ischemic and non-ischemic patientsCGI pts.Non-ischemic pts.PeakΔ-peakMean PCO2PeakΔ-peakMean PCO2StomachB10.6 (3.9)4.0 (3.4)–8.5 (2.7)2.6 (2.0)–D9.9 (1.9)3.7 (1.5)–8.5 (2.3)3.3 (2.5)–CS10.4 (3.0)3.3 (2.2)–8.1 (2.6)1.8 (1.2)–Fasting––7.7 (1.4)a––6.8 (0.7)    Day––6.9 (1.1)––6.5 (0.7)    Night––8.2 (1.8)––6.9 (0.8)JejunumB11.6 (3.2)b3.2 (1.5)–8.8 (1.4)2.1 (0.8)–D12.2 (3.4)c3.7 (2.0)–9.0 (1.7)2.2 (0.7)–CS10.6 (2.2)2.5 (1.6)–9.0 (1.9)1.5 (1.0)–Fasting––8.9 (1.6)d––7.4 (0.7)    Day––8.8 (1.3)––7.5 (0.9)    Night––8.9 (1.9)––7.5 (0.8)CGI = chronic gastrointestinal ischemia; PCO2 = carbon dioxide in kilopascal; B = breakfast, D = dinner, CS = compound solution meal; a P = 0.02, b P = 0.005, c P = 0.04, d P = 0.03Table 4Results of different tests compared to final diagnosisPatientsFinal diagnosisGET24-h tonometryCombination GET––24-h tonometryCGI 1714 (82%)13 (76%)17 (100%)No ischemia1611 (69%)15 (94%)16 (100%)Data presented as number of patients with positive predictive value (PPV) and negative predictive value (NPV); GET = gastric exercise tonometry; CGI = chronic gastrointestinal ischemia; GET = gastric exercise tonometry
Using the previously defined criteria, 13/17 patients with CGI and 15/16 patients without ischemia were correctly identified with 24-h tonometry. The calculated test properties show a sensitivity of 76% and a specificity of 94%, a positive predictive value (PPV) of 76% and a negative predictive value (NPV) of 94% for detection of ischemia by 24-h tonometry alone. Combining the results of GET and 24-h tonometry, 17/17 patients with CGI and 16/16 patients without ischemia could be correctly identified (sensitivity of 100% and specificity of 100%).
Comparing patients with single- and multi-vessel ischemia, or patients with or without postprandial and/or exercise-related complaints, no significant differences in diagnostic accuracy were found.
Discussion
The results of this retrospective study indicate that 24-h gastrojejunal tonometry is feasible and may be clinically useful in diagnosing chronic gastrointestinal ischemia. The measurements were easy to perform, generally well tolerated and no complications occurred.
The fasting baseline PCO2 in both stomach and jejunum was significantly higher in the ischemic patients group compared to the non-ischemic patients. This difference might be explained by the continuous compromised arterial blood flow of the mucosa of the stomach (and/or jejunum) in the ischemic patients group. The significant higher maximum peak after the breakfast and dinner and the borderline significant higher peak after the compound solution meal (P = 0.07 and 0.052 for stomach and jejunum, respectively) support the theory that, with a maximal metabolic oxygen demand, mucosal ischemia is apparent and detectable using tonometry.
Using the cut-off values predicted by the previously performed healthy subjects study, the positive predictive value of 24-h tonometry seems very promising [14]. Comparing the results of detection of ischemia for 24-h tonometry and GET, no significant differences were found. Theoretically it might be expected that 24-h tonometry is more accurate in patients with postprandial complaints, and GET in patients with exercise-predominant complaints, but this was not found in this small patient series. In five patients the results of GET were incorrect (four false-positive and one false-negative result), whereas the 24-h tonometry (retrospectively) correctly predicted the presence (one patient) or absence (four patients) of gastrointestinal ischemia in these patients.
One of the major advantages of 24-h tonometry over GET is the fact that all patients are suitable for 24-h tonometry, in contrast to GET, where patients have to perform submaximal exercise, which is not always possible due to age, concomitant disease, and/or compromised general condition of the patient. Another advantage of the 24-h tonometry is the familiarity with 24-h pH measurement, which is a widely accepted diagnostic tool in gastroenterology. Moreover 24-h tonometry testing is more easily standardized than GET, especially regarding the level of exercise, which is difficult to manage and may cause false positive findings during or after excessive exercise [15]. In this study, the 24 h tonometry was not repeated in a standard fashion after treatment. In two patients who had successful, anatomical and clinical, revascularization 24-h tonometry was repeated, and showed normalization in both patients.
In theory, the compound solution meal (low volume, high calorie content) should be the ideal test meal for provocation of gastrointestinal ischemia. The use of standard meals with large metabolic demand, like the compound solution meal, called for a dose reduction in several patients. These patients already had severely impaired food intake and could hardly tolerate (larger) meals. This dose reduction might have influenced the outcome of the 24-h tonometry, the borderline significant differences between CGI and non-ischemic patients after compound solution meals might be explained by this effect. The results of tonometry after meals have to be interpreted with care. Unsuccessful suppression of acid production and meal-related production of CO2 may influence the results of tonometry. Using optimal acid suppression medication and standardized meals, these effects can be minimized, but not completely ruled out. In this study gastric pH measurement was used to control acid suppression. Furthermore, duodenogastric reflux of jejunal contents and/or pancreatic juices are quite common and might theoretically influence intragastric and -jejunal PCO2 levels in a major way, leading to false positive tonometry findings [16].
In conclusion, this retrospective study shows that 24-h tonometry is feasible, safe, and has a very promising diagnostic accuracy for the detection of gastrointestinal ischemia. Using high-dose PPI acid suppression and standard meals, and previously established normal values, 24-h tonometry identifies gastrointestinal ischemia with an acceptable accuracy. The definitive role of 24-h tonometry in the diagnosis of chronic gastrointestinal ischemia has to be established in (future) prospective studies.

splanchnic stenosis
carbon dioxide
chronic splanchnic syndrome
chronic mesenteric ischemia
gastric tonometry
small bowel tonometry


Pure endoscopic endonasal odontoidectomy: anatomical study

Different disorders may produce irreducible atlanto-axial dislocation with compression of the ventral spinal cord. Among the surgical approaches available for a such condition, the transoral resection of the odontoid process is the most often used. The aim of this anatomical study is to demonstrate the possibility of an anterior cervico-medullary decompression through an endoscopic endonasal approach. Three fresh cadaver heads were used. A modified endonasal endoscopic approach was made in all cases. Endoscopic dissections were performed using a rigid endoscope, 4 mm in diameter, 18 cm in length, with 0 degree lenses. Access to the cranio-vertebral junction was possible using a lower trajectory, when compared to that necessary for the sellar region. The choana is entered and the mucosa of the rhinopharynx is dissected and transposed in the oral cavity in order to expose the cranio-vertebral junction and to obtain a mucosal flap useful for the closure. The anterior arch of the atlas and the odontoid process of C2 are removed, thus exposing the dura mater. The endoscopic endonasal approach could be a valid alternative to the transoral approach for anterior odontoidectomy.
Introduction
Removal of the odontoid process is a procedure often required for the treatment of the basilar impression with compression of the brain stem or cervical spinal cord due to irreducible atlanto-axial translocation. Different disorders may produce atlanto-axial dislocation such as congenital malformation, chronic inflammation, metabolic disorders and trauma.
The transoral approach is the most favoured approach to the odontoid process and it is largely used for the surgical treatment of extradural and also intradural disorders of the cranio-vertebral junction [6–9, 11–13, 15, 16, 22–26]. Despite the fact that such an approach provides a direct route to the odontoid process, it presents several disadvantages such as the deepness of the surgical corridor, the sometimes required splitting of the soft palate, the risk of tongue and teeth damage and, in case of dural opening, the increased risk of post-operative CSF leakage and meningitis.
Based on the experience of endoscopic endonasal pituitary surgery [3, 17], some works have recently reported anatomical studies and clinical applications of a modified endoscopic endonasal approach for the removal of the dens. These studies show the potential applications of the endoscopic endonasal approach for the surgical management of suprasellar, parasellar and retroclival pathologies [1, 2, 4, 5, 10, 14, 18–21].
This anatomic study describes the extended endoscopic endonasal approach to the cranio-vertebral junction, with particular attention to the reconstruction of the surgical route.
Material and methods
For this anatomic study, three fresh cadaver heads were dissected; an extended endoscopic endonasal approach to the cranio-vertebral junction was performed in all cases.
Endoscopic dissections were performed using a rigid endoscope (Karl Storz GmbH, Tuttlingen, Germany), 4 mm in diameter, 18 cm in length, with 0 degree lenses.
The endoscope was connected to a light source through a fiberoptic cable and to a camera fitted with 3CCD sensors. The video-camera was connected to a 21” monitor supporting the high resolution of the 3CCD technology.
Results
The procedure started with the introduction of the endoscope into a nasal vestibule through a lower trajectory as compared to the one employed for reaching the sellar region. Along such trajectory, the first structures to be visualized were the nasal septum medially, the inferior turbinate and the middle turbinate laterally. The inferior margin of the middle turbinate led to the choana which represented the main landmark of the approach.
By advancing the endoscope through the choana it was possible to identify the ostium of the Eustachian tube laterally, the rhinopharynx posteriorly, the soft palate inferiorly and the inferior wall of the sphenoid sinus superiorly; the latter representing the superior limit of the surgical approach. Angling the endoscope to the contralateral nasal cavity, it was possible to visualize the ostium of the contralateral Eustachian tube. The ostia of the two Eustachian tubes represented the lateral limits of this approach (see Fig. 1a,b).
Fig. 1a, b Entering the choana, the rhinopharinx and the Eustachian tube have been bilaterally visualized (iwsphs inferior wall of sphenoid sinus, ET Eustachian tube, Rphx rhinopharinx)
In order to expose the cranio-vertebral junction the mucosa of rhinopharynx was incised along its lateral limits at the edge with the ostia of the Eustachian tube and along the inferior wall of the sphenoid sinus superiorly (see Fig. 2a). The mucosa, the longus capitis and longus colli muscles were gently dissected downward as a single layer, thus creating a muscle-mucosal flap (see Figs. 2b and 3). Proceeding from the inferior wall of the sphenoid sinus to the soft palate of the lower clivus, the atlanto-occipital membrane, the anterior arch of C1 and the body of C2 were visualized.
Fig. 2a The mucosa of the rhinopharynx has been incised in order to create a mucosal flap. b The muscles longus capitis and colli have been dissected together with the mucosa in order to expose the cranio-vertebral junction. (ET Eustachian tube, Rphx rhinopharinx, NS nasal septum, iwsphs inferior wall of sphenoid sinus, C clivus, aom atlanto-occipital membrane, C1 atlas, mmf muscle-mucosal flap)Fig. 3Schematic drawing showing the muscle-mucosal flap and the lower structures (iwsphs inferior wall of sphenoid sinus, ET Eustachian tube, C1 atlas, mmf muscle-mucosal flap, C2 axis, D dens)
Introducing the endoscope in the oral cavity it was possible to reach the dissected mucosa of rhinopharynx and to transpose the muscle-mucosal flap into the oral cavity (see Fig. 4a,b).
Fig. 4a The muscle-mucosal flap is transposed in the oropharinx. b Schematic drawing showing the exposure of the cranio-vertebral junction after replacing the flap. (Ophx oropharynx, mmf muscle-mucosal flap, T tongue)
This manoeuver permitted an adequate endonasal exposure of the cranio-vertebral junction without removing the mucosa of the rhinopharinx, which provides a useful autologous material for closure of the surgical field.
Reintroducing the endoscope into the nasal cavity, the anterior arch of the atlas was removed and the dens with the apical and alar ligaments were exposed (see Fig. 5a,b). The dens was then thinned with a microdrill, separated from the alar and apical ligaments, and finally removed (see Fig. 6a,b).
Fig. 5a The anterior arch of the atlas has been removed. b The dens has been exposed. (C clivus, aom atlanto-occipital membrane, C1 atlas, dm dura mater, al alar ligament, D dens)Fig. 6a The dens has been drilled. b After removal of the odontoid process the transverse ligament and the underling tectorial membrane are visible. (iwsphs inferior wall of sphenoid sinus, ET Eustachian tube, dm dura mater, D dens)
At this point the transverse ligament was identified; it was removed with the tectorial membrane, a double layer membrane positioned behind the transverse ligament, in order to expose the dura mater. At the end of the procedure the muscle-mucosal flap was replaced into the nasal cavity, thus closing the surgical field (see Fig. 7).
Fig. 7The muscle-mucosal flap is replaced in the rhinopharinx (iwsphs inferior wall of sphenoid sinus, ET Eustachian tube, mmf muscle-mucosal flap)
In this study, the endoscopic endonasal approach to the cranio-vertebral junction has been performed using both the one-nostril and the two-nostril technique, without removal of inferior and/or middle turbinate, nasal septum or other nasal structures. Although the procedure can be performed through only one nostril, the binostril technique provides, without any additional surgical trauma, a better manoeuverability of the surgical tools and the possibility to work with “three hands”. As a matter of fact, this technique permits a free-hand use of the endoscope in one nostril, held by the assistant, and the use of the other nostril or both nostrils for the insertion of the surgical instruments.
Furthermore, in the case of a narrow nasal cavity, it is valuable to perform a unilateral middle turbinectomy and removal of the posterior third of the nasal septum to enlarge the surgical corridor.
Discussion
Different pathological disorders may produce atlanto-axial translocation with ventral compression of the brain stem or spinal cord. The most common are congenital malformations, such as Arnold Chiari malformation type II, chronic inflammation, such as rheumatoid arthritis, genetic transformation, such as Down’s syndrome and trauma, such as type II odontoid fracture. Some of these patients are candidate to the resection of the odontoid process for anterior decompression. The indication for odontoid resection is irreducible atlanto-axial subluxation, associated with severe spinal cord compression causing progressive myelopathy.
The most favoured approach to the odontoid process is the transoral approach. This approach provides a direct route to the surgical field, without any neurovascular manipulation and passing through the oropharynx, without injuring major neurovascular structures. The main limitation to this approach is the difficulty of dural closure and the subsequent higher risk of CSF leak and meningitis. For this reason the trans-oral approach is mainly used for extradural lesions [7, 8, 11–13, 15, 22–24], although some studies have reported its application for the surgical treatment of intradural pathology of the lower clivus and ventral cranio-cervical junction [6, 9, 16, 25, 26]. Other minor disadvantages are, however, related to this approach: the split of the soft palate and even of the hard palate is often performed in the case when rostral extension of the approach is required; tongue swelling may occur for prolonged compression; there is risk of damaging the teeth with retractors; velopharyngeal insufficiency may develop; and there is the necessity of nasal feeding in the postoperative stay.
Recently, increased diffusion in the use of the endoscope for transsphenoidal pituitary surgery [3, 17] led some studies to explore the possibility of applying the endoscopic endonasal approach in the surgical treatment of skull base lesions other than pituitary tumors. In recent years some works have reported anatomical studies and surgical experience in the endoscopic endonasal approach to different areas of the midline skull base, from the olfactory groove to the cranio-vertebral junction [1, 2, 4, 5, 10, 14, 18–21].
Thanks to the properties of the endoscope itself, the endonasal approach provides a wider view of the surgical field and a close-up vision, when compared with the transoral microscopic approach. Furthermore, the minimal invasiveness of the endoscopic endonasal route may reduce some morbidities related to the transoral approach. In fact, it is no longer necessary to use mouth retractors, prolonged compression of the tongue or split of the soft palate, and even considering the necessity of a middle turbinectomy or removal of the posterior portion of the nasal septum to enlarge the surgical corridor, these adjunctive manoeuvres do not usually produce morbidity to the patient. These manoeuvres are often performed in the endonasal extended approaches to the area around the sella in live patients and do not cause any respiratory problems.
The possibility of performing an odontoidectomy through the nose is strictly related to the level of the C1–C2 junction. In fact, in the case of a low junction, below the level of the hard palate, it is virtually impossible to remove the odontoid process with an endonasal approach. On the contrary, in the case of a high position of the atlas-axis junction, the dens is more easily reached and removed through the nasal cavities.
Odontoidectomy may be considered one of the most complicated manoeuvres for the transoral approach, in which the split of the soft and even hard palate is often necessary. Thus, this approach could be evaluated for those cases in which a transoral removal is considered more difficult.
However, this kind of approach still presents some of the main problems of the transoral approach. The first problem concerns the risk of CSF leak and subsequent meningitis. Although the endoscope, thanks to its close-up and multi-angled vision, has a greater chance of detecting an occasional CSF leak, it is quite hard to suture the dura and the nasopharynx mucosa with conventional suturing tools through the nose. For this reason, in our anatomical study, we have created a muscle-mucosal flap, comprehensive of the entire muscular and mucosal tissue covering the ventral cranio-vertebral junction. This flap, as shown, is transposed into the oral cavity during the bone’s removal and replaced in its original site at the end of the procedure. Due to the difficulty of anchoring the flap with suture, it is only distended on the defect and its borders are apposed on the corresponding lines of incision. The mucosa of the inferior wall of the sphenoid sinus could be stripped to favour the adherence of the flap and fibrin glue could be used to seal the edges. The creation of a peduncolated muscle-mucosal flap permits a more physiological reconstruction of the surgical corridor and, furthermore, the vascularization of the flap that directly continues with the oropharynx, facilitates a rapid healing. An endoscopic control should be performed one month after surgery to check the recreating integrity of the rhinopharynx mucosa.
The second problem of the transoral approach concerns the stability of the cranio-vertebral junction. The removal of the odontoid process with its ligaments can destabilize the cranio-vertebral junction.
The third problem concerns the haemostasis that is often difficult in the extended endonasal approaches. Bleeding control may become difficult with bipolar coagulation because the endonasal approach presents a long and narrow corridor, with a limited working space between the tips of the bipolar forceps. Nevertheless, specific bipolar forceps (TAKE-APART bipolar forceps; Karl Storz GmbH, Tuttlingen, Germany) have been used to work through the nose in a safe and effective way as well.
Conclusions
This cadaver study has been performed to demonstrate the possibility of an anterior decompression of the upper cervical cord through an endoscopic endonasal approach. Similar to the transoral approach, the endoscopic endonasal approach provides a direct route to the surgical target, but it seems related to less morbidity. For clinical applications of this approach, the most common surgical problems are the risk of CSF leak and meningitis, the instability of the cervico-medullary junction and the bleeding control. The creation of a muscle-mucosal flap may represent a valid modality for closure of the surgical field. For application in live surgery, dedicate surgical instruments, such as endonasal bipolar forceps, high-speed low-profile drill and surgical guidance systems are needed.
In selected cases this approach could be considered a valid alternative to the transoral microscopic approach for the resection of the odontoid process of C2. Obviously, it should be performed only by surgeons very skilled in endoscopic endonasal surgery and in endoscopic cadaver-dissections, while cooperation in a team with ENT surgeons is recommended.

odontoid process
cranio-vertebral junction
endoscopy