Geographic and seasonal patterns and limits on the adaptive response to temperature of European Mytilus spp. and Macoma balthica populations Seasonal variations in seawater temperature require extensive metabolic acclimatization in cold-blooded organisms inhabiting the coastal waters of Europe . Given the energetic costs of acclimatization , differences in adaptive capacity to climatic conditions are to be expected among distinct populations of species that are distributed over a wide geographic range . We studied seasonal variations in the metabolic adjustments of two very common bivalve taxa at European scale . To this end we sampled 16 populations of Mytilus spp. and 10 Macoma balthica populations distributed from 39 ° to 69 ° N . The results from this large-scale comprehensive comparison demonstrated seasonal cycles in metabolic rates which were maximized during winter and springtime , and often reduced in the summer and autumn . Studying the sensitivity of metabolic rates to thermal variations , we found that a broad range of Q 10 values occurred under relatively cold conditions . As habitat temperatures increased the range of Q 10 narrowed , reaching a bottleneck in southern marginal populations during summer . For Mytilus spp. , genetic-group-specific clines and limits on Q 10 values were observed at temperatures corresponding to the maximum climatic conditions these geographic populations presently experience . Such specific limitations indicate differential thermal adaptation among these divergent groups . They may explain currently observed migrations in mussel distributions and invasions . Our results provide a practical framework for the thermal ecophysiology of bivalves , the assessment of environmental changes due to climate change and its impact on -LRB- and consequences for -RRB- aquaculture . Introduction A fundamental step forward in predicting the ecological and economic consequences of climate change would be to identify the mechanistic link between the physiology of species and climatic variations . How and to what extent climatic variations cause stress in eurythermal bivalve species is still not fully understood and is expected to differ among taxa . In general , for organisms that maintain their body temperature by absorbing heat from the environment -LRB- ectotherms -RRB- , temperatures that are too high can act as a stressor in two ways . On the one hand , it may cause the denaturing of sensitive proteins . This damage can be minimized by the actions of heat-shock proteins , which increase the thermostability of proteins and chaperone cellular processes -LRB- Feder and Hofmann 1999 ; Lyons et al. 2003 -RRB- . On the other hand , excessive temperatures may cause oxygen limitation , due to a limited respiratory capacity , resulting in a maximum respiration rate at a specific temperature , beyond which anaerobic metabolic pathways are utilized and respiration rates usually drop drastically -LRB- Pörtner 2001 , 2002 -RRB- . The temperature that corresponds to this respiratory maximum is referred to as the breakpoint temperature . Since breakpoint temperatures tend to correlate with the maximum habitat temperatures of several marine ectotherms -LRB- Somero 2002 -RRB- , climate-change-induced shifts in the distributions of these species may be due to their respiratory limitations . The metabolic rate of an ectotherm is proportional to its respiration rate . To remain energy-efficient , and for protection against oxygen shortage during the warmer seasons , organisms need to adjust their metabolic energy requirements to their maximum food uptake and oxygen consumption rate . Seasonal variation in the respiratory response to temperature reveals how organisms adjust throughout the annual cycle . While several terrestrial and aquatic mollusks apply the strategy of metabolic down-regulation during the summer -LRB- Buchanan et al. 1988 ; McMahon 1973 ; McMahon and Wilson 1981 ; Storey and Storey 1990 ; Wilson and Davis 1984 -RRB- , others do not -LRB- McMahon et al. 1995 -RRB- . The level of metabolic down-regulation is also reflected by the temperature quotient -LRB- Q 10 -RRB- of the metabolic rate , i.e. , the sensitivity of the organisms ' metabolism to changes in body temperature . Experimental work performed by Widdows -LRB- 1976 -RRB- has demonstrated that when thermal fluctuations approach and exceed breakpoint temperatures , this sensitivity usually decreases . Such reduced sensitivities have been found for field populations of M. edulis -LRB- Newell 1969 -RRB- and M. balthica -LRB- Wilson and Elkaim 1991 -RRB- sampled from high-shore habitats in summertime . Taken together , the thermal sensitivity of the metabolic rate -LRB- Q 10 -RRB- is expected to decrease towards the warm end of the species distribution range . Lately , invasions -LRB- Geller 1999 ; Wonham 2004 -RRB- and northward introgression -LRB- Luttikhuizen et al. 2002 -RRB- have been reported for Mytilus spp. , and a range contraction for M. balthica -LRB- Hummel et al. 2000 -RRB- . Aiming to bridge the gap between the observed migrations of these species and the changing climate in Europe , we studied seasonal adjustments to temperature in bivalve metabolism at the European scale , from 39 ° to 69 ° N . The analysis of patterns in the extent of metabolic acclimatization across widely distributed populations will reveal how core populations differ from marginal populations , presenting species-specific responses to cold winters and hot summers near the upper and lower edges of temperature-induced distribution ranges . Such latitudinal gradients may provide a powerful tool that can be used to understand the temperature-dependent distributions of species and to predict their adaptive tolerance to climate change . In macrophysiological studies , the possibility of differential adaptation to regional climates among distinct populations should be taken into account . Based on neutral genetic variation , both European mussels and clams can be subdivided into three main genetic groups -LRB- Hummel 2006 ; Daguin et al. 2001 ; Luttikhuizen et al. 2003 ; Skibinski 1985 -RRB- . Uncertainty exists about the nomenclature of European Mytilus species . Traditionally , mussels from the Mediterranean Sea and the coast of the Iberian Peninsula are referred to as Mytilus galloprovincialis -LRB- Lamarck -RRB- . Mussels from the English Channel , the North Sea coast , and the Atlantic coast of Norway and Iceland are named Mytilus edulis -LRB- L. -RRB- , and the mussels from the Central Baltic Sea are called Mytilus trossulus -LRB- Gould -RRB- , which is based upon their genetic resemblance to Mytilus trossulus from the Atlantic coast of Canada -LRB- Varvio et al. 1988 -RRB- . However , the morphological characteristics of the different holotypes do not diagnostically separate the three genetic groups found in European mussels . In addition , broad hybridization zones -LRB- Daguin et al. 2001 -RRB- and deep introgressions -LRB- Luttikhuizen et al. 2003 -RRB- have been reported ; a genetic characteristic of a single species with separated clades . To avoid confusion , we will not use these species names in this study , but rather refer to them as Mytilus spp. , with reference to their geographic distributions , i.e. , a Baltic Sea group , a North Sea group , and a Mediterranean Sea and Bay of Biscay group . Also , different genetic groups have been distinguished for M. balthica -LRB- Hummel 2006 ; Luttikhuizen et al. 2003 -RRB- that have never been described as different species . The coupling of phylogenetic and ecophysiological analyses is urgently needed to understand and predict current and future migrations of these bivalve taxa and their clades . Methods Fieldwork To study the marginal and core populations of both taxa , including different genetic groups , we defined 21 research sites of interest along the European coastline , and sampled 11 M. balthica populations and 16 Mytilus spp. populations , respectively . All sampling stations are numbered -LRB- 1 -- 21 -RRB- in Fig. 1 . Whenever a station name is mentioned in this text , its number is given between parentheses . The sampling stations were located in the coastal areas of the different sea basins that represent much of the European coastline -LRB- including the Mediterranean Sea , the Bay of Biscay , the North Sea and the Baltic Sea -RRB- , and a variety of microhabitats . The sampling stations in the Mediterranean Sea are characterized by a high and stable salinity -LRB- 38 -- 40 PSU -RRB- . In the Bay of Biscay and North Sea estuaries , the ambient salinity at the sampling stations fluctuated , generally varying between ∼ 35 and ∼ 25 PSU . Due to elevated river runoff , oligohaline conditions may have occurred occasionally at these stations . The Baltic Sea stations were distributed along the Baltic salinity gradient . While the ambient salinity is still ∼ 15 PSU in the Mecklenburg Bight -LRB- 7 -RRB- , it is around 6 -- 7 in the Gulf of Gdansk -LRB- 6 -RRB- and Askö -LRB- 5 -RRB- , and has decreased to 3 PSU in Umeå -LRB- 3 -RRB- . Although high and low peak temperatures occur at the intertidal sampling stations in the Bay of Biscay and the North Sea , water temperatures were intermediate compared to the warmer Mediterranean Sea and the colder Baltic Sea sites -LRB- Fig. 2 -RRB- . In summer , the Baltic Sea warms rapidly , reaching temperatures that are comparable to North Sea conditions . In the tidal estuaries of the Bay of Biscay and the North Sea , sampling was carried out at mid-shore level . Lacking significant tidal movements , Baltic Sea populations of Mytilus spp. and M. balthica , and Mediterranean Sea populations of Mytilus spp. were sampled at a water depth of 0.5 -- 1.0 m . During the period July 2003 -- May 2005 16 populations -LRB- i.e. , 10 Mytilus spp. and 6 M. balthica -RRB- were visited seasonally and the others only once or twice . During each sampling occasion , mussels were sampled from hard substrate , and clams were sieved from the sediment . For Mytilus spp. populations , mean shell lengths ranged from 28 mm -LRB- SD : 2.0 -RRB- for specimens sampled in the Gulf of Gdansk -LRB- 6 -RRB- to 33 mm -LRB- SD : 3.5 -RRB- for mussels sampled from the Santa Giusta Lagoon -LRB- 21 -RRB- . Mean shell lengths of mussels collected from the other populations was in the same range , and standard deviations were < 3.5 . About 95 % of all sampled mussels fell within a size range of 25 -- 35 mm . For M. balthica mean shell lengths ranged from 12 mm -LRB- SD : 1.5 -RRB- for clams sampled from the Mecklenburg Bight -LRB- 7 -RRB- to 16 mm -LRB- SD : 1.8 -RRB- for clams sampled at Point d'Aiguillon -LRB- 15 -RRB- . Mean shell lengths of all other clam populations were within this range , standard deviations did not exceed 2.8 mm , and 95 % of all sampled clams fell within the size range of 10 -- 19 mm . After sampling , the collected animals were stored in foam boxes -LRB- clams were offered sediment from the field to bury -RRB- and transported to a nearby laboratory , where they were kept in -LRB- constantly aerated -RRB- aquaria , under ambient field conditions -LRB- ± 3 °C -RRB- . Measurements were carried out within 24 h after sampling . Fig. 1Map of research area with 21 research sites . The coastal area is subdivided into three parts representing the approximate distributions of the three genetic groups found in Mytilus spp. and M. balthica . Light gray indicates the Baltic Sea group , medium gray the North Sea group and dark gray the Mediterranean Sea and Bay of Biscay group -LRB- hybridization and introgression zones are not indicated -RRB- . The white and the gray circles represent mussel and clam populations , respectively -LRB- see legend -RRB- . Site no . / name : 1 , Rykyavik ; 2/3 , Umeå a/b ; 4 , Fallvikshamn ; 5 , Askö ; 6 , Gulf of Gdansk ; 7 , Lomma ; 8 , Mecklenburg Bight ; 9 , Grevelingenmeer ; 10 , Westerschelde estuary ; 11 , Granville ; 12 , Le Vevier ; 13 , Brest ; 14 , Loire estuary ; 15 , Point d'Aiguillon ; 16 , Bidasoa estuary ; 17 , Mundaka estuary ; 18 , Vias plage ; 19 , Marseille ; 20 , Gulfo di Oristano ; 21 , Santa Giusta lagoon Fig. 2Annual sea surface temperature -LRB- SST -RRB- regimes for the sampling stations in the Baltic Sea , the North Sea , the Bay of Biscay , and the Mediterranean Sea . Lines and error bars represent monthly averages and standard deviations , based on measurements taken by satellite twice daily , at 9 a.m. and 2 p.m. , during the period 2003 -- 2005 . This data were taken from the NASA JPL website -LRB- NASA Jet Propulsion Laboratory 2005 -RRB- Temperature profiles Field temperature profiles were obtained between April 2004 and May 2005 with temperature loggers -LRB- HOBO Water Pro ® , Onset Computers , Bourne , MA , USA -RRB- at research sites 5 , 7 , 9 , 10 , 15 , 16 and 18 , with a resolution of one measurement per 30 min . The loggers were positioned in the direct vicinity of the animals . Logger output was compared with the sea surface temperature -LRB- SST -RRB- profiles obtained by satellite -LRB- NASA Jet Propulsion Laboratory 2005 -RRB- . Mean habitat temperature of the shallow water and intertidal habitats showed a constant relation with SST . In summer SST was about two degrees lower than the mean values calculated from the logger data at all sites , while in winter the SST was slightly lower for the Atlantic and Mediterranean sites . For the Baltic Sea sites , winter SSTs were similar to the logger data . Using the relation between SST and logger data , we estimated the acclimatization temperature of each mussel and clam population for each sampling occasion . This acclimatization temperature is defined in this study as the mean water temperature for the period of 30 days before sampling . We assume that this is a proper indication of the temperature to which the animals should be well adjusted . Respiration rates Within 24 h after sampling , groups of 3 -- 6 mussels and 7 -- 15 clams were gently removed from their aquaria , and without further acclimation transferred to respiration chambers of volume 264 and 154 ml , respectively . The chambers were positioned in a thermostated tank to maintain a constant temperature during the incubations -LRB- ± 0.3 °C -RRB- . The chambers were filled with filtered habitat water , previously aerated to 100 % oxygen saturation . Chamber lids contained Clark-type electrodes to record the change in oxygen tension in the water . In this way , 2 -- 6 replicate measurements were taken per population and temperature after each sampling occasion . Control measurements were carried out using the same experimental setup , without animals . The total number of M. balthica specimens used from the populations that were sampled seasonally ranged from 475 from the Westerschelde estuary -LRB- 10 -RRB- to 685 from the Mecklenburg Bight -LRB- 8 -RRB- . For Mytilus spp. the number of experimental animals ranged from 104 from Point d'Aiguillon -LRB- 15 -RRB- to 322 from Askö -LRB- 5 -RRB- . To avoid light-induced stress in M. balthica , the chambers were made out of tanned Plexiglas . Respiration rates were measured at 3 , 10 , 17 , 24 and 31 °C . Measurements continued until the oxygen tension in the chambers had decreased by 20 -- 30 % . After each measurement , experimental animals were frozen at − 20 °C and subsequently lyophilized for 72 h to a stable weight . From the dried specimens , valves were removed and the soft tissue dry-weights determined to the nearest mg , after which the mass-specific respiration rates and the temperature quotients were calculated . In addition , we estimated the respiration rates and Q 10 values at the acclimatization temperature , per population , per season . Both , respiration rates and Q 10 values were based on the rates that corresponded to the seven-degree temperature interval -LRB- for instance 10 -- 17 °C -RRB- nearest to the acclimatization temperature . The respiration rates were assessed by linear interpolation , and the Q 10 values were calculated with the following equation : . Here k 2 and k 1 are the respiration rates measured at the higher and the lower temperatures , t 2 and t 1 , respectively . Statistical analysis The following working hypothesis was formulated : H0 : `` Season '' or `` genetic group '' have no effect on the metabolic temperature dependence of M. balthica or Mytilus spp. . Because temperature is not the only the factor limiting ectotherm metabolism , commonly used statistical methods such as correlations and regressions are not very well suited for testing this relationship -LRB- Blackburn et al. 1992 ; Cade et al. 1999 ; Thompson 1996 -RRB- . Estimating the function along the upper edge of this distribution would describe the evolutionary relation between temperature and metabolism in our species . Data points scattered below this `` slope of upper bounds '' -LRB- Blackburn et al. 1992 -RRB- are responses induced by other limiting factors . To estimate this slope of maximum respiration rate at a given temperature , we carried out a main axis regression analysis -LRB- after Thompson et al. 1996 -RRB- . The first step in this is a general regression through all data points . Subsequently , the data are divided into points that fall below and above the line of least squares . All data points that were found above are then used to fit a second regression that again divides the data into two subsets ; etc. . This was repeated three times . The regression lines were forced through the x , y point -LRB- − 2 , 0 -RRB- , assuming that at the approximate freezing point of seawater bivalve aerobic metabolism is near to zero . The final regression line for M. balthica populations was based on 12 data points , with an r 2 of 0.95 . For Mytilus spp. populations , the final regression was based on seven data points with an r 2 of 0.99 . The distance between measured respiration rates and this upper slope describes the extent of metabolic down-regulation in the populations . These rate-deviations -LRB- distances -RRB- were estimated for all populations and used for statistical comparison . ANOVAs based on rate deviations were carried out with `` season '' or `` genetic group '' as independent variables . For the `` genetic group '' analysis , only data points from the temperature range at which all three groups were sampled were included , i.e. , the temperature range for the `` genetic group '' comparison for M. balthica was 9 -- 18 °C , and for Mytilus ssp . 9 -- 15 °C . Bonferroni 's multiple comparison test was used to test for specific differences among seasons or genetic groups . Results Respiration rates at experimental temperatures For each population sampled seasonally , mean respiration rates at experimental temperatures are given in Fig. 3 for Mytilus spp. and in Fig. 4 for M. balthica . Standard deviations among replicate measurements were usually less than 20 % of mean values at experimental temperatures near ambient conditions . At high experimental temperature -LRB- 31 °C -RRB- , variation among replicate measurements could be higher , with standard deviations occasionally exceeding 50 % of the mean values . This was caused by the fact that some groups of specimens exhibited high respiration rates , while other groups consumed almost no oxygen . Fig. 3Seasonal variation in the respiratory response to an experimental temperature range for ten European Mytilus spp. populations . Station names and degrees north are given in the graphs . Numbers in square boxes refer to the station names presented in Fig. 1 . See legend for explanation of the symbols Fig. 4Seasonal variation in the respiratory response to an experimental temperature range for six European M. balthica populations . Station names and degrees north are given in the graphs . Numbers in square boxes refer to the station names presented in Fig. 1 . See legend for explanation of the symbols The respiration rate of mussels usually declined between 24 and 31 °C -LRB- Fig. 3 -RRB- . Exceptions were some cold-acclimatized populations that showed maximum rates between 17 and 24 °C -LSB- e.g. , the Askö -LRB- 5 -RRB- , Gulf of Gdansk -LRB- 6 -RRB- , and Grevelingenmeer -LRB- 9 -RRB- populations sampled in January -RSB- . Peaks in respiration rates between 1.5 and 2.5 -LRB- mg O2/g -LRB- dry weight -RRB- / h -RRB- at 24 °C were frequently observed in springtime -LRB- April -- May -RRB- and occasionally in other seasons . Respiration rates never exceeded 1.5 -LRB- mg O2/g -LRB- dry weight -RRB- / h -RRB- in mussels from the Mecklenburg Bight -LRB- 6 -RRB- and the Gulf of Gdansk -LRB- 5 -RRB- . The highest respiration rates for the M. balthica specimens were mainly observed at 31 °C ; the maximum temperature applied in this study -LRB- Fig. 4 -RRB- . Especially in the populations from the Westerschelde estuary -LRB- 10 -RRB- and Point d'Aiguillon -LRB- 15 -RRB- , respiration rates never decreased at high experimental temperatures . However , in the Baltic populations , outside the summer period maximum rates were observed at a lower experimental temperature . In Umeå -LRB- 3 -RRB- , respiration rates measured in January and April declined at experimental temperatures exceeding 10 -- 17 °C . Respiration rates at acclimatization temperatures The respiration rates of both taxa increased with acclimatization temperature -LRB- Fig. 5 -RRB- . In winter and springtime , deviations from the upper edge slope were small for both Mytilus spp. and M. balthica . At acclimatization temperatures of > 12 °C , an increasing number of data points were scattered at increasing distance from the upper edge slope , and the seasonal comparisons -LRB- ANOVA + Bonferroni -RRB- revealed that rate deviations were mainly restricted to measurements taken in summer and autumn -LRB- see column bar plots , superimposed in Fig. 5A , B -RRB- . These data also revealed genetic group specific differences between the respiration rate and the acclimatization temperature for Mytilus spp. -LRB- P < 0.05 -RRB- ; -LRB- Fig. 5C -RRB- . Maximum acclimatized respiration rates occurred between 8 and 14 °C in the Baltic Sea group , 15 -- 19 °C in the North Sea group and 20 -- 24 °C in the Mediterranean Sea and Bay of Biscay group . The rate deviations found for the Mediterranean Sea and Bay of Biscay group differed significantly from those found for the Baltic Sea group . Several data points related to the North Sea group were found to fit the reaction norm of the Mediterranean Sea and Bay of Biscay group between 15 and 20 °C . Thus , the rate deviations of these two groups could not be distinguished -LRB- P > 0.05 -RRB- . No genetic group specific differentiation was observed for M. balthica -LRB- Fig. 5D -RRB- . Fig. 5A -- DRespiration rates as a function of the acclimatization temperature . The black lines are the upper edge slopes . These graphs include measurements from all research sites presented in Fig. 1 . In A and B , different labels represent different sampling seasons -LRB- see legend in A -RRB- . In B and C respiratory response to temperature is presented per genetic group . The gray diamonds , white triangles and black circles represent the Baltic Sea group , the North Sea group and the Mediterranean Sea and Bay of Biscay groups , respectively . Superimposed are the rate deviations calculated per season and per genetic group , in which BS indicates the Baltic Sea group , NS the North Sea group , MS the Mediterranean Sea group and BC the Bay of Biscay group . * P < 0.05 and ** P < 0.01 refer to the statistical differences for a given season compared to `` January '' in A and B and for a given group compared to `` BS '' in C and D Thermal sensitivity of the metabolic rate Seasonal variation in thermal sensitivity of the metabolic rate shows that Q 10 values of greater than four were exclusively found in winter and spring -LRB- Fig. 6 -RRB- . For M. balthica populations , such high Q 10 values were found at low -LRB- January -RRB- and high -LRB- April -RRB- latitudes . In April , Q 10 values decreased significantly with latitude . Maximum Q 10 did not exceed 3.0 in July and October . July values were about one for clams from the Westerschelde estuary -LRB- 10 -RRB- and Point d'Aiguillon -LRB- 15 -RRB- . The clam population at Askö -LRB- 5 -RRB- also exhibited relatively low values -LRB- < 2 -RRB- . Q 10 values of greater than four were only observed in January and April for mussels -LRB- Fig. 6 -RRB- . A significant decrease in Q 10 values with latitude was observed in January -LRB- P = 0.0083 -RRB- , with the lowest values observed -LRB- Q 10 = 1.2 -RRB- for the population from Gulfo di Oristano -LRB- 20 -RRB- , and the highest values for the population from the Gulf of Gdansk -LRB- 6 -RRB- . In April , this trend vanished , mainly due to the reduced Q 10 values of mussels from the northernmost sampling stations . During the following seasons , July and October , mean Q 10 values decreased further and latitudinal variation disappeared . Fig. 6Seasonal and latitudinal variations in mean Q 10 values of M. balthica -LRB- circles -RRB- and Mytilus spp. -LRB- diamonds -RRB- populations . Trend lines represent linear regressions . r 2 and P values are given in each graph As a function of the acclimatization temperature , both low and high Q 10 values were found at low ambient temperatures -LRB- Fig. 7A , B -RRB- . The maximum Q 10 values observed at a given temperature decreased with increasing acclimatization temperature for both taxa . To illustrate this , we fitted lines of maximum Q 10 values as a function of temperature . These lines crossed the Q 10 = 1 line at ∼ 23 °C for M. balthica and at ∼ 24 °C for Mytilus spp. -LRB- Fig. 7A , B , line a -RRB- . In addition to the maximum Q 10 values for all Mytilus spp. populations , group-specific lines could be drawn -LRB- lines a -- c in Fig. 7A -RRB- . This resulted in different intercepts for the Q10 = 1 line : at ∼ 17 °C for the Baltic Sea group , at ∼ 19 °C for the North Sea group and at ∼ 24 °C for the Bay of Biscay and Mediterranean Sea group . No differentiation of the maximum thermal sensitivity of the metabolic rate was observed for M. balthica populations -LRB- Fig. 7B -RRB- . Fig. 7A -- B Q10 values as a function of the acclimatization temperature , presented per genetic group . The diamonds , triangles and circles represent the Baltic Sea group , the North Sea group and the Mediterranean Sea and/or Bay of Biscay group , respectively . These graphs include measurements taken from all research sites . Lines of maximum Q10 values are fitted for M. balthica -LRB- B ; a -RRB- and for Mytilus spp. -LRB- A -RRB- per genetic group : a the Mediterranean Sea and Bay of Biscay group , b the North Sea group , and c the Baltic Sea group Discussion Rates at high experimental temperatures When exposed to experimental temperatures of 24 or 31 °C , respiration rates in both Mytilus spp. and M. balthica may exceed 2.0 -LRB- mg O2/g -LRB- dry weight -RRB- / h -RRB- . Such high rates were mostly observed in winter and spring , probably due to the low activation energy required for enzyme-catalyzed reactions at this time of the year -LRB- Hochachka and Somero 2002 -RRB- . The population from the Mecklenburg Bight -LRB- 7 -RRB- exhibited exceptionally high respiration rates for Baltic Sea mussels in the summer . In general , these high respiration rates measured at high experimental temperatures are not expected to occur in the field . When the summer starts , and peaks in habitat temperatures -LRB- 24 °C + -RRB- occur in the field , the amplitude of the respiratory response at these higher temperatures declined . We propose that this modulation of metabolic thermal sensitivity is a protection mechanism that prevents excessive metabolic rates at high ambient temperatures . At the northern Baltic Sea station -LRB- 3 -RRB- , the high thermal sensitivity of the metabolic rate did not result in high respiration rates in wintertime -LRB- which includes April in this area -RRB- . Rates declined above 10 °C , indicating that the respiratory capacity was low and that acclimatization to increasing temperatures in springtime requires physiological changes in these clams . Comparing both taxa , their respiratory responses to the experimental temperature range were rather different . The most striking difference is the regular occurrence of the breakpoint temperature between 24 and 31 °C in Mytilus spp. , which was mostly absent for M. balthica -LRB- Fig. 8A , B ; in these graphs we summarize all respiration rates assessed for all populations during all seasons between 2003 and 2005 -RRB- . This breakpoint temperature may reflect the thermal tolerance limits of marine ectotherms . It has been suggested that species with lower breakpoint temperatures are less tolerant to high temperatures -LRB- Hochachka and Somero 2002 ; Pörtner 2002 -RRB- . Interestingly , despite its apparent breakpoint temperature between 24 and 31 °C , Mytilus spp. seem to tolerate higher environmental temperatures than M. balthica , given the geographical distribution of mussels , which reaches as far south as northern Africa -LRB- Comesana et al. 1998 -RRB- . Nonetheless , the lethal temperatures of both taxa under submerged conditions are comparable . The LT50 values for both species were 30 -- 31 °C in a 24-h experiment using mussels and clams that were previously acclimatized to 20 -- 25 °C -LRB- Kennedy and Mihursky 1971 ; Wallis 1975 -RRB- . Fig. 8A -- B Mean respiratory responses to temperature of Mytilus spp. -LRB- B ; diamonds -RRB- and M. balthica -LRB- A ; circles -RRB- . Data are presented as the averages of all measurements taken -LRB- all populations and all seasons , 2003 -- 2005 -RRB- . The numbers next to the labels are the number of replicate measurements taken , and the dashed lines indicate the standard deviations Rates at acclimatization temperatures The relations between the mean acclimatized respiration rates of the studied taxa and temperature are based on specimens from a great variety of microhabitats . Therefore , we expect these data to give a representative overview of metabolic temperature dependence in acclimatized mussels and clams . A narrow relation between temperature and acclimatized respiration rates in winter and springtime suggests that variations in the metabolic rate during this time of the year were directly dependent on temperature , and not limited by other physiological or environmental variables . A temperature-limited metabolic rate was also reflected by the high thermal sensitivity of the metabolic rate of some of the populations during those seasons . Only a few observations confirmed that the constant increase in respiration rates with acclimatization temperature can continue in summer and autumn , when most data points were found to be scattered below the upper edge slope . We suggest that the upper edge slopes represent the `` metabolic scopes '' of these taxa . However , since measurements are based on groups of specimens , respiration rates of single individuals can be higher . The relatively high acclimatized respiration rates -LRB- 1.0 -- 1.5 mgO2/g/h -RRB- most probably result from metabolic up-regulation , related to elevated rates of digestion and protein synthesis . The present study did not find any acclimatized routine respiration rates that exceeded 1.5 -LRB- mg O2/g/h -RRB- in mussels or clams . In general , respiration rates exceeding 1.5 mg O2/g -LRB- dry weight -RRB- / h can be considered to be high and will rarely occur under ambient conditions . Also , in other studies no acclimatized routine respiration rates higher than 1.5 mg O2/g -LRB- dry weight -RRB- / h have been reported for M. balthica -LRB- McMahon and Wilson 1981 ; Wilson and Elkaim 1991 ; Hummel et al. 2000 -RRB- or Mytilus spp. -LRB- Arifin and Bendel-Young 2001 ; Bayne and Widdows 1978 ; Tedengren et al. 1999 ; Thompson 1984 -RRB- . Towards tolerance limits , the arising breakpoint temperature will force down the `` metabolic scope , '' as indicated by the mussel populations from the Santa Giusta lagoon -LRB- 21 -RRB- and Gulfo di Oristano -LRB- 20 -RRB- in July , and for clams from Point d'Aiguillon -LRB- 15 -RRB- in July and October . Physiological rates that are acclimatized to -LRB- near -RRB- breakpoint temperatures are rarely described for ectotherms . The relatively low respiration rates at acclimatization temperatures > 12 °C are interpreted as metabolic down-regulation resulting from both intrinsic and extrinsic factors -LRB- Brokordt et al. 2000 ; Burkey 1971 ; Velasco and Navarro 2003 -RRB- . The extremely low respiration rate of mussels from the Bidasoa estuary -LRB- 16 -RRB- in January was an exception , presumably caused by a temporary drop in ambient salinity -LRB- from 34 to 9 PSU -RRB- . Such hypo-osmotic conditions are known to induce a metabolic depression in Mytilus spp. -LRB- Newell 1969 ; Storey and Storey 1990 -RRB- . In general , Baltic Sea populations exhibited relatively low respiration rates , intermediate respiration rates were found in the North Sea populations , and relatively high metabolic rates in the Bay of Biscay and Mediterranean Sea populations . These observations fall together with the low growth rates in bivalves from the Baltic Sea , intermediate growth rates in North Sea populations , and the highest growth rates found in the Bay of Biscay and in some Mediterranean Sea populations -LRB- Bachelet 1980 ; Fuentes et al. 1998 , 2000 ; Gangnery et al. 2004 ; Hummel et al. 1998 ; Peteiro et al. 2006 ; Westerborn et al. 2002 -RRB- . This indicates that mean routine respiration rates , measured at ambient temperatures , do indeed reflect the metabolic rate and ultimately the physiological performance of bivalves . Separate curves describing the respiratory response to acclimatization temperatures were found for the three genetic groups of Mytilus populations . This resulted in group-specific respiration rates at a given temperature , which was significantly lower for the Baltic Sea group that exhibited reduced metabolic rates at intermediate temperatures -LRB- 12 -- 15 °C -RRB- , where populations from the other genetic groups mostly exhibited optimal respiration rates -LRB- see Fig. 5c -RRB- . In line with our earlier conclusion that the observed suboptimal respiration rates represent metabolic adjustment to limiting extrinsic factors -LRB- including energy -- substrate availability -RRB- , we expect that these group-specific response curves mainly reflect the food conditions in the respective sea-basins during the warmer months of the year . This assumption is supported by the seasonal variation in chlorophyll concentrations The chlorophyll concentrations in the Baltic Sea decline -LRB- Heiskanen and Leppänen 1995 -RRB- at thermal conditions that correspond to the maximum annual chlorophyll concentrations in the North Sea and the Bay of Biscay -LRB- Colebrook 1979 -RRB- and their adjacent estuaries -LRB- Rybarczyk et al. 1993 ; van Bergeijk et al. 2006 -RRB- . It also explains the exceptionally high respiration rates of some populations from the North Sea group at high habitat temperatures , e.g. , specific dynamic action , facilitated by high ambient food availability . Still , differential genetic adaptation to temperature may add to the observed physiological differences , and can not be excluded as an explanation . The relation between the respiration rate and the acclimatization temperature shows great overlap upon comparing Mytilus spp. with M. balthica . Further comparison with other studies demonstrates that seasonal variation in the acclimatized respiration rates obtained from two Mytilus populations from England -LRB- Bayne and Widdows 1978 -RRB- fits the relation described in this study . The respiratory performances of other bivalve species , such as Cerastoderma edule -LRB- Newell and Bayne 1980 -RRB- , Ostrea edulis -LRB- Beiras et al. 1994 -RRB- , or Dreissena polymorpha -LRB- Sprung 1995 -RRB- , were highly comparable as well . This great similarity in respiratory performance among European bivalve species suggests that they share a comparable evolutionary relation with temperature . Sensitivity of the metabolic rate to temperature changes We hypothesized that the sensitivity to temperature of the metabolic rate would decrease towards more southern localities , especially in the warmer seasons . Such latitudinal clines were only observed in January for Mytilus spp. , and in April for M. balthica populations . In October no specific pattern was observed for Mytilus populations , since the Q 10 values were low in all populations . This may be related to limiting food conditions in autumn . Absence of significant latitudinal clines in July was caused by cline-interruption , which corresponded to the geographic transition of one genetic group to the next . These genetic group specific clines became especially apparent in mussels when the Q 10 was presented as a function of the acclimatization temperature -LRB- Fig. 6 -RRB- . The obtained Q 10 values decreased with increasing acclimatization temperature for three reasons . First , metabolic down-regulation for energetic balancing results in a reduced Q 10 . Second , Q 10 will decrease near breakpoint temperatures . Third , during thermal fluctuations that involve high peaks in habitat temperature , ectotherms will minimize the sensitivity of their metabolic rate , avoiding excessive rates when exposed to elevated temperatures -LRB- Peck et al. 2002 ; Widdows 1976 ; Wilson and Elkaim 1991 -RRB- . Thus , the increasing abundance of relatively nutrient-poor and thermally dynamic habitats causes a gradual shrinking of the ecological niche of these bivalve taxa towards the warm end of their distribution range . The group-specific clines discussed in the preceding paragraph indicated differential adaptation to temperature among Mytilus spp. populations . Since these bivalve species have great dispersal capacities , strongly coupled to hydrodynamic circulation -LRB- Gilg and Hilbish 2002 -RRB- , genetic divergence within these species requires geographic isolation . During isolation in different climatic regions , selective genetic variation may have evolved at the same spatial scale as the observed neutral genetic variation . This may explain why the biogeography of these genetic groups is associated with European temperature gradients . Physiological studies revealed that mussels from different genetic groups exhibit different growth rates when hatched under similar conditions -LRB- Beaumont et al. 2004 ; Hillbish et al. 1994 -RRB- . Differential thermal adaptation has recently been demonstrated for different mussel species from the West coast of North America as well -LRB- Fields et al. 2006 -RRB- . The differential adaptation to temperature indicated by our results , combined with the strong spatial variability of the coastal climate in the Bay of Biscay -LRB- Puillat et al. 2004 -RRB- , may explain the broad and mosaic-like transition from one mussel-group present in this area to the next -LRB- Bierne et al. 2003 -RRB- . Q10 values lower than one only occur beyond the breakpoint temperature , where the metabolic rate decreases with increasing temperature . Since thermal conditions beyond breakpoint temperatures are not beneficial for bivalve performance and are most probably lethal when extended , it is most interesting to observe that the southernmost Mytilus spp. populations in our research area exhibited Q10 values of less than one at acclimatization temperatures in July 2004 . In the Santa Giusta Lagoon -LRB- 21 -RRB- , the monthly mean water temperature reached 27 °C , exceeding the breakpoint temperature of mussels . Very few bivalves survived the summer of 2004 in the Santa Giusta lagoon -LRB- 21 -RRB- , indicating that thermal tolerance limits were indeed crossed under field conditions . Survival of temperature-induced stress depends on its duration and on the physiological status and condition of the organisms . Widdows and Bayne -LRB- 1971 -RRB- found that mussels can cope with relatively high temperatures so long as they can regularly recover in water at a suitably low temperature . This is an important strategy that allows survival of temporary heat exposure , e.g. , when exposed to the air during low tide in summer . The range and limits of this relation for mussels or clams have not been studied in depth yet . In conclusion , we demonstrated that the respiratory responses to temperature of two European bivalve taxa are greatly dependent on seasonal variations in temperature . These responses , obtained throughout all seasons and at a large geographic scale , fit together in a framework when presented as a function of the acclimatization temperature . This framework is useful in both the fundamental and the applied sciences , facilitating the interpretation of respiration rates measured under ambient conditions , and the further development of ecophysiological theory . We observed that the maximum thermal sensitivity of the metabolic rate decreases with increasing acclimatization temperature , crossing a threshold -LRB- Q 10 = 1 -RRB- in Mytilus spp. at the maximum acclimatization temperatures observed in the field . Whether the temperature quotient will become less than one in M. balthica populations when the acclimatization temperature exceeds 23 °C can not be answered with any certainty , since no breakpoint temperature is observed in the experimental southern populations under or near ambient conditions . -LRB- Onto -RRB- genetic adaptation to regionally different climates implies that climate change will affect not only marginal populations via their metabolic rates , but all genetic groups are expected to shift northward with increasing temperatures . Although the dispersal capacity of mussel larvae and the active transport of juvenile and adult mussels for aquaculture purposes support range shifts with the speed of climate change , other ecological and physiological variables and their impact on the environment need to be investigated to predict the fate of mussels and other bivalve populations under changing climatic conditions . For M. balthica populations , no differential adaptation to temperature was observed among divergent groups , which leads us to expect that the direct impact of climate-induced temperature changes will be restricted to the southernmost populations . Electronic supplementary material Below is the link to the electronic supplementary material . -LRB- DOC 57 kb -RRB-

O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O

climate change
respiration rate
thermal tolerance
distribution range
metabolic rate


Surgical

management

of

dural

arteriovenous

fistulas

with

transosseous

arterial

feeders

involving

the

jugular

bulb

Dural

arteriovenous

fistulas

located

in

the

vicinity

of

the

jugular

foramen

are

complex

vascular

malformations

and

belong

to

the

most

challenging

skull

base

lesions

to

treat

The

authors

comprehensively

analyze

multiple

features

in

a

series

of

dural

arteriovenous

fistulas

with

transosseous

arterial

feeders

involving

the

jugular

bulb

Four

patients

who

underwent

surgery

via

the

transcondylar

approach

to

treat

dural

arteriovenous

fistulas

around

the

jugular

foramen

were

retrospectively

reviewed

Previously

endovascular

treatment

was

attempted

in

all

patients

The

success

of

the

surgical

treatment

was

examined

with

postoperative

angiography

Complete

obliteration

of

the

dural

arteriovenous

fistulas

-LRB-

DAVFs

-RRB-

was

achieved

in

three

patients

and

significant

flow

reduction

in

one

individual

All

patients

had

a

good

postoperative

outcome

and

only

one

experienced

mild

hypoglossal

nerve

palsy

Despite

extensive

bone

drilling

an

occipitocervical

fusion

was

necessary

in

only

one

patient

with

bilateral

lesions

The

use

of

an

individually

tailored

transcondylar

approach

to

treat

dural

arteriovenous

fistulas

at

the

region

of

the

jugular

foramen

is

most

effective

This

approach

allows

for

complete

obliteration

of

the

connecting

arterial

feeders

and

removal

of

bony

structures

containing

pathological

vessels

Introduction

Ten

to

of

intracranial

arteriovenous

fistulas

are

dural

lesions

-LSB-

-RSB-

and

these

are

most

commonly

related

to

dural

venous

sinuses

-LSB-

-RSB-

Only

a

few

previous

articles

have

reported

the

less

common

intraosseous

dural

arteriovenous

fistulas

occurring

at

the

anterior

or

posterior

skull

base

-LSB-

-RSB-

Although

the

pathogenesis

of

dural

arteriovenous

fistulas

-LRB-

DAVFs

-RRB-

is

not

yet

well

understood

angiogenic

factors

and

local

hypoxia

might

play

the

most

important

roles

in

angiogenesis

of

DAVFs

-LSB-

-RSB-

The

known

experience

suggests

that

the

natural

history

of

DAVFs

is

sometimes

progressive

and

intervention

aiming

at

closure

of

these

fisulas

should

be

considered

in

selected

cases

either

surgically

endovascularly

or

radiosurgically

-LSB-

-RSB-

In

some

circumstances

successful

obliteration

may

not

be

possible

by

endovascular

means

or

patients

may

refuse

the

radiosurgical

treatment

Direct

surgery

may

be

the

best

treatment

option

in

such

cases

Surgical

treatment

of

the

DAVFs

at

the

jugular

foramen

region

aims

at

removal

of

the

bony

parts

that

contain

the

pathological

vessels

and

physical

interruption

or

obliteration

of

the

arterialised

leptomeningeal

venous

connection

In

the

patients

we

have

treated

so

far

the

fistula

complex

was

located

within

or

in

the

vicinity

of

the

occipital

condyle

rendering

the

suboccipital

transcondylar

approach

as

the

best

access

route

for

surgical

treatment

Several

previous

studies

related

to

fistulas

with

transosseous

arterial

feeders

dealt

with

endovascular

embolization

or

with

a

similar

surgical

technique

but

in

many

aspects

different

from

ours

-LSB-

-RSB-

It

was

the

aim

of

the

present

study

to

detail

our

surgical

technique

for

the

treatment

of

DAVFs

in

the

region

of

the

jugular

foramen

and

to

retrospectively

review

the

clinical

outcome

of

four

patients

treated

at

our

institute

during

a

period

Patients

and

methods

Patients

Between

June

and

February

four

patients

underwent

surgery

at

the

Department

of

Neurosurgery

Philipps

University

for

removal

of

DAVFs

involving

the

jugular

foramen

Patients

ranged

in

age

from

to

years

with

a

mean

of

years

There

were

three

females

and

one

male

one

individual

had

bilateral

lesions

Four

lesions

were

located

on

the

right

and

one

on

the

left

side

All

patients

were

symptomatic

the

most

common

presenting

symptom

being

pulsatile

bruit

The

clinical

details

are

summarized

in

Table

Table

of

clinical

featuresCase

no.Age

sexPresentationLocationEmbolizationAngiographyAttempts

and

bruit

rt.

hypoglossal

nerve

paresisRt

jugular

process

and

bulbYesFeeders

rt.

ascending

pharyngeal

and

occipital

arteries

of

daysNo

additional

deficits

symptom

bruit

swelling

of

rt.

upper

and

lower

eyelidsRt

jugular

process

and

bulbYesFeeders

Both

ascending

pharyngeal

and

rt.

occipital

arteries

of

daysNo

deficits

symptoms

bruitDorsal

rim

of

foramen

magnum

both

occipital

condyles

and

jugular

processesYesFeeders

Both

internal

maxillary

and

occipital

arteries

of

monthNo

deficits

bruitRt

Jugular

tubercle

and

bulbYesFeeders

rt.

ascending

pharyngeal

and

occipital

arteries

of

daysMild

hypoglossal

nerve

palsy

symptom-freeAbbreviations

Y

years

M

male

F

female

Rt

right

ECA

external

carotid

artery

Attempts

and

interval

attempts

of

endovascular

embolization

and

timing

between

the

last

endovascular

and

surgical

treatment

All

patients

underwent

preoperative

angiography

and

at

least

two

attempts

of

endovascular

embolization

For

the

occlusion

of

arterial

feeders

Guglielmi

electrolytically

detachable

platinum

coils

were

used

The

decision

for

surgical

intervention

was

made

after

the

endovascular

approach

proved

unsuccessful

in

terms

of

complete

obliteration

and

the

patient

developed

neurological

deficits

or

intolerable

symptoms

of

pulsatile

bruit

Case

histories

Case

A

male

presented

with

a

history

of

pulsatile

tinnitus

in

the

right

ear

Neurological

examination

revealed

a

partial

right-sided

hypoglossal

palsy

Superselective

angiography

disclosed

multiple

DAVFs

between

the

distal

right

sigmoid

sinus

and

transosseous

arterial

feeders

from

the

right

ascending

pharyngeal

and

right

occipital

arteries

Although

the

endovascular

intervention

resulted

in

coil

occlusion

of

the

occipital

artery

the

DAVFs

still

persisted

-LRB-

Fig.

-RRB-

Microsurgical

intervention

was

performed

due

to

intolerable

pulsatile

tinnitus

with

the

patient

in

the

sitting

position

Only

minimal

bony

involvement

around

the

jugular

foramen

was

detectable

on

the

CT

scan

-LRB-

Fig.

-RRB-

Fig.

with

transosseous

arterial

feeders

Right

external

carotid

angiogram

antero-posterior

-LRB-

AP

-RRB-

-LRB-

a

-RRB-

and

lateral

-LRB-

b

-RRB-

views

demonstrate

arteriovenous

fistulas

-LRB-

arrows

-RRB-

adjacent

to

the

right

internal

jugular

bulb

The

fistulas

are

mainly

fed

by

the

right-sided

ascending

pharyngeal

and

occipital

arteries

Symptoms

were

improved

following

transarterial

embolization

with

coils

-LRB-

c

-RRB-

but

the

fistulas

persisted

Intraoperative

photograph

with

the

patient

in

the

sitting

position

showing

the

electrodes

for

lower

cranial

nerve

monitoring

-LRB-

d

-RRB-

Postoperative

angiograms

-LRB-

e

and

f

-RRB-

demonstrate

cure

of

the

DAVFs

The

same

patient

's

axial

CT

scan

reveals

the

preoperative

intraosseous

lesion

near

the

jugular

process

-LRB-

g

-RRB-

Postoperative

CT

scan

shows

minimal

bony

removal

-LRB-

h

-RRB-

Case

This

female

had

suffered

from

pulsatile

tinnitus

in

the

right

ear

for

more

than

years

During

this

period

the

patient

was

angiographically

diagnosed

as

having

DAVFs

in

the

region

of

the

right

jugular

bulb

Four

sessions

of

endovascular

intervention

were

performed

without

success

Several

months

before

admission

the

patient

experienced

a

clinical

deterioration

in

the

form

of

right

periorbital

swelling

In

addition

there

was

excessive

lacrimation

of

the

right

eye

and

progressive

numbness

occurred

around

her

right

ear

On

the

CT

scan

a

bony

erosion

of

the

medial

portion

of

the

right

occipital

condyle

and

jugular

tubercle

became

evident

A

recent

angiography

disclosed

the

typical

early

filling

of

the

right

jugular

bulb

and

right

sigmoid

and

transverse

sinuses

through

intraosseous

DAVFs

mainly

supplied

by

both

ascending

pharyngeal

arteries

and

both

occipital

arteries

-LRB-

Fig.

-RRB-

The

patient

subsequently

underwent

surgical

intervention

in

the

left

park

bench

position

-LRB-

Fig.

-RRB-

Fig.

-LRB-

a

-RRB-

and

AP

-LRB-

b

-RRB-

preoperative

angiograms

of

the

right

common

carotid

artery

-LRB-

CCA

-RRB-

demonstrating

the

right

intraosseous

DAVFs

-LRB-

arrows

-RRB-

Postoperative

right

CCA

angiogram

revealing

the

remaining

fistula

-LRB-

c

-RRB-

On

the

CT

scan

-LRB-

d

-RRB-

bony

erosion

of

the

medial

portion

of

the

right

jugular

tubercle

becomes

evident

-LRB-

white

arrows

-RRB-

Selective

injection

of

preoperative

right

occipital

artery

reveals

intraosseous

fistula

-LRB-

e

-RRB-

The

patient

is

positioned

in

the

left

lateral

park

bench

position

-LRB-

f

-RRB-

Case

A

female

presented

with

a

history

of

bilateral

pulsatile

tinnitus

predominant

in

the

right

ear

Neurological

examination

was

irrelevant

and

superselective

angiography

revealed

numerous

bilateral

DAVFs

in

the

foramen

magnum

region

affecting

both

occipital

condyles

and

jugular

processes

-LRB-

Fig.

-RRB-

The

fistula

drained

into

both

jugular

veins

respectively

Feeding

arteries

were

branches

from

the

internal

maxillary

and

occipital

arteries

After

partial

occlusion

of

feeders

on

the

right

side

the

intensity

of

the

tinnitus

decreased

but

still

persisted

The

patient

was

severely

affected

by

this

symptom

Surgery

was

therefore

carried

out

using

a

right

transcondylar

exposure

and

post-operatively

the

patient

reported

further

improvement

with

minimal

residual

tinnitus

During

a

follow-up

the

intensity

of

left

pulsatile

bruit

increased

Additionally

the

patient

developed

a

movement-related

neck

pain

which

proved

to

be

caused

by

a

fracture

of

the

right

occipital

condyle

with

dislocation

of

a

bony

fragment

and

craniocervical

instability

-LRB-

Fig.

-RRB-

She

underwent

a

second

surgical

procedure

via

a

left

transcondylar

approach

to

treat

the

left

DAVFs

followed

by

an

occipitocervical

fusion

performed

in

the

same

surgical

setting

-LRB-

Fig.

-RRB-

Fig.

intraosseous

DAVFs

causing

bilateral

pulsatile

tinnitus

Right

lateral

-LRB-

a

-RRB-

and

AP

-LRB-

b

-RRB-

external

carotid

angiograms

as

well

as

right

AP

-LRB-

c

-RRB-

common

carotid

angiogram

demonstrate

multiple

arteriovenous

shunts

fed

by

the

right

internal

maxillary

and

occipital

arteries

MRI

-LRB-

d

-RRB-

and

CT

-LRB-

e

-RRB-

studies

show

the

abnormal

vessels

posterior

to

the

right

jugular

tubercle

and

the

enlarged

jugular

foramen

with

its

surrounding

bony

erosion

respectively

-LRB-

arrows

-RRB-

The

photograph

shows

the

skin

incision

for

the

right

transcondylar

approach

-LRB-

f

-RRB-

Intraoperative

screenshot

of

navigation

applied

for

localizing

the

exent

of

the

arteriovenous

fistulas

-LRB-

g

-RRB-

Fig.

CT

scan

of

the

same

patient

shown

in

Fig.

reveals

a

fracture

of

the

right

occipital

condyle

with

dislocation

of

a

bony

fragment

-LRB-

a

-RRB-

Postoperative

angiograms

of

the

right

external

carotid

artery

-LRB-

ECA

-RRB-

lateral

-LRB-

b

-RRB-

and

AP

-LRB-

c

-RRB-

views

showing

no

arteriovenous

fistula

after

the

surgical

resection

of

right

intraosseous

DAVFs

Preoperative

angiogram

of

the

left

ECA

revealing

arterial

filling

of

the

jugular

vein

and

left-side

DAVFs

-LRB-

d

-RRB-

The

patient

is

placed

in

the

prone

position

for

the

surgery

of

the

left

intraosseous

DAVFs

and

the

occipito-cervical

fusion

-LRB-

e

-RRB-

Postoperative

lateral

plain

radiogram

-LRB-

f

-RRB-

and

a

schematic

drawing

-LRB-

g

-RRB-

demonstrating

the

instrumentation

used

for

the

occipitocervical

fusion

-LRB-

g

-RRB-

Case

This

female

complained

of

progressive

pulsatile

right-sided

tinnitus

for

year

Neurological

examination

was

irrelevant

An

angiogram

obtained

at

our

institution

furnished

evidence

of

DAVFs

at

the

right

occipital

condyle

and

jugular

tubercle

The

fistula

was

mainly

fed

by

meningeal

branches

of

the

right

occipital

and

ascending

pharyngeal

arteries

The

patient

underwent

embolization

of

the

right

occipital

artery

aimed

at

reducing

the

arterial

supply

Due

to

persistent

arteriovenous

connection

and

impairment

of

the

patient

's

quality

of

life

surgery

was

subsequently

performed

Surgical

technique

All

surgical

procedures

were

performed

by

the

senior

author

-LRB-

H.B.

-RRB-

The

first

aim

of

surgery

was

an

adequate

exposure

of

the

dorsolateral

suboccipital

region

including

the

medial

portion

of

the

occipital

condyle

the

lateral

rim

of

the

foramen

magnum

the

arch

of

the

atlas

and

the

horizontal

portion

of

the

vertebral

artery

as

well

as

the

medial

mastoid

and

particularly

the

jugular

process

region

-LRB-

Fig.

-RRB-

The

patient

was

placed

either

in

the

sitting

or

in

the

lateral

park

bench

position

with

the

head

flexed

turned

to

the

ipsilateral

and

slightly

tilted

to

the

contralateral

side

It

was

considered

important

to

reduce

the

venous

congestion

by

avoiding

jugular-vein

compression

or

by

elevating

the

head

when

the

lateral

park

bench

position

was

chosen

Arterial

feeders

were

occasionally

encountered

during

muscular

dissection

in

the

course

of

the

occipital

artery

in

those

patients

in

whom

the

artery

has

not

been

completely

obliterated

endovascularly

before

surgery

Fig.

particular

arteriovenous

fistulas

are

located

within

the

occipital

condyle

and

the

jugular

foramen

region

These

fistulas

are

fed

by

dural

branches

of

both

internal

and

external

carotid

arteries

-LRB-

upper

-RRB-

The

drawing

demonstrates

the

intraosseous

fistulas

arterialized

diploic

veins

and

draining

vein

-LRB-

lower

-RRB-

First

a

small

dorso-lateral

suboccipital

craniectomy

was

performed

which

basically

corresponds

to

a

dorso-lateral

enlargement

of

the

foramen

magnum

Bone

drilling

began

in

the

supracondylar

fossa

and

was

extended

both

medially

towards

the

rim

of

the

foramen

magnum

and

laterally

towards

the

mastoid

By

gradually

exposing

the

distal

sigmoid

sinus

and

the

dura

mater

of

the

suboccipital

and

upper

cervical

region

transosseous

arterial

feeders

were

encountered

which

occasionally

caused

a

brisk

arterial

bleeding

-LRB-

Fig.

-RRB-

To

control

this

bony

bleeding

drilling

was

temporarily

performed

using

the

diamond

burrs

without

saline

irrigation

-LRB-

Aesculap

drills

-RRB-

Application

of

bone

wax

or

bipolar

coagulation

to

stop

the

bleeding

was

usually

ineffective

In

the

patients

with

severe

bony

involvement

the

consistency

of

the

cancellous

bone

was

remarkably

altered

In

these

cases

the

bone

marrow

was

packed

with

Surgicel

and

then

slightly

compressed

with

cottonoid

to

control

the

bleeding

In

some

cases

the

arteriovenous

fistulas

involved

the

posterior

condylar

emissary

vein

located

within/around

the

posterior

condylar

canal

-LRB-

Fig.

-RRB-

These

bony

portions

were

completely

drilled

away

While

continuing

drilling

within

the

occipital

condyle

the

hypoglossal

canal

and

the

medial

portion

of

the

jugular

bulb

were

gradually

exposed

The

medial

wall

of

the

jugular

bulb

being

the

site

of

the

arteriovenous

fistulas

was

coagulated

to

interrupt

small

arterial

feeders

of

this

area

-LRB-

Fig.

-RRB-

Fig.

illustration

showing

the

transcondylar

approach

as

applied

to

interrupt

the

connecting

arterial

feeders

the

extent

of

the

bony

removal

is

judged

according

to

the

extent

of

the

arteriovenous

fistulas

Transosseous

arterial

feeders

are

encountered

which

may

occasionally

cause

a

brisk

arterial

bleedingFig

drawing

of

intraosseous

dural

arteriovenous

fistulas

in

the

right

hypoglossal

canal

and

in

the

vicinity

of

the

jugular

foramen

region

The

feeders

are

the

dural

branches

of

the

ascending

pharyngeal

artery

These

arterial

feeders

connect

with

the

inferior

petrosal

sinus

the

jugular

bulb

and

the

posterior

condylar

emissary

vein

-LRB-

right

jugular

bulb

right

posterior

emissary

vein

right

inferior

petrosal

sinus

arterialized

venous

plexus

within

the

right

hypoglossal

canal

right

ascending

pharyngeal

artery

a

right

internal

auditory

canal

b

pars

nervosa

of

the

right

jugular

foramen

c

right

hypoglossal

canal

d

right

occipital

condyle

e

anterior

rim

of

the

foramen

magnum

-RRB-

Intraosseous

DAVFs

were

also

encountered

around

the

hypoglossal

canal

with

arteriovenous

shunts

flowing

into

the

venous

plexus

surrounding

the

hypoglossal

canal

and

more

anteriorly

in

the

region

of

the

inferior

petrosal

sinus

To

reach

this

area

the

bony

resection

was

extended

into

a

deeper

region

Use

of

the

intraoperative

microdoppler

probe

gave

a

good

impression

of

the

arterialization

of

the

jugular

bulb

Thus

persistence

of

intraosseous

arterial

feeders

indicated

that

bony

resection

had

to

be

continued

by

drilling

the

jugular

tubercle

the

occipital

condyle

and

the

jugular

process

The

required

extent

of

bone

removal

was

also

estimated

from

preoperative

imaging

and

was

related

to

anatomical

landmarks

such

as

the

hypoglossal

canal

the

posterior

condylar

emissary

canal

and

the

dural

entrance

of

the

vertebral

artery

Drilling

was

stopped

only

when

no

more

arterial

feeders

were

encountered

indicating

that

all

feeders

had

been

interrupted

Normalization

of

blood

flow

within

the

jugular

bulb

could

be

documented

by

using

the

microdoppler

probe

To

adequately

drill

the

dorsomedial

portion

of

the

occipital

condyle

a

small

portion

of

the

lateral

atlantal

mass

had

to

be

resected

in

some

instances

as

well

In

such

cases

complete

exposure

of

the

horizontal

portion

of

the

vertebral

artery

was

necessary

However

there

was

no

need

for

complete

hemilaminectomy

The

suboccipital

dura

mater

was

not

opened

since

an

intradural

inspection

of

the

jugular

foramen

was

unnecessary

as

there

were

no

intradural

arteriovenous

shunts

After

meticulous

extradural

hemostasis

wound

closure

was

obtained

in

several

layers

Results

All

four

patients

underwent

surgical

obliteration

of

their

DAVFs

via

the

transcondylar

approach

This

access

route

provided

a

good

exposure

of

the

target

site

and

allowed

occlusion

of

the

intraosseous

pathological

vessels

There

were

no

intra-operative

complications

and

no

permanent

major

postoperative

deficit

occurred

Despite

a

certain

blood

loss

during

surgery

no

patient

required

intra-operative

or

postoperative

blood

transfusion

Although

an

extensive

resection

of

the

involved

occipital

condyle

jugular

process

and

jugular

tubercle

was

carried

out

in

all

patients

an

occipito-cervical

fusion

was

necessary

only

in

patient

with

bilateral

lesions

There

were

no

additional

neurological

deficits

with

the

exception

of

patient

who

experienced

mild

hypoglossal

nerve

palsy

postoperatively

Postoperative

angiography

was

obtained

in

each

patient

to

confirm

obliteration

of

the

DAVFs

Three

patients

showed

radiological

cures

with

no

further

treatment

necessary

In

patient

the

DAVFs

were

significantly

reduced

surgically

but

still

persisted

Therefore

a

second

surgical

intervention

was

proposed

to

the

patient

who

eventually

refused

While

preoperative

complaints

disappeared

in

three

patients

they

were

clearly

improved

in

one

individual

Discussion

Definition

terminology

pathology

and

symptoms

Dural

arteriovenous

fistulas

-LSB-

DAVFs

-RSB-

are

defined

as

abnormal

arteriovenous

connections

occurring

within

the

leaflets

of

the

dura

mater

usually

within

or

near

the

walls

of

a

dural

sinus

-LSB-

-RSB-

Although

the

term

dural

arteriovenous

malformations

-LSB-

DAVMs

-RSB-

has

been

used

widely

in

the

neuroscience

literature

current

nomenclatures

include

terms

such

as

DAVFs

and

dural

arteriovenous

shunts

according

to

an

accepted

view

that

many

of

these

lesions

are

acquired

-LSB-

-RSB-

Initially

DAVFs

were

described

only

in

association

with

venous

sinuses

Subsequently

they

have

been

found

in

other

locations

such

as

the

tentorium

the

skull

base

and

the

intraorbital

area

as

well

-LSB-

-RSB-

Piske

and

Lasjaunias

hypothesized

that

DAVFs

can

develop

wherever

veins

have

their

course

-LSB-

-RSB-

This

would

explain

why

DAVFs

can

be

located

entirely

within

the

bone

because

emissary

veins

have

transosseous

courses

The

particular

group

of

dural

arteriovenous

fistulas

located

within

the

occipital

condyle

and

jugular

foramen

region

are

intracavarial

-LRB-

intracranial

-RRB-

arteriovenous

shunts

fed

by

dural

branches

of

both

internal

and

external

carotid

arteries

Some

authors

have

named

this

particular

lesion

intraosseous

DAVMs

-LSB-

-RSB-

or

intraossous

DAVFs

-LSB-

-RSB-

The

fistulas

are

located

within

the

bony

structures

surrounding

the

jugular

bulb

-LRB-

the

major

draining

vein

-RRB-

and

may

involve

the

adjacent

draining

veins

-LSB-

-RSB-

DAVFs

involving

the

transverse

and

sigmoid

sinuses

always

cause

a

pulsatile

tinnitus

-LSB-

-RSB-

It

seems

that

this

symptom

is

related

to

venous

turbulence

in

contact

with

the

petrous

bone

or

to

the

high

shunt

flow

into

the

petrosal

sinus

-LSB-

-RSB-

This

might

explain

why

all

our

patients

presented

with

bruit

as

the

predominant

symptom

Imaging

DAVFs

are

often

invisible

on

CT

and

MR

studies

-LSB-

-RSB-

Consequently

a

normal

contrast-enhanced

CT

or

MR

study

does

not

exclude

a

DAVF

Contrary

to

the

ordinary

DAVFs

CT

and

MRI

studies

aid

in

giving

the

diagnosis

of

this

particular

DAVFs

when

the

patient

presents

with

pulsatile

tinnitus

due

to

demonstrable

abnormal

vessels

in

the

soft

tissue

beneath

the

skull

base

-LSB-

-RSB-

or

when

bony

erosion

due

to

intraosseous

abnormal

vessels

is

present

as

in

the

patients

of

our

series

However

cerebral

angiography

remains

the

most

important

modality

in

evaluating

DAVFs

General

management

and

endovascular

intervention

According

to

current

opinion

no

single

treatment

is

ideal

for

the

obliteration

of

DAVFs

and

management

requires

an

interdisciplinary

team

approach

which

must

be

individualized

for

each

patient

Malik

et

al.

reported

two

patients

with

intraosseous

dural

arteriovenous

fistulas

located

at

the

foramen

magnum

He

postulated

that

the

intraosseous

nature

was

related

to

the

large

number

of

emissary

veins

in

this

region

and

recommended

the

exploration

of

the

adjacent

bone

until

the

entire

fistula

is

exposed

-LSB-

-RSB-

Our

observations

and

intraoperative

findings

confirm

this

operative

experience

that

considerable

but

controllable

hemorrhage

can

occur

during

bone

removal

As

being

less

invasive

than

surgery

endovascular

technique

is

given

preference

as

the

primary

treatment

However

transvenous

embolization

or

transarterial

coil

embolization

of

the

ascending

pharyngeal

artery

during

treatment

of

hypoglossal

DAVFs

may

sometimes

be

associated

with

complications

-LSB-

-RSB-

An

alternative

surgical

therapy

is

warranted

if

the

endovascular

technique

eventually

fails

as

it

happened

to

all

patients

of

this

study

The

reason

for

failure

of

the

endovascular

intervention

is

probably

the

great

number

of

arterial

feeders

that

traverse

through

the

occipital

condyle

and

jugular

process

to

enter

the

jugular

bulb

A

transvenous

embolization

was

not

carried

out

in

our

patients

to

avoid

the

risk

of

major

venous

occlusion

Although

stereotactic

radiosurgery

either

followed

or

not

followed

by

transarterial

particulate

embolization

of

accessible

external

carotid

feeding

vessels

became

the

primary

mode

of

treatment

at

some

institutions

-LSB-

-RSB-

it

may

not

always

replace

open

surgery

Radiosurgery

is

expected

to

cause

obliteration

of

DAVFs

between

and

years

after

treatment

-LSB-

-RSB-

and

it

is

not

considered

as

a

standard

therapy

for

all

types

of

DAVFs

Benign

cranial

DAVFs

-LSB-

-RSB-

though

are

a

developing

indication

for

radiosurgery

-LSB-

-RSB-

stereotactic

radiosurgery

may

be

considered

as

an

alternative

treatment

for

this

type

of

DAVFs

that

have

failed

other

treatments

-LSB-

-RSB-

Surgical

technique

and

avoidance

of

complications

In

the

majority

of

our

previously

treated

patients

we

have

used

the

juxtacondylar/transcondylar

approach

to

expose

various

intradural

craniospinal

lesions

-LSB-

-RSB-

To

treat

DAVFs

this

approach

was

slightly

modified

and

primarily

applied

with

the

purpose

of

interrupting

the

pathological

arterial

feeders

The

extent

of

bony

resection

at

the

skull

base

was

therefore

individually

tailored

according

to

the

extent

of

arteriovenous

fistulas

under

intraoperative

microdoppler

guidance

The

use

of

this

surgical

procedure

was

most

effective

as

all

patients

in

our

study

showed

postoperative

clinical

improvement

and

complete

obliteration

of

the

intraosseous

DAVF

in

three

patients

Only

one

patient

-LRB-

patient

-RRB-

whose

angiogram

revealed

residual

AV

fistulas

experienced

previously

developed

mild

periorbital

edema

We

believe

that

this

was

due

to

residual

pathological

vessels

anterior

to

the

jugular

bulb

an

area

very

difficult

to

reach

surgically

During

the

removal

of

pathological

bone

containing

abnormal

fistulas

in

this

patient

the

dilated

thin

wall

of

the

jugular

bulb

was

slightly

injured

After

packing

this

area

of

venous

bleeding

with

muscle

fascia

no

space

for

further

drilling

was

available

A

second

slightly-modified

surgical

intervention

was

therefore

proposed

to

the

patient

to

obliterate

the

remaining

fistulas

but

she

refused

Partial

resection

of

the

occipital

condyle

in

DAVFs

may

be

associated

with

the

risk

of

injury

to

the

vertebral

artery

and/or

jugular

bulb

or

damage

to

the

hypoglossal

nerve

Since

the

arteriovenous

fistulas

may

be

located

within

and

around

the

hypoglossal

canal

as

in

patient

of

our

series

the

rootlets

of

the

nerve

may

be

injured

by

surgical

manipulation

even

in

the

hands

of

a

very

experienced

neurosurgeon

Preoperative

imaging

with

thin-slice

CT

scans

or

image

fusion

technique

-LRB-

which

was

applied

in

the

last

three

patients

-RRB-

-LSB-

-RSB-

can

provide

valuable

information

about

the

local

topographical

anatomy

This

information

comprises

the

variable

anatomical

configuration

of

the

jugular

tubercle

the

course

of

the

canal

containing

the

posterior

condylar

emissary

vein

and

the

size

and

exact

location

of

arteriovenous

fistulas

Usually

the

partial

resection

of

the

occipital

condyle

with

opening

of

the

atlanto-occipital

joint

does

not

create

atlanto-occipital

instability

-LSB-

-RSB-

Only

in

the

case

of

extensive

bony

drilling

within

the

condyle

necessary

due

to

the

large

number

of

transosseous

pathological

feeders

a

partial

condylar

fracture

may

occur

as

it

happened

in

patient

of

this

series

However

an

occipito-cervical

fusion

was

undertaken

in

this

patient

only

because

she

harbored

bilateral

intraosseous

DAVFs

and

a

second

procedure

on

the

opposite

side

was

required

that

would

have

significantly

destabilized

the

atlanto-occipital

region

Conclusion

Dural

arteriovenous

fistulas

located

around

the

jugular

foramen

are

a

less

common

type

of

DAVFs

The

suboccipital

transcondylar

approach

is

considered

the

best

access

route

when

surgery

of

this

particular

pathology

is

intended

The

amount

of

pathological

bone

that

must

be

removed

by

drilling

depends

upon

the

extent

of

transosseous

arterial

feeders

Surgical

obliteration

of

this

complex

vascular

malformation

is

possible

at

least

in

the

cases

in

which

the

arterial

feeders

do

not

extend

too

far

anterior

to

the

jugular

bulb

With

this

surgical

technique

an

atlanto-occipital

instability

may

occur

in

very

large

or

bilateral

lesions

requiring

occipito-cervical

fusion

O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O B I O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O B I O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O O B I O O O O O O O O O O O O O O O O O O O O O O

intraosseous davfs
jugular bulb
occipital condyle
transcondylar approach

dural arteriovenous fistula
transosseous arterial feeder