Dominant role of interface over knee angle for cushioning impact loading and regulating initial leg stiffness

For in vivo impact loadings administered under controlled initial conditions, it was hypothesized that larger initial knee angles (IKA) and softer impacting interfaces would reduce impact loading and initial leg stiffness. A human pendulum was used to deliver controlled impacts to the right foot of 21 subjects for three IKA (0, 20 and 40°) and three interfaces (barefoot, soft and hard EVA foams). The external impact force and the shock experienced by the subjects' shank were measured simultaneously with a wall mounted force platform and a skin mounted accelerometer, respectively. Stiffness of the leg was derived using impact velocity and wall reaction force data. The results disproved the role of the knee joint in regulating initial leg stiffness and provided only partial support for the hypothesized improved cushioning. Larger knee flexion at contact reduced impact force but increased the shock travelling throughout the shank. Conversely, softer interfaces produced sizable reductions in both initial leg stiffness and severity of the impact experienced by the lower limb. Force rate of loading was found to be highly correlated (r=0.95) to limb stiffness that was defined by the heel fat pad and interface deformations. These results would suggest that interface interventions are more likely to protect the locomotor system against impact loading than knee angle strategies.     

All leg joints contribute to quiet human stance: A mechanical analysis

According to the state of the art model (single inverted pendulum) the regulation of quiet human stance seems to be dominated by ankle joint actions. Recent findings substantiated both in-phase and anti-phase fluctuations of ankle and hip joint kinematics can be identified in quiet human stance. Thus, we explored in an experimental study to what extent all three leg joints actually contribute to the balancing problem of quiet human stance. We also aimed at distinguishing kinematic from torque contributions. Thereto, we directly measured ankle, knee, and hip joint kinematics with high spatial resolution and ground reaction forces. Then, we calculated the six respective joint torques and, additionally, the centre of mass kinematics. We searched for high cross-correlations between all these mechanical variables. Beyond confirming correlated anti-phase kinematics of ankle and hip, the main results are: (i) ankle and knee joint fluctuate tightly (torque) coupled and (ii) the bi-articular muscles of the leg are well suited to fulfil the requirements of fluctuations around static equilibrium. Additionally, we (iii) identified high-frequency oscillations of the shank between about 4 and 8 Hz and (iv) discriminated potentially passive and active joint torque contributions. These results demonstrate that all leg joints contribute actively and concertedly to quiet human stance, even in the undisturbed case. Moreover, they substantiate the single inverted pendulum paradigm to be an invalid model for quiet human stance.     

Kinematics of lower limbs during walking are emulated by springy walking model with a compliantly connected,off-centered curvy foot

The dynamics of the center of mass (CoM) during walking and running at various gait conditions are well described by the mechanics of a simple passive spring loaded inverted pendulum (SLIP). Due to its simplicity, however, the current form of the SLIP model is limited at providing any further information about multi-segmental lower limbs that generate oscillatory CoM behaviors and their corresponding ground reaction forces. Considering that the dynamics of the CoM are simply achieved by mass-spring mechanics, we wondered whether any of the multi-joint motions could be demonstrated by simple mechanics. In this study, we expand a SLIP model of human locomotion with an off-centered curvy foot connected to the leg by a springy segment that emulates the asymmetric kinematics and kinetics of the ankle joint. The passive dynamics of the proposed expansion of the SLIP model demonstrated the empirical data of ground reaction forces, center of mass trajectories, ankle joint kinematics and corresponding ankle joint torque at various gait speeds. From the mechanically simulated trajectories of the ankle joint and CoM, the motion of lower-limb segments, such as thigh and shank angles, could be estimated from inverse kinematics. The estimation of lower limb kinematics showed a qualitative match with empirical data of walking at various speeds. The representability of passive compliant mechanics for the kinetics of the CoM and ankle joint and lower limb joint kinematics implies that the coordination of multi-joint lower limbs during gait can be understood with a mechanical framework.     

Lower extremity control during turns initiated with and without hip external rotation

The pirouette turn is often initiated in neutral and externally rotated hip positions by dancers. This provides an opportunity to investigate how dancers satisfy the same mechanical objectives at the whole-body level when using different leg kinematics. The purpose of this study was to compare lower extremity control strategies during the turn initiation phase of pirouettes performed with and without hip external rotation. Skilled dancers (n=5) performed pirouette turns with and without hip external rotation. Joint kinetics during turn initiation were determined for both legs using ground reaction forces (GRFs) and segment kinematics. Hip muscle activations were monitored using electromyography. Using probability-based statistical methods, variables were compared across turn conditions as a group and within-dancer. Despite differences in GRFs and impulse generation between turn conditions, at least 90% of each GRF was aligned with the respective leg plane. A majority of the net joint moments at the ankle, knee, and hip acted about an axis perpendicular to the leg plane. However, differences in shank alignment relative to the leg plane affected the distribution of the knee net joint moment when represented with respect to the shank versus the thigh. During the initiation of both turns, most participants used ankle plantar flexor moments, knee extensor moments, flexor and abductor moments at the push leg׳s hip, and extensor and abductor moments at the turn leg׳s hip. Representation of joint kinetics using multiple reference systems assisted in understanding control priorities.     

Leg and Joint Stiffness in Children with Spastic Diplegic Cerebral Palsy during Level Walking

Individual joint deviations are often identified in the analysis of cerebral palsy (CP) gait. However, knowledge is limited as to how these deviations affect the control of the locomotor system as a whole when striving to meet the demands of walking. The current study aimed to bridge the gap by describing the control of the locomotor system in children with diplegic CP in terms of their leg stiffness, both skeletal and muscular components, and associated joint stiffness during gait. Twelve children with spastic diplegia CP and 12 healthy controls walked at a self-selected pace in a gait laboratory while their kinematic and forceplate data were measured and analyzed during loading response, mid-stance, terminal stance and pre-swing. For calculating the leg stiffness, each of the lower limbs was modeled as a non-linear spring, connecting the hip joint center and the corresponding center of pressure, with varying stiffness that was calculated as the slope (gradient) of the axial force vs. the deformation curve. The leg stiffness was further decomposed into skeletal and muscular components considering the alignment of the lower limb. The ankle, knee and hip of the limb were modeled as revolute joints with torsional springs whose stiffness was calculated as the slope of the moment vs. the angle curve of the joint. Independent t-tests were performed for between-group comparisons of all the variables. The CP group significantly decreased the leg stiffness but increased the joint stiffness during stance phase, except during terminal stance where the leg stiffness was increased. They appeared to rely more on muscular contributions to achieve the required leg stiffness, increasing the muscular demands in maintaining the body posture against collapse. Leg stiffness plays a critical role in modulating the kinematics and kinetics of the locomotor system during gait in the diplegic CP.     

Joint stiffness of the ankle and the knee in running

The spring-mass model is a valid fundament to understand global dynamics of fast legged locomotion under gravity. The underlying concept of elasticity, implying leg stiffness as a crucial parameter, is also found on lower motor control levels, i.e. in muscle-reflex and muscle-tendon systems. Therefore, it seems reasonable that global leg stiffness emerges from local elasticity established by appropriate joint torques. A recently published model of an elastically operating, segmented leg predicts that proper adjustment of joint elasticities to the leg geometry and initial conditions of ground contact provides internal leg stability. Another recent study suggests that in turn the leg segmentation and the initial conditions may be a consequence of metabolic and bone stress constraints. In this study, the theoretical predictions were verified experimentally with respect to initial conditions and elastic joint characteristics in human running. Kinematics and kinetics were measured and the joint torques were estimated by inverse dynamics. Stiffnesses and elastic nonlinearities describing the resulting joint characteristics were extracted from parameter fits. Our results clearly support the theoretical predictions: the knee joint is always stiffer and more extended than the ankle joint. Moreover, the knee torque characteristic on the average shows the higher nonlinearity. According to literature, the leg geometry is a consequence of metabolic and material stress limitations. Adapted to this given geometry, the initial joint angle conditions in fast locomotion are a compromise between metabolic and control effort minimisation. Based on this adaptation, an appropriate joint stiffness ratio between ankle and knee passively safeguards the internal leg stability. The identified joint nonlinearities contribute to the linearisation of the leg spring.     

A bipedal compliant walking model generates periodic gait cycles with realistic swing dynamics

A simple spring mechanics model can capture the dynamics of the center of mass (CoM) during human walking, which is coordinated by multiple joints. This simple spring model, however, only describes the CoM during the stance phase, and the mechanics involved in the bipedality of the human gait are limited. In this study, a bipedal spring walking model was proposed to demonstrate the dynamics of bipedal walking, including swing dynamics followed by the step-to-step transition. The model consists of two springs with different stiffnesses and rest lengths representing the stance leg and swing leg. One end of each spring has a foot mass, and the other end is attached to the body mass. To induce a forward swing that matches the gait phase, a torsional hip joint spring was introduced at each leg. To reflect the active knee flexion for foot clearance, the rest length of the swing leg was set shorter than that of the stance leg, generating a discrete elastic restoring force. The number of model parameters was reduced by introducing dependencies among stiffness parameters. The proposed model generates periodic gaits with dynamics-driven step-to-step transitions and realistic swing dynamics. While preserving the mimicry of the CoM and ground reaction force (GRF) data at various gait speeds, the proposed model emulated the kinematics of the swing leg. This result implies that the dynamics of human walking generated by the actuations of multiple body segments is describable by a simple spring mechanics.     

Joit torque and energy patterns in normal gait

Experiments were conducted on normal level gait to determine the synergistic patterns present in the forces causing joint moments and those associated with the generation, absorption and transfer of mechanical energy. The following generalizations can be made about the patterns: (i) During swing phase three forces (gravitational, muscle and knee joint acceleration) are responsible for shank rotation, and are shown to act together during both acceleration and deceleration.—(ii) The patterns of generation, absorption and transfer of mechanical energy at the joints are detailed. These patterns demonstrate inter-segment transfers of energy through the joint centres, and through the muscles, as well as the more recognized generation and absorption by the muscles themselves.—As a result of the complexity shown in these patterns it is cautioned that fundamental relationships that may have been derived from controlled biomechanical experiments (such as horizontal flexion and extension of the forearm) are not likely to apply to more normal movements such as gait.     

Computational stability of human knee joint at early stance in Gait: Effects of muscle coactivity and anterior cruciate ligament deficiency

As one of the most complex and vulnerable structures of body, the human knee joint should maintain dynamic equilibrium and stability in occupational and recreational activities. The evaluation of its stability and factors affecting it is vital in performance evaluation/enhancement, injury prevention and treatment managements. Knee stability often manifests itself by pain, hypermobility and giving-way sensations and is usually assessed by the passive joint laxity tests. Mechanical stability of both the human knee joint and the lower extremity at early stance periods of gait (0% and 5%) were quantified here for the first time using a hybrid musculoskeletal model of the lower extremity. The roles of muscle coactivity, simulated by setting minimum muscle activation at 0–10% levels and ACL deficiency, simulated by reducing ACL resistance by up to 85%, on the stability margin as well as joint biomechanics (contact/muscle/ligament forces) were investigated. Dynamic stability was analyzed using both linear buckling and perturbation approaches at the final deformed configurations in gait. The knee joint was much more stable at 0% stance than at 5% due to smaller ground reaction and contact forces. Muscle coactivity, when at lower intensities (<3% of its maximum active force), increased dynamic stability margin. Greater minimum activation levels, however, acted as an ineffective strategy to enhance stability. Coactivation also substantially increased muscle forces, joint loads and ACL force and hence the risk of further injury and degeneration. A deficiency in ACL decreases total ACL force (by 31% at 85% reduced stiffness) and the stability margin of the knee joint at the heel strike. It also markedly diminishes forces in lateral hamstrings (by up to 39%) and contact forces on the lateral plateau (by up to 17%). Current work emphasizes the need for quantification of the lower extremity stability margin in gait.     

Biomechanical modeling of deep squatting: Effects of the interface contact between posterior thigh and shank

Epidemiological studies indicate that occupational activities that require extended deep knee flexion or kneeling are associated with a higher prevalence of knee osteoarthritis. In many sport activities, such as a catcher in a baseball or a softball game, athletes have to make repetitive deep squatting motions, which have been associated with the development of osteochondritis dissecans. Excessive deep knee flexion postures may cause excessive loading in the knee joint. In deep knee flexion postures, the posterior aspect of the shank will contact the posterior thigh, resulting in a compressive force within the soft tissues. The current study was aimed at analyzing the effects of the posterior thigh/shank contact on the joint loading during deep knee flexion in a natural knee. An existing, whole body model with detailed anatomical components of the knee (AnyBody) has been adopted and modified for this study. The effects of the posterior thigh/shank contact were evaluated by comparing the results of the inverse dynamic analysis for two scenarios: with and without the posterior thigh/shank contact force. Our results showed that, in a deep squatting posture (knee flexion 120+ degrees), the posterior thigh/shank contact helps reduce the patellofemoral (PF) and tibiofemoral (TF) normal contact forces by 42% and 57%, respectively.     

Effects of soft tissue artifacts on the calculated kinematics and kinetics of the knee during stair-ascent

Biomechanics of the knee during stair-ascent has mostly been studied using skin-marker-based motion analysis techniques, but no study has reported a complete assessment of the soft tissue artifacts (STA) and their effects on the calculated joint center translation, angles and moments at the knee in normal subjects during this activity. This study aimed to bridge the gap. Twelve young adults walked up a three-step stair while data were acquired simultaneously from a three-dimensional motion capture system, a force plate and a dynamic fluoroscopy system. The "gold standards" of poses of the knee were obtained using a 3D fluoroscopy method. The STA of the markers on the thigh and shank were then calculated, together with their effects on the calculated joint center translations, angles and moments at the knee. The STA of the thigh markers were greater than those on the shank, leading to significantly underestimated flexion and extensor moments, but overestimated joint center translations during the first half of the stance phase. The results will be useful for a better understanding of the normal biomechanics of the knee during stair-ascent, as a baseline for future clinical applications and for developing a compensation method to correct for the effects of STA.     

Human Gait Recognition Using Hip,Knee and Ankle Joint Ratios

The estimation of joint angle ratios for healthy and afflicted subjects in characterizing the human gait has great significance in the development of limb prosthetics. The two dimensional analysis of human gait was performed and the ratio of hip to knee, knee to ankle, hip to ankle as well as the time taken for achieving a gait were determined. The percentage of affliction was computed based on the joint angle ratios and comparison was made with healthy gait. The joint ratios were fed as input to the driving system which comprises of six DC motors for the positioning of knee, hip and ankle during gait. Then different control strategies like P, PI and PID were tested. The t-test and ANOVA analysis were conducted between healthy, afflicted and PID controller to determine the significant difference between their joint angle ratios. The estimation of joint angle ratio improved the accuracy of the control system drive (desired position of knee, hip and ankle motors). The presence of oscillations in the output response was reduced for P and PI controllers. The implementation of PID controller eliminated the presence of peak overshoot and more settling time. Thus the joint angle ratio provides the best possible assistance to the disabled persons by appropriately compensating the affliction.     

Novel approach to ambulatory assessment of human segmental orientation on a wearable sensor system

A new method using a double-sensor difference based algorithm for analyzing human segment rotational angles in two directions for segmental orientation analysis in the three-dimensional (3D) space was presented. A wearable sensor system based only on triaxial accelerometers was developed to obtain the pitch and yaw angles of thigh segment with an accelerometer approximating translational acceleration of the hip joint and two accelerometers measuring the actual accelerations on the thigh. To evaluate the method, the system was first tested on a 2° of freedom mechanical arm assembled out of rigid segments and encoders. Then, to estimate the human segmental orientation, the wearable sensor system was tested on the thighs of eight volunteer subjects, who walked in a straight forward line in the work space of an optical motion analysis system at three self-selected speeds: slow, normal and fast. In the experiment, the subject was assumed to walk in a straight forward way with very little trunk sway, skin artifacts and no significant internal/external rotation of the leg. The root mean square (RMS) errors of the thigh segment orientation measurement were between 2.4° and 4.9° during normal gait that had a 45° flexion/extension range of motion. Measurement error was observed to increase with increasing walking speed probably because of the result of increased trunk sway, axial rotation and skin artifacts. The results show that, without integration and switching between different sensors, using only one kind of sensor, the wearable sensor system is suitable for ambulatory analysis of normal gait orientation of thigh and shank in two directions of the segment-fixed local coordinate system in 3D space. It can then be applied to assess spatio-temporal gait parameters and monitoring the gait function of patients in clinical settings.     

All joint moments significantly contribute to trunk angular acceleration

Computationally advanced biomechanical analyses of gait demonstrate the often counter-intuitive roles of joint moments on various aspects of gait such as propulsion, swing initiation, and balance. Each joint moment can produce linear and angular acceleration of all body segments (including those on which the moment does not directly act) due to the dynamic coupling inherent in the interconnected musculoskeletal system. This study presents quantitative relationships between individual joint moments and trunk control with respect to balance during gait to show that the ankle, knee, and hip joint moments all affect the angular acceleration of the trunk. We show that trunk angular acceleration is affected by all joints in the leg with varying degrees of dependence during the gait cycle. Furthermore, it is shown that inter-planar coupling exists and a two-dimensional analysis of trunk balance neglects important out-of-plane joint moments that affect trunk angular acceleration.     

Image based weighted center of proximity versus directly measured knee contact location during simulated gait

To understand the mechanical consequences of knee injury requires a detailed analysis of the effect of that injury on joint contact mechanics during activities of daily living. Three-dimensional (3D) knee joint geometric models have been combined with knee joint kinematics to dynamically estimate the location of joint contact during physiological activities—using a weighted center of proximity (WCoP) method. However, the relationship between the estimated WCoP and the actual location of contact has not been defined. The objective of this study was to assess the relationship between knee joint contact location as estimated using the image-based WCoP method, and a directly measured weighted center of contact (WCoC) method during simulated walking. To achieve this goal, we created knee specific models of six human cadaveric knees from magnetic resonance imaging. All knees were then subjected to physiological loads on a knee simulator intended to mimic gait. Knee joint motion was captured using a motion capture system. Knee joint contact stresses were synchronously recorded using a thin electronic sensor throughout gait, and used to compute WCoC for the medial and lateral plateaus of each knee. WCoP was calculated by combining knee kinematics with the MRI-based knee specific model. Both metrics were compared throughout gait using linear regression. The anteroposterior (AP) location of WCoP was significantly correlated with that of WCoC on both tibial plateaus in all specimens (p<0.01, 95% confidence interval of Pearson?s coefficient r>0), but the correlation was not significant in the mediolateral (ML) direction for 4/6 knees (p>0.05). Our study demonstrates that while the location of joint contact obtained from 3D knee joint contact model, using the WCoP method, is significantly correlated with the location of actual contact stresses in the AP direction, that relationship is less certain in the ML direction.     

Gait and neuromuscular pattern changes are associated with differences in knee osteoarthritis severity levels

Knee osteoarthritis (OA) is a multifactoral, progressive disease process of the musculoskeletal system. Mechanical factors have been implicated in the progression of knee OA, but the role of altered joint mechanics and neuromuscular control strategies in progressive mechanisms of the disease have not been fully explored. Previous biomechanical studies of knee OA have characterized changes in joint kinematics and kinetics with the disease, but it has been difficult to determine if these biomechanical changes are involved in the development of disease, are in response to degenerative changes in the joint, or are compensatory mechanisms in response to these degenerative changes or other related factors as joint pain. The goal of this study was to explore the association between biomechanical changes and knee OA severity in an effort to understand the changing role of biomechanical factors in the progression of knee OA. A three-group cross-sectional model was used that included asymptomatic subjects, subjects clinically diagnosed with moderate knee OA and severe knee OA subjects just prior to total joint replacement surgery. Principal component analysis and discriminant analysis were used to determine the combinations of electromyography, kinematic and kinetic waveform pattern changes at the knee, hip and ankle joints during gait that optimally separated the three levels of severity. Different biomechanical mechanisms were important in discriminating between severity levels. Changes in knee and hip kinetic patterns and rectus femoris activation were important in separating the asymptomatic and moderate OA gait patterns. In contrast, changes in knee kinematics, hip and ankle kinetics and medial gastrocnemius activity were important in discriminating between the moderate and severe OA gait patterns.     

Elastic properties of an intact and ACL-ruptured knee joint: measurement, mathematical modelling, and haptic rendering

An analytical, dynamic model of the human knee joint has been developed to simulate the unloaded knee joint behaviour in 6 degrees of freedom. It is based on extensive robot-based measurements of the elastic properties of a human cadaver knee joint. The measured data are compared with data from the literature to ensure that a proper database for modelling is used. The analytical modelling of the passive elastic joint properties is done with Local Linear Model Trees. The deduced knee joint model incorporates passive elastic properties of the internal knee joint structures, passive elastic muscle forces, damping forces, gravitational forces, and external forces. There are two sets of parameters, one simulating the movement of the intact knee joint, and a second simulating the knee joint with ruptured anterior cruciate ligament. The dynamic model can be easily processed in real-time. It is implemented in the haptic display of the Munich Knee Joint Simulator (MKS), which enables a person to move a plastic leg driven by a robot manipulator and feel the simulated knee joint force. Orthopaedic physicians judged the performance of the dynamic knee joint model by executing physical knee joint tests at the MKS.     

Comparison of strain-gage and fiber-optic goniometry for measuring knee kinematics during activities of daily living and exercise

There is increasing interest in wearable sensor technology as a tool for rehabilitation applications in community or home environments. Recent studies have focused on evaluating inertial based sensing (accelerometers, gyroscopes, etc.) that provide only indirect measures of joint motion. Measurement of joint kinematics using flexible goniometry is more direct, and still popular in laboratory environments, but has received little attention as a potential tool for wearable systems. The aim of this study was to compare two goniometric devices: a traditional strain-gauge flexible goniometer, and a fiberoptic flexible goniometer, for measuring dynamic knee flexion/extension angles during activity of daily living: chair rise, and gait; and exercise: deep knee bends, against joint angles computed from a "gold standard" Vicon motion tracking system. Six young adults were recruited to perform the above activities in the lab while wearing a goniometer on each knee, and reflective markers for motion tracking. Kinematic data were collected simultaneously from the goniometers (one on each leg) and the motion tracking system (both legs). The results indicate that both goniometers were within 2-5 degrees of the Vicon angles for gait and chair rise. For some deep knee bend trials, disagreement with Vicon angles exceeded ten degrees for both devices. We conclude that both goniometers can record ADL knee movement faithfully and accurately, but should be carefully considered when high (>120?deg) knee flexion angles are required.     

Resonance-based oscillations could describe human gait mechanics under various loading conditions

The oscillatory behavior of the center of mass (CoM) and the corresponding ground reaction force (GRF) of human gait for various gait speeds can be accurately described in terms of resonance using a spring–mass bipedal model. Resonance is a mechanical phenomenon that reflects the maximum responsiveness and energetic efficiency of a system. To use resonance to describe human gait, we need to investigate whether resonant mechanics is a common property under multiple walking conditions. Body mass and leg stiffness are determinants of resonance; thus, in this study, we investigated the following questions: (1) whether the estimated leg stiffness increased with inertia, (2) whether a resonance-based CoM oscillation could be sustained during a change in the stiffness, and (3) whether these relationships were consistently observed for different walking speeds. Seven healthy young subjects participated in over-ground walking trials at three different gait speeds with and without a 25-kg backpack. We measured the GRFs and the joint kinematics using three force platforms and a motion capture system. The leg stiffness was incorporated using a stiffness parameter in a compliant bipedal model that best fitted the empirical GRF data. The results showed that the leg stiffness increased with the load such that the resonance-based oscillatory behavior of the CoM was maintained for a given gait speed. The results imply that the resonance-based oscillation of the CoM is a consistent gait property and that resonant mechanics may be useful for modeling human gait.     

Segment and joint angles of hind limb during bipedal and quadrupedal walking of the bonobo (Pan paniscus)

We describe segment angles (trunk, thigh, shank, and foot) and joint angles (hip, knee, and ankle) for the hind limbs of bonobos walking bipedally ("bent-hip bent-knee walking," 17 sequences) and quadrupedally (33 sequences). Data were based on video recordings (50 Hz) of nine subjects in a lateral view, walking at voluntary speed. The major differences between bipedal and quadrupedal walking are found in the trunk, thigh, and hip angles. During bipedal walking, the trunk is approximately 33-41 degrees more erect than during quadrupedal locomotion, although it is considerably more bent forward than in normal human locomotion. Moreover, during bipedal walking, the hip has a smaller range of motion (by 12 degrees ) and is more extended (by 20-35 degrees ) than during quadrupedal walking. In general, angle profiles in bonobos are much more variable than in humans. Intralimb phase relationships of subsequent joint angles show that hip-knee coordination is similar for bipedal and quadrupedal walking, and resembles the human pattern. The coordination between knee and ankle differs much more from the human pattern. Based on joint angles observed throughout stance phase and on the estimation of functional leg length, an efficient inverted pendulum mechanism is not expected in bonobos.