Ligaments and joints

It is widely accepted that pregnancy increases the compliance of the ligaments in the pelvic area (Ritchie, 2003; Borg-Stein et al., 2005; Rundgren, 1974; Perezgrovas and An-derson, 1982; Musah et al., 1986). Increased compliance is attributed to increased hRLX levels being secreted by the corpus luteum in the ovary and by the placenta (Conrad and Baker, 2013; Goh et al., 2013). The hormone hRLX has been found to trigger the synthesis of new collagen by activating fbroblasts in the collagen fbers (MacLennan, 1991). This contributes to a change in the collagen fber distribution from large to small diameters (Blecher and Richmond, 1998) decreasing the stifness of the tissue (Rundgren, 1974;

Vol-lestad et al., 2012).

Increased compliance of the pelvic ligaments is essential to facilitate the passage of the fetus during childbirth (Rundgren, 1974; Ritchie, 2003; Borg-Stein et al., 2005; Perezgro-vas and Anderson, 1982; Musah et al., 1986). Previous radiological analyses in pregnant women have shown that the widening of the symphysis can increase by up to 9 mm (re-viewed in Young, 1940). Increased compliance of the pelvic ligaments during pregnancy is at the same time assumed to increase pelvic joint mobility which is associated with the high prevalence of low back pain and pelvic girdle pain in pregnant women (Ritchie, 2003;

Kristiansson et al., 1996; MacLennan et al., 1986b; Mens et al., 2009).

Apart from the pelvic ligaments, other types of ligaments are also assumed to be af-fected by increased compliance during pregnancy. One study by Rateitschak (1967), for example, detected a signifcant increase in tooth mobility in six of seven women in their last month of pregnancy. As the authors did not establish any changes in the bone socket, they concluded that the increased mobility is most likely attributed to an increased com-pliance of the periodontal ligaments (Rateitschak, 1967).

Evidence from hypermobility measurements with gonio- and hyperextensometers (Schau-berger et al., 1996; Lindgren and Kristiansson, 2014; Ostgaard et al., 1993; Marnach et al., ¨ 2003) that demonstrates an increased range of motion in several peripheral joints during pregnancy may indicate that peripheral ligaments become more compliant during preg-nancy, as well. Schauberger et al. (1996) conducted joint mobility measurements at the knee joint using a clinical KT1000 arthrometer. The authors observed an 83 % larger ex-tent of anterior tibial translation relative to the femur in the ninth month of pregnancy compared to in the EP. Other research groups (Lindgren and Kristiansson, 2014; Ostgaard ¨ et al., 1993) investigated the abduction angle of the fourth fnger and found the largest increase with 2 - 5 % in the 24^th WoP. An increase in the fexion-extension and medio-lateral (M-L) mobility of the wrist has been observed to be 10 % and 5 % larger in T3 compared to the values measured in T1 (Marnach et al., 2003).

There is disagreement about whether the pregnancy-induced peripheral joint laxity re-mains after delivery. Dumas and Reid (1997) used a clinical KT1000 arthrometer in 65 pregnant women to establish a 14 % decrease of anterior tibial translation from the

ffth month of pregnancy until the fourth month postpartum. In contrast, Schauberger et al. (1996) using the same KT1000 arthrometer in 21 pregnant women reported a further increase in the anterior tibial translation of 34 % two weeks after delivery (Schauberger et al., 1996). An increase in joint laxity in the PP has also been observed by Lindgren and Kristiansson (2014) who detected the largest abduction angle of the left fourth fnger at as late as 13 weeks postpartum.

A pregnancy-related increase in peripheral joint laxity is believed to be direction-specifc.

Measures from pregnancy and the PP demonstrated that the tibia displacement relative to the femur in the anterior direction signifcantly increases, while the displacement in the coronal plane and in the posterior direction decreases (Chu et al., 2019).

Furthermore, peripheral joint laxity seems to be related to the parity status. While Chu et al. (2019) observed an increased anterior knee joint laxity in primiparous women on-ly, previous studies, in contrast, reported an increased extent of fnger joint mobility in multiparous women (Calguneri et al., 1982; Ostgaard et al., 1993). According to Calgu-¨ neri et al. (1982), the largest extension of the metacarpophalangeal joint of the index fnger occurs during the second pregnancy. This change is likely to be persistent as the authors observed similar values in the third and fourth pregnancy (Calguneri et al., 1982).

In addition to range of motion measures in humans that do not directly measure joint laxity, Hart et al. (2000) determined the knee joint laxity in gestating and non-gestating rabbits by means of in vitro testing, thereby assessing translational movements of the tibia relative to the femur. Similar to observations in pregnant women, the knee joints of gestating rabbits demonstrated a signifcant increase in laxity compared to the non-gestating rabbits.

While an increased laxity of the pelvic joints during pregnancy is assumed to be associated with increased hRLX levels, it is also likely that hRLX leads to an increased peripheral joint laxity. However, two experimental studies failed to establish a relationship between these parameters (Schauberger et al., 1996; Marnach et al., 2003). Schauberger et al.

(1996) detected the highest hRLX levels in the EP when the extent of anterior tibial translation relative to the femur was marginally increased by 2 % of the total increase in

the end of pregnancy. Marnach et al. (2003) also reported the largest hRLX levels in T1 when the fexion-extension angle of the wrist was at the minimum. Only one study on pregnant women was found to report a positive correlation between hRLX levels and the ability to actively raise a straight leg from a lying position. This fnding might indicate that hRLX is more likely to afect the pelvic ligaments than the peripheral ligaments (Vollestad et al., 2012).

An increased knee joint laxity has also been assumed to be attributed to increased le-vels of estrogen during pregnancy. Charlton et al. (2001) determined the anterior knee joint laxity in the knees of 20 pregnant women using KT1000 arthrometer in the 30^th WoP and the ffth to the seventh week postpartum. In line with the 215-fold increase in the estrogen levels during pregnancy (during pregnancy: 10,755 ng/l, postpartum: 50 ng/l) the authors also measured signifcant larger knee joint laxity values during pregnancy (incre-ase: 33 %) than in the PP.

There is no evidence supporting the assumption that a reduced stifness of peripheral ligaments may lead to an increased peripheral joint laxity as has been shown for the pel-vic joint laxity (Young, 1940; Ritchie, 2003; Kristiansson et al., 1996; MacLennan et al., 1986b; Mens et al., 2009). Two animal studies analyzed gestation-related changes in the mechanical properties of ligaments at the knee joint by means of material testing (Hart et al., 2000; Rundgren, 1974). Hart et al. (2000) did not observe any efect of gestation on the ligament stifness of the medial collateral ligaments of gestating rabbits. Similarly, Rundgren (1974) did not observe any changes in the mechanical properties of the posteri-or cruciate ligament in gestating rats (Rundgren, 1974). It was only within the frst three days of the PP that the maximum load was reduced; it returned to control levels or levels higher than the control level thereafter.

In sum, pregnancy leads to an increased compliance of the pelvic ligaments to facili-tate childbirth (Rundgren, 1974; Ritchie, 2003; Borg-Stein et al., 2005; Perezgrovas and Anderson, 1982; Musah et al., 1986). It is assumed that the compliance of other liga-ments such as the peripheral ligaliga-ments may similarly increase (Schauberger et al., 1996;

Lindgren and Kristiansson, 2014; Ostgaard et al., 1993; Marnach et al., 2003). Increased ¨

compliance of peripheral ligaments is believed to be associated with an increased peri-pheral joint laxity that has been found to remain after delivery and to further increase with repeated pregnancies (Calguneri et al., 1982; Ostgaard et al., 1993). ¨

In contrast to the pelvic joint laxity, peripheral joint laxity is unlikely to be attributed to increased hRLX levels during pregnancy (Schauberger et al., 1996; Marnach et al., 2003).

Instead, increased levels of estrogen may afect the peripheral joints (Charlton et al., 2001). Information from two studies reveals that peripheral ligament stifness does not change during pregnancy (Hart et al., 2000; Rundgren, 1974).