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https://doi.org/10.11613/BM.2024.030501

Laboratory medicine and sports: where are we now?

Lovorka Đerek orcid id orcid.org/0000-0002-3041-7718 ; Clinical Department for Laboratory Diagnostics, University Hospital Dubrava, Zagreb, Croatia;School of Medicine, Catholic University of Croatia, Zagreb, Croatia *
Vanja Radišić Biljak ; Department of Medical Laboratory Diagnostics, University Hospital Sveti Duh, Zagreb, Croatia; Faculty of Kinesiology, University of Zagreb, Zagreb, Croatia
Sanja Marević ; Clinical Department for Laboratory Diagnostics, University Hospital Dubrava, Zagreb, Croatia
Brankica Šimac ; Clinical Department for Laboratory Diagnostics, University Hospital Dubrava, Zagreb, Croatia
Marko Žarak ; Clinical Department for Laboratory Diagnostics, University Hospital Dubrava, Zagreb, Croatia;Faculty of Pharmacy and Biochemistry, University of Zagreb, Zagreb, Croatia
Antonija Perović ; Medical Biochemistry Laboratory, Health Care Institution Glavić, Dubrovnik, Croatia;Faculty of nursing and clinical nursing, University of Dubrovnik, Dubrovnik, Croatia
Domagoj Marijančević ; School of Medicine, Catholic University of Croatia, Zagreb, Croatia; Department of Clinical Chemistry, Sestre milosrdnice University Hospital Center, Zagreb, Croatia
Robert Buljubašić ; Department for Orthopedics and Traumatology, Clinic for Surgery, University Hospital Dubrava, Zagreb, Croatia
Luka Matanović ; Department for Orthopedics and Traumatology, Clinic for Surgery, University Hospital Dubrava, Zagreb, Croatia
Maja Cigrovski Berković ; Faculty of Kinesiology, University of Zagreb, Zagreb, Croatia

* Dopisni autor.


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Sažetak

Laboratory medicine in sport and exercise has significantly developed during the last decades with the awareness that physical activity contributes to improved health status, and is present in monitoring both professional and recreational athletes. Training and competitions can modify concentrations of a variety of laboratory parameters, so the accurate laboratory data interpretation includes controlled and known preanalytical and analytical variables to prevent misleading interpretations. The paper represents a comprehensive summary of the lectures presented during the 35th Annual Symposium of the Croatian Society of Medical Biochemistry and Laboratory Medicine. It describes management of frequent sport injuries and sums up current knowledge of selected areas in laboratory medicine and sports including biological variation, changes in biochemical parameters and glycemic status. Additionally, the paper polemicizes sex hormone disorders in sports, encourages and comments research in recreational sports and laboratory medicine. In order to give the wider view, the connection of legal training protocols as well as monitoring prohibited substances in training is also considered through the eyes of laboratory medicine.

Ključne riječi

sports; medical laboratory science; endocrinology; orthopaedics; biological variation

Hrčak ID:

321330

URI

https://hrcak.srce.hr/321330

Datum izdavanja:

15.10.2024.

Posjeta: 137 *




Introduction

Laboratory medicine in sport and exercise is not an old branch of laboratory science, but it has developed during the last decades with the awareness that physical activity contributes to improved health status (1,2). In that sense, laboratory medicine is present in monitoring both professional and recreational athletes. Knowing that sport can provide benefits in health as well as in disease, laboratory medicine in sports is considered to be a preventive science. Evaluation of the condition of an athlete includes monitoring of workloads and recovery period using various laboratory tests all to achieve top performance (3). That way it is possible to screen for injuries or medical conditions that can endanger the athlete as well as to optimize the training and recovery process (2,3). Training and competitions can modify concentrations of a variety of laboratory parameters, so the accurate laboratory data interpretation includes controlled and known preanalytical and analytical variables to prevent misleading interpretations (4). Sports physicians collect extensive amounts of clinical information, which, when combined with biochemical data, can improve understanding of sports physiology and pathology. Nevertheless, caution is necessary in their interpretation because the reference ranges differ between sedentary populations, recreational athletes, and especially elite athletes. Clinical interpretation of laboratory abnormalities in sport often does not reflect the onset of pathology, but could reflect a decrease of performances. That way it could lead to better management of overtraining and overreaching and defining athlete profile that all adds to preventive science description (5).

This paper gives an overview of the lectures presented at the 35th annual symposium ˝Laboratory medicine and sport: where are we now?“ organized by University Hospital Dubrava and under the auspices of Croatian Society of Medical Biochemistry and Laboratory Medicine (CSMBLM).

Biological variability in athletes

Beginning with the pioneer work of Ricos et al. and the first integrated table of analytes and derived laboratory performance specifications, freely available at the Westgard quality control web page, through 2014 European Federation of Clinical Chemistry and Laboratory Medicine (EFLM) 1st Strategic Conference for the defining analytical performance specifications, where analytical performance specifications were defined, among other models, by the model based on components of biological variation (BV) of the measurand, to the new EFLM updated biological variation database based on the strict meta-analysis of the published studies, biological variability has become an integrated part of laboratory medicine (6-8). The BV data are reference data that have many applications in laboratory medicine. The biological variability data describe the variability of clinically important measurands around homeostatic set points within subjects (intra-individual coefficient of variation - CVI) and between subjects (inter-individual CV), which enables the interpretation of laboratory results in clinical settings through reference change value (RCV). In a steady state setting, the concentration of most measurands is characterized by random variation around a homeostatic set point, whereas the concentration of some measurands is also influenced by different life phases or predictable cyclic variation (9). One of the newest possible applications of BV data is establishing individual reference intervals (9). However, it is worth emphasizing that the BV literature data is available mostly from studies performed on healthy non-athlete individuals. It is well known that intensive physical activity causes significant functional and metabolic changes and adaptations in the athlete’s organism. These adaptation changes encompass cells, tissues, organs, as well as total body physiological changes (10). The observed physiological changes result in scarcely described altered biochemical and hematological parameters. However, the newest initiative in anti-doping testing relies exclusively on observing the long-term physiological changes in the hematological and steroidal biochemical parameters in the blood of the athlete, the so-called Athlete Biological Passport (APB) (11). The APB comprises repeated measurements of hematological and steroidal markers which enables to establishment of the athlete’s laboratory results baseline. The APB longitudinally follows the athlete’s collected data and the possible observed differences are defined by BV. As a high level of physical exercise most probably influences BV, the studies performed on healthy non-athlete volunteers cannot be simply transferred to athletes (12). Recently, some BV studies performed on athletes were published. Diaz-Garzon et al. observed higher CVI estimates for routine laboratory biochemistry measurands in athletes than what has been reported for the general population (13). The observed differences may be related to physiological stress over time caused by the continuous practice of exercise. However, in a similar study performed by the same group of authors, CVI estimates of most hematological parameters in a group of recreational endurance athletes were similar to the general population and were not influenced by exercise or athletes’ state of health (14). It is evident from these conflicting results that there is substantial variability even among athletes, and future studies regarding BV data in this particular group of males and females are needed.

Effects of physical activity on biochemical tests

A sedentary life style can raise risks for various diseases, such as diabetes mellitus (DM), cardiovascular diseases (CVD), hypertension, but also cancer, so physical exercise is of utmost importance for the overall health status. Biochemical and hematological tests are prone to changes in blood of individuals, depending on the duration, intensity and frequency of physical exercises. These changes, which are not considered as preanalytical errors, may lead to benefits, such as reduced risk factors as lower lipid blood profile, but also to pathophysiological changes, such as cell injuries. Interpretation of these changes in the context of physically active subjects is crucial. Although, the majority of literature is investigating these parameters in professional athletes, there are evidences about many beneficial effects in average individuals but also in people with some morbidities (15-17).

Although, physical activity is an important preanalytical factor in biochemical tests, according to good laboratory practice (GLP) individuals should prior to phlebotomy, avoid physical activity at least 48 h (15). However, this GLP can’t always be respected when a patient is admitted to the emergency department.

The influence of physical exercise on a variety of common biochemical parameters are well known. First, there are changes of plasma volume which depend on the type of training exercises, so when interpreting laboratory tests, one should always take into consideration the extent of the possible hemoconcentration and/or hemodilution (15,16). Elevation of serum enzymes from the skeletal muscles like creatine kinase, aspartate aminotransferase (AST) and lactate dehydrogenase, depends on the duration and intensity of exercise, with highest values in untrained individuals (16).

According to literature, physical exercise in healthy women and men are related to higher HDL, lower LDL and triglycerides values, which contributes to lower risk for CVD (18-20). However, lipoprotein(a) (Lp(a)) and apolipoprotein B (apoB) remain unchanged (19). Additionally, lower concentrations of glucose, glycated haemoglobin (HbA1c), C-reactive protein (CRP), estimated glomerular filtration rate but higher concentrations of creatinine, iron, plasma calcium after aerobic or strength exercise are present (18). However, most of these parameters remain in the reference intervals, but there should be care regarding interpretation of these parameters, especially creatinine concentrations (18). In context of the type and frequency of exercise or gender, various influences are observed regarding concentrations of total cholesterol, AST, gamma-glutamyl transferase, alkaline phosphatase, uric acid, total bilirubin, and total iron binding capacity (18). The most frequent cause of anemia is iron deficiency, especially in female endurance athletes (16).

In patients with DM type 2, high intensity interval training resulted in whole body mass decrease, but also in lower concentrations of fasting and postprandial glucose and HbA1c (21).

Diagnosing and preventing hypoglycemia during and after exercise

Exercise is advocated in diabetes management guidelines as an important attribute to reaching glycemic goals and avoiding vascular complications in both people with type 2 and type 1 diabetes. On the other hand, exercise-related hypoglycemia is a major concern of people with diabetes; primarily those on insulin treatment (22). Therefore, balancing between regular exercise (and sports) participation and attainment of normoglycemia is of utmost importance, and modern technology in terms of improved insulins, means of their delivery, and glucose monitoring systems, is an important accomplice on this path (23). In addition, choosing the right exercise type and intensity and timing of the exercise during the day, can all influence exercising safety, i.e., minimize the risk of glycemic excursions into hyper- or hypoglycemic direction. Although the use of technology, especially continuous glucose monitoring (CGM) and intermittently scanned CGM made around-exercise glucose management safer and easier, there is still a need to extrapolate from the huge amount of data gained from technology to implement it in the user-friendly real-life setting and accommodate quick-decision making which is especially important during exercise and sport (24). The possible limitations related to new glucose monitoring systems must be taken into account. Mentioned primarily relates to acknowledging the lag time, which might be crucial during the exercise, where physiological factors such as body temperature and acidity related to working muscle and blood flow alterations can impact the sensor-measured accuracy of interstitial glucose concentrations. In addition, there are unanswered questions related to the positioning of the sensor in the context of different sports i.e., should for example cyclist wear the sensor on the leg instead of the forearm to increase the accuracy of glucose measurements? Yet another important aspect of technology use in sports is its implementation in sports nutrition and understanding of how interstitial glucose influences muscle fuelling in the setting of training or competition. Therefore, CGM use is an important tool to help prevent hypoglycemia during or after exercise, understand how different foods influence insulin sensitivity and therefore optimize pre-exercise/competition nutrition (25-27). Current guidelines attempted to set safe glucose targets around the exercise for people with type 1 diabetes concerning the intensity of exercise they participate in and based on their risk of hypoglycemia, incorporating the glucose trends gathered from sensor glucose measurements. Generally, the safe glucose ranges for starting the exercise and during the exercise is between 7 and 12 mmol/L. At the same time, values below or above this target might prompt carbohydrate intake and/or insulin dose reduction or postponement of exercise and insulin bolus and hydration, respectively (22,24). But it is important to keep in mind that each person is an individual and therefore guidelines are just provisory, while CGM will give individual insights that must be used as a learning tool to offer true precision care.

Sex hormone disorders - the other side of sports

Androgens have the potential to enhance athletic performance by influencing the structure of muscle tissue, bone mass, erythropoietin (EPO) effects, the immune system and behavioural patterns (28,29). Experimental findings indicate that testosterone increases skeletal muscle myostatin concentration, mitochondrial biogenesis, myoglobin expression and insulin-like growth factor I muscle content, potentially increasing skeletal muscle activity (30). Androgens promote bone growth, both directly and indirectly, through the local aromatization of estrogens (31). Increased bone mass and strength may be advantageous for sports involving explosive motions like throwing and jumping. Additionally, testosterone increases circulating hemoglobin concentrations and promotes the production of new erythrocytes, presumably by inducing lower hepcidin and higher EPO secretion (32,33). Furthermore, there was a positive correlation observed between the athletes’ performance and serum concentrations of dihydrotestosterone (DHT) and dehydroepiandrosterone (DHEA) (34). This finding is important since growing evidence suggests that DHEA is the major precursor of bioactive androgens in women, intracellularly transformed into testosterone and DHT, which bind to the androgen receptor (35). All of these results show that lean mass and physical performance have a positive correlation with endogenous androgen concentrations, regardless of whether they are beyond the reference intervals. In comparison to other female athletes with the same body mass index (BMI), endurance athletes with polycystic ovary syndrome (PCOS) perform significantly better in the multi-stage fitness test to determine a person’s aerobic capacity and demonstrate higher maximal oxygen uptake (VO2 max) during the treadmill fatigue test (36). Regardless of body composition, the PCOS women had superior muscle strength (bench press, leg extension, and handgrip strength). In the PCOS group, there was a positive association between elevated muscle strength and serum testosterone concentrations (37). Additionally, Olympic athletes had higher rates of PCOS and polycystic ovaries (38). These findings suggest that moderate forms of hyperandrogenism, especially PCOS, may enhance physical performance and affect women’s decision to participate in competitive sports. The concept of reverse causality is unsupported. Elite female athletes are more likely to have XY differences/disorders of sex development, which implies that these disorders may enhance physical performance. According to predictions, having testosterone concentrations in the “male” range gives female athletes an ergogenic advantage of more than 9% (39).

Hackney and colleagues described the rate of testosterone reduction required to identify an athlete as having the “Exercise Hypogonadal Male Condition” (40,41). These researchers proposed this differentiation as a relative form of functional hypogonadotropic hypogonadism required sustained testosterone concentrations at least 25% to 50% lower than expected for their age, representing a potential adaptive response in the hypothalamic-pituitary-gonadal (HPG) axis, from chronic, long-term exercise exposure. Evidence indicates that in males with Overtraining Syndrome and/or Triad/“Reduced Energy Deficiency in Sports” condition, a decrease in testosterone caused by exercise-induced relative hypogonadism is harmful. These individuals are unable to compete at their highest level or full potential due to deprived health and physical performance. Such individuals are suffering from a well-known endocrine dysfunction. However, it is crucial to remember that low testosterone-hypogonadism can occur in athletes as a result of additional circumstances, such as traumatic brain injuries incidents or anabolic androgenic steroids usage (42,43).

Recreational diving and laboratory medicine - can the depths of the sea change the results of laboratory tests?

Croatia is a Mediterranean country whose tourism activity is for its most part directly connected to the coast of the Adriatic Sea. According to the data of the Croatian Diving Association, which is a member of the World Diving Confederation (CMAS), 150 diving clubs and 150 diving centres are currently registered in Croatia (44). Since recreational SCUBA (self-contained underwater breathing apparatus) diving has become a very popular sport in the last 20 years, with millions of recreational divers worldwide and thousands in Croatia every year, there is a need to understand how it affects the physiology of the human body and whether the sea depths can affect the results of laboratory tests in healthy individuals who practice this sport recreationally. This information is especially important for laboratory professionals who work in laboratories located in the coastal region of Croatia.

SCUBA diving is a special form of physical activity that, due to changed environmental conditions (exposure to the hyperbaric conditions, elevated breathing pressure, effect of immersion, exposure to cold temperature) together with increased physical load, triggers stress response of the organism (45). According to their purpose, modern forms of diving can be divided into amateur (sports/recreational) and professional (technical) diving, of which more common is recreational diving. European (EN 14153-2) and international standards (ISO 24801-2) together with the CMAS documentation define recreational SCUBA diving as a form of diving limited to depths up to 40 meters using only compressed air or nitrox (a gas mixture of oxygen and nitrogen, where the proportion of oxygen does not exceed 40%) with direct, vertical access to the surface and gradual surfacing without decompression stop (46).

Numerous Croatian studies on Croatian divers have shown that all forms of diving can affect the results of laboratory tests that indicate activation, adaptation, or impairment (transient or permanent) of specific organ or organic system, depending on depth, duration and repetition (acute or chronic/repetitive effect). Those changes can be, not only statistically, but also clinically significant in healthy individual as compared to biological variation of specific parameters (RCV). Up to date, we know that SCUBA diving can cause changes in routine hematological parameters and erythropoiesis (47,48). It can also change oxidant/antioxidant status of the whole organism (49). Many studies have noticed transient impairment and adaptation of cardiac, muscular, and immune systems (50-52). Furthermore, it has recently been discovered that recreative SCUBA diving can also impact neurohormonal response and myokines-mediated communication between muscles and the brain (53). Finally, there are many other routine laboratory results that do not change after diving. The important goal of the further studies on Croatian population of divers should be inclusion of more participants, since all the studies have been performed on maximum of 15 to 20 divers.

As a concluding remark, the effects that recreative SCUBA diving induces in numerous organs and organic systems merit the attention and caution of clinicians and laboratory professionals when interpreting the laboratory test results in people who practice the sport. The added value brought by the presented studies is a translational potential in improving the health check strategy for professional divers.

The oxygen paradox - can intermittent hyperoxia have similar effects as altitude training?

In many sports, altitude or hypoxic training has become a standard training protocol before important competitions. There are several models of hypoxic training, such as live high-train high (LH-TH), live high-train low (LH-TL) and live low-train high (LL-TH), and the purpose of all of them is to stimulate adaptation mechanisms to a hypoxic condition resulting in improved endurance of athletes in a normoxic environment (54). Hypoxia provokes a natural and multiple response in the organism, activating biological processes at the cellular level and affecting various systems such as the hematopoietic, metabolic, respiratory, and cardiovascular (55). The hypoxic stress inside cells activates a family of transcriptional factors called Hypoxia Inducible Factors (HIFs) (56). HIFs modulate the response to hypoxia by prompting the expression of hundreds of genes that are involved in metabolism regulation, erythrocyte production, angiogenesis, cell growth/death, proliferation and differentiation, glycolysis, mitochondrial metabolism, immune and inflammatory response (57). For athletes, the key effect of altitude training or hypoxia exposure is the stimulation of EPO production, which accelerates erythropoiesis and oxygen delivery to the cells (58).

It has also been shown that oxygen concentration fluctuations, as a consequence of exposure to hyperoxia, can have a similar effect as hypoxia on EPO concentrations (55). A phenomenon known as the “oxygen paradox” was first observed and described in healthy subjects after breathing 100% oxygen at normal pressure (exposure to normobaric hypoxia for 2 h) (59). Later, an increase in EPO concentration was also observed after saturation dives (long-term exposure to hyperbaric hyperoxia) and recreational SCUBA diving performed once a week for five consecutive weeks (continuous short-term intermittent hyperbaric hyperoxia) (48,60,61). According to the “oxygen paradox” hypothesis, the return to normoxia, after exposure to hyperoxia, is interpreted by cells as hypoxia and gene expression regulated by HIFs is stimulated. It is postulated that these complex cellular signaling mechanisms are associated with changes in the oxidant-antioxidant status during hyperoxia and normoxia resulting in the stabilization of HIFs (62).

The EPO response after hyperoxic exposure opens up many areas of interest, not only for the improvement of athletes’ performance. Although the “oxygen paradox” theory provides a promising strategy for increased EPO production, further studies are needed.

Laboratory testing of athletes to detect doping

The Festina affair was a series of doping scandals in professional cycling that occurred during and after the 1998 Tour de France. This event prompted worldwide sports organisations to take action, leading to the establishment of the international independent World Anti-Doping Agency (WADA) in 1999. WADA’s main task is to develop, promote and coordinate anti-doping rules and measures in all sports and countries in order to ensure doping-free sport (63). According to the traditional definition, doping is the use of prohibited drugs or methods with the aim of improving psychophysical abilities. Today, doping is defined as one or more violations of the anti-doping rules laid down in the World Anti-Doping Code adopted by WADA (64).

The main document listing substances and methods of doping in sport is the WADA prohibited list, which is updated annually. In 2024, it includes 11 classes of prohibited substances (S0-S9 plus P1) and three categories of prohibited methods (M1-M3) (65). Athletes’ samples may only be analyzed in WADA-accredited laboratories, of which there are currently around 30 worldwide (66). Before WADA grants accreditation, laboratories must be accredited in accordance with the requirements of ISO/IEC 17025. Laboratories that are not accredited by WADA may be approved by WADA to perform blood sample analyses in support of the hematology module of the ABP. Athlete Biological Passport laboratories may be accredited to either ISO/IEC 17025 or ISO 15189 (67).

Laboratories must follow WADA’s International Standard for Laboratories to ensure that they report valid test results and facilitate the harmonisation of analytical testing of samples (67). Laboratories are required to perform all prescribed analytical test procedures set out by WADA in specific technical documents, technical letters or laboratory guidelines (68).

For most anabolic androgenic steroids and other anabolic agents, as well as for growth hormone, its fragments and releasing factors, β2-agonists, hormone and metabolic modulators and stimulants, the method of choice is gas (GC) or liquid chromatography coupled to mass spectrometry (MS) for both the initial testing procedure and the confirmation procedure in case of an initial adverse analytical finding or an atypical finding (67). A more specific example refers to a case of suspicious steroid profile data, when the confirmatory method of choice is GC/combustion/Isotope Ratio MS to determine if significant differences exist between the carbon isotope signatures of target compounds and endogenous reference compounds such as pregnanediol, pregnanetriol, 11β-hydroxy-androsterone and 11-oxo-etiocholanolone (69).

Electrophoretic methods, affinity binding assays (e.g. immunoassays) and other analytical methods are also routinely used to detect various macromolecules in samples. It is important to note that affinity binding assays must differ in the use of affinity reagents (e.g. antibodies) depending on whether they are used for initial or confirmatory testing. They should recognise different epitopes of the macromolecule being analyzed, unless a purification (e.g. immunopurification) or separation method (e.g. electrophoresis, chromatography) is used prior to the application of the affinity binding assay to eliminate potential cross-reactivity (67).

The further optimisation and refinement of analytical methods, the expansion of knowledge about the metabolism and disposition of drugs, but also about the possibilities of eliminating interfering factors, are currently the most important goals of laboratory medicine-related research in the anti-doping community (70).

Achilles tendon rupture - operative versus nonoperative treatment - does the room for the laboratory medicine appear?

Achilles tendon ruptures (ATR) are among the most common injuries in professional and recreational athletes with estimated annual incidence between 13 and 55 per 100,000 (71,72). Due to the possibility of severe functional limitations of professional athletes, a rational decision about optimal treatment has to be made on evidence-based principles. The summary of the dilemma when choosing between operative and conservative treatment is that the surgical approach yields a lower re-rupture risk but concomitantly associates with an increase in complication risks such as infections or nerve damage (72). The surgeon chooses the treatment method individually based on the clinical examination, patient characteristics, and expectations, combined with the ultrasound findings. In the moment of deciding for the type of treatment, laboratory findings do not play a significant role. Nevertheless, they are helpful in perioperative days serving as reliable indicators of efficient and fast recovery by better monitoring of patient fitness status and timely detection of the complication. Nowadays, there is a shifting trend among Orthopedics and Traumatology surgeons with an increased number of studies suggesting that operative treatment of acute ATR is not superior to conservative methods.

A literature review of the current knowledge in treating acute traumatic ATR was performed in order to test the hypothesis that nonoperative treatment is „equivalent“ to operative treatment in terms of re-rupture rate and long-term patient satisfaction. We have searched the PubMed database for the terms „Achilles tendon rupture“ and „operative vs nonoperative“ and obtained 27 results. After including the studies published from 2020 until 2024, and excluding inapplicable studies, we selected 5 studies that matched the topic.

Of the 5 studies included in this research, 3 were comparing patient satisfaction, re-rupture rate and complication rate, while 2 studies provided the cost-benefit analysis of operative vs nonoperative treatment. The oldest study from this group was published in 2020 which concluded that there was no demonstrable difference in patient-reported outcome, satisfaction, or re-rupture rates at long-term follow-up (73). Next study from 2022 suggested that nonoperative treatment of ATR may have up to 6.4% higher relative risk of re-rupture and that previous studies were only comparing the absolute risk of re-rupture (74). The newest study from this group was published in 2023 indicated no differences in reoperation rates between operative and nonoperative management of ATR (75). Also, operative management was associated with an increased risk of complications and higher initial costs, which dissipated over time. Both cost-benefit analyses were on average in favour of nonoperative treatment (71,75). Surgical repair is associated with greater costs partially because of the greater utilization of clinic visits, imaging, and physical therapy sessions. Nonoperative treatment is associated with higher prescription costs secondary to a longer duration of opioid use.

Current papers available on this topic prove that nonoperative treatment has similar long-term patient satisfactory results compared to operative management. Furthermore, the cost of nonoperative treatment seems to be less, which is also a factor that should not be ignored. Still, decisions on treatment should be made by the surgeon on an individual basis. Helping tools such as Copenhagen Achilles Rupture Treatment Algorithm could help in this decision-making process. A new biological approach through multiple platelet-rich plasma injections is also gaining popularity lately (76). The goal of achieving optimally efficient and safe outcomes with biological therapy opens a novel niche for laboratory medicine in a comprehensive and multidisciplinary ATR management.

Conclusions

Laboratory medicine in sport and exercise has significantly developed during the last decades with the awareness that physical activity contributes to improved health status, and is present in monitoring both professional and recreational athletes. Laboratory medicine extends to almost every aspect of sports, even to prevention of injuries but with less extent when the injury has occurred.

Training and competitions can modify concentrations of a variety of laboratory parameters, so the accurate laboratory data interpretation includes controlled and known preanalytical and analytical variables to prevent misleading interpretations. A corresponding “to-do” list in front of laboratory medicine specialists is extensive and challenging. Its core has four elements: continuous knowledge improvements about sport (patho)biology, resolving challenges brought by new analytical technologies, collaboration with other healthcare professionals involved in the field, and competencies to educate patients on minimizing the adverse effects of their sports and recreational activities on lab test results.

Notes

[1] Conflicts of interest Potential conflict of interest

None declared.

Data availability statement

No data was generated during this study, so data sharing statement is not applicable to this article.

References

1 

Lippi G, Banfi G, Botrè F, de la Torre X, De Vita F, Gomez-Cabrera MC, et al. Laboratory medicine and sports: between Scylla and Charybdis. Clin Chem Lab Med. 2012;50:1309–16. https://doi.org/10.1515/cclm-2012-0062 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/22868795

2 

Lombardo B, Izzo V, Terracciano D, Ranieri A, Mazzaccara C, Fabio Fimiani F, et al. Laboratory medicine: health evaluation in elite athletes. Clin Chem Lab Med. 2019;57:1450–73. https://doi.org/10.1515/cclm-2018-1107 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/30835249

3 

Banfi G, Colombini A, Lombardi G, Lubkowska A. Metabolic markers in sports medicine. Adv Clin Chem. 2012;56:1–54. https://doi.org/10.1016/B978-0-12-394317-0.00015-7 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/22397027

4 

Lippi G, Banfi G, Maffulli N. Preanalytical variability: the dark side of the moon in blood doping screening. Eur J Appl Physiol. 2010;109:1003–5. https://doi.org/10.1007/s00421-010-1437-3 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/20333397

5 

Lippi G. Genomics and sports: building a bridge towards a rational and personalized training framework. Int J Sports Med. 2008;29:264–5. https://doi.org/10.1055/s-2008-1038323 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/18278710

6 

Ricós C, Alvarez V, Cava F, Garcia-Lario JV, Hernandez A, Jimenez CV, et al. Current databases on biologic variation: pros, cons and progress. Scand J Clin Lab Invest. 1999;59:491–500. https://doi.org/10.1080/00365519950185229 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/10667686

7 

Sandberg S, Fraser CG, Horvath AR, Jansen R, Jones G, Oosterhuis W, et al. Defining analytical performance specifications: Consensus Statement from the 1st Strategic Conference of the European Federation of Clinical Chemistry and Laboratory Medicine. Clin Chem Lab Med. 2015;53:833–5. https://doi.org/10.1515/cclm-2015-0067 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/25719329

8 

Aarsand AK, Fernandez-Calle P, Webster C, Coskun A, Gonzales-Lao E, Diaz-Garzon J, et al. The EFLM Biological Variation Database. Available from:https://biologicalvariation.eu/. Accessed February 23rd 2024.

9 

Sandberg S, Carobene A, Bartlett B, Coskun A, Fernandez-Calle P, Jonker N, et al. Biological variation: recent development and future challenges. Clin Chem Lab Med. 2022;61:741–50. https://doi.org/10.1515/cclm-2022-1255 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/36537071

10 

Heimer S, Čajavec R, et al., editors. [Medicina sporta]. Zagreb: Kineziološki fakultet Sveučilišta u Zagrebu; 2006. (in Croatian)

11 

World Anti-Doping Agency (WADA). Athlete Biological Passport Operating Guidelines. Version 9.0 July 2023. Available from:https://www.wada-ama.org/en/resources/world-anti-doping-program/athlete-biological-passport-abp-operating-guidelines. Accessed February 23rd 2024.

12 

Krumm B, Fais R. Factors confounding the athlete biological passport: A systematic narrative review. Sports Med Open. 2021;7:65. https://doi.org/10.1186/s40798-021-00356-0 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/34524567

13 

Diaz-Garzon J, Fernandez-Calle P, Aarsand AK, Sandberg S, Coskun A, Carobene A, et al. Long-term within- and between-subject biological variation of 29 routine laboratory measurands in athletes. Clin Chem Lab Med. 2021;60:618–28. https://doi.org/10.1515/cclm-2021-0910 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/34800014

14 

Diaz-Garzon J, Fernandez–Calle P, Aarsand AK, Sandberg S, Coskun A, Equey T, et al. Long-term within- and between-subject biological variation data of hematological parameters in recreational endurance athletes. Clin Chem. 2023;69:500–9. https://doi.org/10.1093/clinchem/hvad006 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/36786725

15 

Sanchis-Gomar F, Lippi G. Physical activity - An important preanalytical variable. Biochem Med (Zagreb). 2014;24:68–79. https://doi.org/10.11613/BM.2014.009 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/24627716

16 

Thomas L, Röcker L, Kiesewetter H. Clinical Laboratory Diagnostics. Effect of physical exercise on laboratory test results. Available from:https://www.clinical-laboratory-diagnostics.com/k51.html. Accessed March 19th 2024.

17 

Thomas RJ. kenfield SA, Jimenez A. Exercise-induced biochemical changes and their potential influence on cancer: A scientific review. Br J Sports Med. 2017;51:640–4. https://doi.org/10.1136/bjsports-2016-096343 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/27993842

18 

Fragala MS, Bi C, Chaump M, Kaufman HW, Kroll MH. Associations of aerobic and strength exercise with clinical laboratory test values. PLoS One. 2017;12:e0180840. https://doi.org/10.1371/journal.pone.0180840 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/29059178

19 

Wang Y, Xu D. Effects of aerobic exercise on lipids and lipoproteins. Lipids Health Dis. 2017;16:132. https://doi.org/10.1186/s12944-017-0515-5 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/28679436

20 

Foran SE, Lewandrowski KB, Kratz A. Effects of exercise on laboratory test results. Lab Med. 2003;34:736–42. https://doi.org/10.1309/3PDQ4AH662ATB6HM

21 

Winding KM, Munch GW, Iepsen UW, Van Hall G, Pedersen BK, Mortensen SP. The effect on glycaemic control of low-volume high-intensity interval training versus endurance training in individuals with type 2 diabetes. Diabetes Obes Metab. 2018;20:1131–9. https://doi.org/10.1111/dom.13198 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/29272072

22 

Riddell MC, Peters AL. Exercise in adults with type 1 diabetes mellitus. Nat Rev Endocrinol. 2023;19:98–111. https://doi.org/10.1038/s41574-022-00756-6 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/36316391

23 

Bowler AM, Whitfield J, Marshall L, Coffey VG, Burke LM, Cox GR. The use of continuous glucose monitors in sport: Possible applications and considerations. Int J Sport Nutr Exerc Metab. 2022;33:121–32. https://doi.org/10.1123/ijsnem.2022-0139 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/36572039

24 

Moser O, Yardley JE, Bracken RM. Interstitial glucose and physical exercise in Type 1 Diabetes: Integrative physiology, technology, and the gap in-between. Nutrients. 2018;10:93. https://doi.org/10.3390/nu10010093 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/29342932

25 

Yardley JE, Sigal RJ, Kenny GP, Riddell MC, Lovblom LE, Perkins BA. Point accuracy of interstitial continuous glucose monitoring during exercise in type 1 diabetes. Diabetes Technol Ther. 2013;15:46–9. https://doi.org/10.1089/dia.2012.0182 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/23137050

26 

Facchinetti A, Sparacino G, Guerra S, Luijf YM, DeVries JH, Mader JK, et al. Real-time improvement of continuous glucose monitoring accuracy: the smart sensor concept. Diabetes Care. 2013;36:793–800. https://doi.org/10.2337/dc12-0736 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/23172973

27 

Didyuk O, Econom N, Guardia A, Livingston K, Klueh U. Continuous glucose monitoring devices: Past, present, and future focus on the history and evolution of technological innovation. J Diabetes Sci Technol. 2021;15:676–83. https://doi.org/10.1177/1932296819899394 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/31931614

28 

Hooper DR, Kraemer WJ, Focht BC, Volek JS, DuPont WH, Caldwell LK, et al. Endocrinological roles for testosterone in resistance exercise responses and adaptations. Sports Med. 2017;47:1709–20. https://doi.org/10.1007/s40279-017-0698-y PubMed: http://www.ncbi.nlm.nih.gov/pubmed/28224307

29 

Sinha-Hikim I, Artaza J, Woodhouse L, Gonzalez-Cadavid N, Singh AB, Lee MI, et al. Testosterone-induced increase in muscle size in healthy young men is associated with muscle fiber hypertrophy. Am J Physiol Endocrinol Metab. 2002;283:E154–64. https://doi.org/10.1152/ajpendo.00502.2001 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/12067856

30 

Mänttäri S, Anttila K, Jarvilehto M. Testosterone stimulates myoglobin expression in different muscles of the mouse. J Comp Physiol B. 2008;178:899–907. https://doi.org/10.1007/s00360-008-0280-x PubMed: http://www.ncbi.nlm.nih.gov/pubmed/18548256

31 

Almeida M, Laurent MR, Dubois V, Claessens F, O’Brien CA, Bouillon R, et al. Estrogens and androgens in skeletal physiology and pathophysiology. Physiol Rev. 2017;97:135–87. https://doi.org/10.1152/physrev.00033.2015 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/27807202

32 

Shahani S, Braga-Basaria M, Maggio M, Basaria S. Androgens and erythropoiesis: past and present. J Endocrinol Invest. 2009;32:704–16. https://doi.org/10.1007/BF03345745 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/19494706

33 

Bachman E, Travison TG, Basaria S, Davda MN, Guo W, Li M, et al. Testosterone induces erythrocytosis via increased erythropoietin and suppressed hepcidin: evidence for a new erythropoietin/hemoglobin set point. J Gerontol A Biol Sci Med Sci. 2014;69:725–35. https://doi.org/10.1093/gerona/glt154 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/24158761

34 

Eklund E, Berglund B, Labrie F, Carlström K, Ekström L, Hirschberg AL. Serum androgen profile and physcial performance in women Olympic athletes. Br J Sports Med. 2017;51:1301–8. https://doi.org/10.1136/bjsports-2017-097582 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/28646101

35 

Labrie F, Martel C, Belanger A, Pelletier G. Androgens in women are essentially made from DHEA in each peripheral tissue according to intracrinology. J Steroid Biochem Mol Biol. 2017;168:9–18. https://doi.org/10.1016/j.jsbmb.2016.12.007 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/28153489

36 

Rickenlund A, Carlström K, Ekblom B, Brismar TB, von Schoultz B, Hirschberg AL. Hyperandrogenicity is an alternative mechanism underlying oligomenorrhea and amenorrhea in female athletes and may improve physical performance. Fertil Steril. 2003;79:947–55. https://doi.org/10.1016/S0015-0282(02)04850-1 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/12749436

37 

Kogure GS, Silva RC, Picchi Ramos FK, Miranda-Furtado CL, Lara LA, Ferriani RA, et al. Women with polycystic ovary syndrome have greater muscle strength irrespective of body composition. Gynecol Endocrinol. 2015;31:237–42. https://doi.org/10.3109/09513590.2014.982083 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/25430509

38 

Hsu B, Cumming RG, Handelsman DJ. Testosterone, frailty and physical function in older men. Expert Rev Endocrinol Metab. 2018;13:159–65. https://doi.org/10.1080/17446651.2018.1475227 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/30058896

39 

Bermon S. Androgens and athletic performance of elite female athletes. Curr Opin Endocrinol Diabetes Obes. 2017;24:246–51. https://doi.org/10.1097/MED.0000000000000335 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/28234801

40 

Hackney AC, Moore AW, Brownlee KK. Testosterone and endurance exercise: development of the “exercise-hypogonadal male condition.”. Acta Physiol Hung. 2005;92:121–37. https://doi.org/10.1556/APhysiol.92.2005.2.3 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/16268050

41 

Hackney AC, Hackney ZC. The exercise hypogonadal male condition and endurance exercise training. Curr Trends Endocinol. 2005;1:101–6. PubMed: http://www.ncbi.nlm.nih.gov/pubmed/31723314

42 

Loucks AB, Kiens B, Wright HH. Energy availability in athletes. J Sports Sci. 2011;29:S7–15. https://doi.org/10.1080/02640414.2011.588958 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/21793767

43 

Hackney AC. Hypogonadism in exercising males: dysfunction or adaptive-regulatory adjustment? Front Endocrinol (Lausanne). 2020;11:11. https://doi.org/10.3389/fendo.2020.00011 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/32082255

44 

Croatian Diving Association (CDA). Available from:https://www.diving-hrs.hr/. Accessed March 15th 2024.

45 

Perović A, Unić A, Dumić J. Recreational scuba diving: negative or positive effects of oxidative and cardiovascular stress? Biochem Med (Zagreb). 2014;24:235–47. https://doi.org/10.11613/BM.2014.026 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/24969917

46 

CMAS. Universal standards and procedures. Available from:http://www.cmas.org/technique/general-documents. Accessed March 15th 2024.

47 

Perović A, Nikolac N, Bratičević MN, Milcic A, Sobočanec S, Balog T, et al. Does recreational scuba diving have clinically significant effect on routine haematological parameters? Biochem Med (Zagreb). 2017;27:325–31. https://doi.org/10.11613/BM.2017.035 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/28694723

48 

Perović A, Žarak M, Njire Bratičević M, Dumić J. Effects of recreational scuba diving on erythropoiesis-“normobaric oxygen paradox” or “plasma volume regulation” as a trigger for erythropoietin? Eur J Appl Physiol. 2020;120:1689–97. https://doi.org/10.1007/s00421-020-04395-5 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/32488585

49 

Perović A, Sobočanec S, Dabelić S, Balog T, Dumić J. Effect of scuba diving on the oxidant/antioxidant status, SIRT1 and SIRT3 expression in recreational divers after a winter nondive period. Free Radic Res. 2018;52:188–97. https://doi.org/10.1080/10715762.2017.1422211 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/29334806

50 

Žarak M, Perović A, Dobrović I, Šupraha Goreta S, Dumić J. Galectin-3 and cardiovascular biomarkers reflect adaptation response to scuba diving. Int J Sports Med. 2020;41:285–91. https://doi.org/10.1055/a-1062-6701 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/31975358

51 

Žarak M, Perović A, Njire Bratičević M, Šupraha Goreta S, Dumić J. Adaptive response triggered by the repeated SCUBA diving is reflected in cardiovascular, muscular, and immune biomarkers. Physiol Rep. 2021;9:e14691. https://doi.org/10.14814/phy2.14691 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/33463896

52 

Dumić J, Cvetko A, Abramović I, Šupraha Goreta S, Perović A, Njire Bratičević M, et al. Changes in specific biomarkers indicate cardiac adaptive and anti-inflammatory response of repeated recreational SCUBA diving. Front Cardiovasc Med. 2022;9:855682. https://doi.org/10.3389/fcvm.2022.855682 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/35360010

53 

Njire Bratičević M, Žarak M, Šimac B, Perović A, Dumić J. Effects of recreational SCUBA diving practiced once a week on neurohormonal response and myokines-mediated communication between muscles and the brain. Front Cardiovasc Med. 2023;10:1074061. https://doi.org/10.3389/fcvm.2023.1074061 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/37063956

54 

Płoszczyca K, Langfort J, Czuba M. The effects of altitude training on erythropoietic response and hematological variables in adult athletes: a narrative review. Front Physiol. 2018;9:375. https://doi.org/10.3389/fphys.2018.00375 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/29695978

55 

Salvagno M, Coppalini G, Taccone FS, Strapazzon G, Mrakic-Sposta S, Rocco M, et al. The normobaric oxygen paradox-hyperoxic hypoxic paradox: a novel expedient strategy in hematopoiesis clinical issues. Int J Mol Sci. 2022;24:82. https://doi.org/10.3390/ijms24010082 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/36613522

56 

Yuan X, Ruan W, Bobrow B, Carmeliet P, Eltzschig HK. Targeting hypoxia-inducible factors: therapeutic opportunities and challenges. Nat Rev Drug Discov. 2024;23:175–200. https://doi.org/10.1038/s41573-023-00848-6 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/38123660

57 

Kindrick JD, Mole DR. Hypoxic regulation of gene transcription and chromatin: cause and effect. Int J Mol Sci. 2020;21:8320. https://doi.org/10.3390/ijms21218320 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/33171917

58 

Saugy JJ, Schmoutz T, Botrè F. Altitude and erythropoietin: comparative evaluation of their impact on key parameters of the athlete biological passport: a review. Front Sports Act Living. 2022;4:864532. https://doi.org/10.3389/fspor.2022.864532 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/35847455

59 

Balestra C, Germonpré P, Poortmans JR, Marroni A. Serum erythropoietin levels in healthy humans after a short period of normobaric and hyperbaric oxygen breathing: the “normobaric oxygen paradox”. J Appl Physiol. 2006;100:512–8. https://doi.org/10.1152/japplphysiol.00964.2005 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/16239610

60 

Revelli L, Vagnoni S, D’Amore A, Di Stasio E, Lombardi CP, Storti G, et al. EPO modulation in a 14-days undersea scuba dive. Int J Sports Med. 2013;34:856–60. https://doi.org/10.1055/s-0033-1334912 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/23670359

61 

Kiboub FZ, Balestra C, Loennechen Ø, Eftedal I. Hemoglobin and erythropoietin after commercial saturation diving. Front Physiol. 2018;9:1176. https://doi.org/10.3389/fphys.2018.01176 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/30246801

62 

Hadanny A, Efrati S. The hyperoxic-hypoxic paradox. Biomolecules. 2020;10:958. https://doi.org/10.3390/biom10060958 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/32630465

63 

World Anti-Doping Agency (WADA). Available from:https://www.wada-ama.org/en. Accessed March 1st 2024.

64 

World Anti-Doping Agency. The World Anti-doping Code 2021. Available from:https://www.wada-ama.org/sites/default/files/resources/files/2021_wada_code.pdf. Accessed March 1st 2024.

65 

World Anti-Doping Agency. The 2024 Prohibited List. Available from:https://www.wada-ama.org/sites/default/files/2023-09/2024list_en_final_22_september_2023.pdf. Accessed March 1st 2024.

66 

World Anti-Doping Agency. List of WADA-Accredited Laboratories. Available from:https://www.wada-ama.org/sites/default/files/2024-03/wada_accredited_laboratories_en_march_doc.pdf. Accessed March 1st 2024.

67 

World Anti-Doping Agency. The World Anti-Doping Code International Standard for Laboratories (ISL). Available from:https://www.wada-ama.org/sites/default/files/resources/files/isl_2021.pdf. Accessed March 1st 2024.

68 

World Anti-Doping Agency. Current versions of WADA ISL, Technical Documents and Laboratory Guidelines. Available from:https://www.wada-ama.org/en/anti-doping-partners/laboratories. Accessed March 1st 2024.

69 

WADA Technical Document TD IRMS: Detection of Synthetic Forms of Prohibited Substances by GC/C/IRMS. Available from:https://www.wada-ama.org/sites/default/files/2022-01/td2022irms_v1.0_final_eng_0_0.pdf. Accessed March 1st 2024.

70 

Thevis M, Kuuranne T, Geyer H. Annual banned-substance review 16th edition - Analytical approaches in human sports drug testing 2022/2023. Drug Test Anal. 2024;16:5-29. https://doi.org/10.1002/dta.3602 https://doi.org/10.1002/dta.3602

71 

Murdock CJ, Ochuba AJ, Xu AL, Snow M, Bronheim R, Vulcano E, et al. Operative vs nonoperative management of Achilles tendon rupture: A cost analysis. Foot Ankle Orthop. 2023;8:24730114231156410. https://doi.org/10.1177/24730114231156410 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/36911422

72 

Hansen MS, Bencke J, Kristensen MT, Kallemose T, Hölmich P, Barfod KW. Achilles tendon gait dynamics after rupture: A three-armed randomized controlled trial comparing an individualized treatment algorithm vs. operative or non-operative treatment. Foot Ankle Surg. 2023;29:143–50. https://doi.org/10.1016/j.fas.2022.12.006 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/36528540

73 

Maempel JF, Clement ND, Wickramasinghe NR, Duckworth AD, Keating JF. Operative repair of acute Achilles tendon rupture does not give superior patient-reported outcomes to nonoperative management. Bone Joint J. 2020;102-B:933–40. https://doi.org/10.1302/0301-620X.102B7.BJJ-2019-0783.R3 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/32600149

74 

Reito A, Mattila V, Karjalainen T. Operative vs nonoperative treatment of Achilles tendon ruptures using early functional rehabilitation: Critical analysis of evidence. Foot Ankle Int. 2022;43:887–90. https://doi.org/10.1177/10711007221083691 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/35382647

75 

Crook BS, Varshneya K, Meyer LE, Anastasio A, Cullen MM, Lau BC. Operative versus nonoperative treatment of acute Achilles tendon rupture: A propensity score-matched analysis of a large national dataset. Orthop J Sports Med. 2023;11:23259671231152904. https://doi.org/10.1177/23259671231152904 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/36874053

76 

Filardo G, Lo Presti M, Kon E, Marcacci M. Nonoperative biological treatment approach for partial Achilles tendon lesion. Orthopedics. 2010;33:120–3. https://doi.org/10.3928/01477447-20100104-31 PubMed: http://www.ncbi.nlm.nih.gov/pubmed/20192152


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