Induction of lipid peroxidation of pulmonary surfactant by plasma of preterm babies

doi:10.1016/0140-6736(93)92557-A

The Lancet

Volume 341, Issue 8837, 9 January 1993, Pages 79-82

https://doi.org/10.1016/0140-6736(93)92557-A Get rights and content

Abstract

Respiratory distress syndrome of the preterm baby is believed to be caused by a deficiency of pulmonary surfactant and leakage of plasma into the alveolar spaces. Since the two pathogenetic factors seem to be inter-related, we postulated that peroxidation of surfactant by plasma iron could be the linking mechanism. We obtained cord blood samples from 22 preterm babies (mean gestational age 32·2 [SD 2·7] weeks) and 24 term babies (40·1 [1·6] weeks), and venous blood samples from 18 healthy adults. No adult had detectable non-protein-bound iron in the plasma, but 10/21 (48%) preterm babies and 6/24 (25%) term babies had detectable concentrations (rate difference 23% [95% Cl -5 to 51%], p=0·20). Transferrin and haptoglobin concentrations were higher and free haemoglobin concentrations lower in adults than in babies (p<0·005). Only transferrin differed significantly between term and preterm babies. Plasma from all 18 adults and from 23 (96%) term babies inhibited iron-catalysed lipid peroxidation of pulmonary surfactant liposomes. By contrast, plasma from 11 (50%) preterm babies stimulated such peroxidation (difference in stimulation rate 46% [20-71%], p<0·005 for preterm vs term babies); the ability to stimulate peroxidation was related to the presence of non-protein-bound iron (p<0·001). Peroxidation decreased in the babies when apotransferrin was added to plasma and in all subjects when α-tocopherol was incorporated into the surfactant liposomes. Lipid peroxidation of surfactant may contribute to the pathogenesis of respiratory distress syndrome. Possible therapeutic approaches are increasing babies' iron-binding capacity by plasma transfusions and increasing the antioxidant capacity of commercial surfactant.

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This indicates lower antioxidant enzymatic activity in the former (Table 1). Preterm newborns also exhibit lower levels of non-enzymatic antioxidants such as erythrocyte vitamin E [19], blood vitamin E [11,17], blood vitamin A [11,17,21,27–29], blood vitamin C [11], erythrocyte reduced glutathione (GSH) [14], blood transferrin [22] and tracheal aspirates GSH [30] (Table 1). Two study however, reported higher blood vitamin C levels in preterm compared to full-term newborns [20,31].
Preterm birth is a global health issue that can induce lifelong medical sequela. Presently, at least one in ten newborns are born prematurely. At birth, preterm newborns exhibit higher levels of oxidative stress (OS) due to the inability to face the oxygen rich environment in which they are born into. Moreover, their immature respiratory, digestive, immune and antioxidant defense systems, as well as the potential numerous medical interventions following a preterm birth, such as oxygen resuscitation, nutrition, phototherapy and blood transfusion further contribute to high levels of OS. Although the acute effects seem well established, little is known regarding the long-term effects of preterm birth on OS. This matter is especially important given that chronically elevated OS levels may persist into adulthood and consequently contribute to the development of numerous non-communicable diseases observed in people born preterm such as diabetes, hypertension or lung disorders. The purpose of this review is to summarize the current knowledge regarding the consequences of preterm birth on OS levels from newborn to adulthood. In addition, the effects of physical activity and hypoxia, both known to disrupt redox balance, on OS modulation in preterm individuals are also explored.
Haptoglobin phenotype and reproductive success in repeated spontaneous abortion
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Hp has been found associated with the prevalence and clinical evolution of many inflammatory diseases, including infections, atherosclerosis, and autoimmune disorders [9,10], with venous thromboembolism [11]. Hp influences the Th1/Th2 balance [12], its absence may favour lipid peroxidation of pulmonary surfactant in preterm babies [13], it plays a critical role in the atherosclerotic plaque and in coronary hearth disease [14], and is associated with celiac disease [6]. Recently researchers have demonstrated that an allelic polymorphism in the haptoglobin gene is predictive of the risk for numerous microvascular and macrovascular diabetic complications (e.g. nephropathy, retinopathy, cardiovascular disease, vascular complications), and is a regulator of reverse cholesterol transport [15,16].
To study the reproductive success of couples with a history of repeated spontaneous abortion (RSA) with respect to the haptoglobin (Hp) phenotypes of both the wife and husband.
This study examined maternal and paternal Hp in 194 couples with primary and secondary RSA recruited from the Center for Reproductive Disorders of the Institute of Obstetrics and Gynaecology at the University of Rome, La Sapienza. Reproductive success was indicated by the presence of at least one live-born infant after more than 5 years of follow-up.
The proportion of wives carrying Hp2/1 phenotype and with at least one live-born infant is significantly lower than that of wives without a live-born infant. Moreover, the proportion of couples in which both wife and husband possess the Hp2/1 phenotype is much lower in those with at least a live-born infant than in those without a live-born infant. Both maternal and paternal Hp contribute to reproductive success. However, the contribution of maternal Hp appears stronger than that of paternal Hp.
Hp may play an important role in implantation and/or embryo survival. Couples in which both partners carry the Hp2/1 phenotype have a low probability of producing a live-born infant.
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Indeed, recent observations suggest that Hp influences the Th1/Th2 balance (13). Since Hp is a protection against the action of free radicals, it has been suggested that the absence of Hp in newborns may favor lipid peroxidation of pulmonary surfactant in preterm babies (14). Owing to its higher diffusibility, the Hp∗1/∗1 genotype may be more protective against oxidative damage compared with other Hp phenotypes (8).
To search for possible effects of two polymorphisms and of the solar cycle of illumination on reproductive success.
Study of haptoglobin (Hp) and ACP1 polymorphisms in consecutive puerperae and analysis of phenotype distribution in relation to time of conception.
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In the first months of the year there is a steady increase in solar illumination, and this phase corresponds to the best period for reproduction in most plants and animals. This period is also the coldest in the Italian latitudes. Although humans are not seasonal breeders, it is possible that women having a genetic background best adapted to the metabolic demand of the cold period of the year will respond better to reproductive stimuli, resulting in a higher probability of conceiving in the first part of the year.
Early neonatal antioxidant capacity after preexisting impaired placental function
2003, Early Human Development
Plasma antioxidant capacity in very preterm infants (n=17), measured as the ferric-reducing ability of plasma (FRAP), increased significantly until day 2 postpartum and decreased thereafter until day 7. Within this period, the FRAP values in matched infants, born after impaired placental function (IPF, n=17), did not change. Their FRAP values were lower and the incidence of oxidative stress-related diseases was significantly higher in these infants.
Bronchopulmonary dysplasia - Oxidative stress and antioxidants
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There is increasing evidence that oxidative stress is implicated in the development of bronchopulmonary dysplasia. Several important factors contribute to augmented oxidative stress in the newborn and especially the preterm infant: first, because of its immaturity, the lung of preterm infants is frequently exposedto oxygen therapy and hyperoxia. Second, the antioxidant defense and its ability to be induced during an hyperoxic challenge are impaired. Third, the preterm infant has an increased susceptibility to infection and inflammation, which increases oxidative stress. Fourth, free iron, which catalyzes the production of toxic reactive oxygen species, can be detected in preterm infants. The molecular and cellular mechanisms for free radical-induced injury are now understood in more detail, and it is clear that oxidative stress plays an important role in triggering apoptosis, in serving as second messenger and in signal transduction. This new insight mightlead to novel and efficient therapies. So far, there has been no significant breakthrough regarding antioxidant therapies. Care should, however, be exercised in supplementing the preterm infant with antioxidants since this may affect growth and development.
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ARTICLESInduction of lipid peroxidation of pulmonary surfactant by plasma of preterm babies

Abstract

Biochim Biophys Acta

Chem Phys Lipids

Lancet

J Pediatr

Free Rad Biol Med

Biochim Biophys Acta

Lancet

Thorac Cardiovasc Surg

Biochim Biophys Acta

J Pediatr

Surfactant-replacement therapy

N Engl J Med

Surfactant for the treatment of respiratory distress syndrome

Am Rev Respir Dis

The pulmonary surfactant system: biochemical aspects and functional significance

Physiol Rev

Inactivation of exogenous surfactant by pulmonary edema fluid

Pediatr Res

Activity of pulmonary surfactant after blocking the associated proteins SP-A and SP-B

J Appl Physiol

ARTICLES
Induction of lipid peroxidation of pulmonary surfactant by plasma of preterm babies